Carotenoid-based bill and eye ring coloration as honest signals of condition: an experimental test in the red-legged partridge (Alectoris rufa)

Abstract

Carotenoid pigments cannot be synthesized by vertebrates but must be ingested through the diet. As they seem to be a limited resource, carotenoid-based ornaments are particularly interesting as possible honest signals of individual quality, in particular of foraging efficiency and nutritional status. Some studies have demonstrated the condition dependence of carotenoid-based plumage in birds. However, many other carotenoid-pigmented bare parts (i.e. skin, caruncles, bills, cere, and tarsi) are present in birds but, in comparison with plumage, little is known about these traits as indicators of individual quality. Here, we show that the eye ring pigmentation and bill redness of the red-legged partridge (Alectoris rufa) are positively associated to body condition and recent changes in body mass. Also, we found a negative relationship between these two traits and heterophil-to-lymphocyte ratio, an indicator of physiological stress (the relationship with bill redness being significant only for males). In an experiment, we found that after a period of reduction in food intake (with the consequent loss of body mass), food-restricted birds showed lower eye ring pigmentation than ad-libitum-fed birds. Therefore, different ornaments seem to reflect changes in body condition but at different speeds or intensities (eye ring, a fleshy ornament, appears to respond more rapidly to changes in the nutritional status than a keratinized structure as the bill). These results indicate that carotenoid-based ornaments are condition-dependent traits in the red-legged partridge, being therefore susceptible to be employed as honest signals of quality in sexual selection.

Integument colouration in relation to persistent organic pollutants and body condition in arctic breeding black-legged kittiwakes (Rissa tridactyla)

“…Contrary to fleshy integuments with rapid colour changes, e.g. 48 h for the skin of the blue-footed booby Sulax nebouxi (Velando et al, 2006), the bill is a keratinized structure and the turnover of carotenoids deposited in the bill is obviously slower (Pérez-Rodríguez and Viñuela, 2008). Moreover, body condition and POP levels of kittiwakes from the studied colony are known to vary rapidly through the breeding season (Moe et al, 2002;Nordstad et al, 2012).…”

“…However, this method has already been investigated on black-legged kittiwakes (Leclaire, 2010;Leclaire et al, 2011aLeclaire et al, , 2011b) and information obtained from digital pictures is still very useful as it reveals patterns and effects of biological meaning (Alonzo-Alvarez et al, 2004;Bortolotti et al, 2003;Kilner, 1997;Leclaire, 2010;Leclaire et al, 2011aLeclaire et al, , 2011bMassaro et al, 2003;Mougeot et al, 2007;Pérez-Rodríguez and Viñuela, 2008;Pérez et al, 2010b). Furthermore, using photography rather than spectrometry might be advantageous because digital photography is a much easier method for quantifying colouration of wet, hard to reach, and irregular surfaces such as gapes, irises and bills (Montgomerie, 2006).…”

“…the most colourful kittiwakes are those with the best immunological status. This implies that healthy individuals should require fewer carotenoids for immune defenses and could therefore allocate more carotenoids to enhance colouration (Pérez et al, 2010a;Pérez-Rodríguez and Viñuela, 2008). However, this hypothesis could only be confirmed by measuring carotenoids in integuments and plasma coupled to the measure of immunological parameters.…”

“…Consequently, carotenoids promote survival (immunity, antioxidant capacity) suggesting that a tradeoff may exist between allocations of carotenoids to sexual ornaments signaling versus physiological functions for self-maintenance (Eraud et al, 2007;Pérez et al, 2010a;Von Schantz et al, 1999). It is widely assumed that condition-dependence is a common feature of sexual displays (Kristiansen et al, 2006;Martinez-Padilla et al, 2007;Mougeot et al, 2006Mougeot et al, , 2007Pérez-Rodríguez and Viñuela, 2008;Velando et al, 2006).…”

“…Several studies have already highlighted some correlational evidences between carotenoid-based colouration and body condition, a frequently used index of individual quality (Birkhead et al, 1998;Bustnes et al, 2007;Massaro et al, 2003;Mougeot et al, 2006Mougeot et al, , 2007Pérez-Rodríguez and Viñuela, 2008;Pérez et al, 2010b). As birds cannot synthetize carotenoids de novo, they have to acquire them through their diet and thus, carotenoid pigmentation depends on the quality and/ or quantity of food ingested (Goodwin, 1986).…”