Better red than dead: carotenoid-based mouth coloration reveals infection in barn swallow nestlings

Abstract

Nestling birds solicit food from their parents by displaying their open brightly coloured gapes. Carotenoids a¡ect gape colour, but also play a central role in immunostimulation. Therefore, we hypothesize that, by di¡erentially allocating resources to nestlings with more brightly coloured gapes, parents favour healthy o¡spring which are able to allocate carotenoids to gape coloration without compromising their immune defence. We demonstrated that, in the barn swallow Hirundo rustica, (i) parents di¡erentially allocate food to nestlings with an experimentally brighter red gape, (ii) nestlings challenged with a novel antigen (sheep red blood cells, SRBCs) have less bright gape colour than their control siblings, (iii) nestlings challenged with SRBCs but also provided with the principal circulating carotenoid (lutein) have more brightly coloured red gapes than their challenged but unsupplemented siblings and (iv) the gape colour of nestlings challenged with SRBCs and provisioned with lutein exceeds that of siblings that were unchallenged. This suggests that parents may favour nestlings with superior health by preferentially feeding o¡spring with the brightest gapes.

The Role of the Immune System in Behavioral Strategies of Reproduction

“…Free radicals generated by activated phagocytes are considered as main internal factor that is responsible for the parasite-induced reduction of comb size, coloration of plumage or skin, and song repertoire [173]. In barn swallow, H. rustica, nestlings challenged with a novel antigen SRBC have less bright gape color than their control sibling, probably due to reallocation of carotenoids from soft tissues to blood stream [174] Since blood level of carotenoids correlated positively with resistance to disease this reallocation plays defensive function [175].…”

Trade-offs in the early development of tree swallows (Tachycineta bicolor): offspring characteristics, offspring quality, and parental care

“…Dugas and McGraw (2011) finally confirmed that carotenoids are, in fact, present in nestling flanges by extracting the carotenoids lutein and zeaxanthin from the flange tissue of nestling house sparrows (Passer domesticus) . The fact that carotenoids are involved both in colouring the gape and in the immune system has led to the hypothesis that gape colour may be a reliable signal of nestling need or condition (Kilner 1997;Saino et al 2000). Supporting this hypothesis is the finding that parent barn swallows (Hirundo rustica) preferentially feed nestlings with redder gapes, and nestlings which have been challenged with a novel antigen have gapes that are less intensely red than those of control siblings (Saino et al 2000).…”

“…Two main hypotheses have been put forward for the function of colourful gapes and flanges in nestlings, both human visible and in the ultraviolet (UV) range. The detectability hypothesis proposes that conspicuous colouration makes nestlings more visible in a dark nest environment so that parents are more easily able to feed them (Pycraft 1907;Swynnerton 1916), and the need-signalling hypothesis states that colouration signals need or condition to parents (Kilner 1997;Saino et al 2000). Many studies have reported a positive effect of both UV reflectance or carotenoidrich appearance of flanges (Jourdie et al 2004;de Ayala et al 2007;Loiseau et al 2008;Dugas 2009;Tanaka et al 2011 ;Wiebe & Slagsvold 2012) and reddened gapes (Gotmark & Ahlstrom 1997;Kilner 1997;Saino et al 2000) on parental feeding of offspring, although some studies have observed no effect of either UV reflectance of flanges (Wiebe & Slagsvold 2009) or gape redness (Noble et al 1999) on parental provisioning preferences.…”

“…The fact that carotenoids are involved both in colouring the gape and in the immune system has led to the hypothesis that gape colour may be a reliable signal of nestling need or condition (Kilner 1997;Saino et al 2000). Supporting this hypothesis is the finding that parent barn swallows (Hirundo rustica) preferentially feed nestlings with redder gapes, and nestlings which have been challenged with a novel antigen have gapes that are less intensely red than those of control siblings (Saino et al 2000). This suggests that young with redder gapes are in better health and parents preferentially feed such nestlings.…”

Effect of UV-reflectance of chick flanges on begging behaviour and body condition in Barn Swallow (Hirundo rustica, Aves: Hirundinidae) chicks

“…Food allocation within the brood is influenced by visual and acoustic begging displays, reflecting both short-term need (posturing and calling; Boncoraglio et al , 2009) and individual quality (mouth colour, reflecting immunocompetence; Saino et al 2000a) of the chicks. Nestling flanges (i.e., the region including the external sides of the beak) and palate show large reflectance peaks in the UV range (320-370 nm).…”