Carotenoid-Based Masks in the European Goldfinch Carduelis Carduelis Reflect Different Information in Males and Females
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Carotenoid-based masks in the European Goldfinch Carduelis carduelis reflect different information in males and females Guillermo López1,*, Jordi Figuerola2 and Ramón Soriguer1 López G., Figuerola J. & Soriguer R. 2008. Carotenoid-based masks in the European Goldfinch Carduelis carduelis reflect different information in males and females. Ardea 96(2): 233–242. Sexual selection may play an important role in the evolution of carotenoid-based signals. According to the parasite-mediated sexual selection hypothesis, organism health, parasite resistance and the expression of ornaments are linked. While some studies have analysed the expression of male carotenoid-based ornaments in relation to para- sites and immune system capacities, few studies have focused on carotenoid-derived colour patches expressed in both sexes. We analysed the relationships between endoparasite (blood and systemic parasites) loads, haematological values and the components of red mask colour in wild European Goldfinches Carduelis carduelis, a species with a carotenoid-based facial mask in both sexes. Both, males and females were assessed for immune quality and face mask expression. Face mask coloration was sexually dichromatic, males have less orange masks than females. The yellow component of the mask showed less intensity in females infected with Haemoproteus blood parasites. The total leukocyte count was inversely correlated to the yellow component of the mask in females, suggesting that mask colour reflects the immune status of females during the breeding season. Isospora infection appeared to limit the UV reflection of the red mask of females. Key words: sexual selection, Goldfinch, bird, carotenoid, ornament, parasites, Coccidia, Haemoproteus 1Department of Biodiversity, Conservation and Applied Ecology, Estación Biológica de Doñana, Avda. María Luisa s/n, 41013, Seville, Spain; 2Department of Wetland Ecology, Estación Biológica de Doñana, Avda. María Luisa s/n, 41013, Seville, Spain; *corresponding author ([email protected]) INTRODUCTION colour signals requires the ingestion of carotenoids with food, as well as its absorption, transport, Carotenoid pigments are responsible for many of sometimes metabolism and incorporation into the the brightest colours and most conspicuous signals feathers, all processes that are generally consider- in birds (Hill 1999, Hill 2002). However, birds are ed costly to individuals (Hill 2002, McGraw et al. not capable of synthesizing carotenoids from basic 2005, McGraw et al. 2006). Scarcity of carotenoids biological precursors (Goodwin 1984), and there- in the food, or even the energetic cost of enzyme fore, the expression of carotenoid pigments as production and manipulation of carotenoids, 234 ARDEA 96(2), 2008 remain unclear. Carotenoids are also involved in (Merino et al. 2000): they have little impact when metabolic pathways related to host immunity and resources are abundant (Weatherhead & Bennett a trade-off between the ornamental and health 1992, Friend & Franson 2001), but affect nega- functions of carotenoids has been proposed (Hõrak tively the host when resources are scarce (Ots & et al. 2004a, Møller et al. 2004). According to this Hõrak 1998, Ilmonen et al. 1999). The mecha- hypothesis, signals based on carotenoid pigments nisms leading Coccidia to limit the expression of are costly and therefore act as honest indicators of carotenoid-based ornaments may work in at least an individual’s quality. two different direct ways. First, they may reduce The features that each carotenoid-based orna- the absorption of carotenoids through the intestine ment reflect have been mainly studied in males of (Tyczkowski et al. 1991, Allen 1992) and, second, very dimorphic species. Carotenoid-based orna- they may reduce the release of high-density ments have been shown to be related to body con- lipoproteins (Allen 1987), which are responsible dition (McGraw et al. 2002, Saks et al. 2003, for the transport of carotenoids in the bloodstream Jawor & Breitwisch 2004, Jawor et al. 2004), sex- to the tissues. Moreover, a third indirect mecha- ual selection (Collias et al. 1979, Hill 1991, nism related to body condition – to which both Drachman 1997) and even parasite loads carotenoid ornamentation and immunity have (Figuerola et al. 2003, Hill et al. 2004, Hõrak et al. shown to be linked – may also be at work (see 2004). In the case of parasites, studies have Smith et al. 2007). The mechanisms through reported variously negative (Thompson et al. which Haematozoa may limit the expression of 1997, Brawner et al. 2000, Figuerola et al. 2003, carotenoid-based ornaments are still unknown. Hõrak et al. 2004b), positive (Burley et al. 1991, Most of the relationships described up to now VanHoort & Dawson 2005) and non-significant between parasites and the expression of orna- (Seutin 1994) relationships between parasites and ments have been made focusing on conspicuous the expression of a carotenoid-based