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Sexual dimorphism is widely used as an indirect measure of the intensity of sexual selection. It is also a way to evaluate whether different selective pressures act on males and females. Dichromatism, defined as a difference in colouration between males and females, may for instance result from selection for crypsis in females and selection for conspicuousness in males. Here, we conducted a study to investigate whether differential sexual selective pressures might act on the colour traits of two colonial seabird species, the Atlantic puffin Fratercula artica and the black-legged kittiwake Rissa tricactyla. First, we used spectrophotometry and visual modelling to determine whether these presumed monomorphic birds are really monochromatic from an avian perspective (birds and humans have a different vision). Second, we estimated whether some of their colourations have the potential to be sexually or socially selected by determining whether these colourations were related to body condition in males and females, and whether the yellow, orange and red colourations may contain carotenoid pigments. Our results indicated that both species were fully monochromatic from an avian perspective. Moreover, our preliminary analyses suggested that the yellow, orange and red colours of these birds contained carotenoids. Lastly, some indices of colouration were positively linked to estimates of condition. Birds in better condition had redder gape (both species) and bill (puffins). In puffins, the relation between condition and gape colouration was significantly stronger in females than males. By contrast, the size of the gape rosette was larger in males than females. The positive links we found between colour indices and condition, together with the absence of sexual dichromatism, suggest that mutual sexual selection may act in these two species.
Sexual dimorphism is widely used as an indirect measure of sexual selection in comparative studies (Badyaev and Hill 2000, Morrow and Pitcher 2003, Ord and Stuart-Fox 2006). Dichromatism is a special case of sexual dimorphism whereby males and females differ in colouration. Dichromatism is widespread and highly variable at the interspecific level. Extreme dichromatism can be encountered for instance in the mallard Anas platyrhynchos: males and females are so different that they had been identified as two different species when first described (Anderson 1994). By contrast, a highly subtle dichromatism that cannot be detected by human eyes can be found in other species (e.g. black-capped chickadee Parus atricapillus:Mennill et al. 2004).
Sexual dichromatism can be explained by differences in the relative strength of selective pressures acting on both sexes: stronger sexual selection can lead to the elaboration of colour traits while a stronger natural selection can lead to crypsis (Badyaev and Hill 2003, Owens 2006, Gomez and Thery 2007). The intensity and diversity of sexual dichromatism in animal signals can be explained by the variation in several major ecological factors and life history traits such as mating systems, social competition in both sexes, intensity of parental care, extra pair paternity, latitude, predation, habitat, ambient light or diet (Badyaev and Hill 2003, Owens 2006). From comparative and theoretical studies, it can be globally predicted that species with biparental care where both sexes feed and incubate or where one sex incubates in a relatively safe place like a cavity, should be monochromatic (Owens 2006, Kraaijeveld et al. 2007). By contrast, sexual dichromatism can be predicted if only one sex feeds and incubates and if the evolution of cryptic colouration reduces predator detection in the sex that invests most in reproduction. Dichromatism could also be predicted if one sex invests more in territorial defence.
An intense sexual dichromatism is generally used as an indication of an intense sexual selection in males. However, more and more studies are showing that sexual or social selection may be acting equally in both sexes (Roulin et al. 2001, Lebas 2006, Clutton-Brock 2007, Kraaijeveld et al. 2007, Doutrelant et al. 2008, 2012, Rubenstein and Lovette 2009, Midamegbe et al. 2011). Hence, the absence of dichromatism should not preclude that these species bear intensively selected traits in both sexes. To test the potential signalling function of colouration in both sexes, an important step is to determine whether colouration honestly signals quality in males and females.
Condition-dependence is one of the main mechanisms supposed to insure that individuals reliably signal their quality or condition (Zahavi 1975, Grafen 1990, Iwasa and Pomiankowski 1994, 1999). Condition-dependence suggests that signals have to be costly so that only high- quality individuals in a population can present exaggerated sexual ornaments, armaments or displays and be viable afterwards (i.e. be fecund and survive). It assumes a positive link between the conspicuousness of the ornaments or armaments and indices of conditions such as body condition or immunocompetence. It also assumes that ornaments or armaments are constituted by costly elements.