ornament. male ornaments, but little attention have been tra- The potential causes of these contradictory results ditionally paid to such a relation in female orna- could stem from varying methods of study (e.g. ments. Roulin (2001), for instance, conducted an correlational vs. experimental, ranges or doses of experimental study by comparing the degree of experimental treatments used), different impacts female Barn Owl Tyto alba ornamentation (eume- on parasites on their hosts and environmental- lanin-based spottiness) with parasite resistance in dependent effects of parasites on host condition their offspring raised by foster parents. He found (Figuerola et al. 2003). Work published up to now that in females ornamentation positively reflects has generally focused on a single type of parasite, parasite resistance ability. Some observational above all blood parasites, and analysis of the rela- studies have also demonstrated that the expression tive and combined impact of different types of par- of ornaments is negatively related to the parasite asites on ornament expression is still lacking. load in female birds (Hõrak et al. 2001, Piersma et Haematozoan parasites are blood-cell parasite al. 2001). protozoa transmitted by blood-sucking arthropods The aim of this study was to explore the rela- that are quite prevalent in wild passerines tionship between the colour of the carotenoid- (Deviche et al. 2001). Coccidian protozoa are based red mask of European Goldfinches, and a widespread intestinal epithelium parasites with a number of indices of condition (haematological direct biological cycle; transmission results from parameters and different parasite loads) in both the ingestion of oocysts liberated in the faeces of sexes, paying attention to possible inter-sex differ- an infected individual. Passerines are mainly ences. The study was carried out with free-living infected by genus Isospora (Hill 2002, Hõrak et al. birds during the breeding season, just after mate 2006). Both haematozoan and coccidian parasites choice had occurred, when individuals were going affect their hosts in a condition-dependent way through the costly task of raising young, because López et al.: GOLDFINCH RED MASK IMPLICATIONS 235 under these conditions we expected the effect of Svensson 1996). We also measured body mass (to parasites on their hosts to be maximal. To our the nearest 0.1 g) and wing length (maximum knowledge, this is the first study done analysing chord). Birds were kept individually in clean ring- the relationship between plumage coloration in ing bags for 20 minutes to collect faecal samples. both sexes and several groups of parasites at a Faeces were immediately placed in individually time. marked vials containing 5% formol, and the time of collection was recorded for each sample. To con- trol the mass of faecal samples, we avoided taking METHODS the urine-based part of the excretion and only col- lected the intestinal-based portion. We drew 0.1 The European Goldfinch is a 12-cm long, seed-eat- ml of blood from the jugular vein using 29 G ster- ing finch that has a unique colour pattern on its ile insulin syringes and prepared smears on a head. The front of the face has a conspicuous crim- microscopy slide as per Bennett (1970), which son patch, which is known to be composed of four were air-dried, fixed and stained using Diff-Quick carotenoid pigments (Stradi et al. 1995): a) ε,ε- solution. To confirm field sexing an analysis of the carotene-3,3'-dione, b) 3-hydroxy-ε,ε-carotene-3'- cellular fraction of a drop of blood was performed. one, c) 4,4'-dihydroxy-ε,ε-carotene-3,3'-dione (iso- Sex was determined from blood cell DNA via a astaxanthin), and d) 4-hydroxy-ε,ε-carotene-3,3'- polymerase chain reaction (PCR) amplification of dione. the CHD genes (Ellegren 1996, Griffiths et al. Although ε,ε-carotene-3,3'-dione and 3-hydroxy- 1998). After blood extraction, we took two colour ε,ε-carotene-3'-one are very common yellow pig- measurements of the frontal area of the red mask ments in cardueline finches, isoastaxanthin and 4- in the 57 trapped birds using a MINOLTA CM- hydroxy-ε,ε-carotene-3,3'-dione have not yet been 2600d spectrometer, which measures the charac- found in any other species studied to date. These teristics of reflected light by illuminating the two pigments provide the red colour in the mask feather surface under standard light conditions. together with the keratin bond arrangement the We obtained the reflectance curve of the mask, pigments have in the feathers (Stradi et al. 1995). that is, the light reflection from the UVA (360 nm) Although both sexes are superficially similar to the end of the visible spectrum (740 nm), mea- (Cramp & Perrins 1994), small differences in the sured at 10 nm intervals (39 intervals). The UVA size of the patch exist, being larger on average in reflection is visible to birds and has important males (Svensson 1996). To our knowledge, differ- implications in sexual selection in some passerine ences between the sexes in mask colour have species (Saetre 1994, Siitari et al. 2002, Pearn et never been investigated. al.