In many species, colouration is due to pigments such as carotenoids or melanine and/or to structures (Hill and Mcgraw 2006 ). To date, most experimental studies have shown that colouration is condition-dependent because some structures are costly to elaborate, some pigments are costly to acquire or submitted to allocation tradeoff (Mcgraw et al. 2002, Faivre et al. 2003, Mcgraw and Ardia 2003, Hill et al. 2009, Doutrelant et al. 2012). Given that different colours may signal different aspects of quality, identifying the pigments of ornamental colours is important to determine the type of information contained in coloured traits (Mcgraw et al. 2002, 2005b). For instance, carotenoids are fat soluble pigments that are only acquired by food intake and are often considered as a limited resource (Olson and Owens 1998). They have antioxidant properties (Von Schantz et al. 1999, Svensson and Wong 2011; but see Hartley and Kennedy 2004, Costantini and Møller 2008, Olsson et al. 2008) and are also immunomodulators that regulate and stimulate the immune system (Lozano 1994, Olson and Owens 1998, Møller et al. 2000). As such, carotenoids are often assumed to be relevant indicators of individual health and foraging ability. Identifying the structure or pigments is especially informative when coloration is a dynamic trait that may therefore convey a continual update on individual condition. This is the case of bare part coloration (i.e. the coloration of beaks, legs for instance in birds) that have been shown by several experimental studies to vary within few weeks (Blount et al. 2003, Faivre et al. 2003, McGraw and Ardia 2003) to few days (Velando et al. 2006).
Seabirds stand a particularly interesting group regarding colour ornaments. Most species are black and white and appear monochromatic to humans, but they also often harbour colourful traits (including in bare parts) during the breeding season. Nevertheless, we know very little about the role of colouration in most seabird species (but see Jones and Hunter 1993, Massaro et al. 2003, Nolan et al. 2005, Torres and Velando 2005, Kristiansen et al. 2006).
In the current study, we worked on two seabird species that appear monochromatic to a human eye: the Atlantic puffin Fratercula artica and the black-legged kittiwake Rissa tridactyla. Our first aim was to determine whether these species were really monochromatic when bird vision was taken into account. We then identified the potential condition dependence of their colouration by examining whether their expression was linked to body condition and whether the yellow, orange, and red bare parts of both species contained carotenoids. For puffins, we also examined the potential size dimorphism in the gap rosette size.
To explore these questions, we quantified colouration using quantitative spectrometry and avian vision modelling (Endler and Mielke 2005, Gomez and Thery 2007). Birds have a different vision compared to humans, with sensitivity to ultraviolet (UV) radiation (Bennett and Cuthill 1994). Hence, it is crucial to accurately and objectively measure coloration – by using spectrometry – and to model avian vision to understand signals from their perspective, and the role of sexual selection in their evolution. For puffins and kittiwakes, we predicted a slight or an absence of sexual dichromatism. Indeed, both species present life history traits that should be linked to monochromatism (Owens 2006, Kraaijeveld et al. 2007). Both are long-lived monogamous species, with similar survival, nest care, incubation, and chick feeding (Creelman and Storey 1991, Coulson and Johnson 1993, Coulson 2011, Harris and Wanless 2011). In addition, both species present a null or very low level of extra pair paternity-EPP (between 0 and 8%: Helfenstein et al. 2004, Anker-Nilssen et al. 2008) and a moderate level of divorces (less than 7% in puffins and around 20% in kittiwakes: Coulson 1972, Hatch et al. 1993, Naves et al. 2006, Harris and Wanless 2011).
We estimated the potential condition-dependence of coloration by relating colouration to body condition. Puffins and kittiwakes present coloured bare parts and feathers. Given that bare part colouration represents a more dynamic signal of quality than feather colouration (feathers are formed only once or twice earlier in the season, bare part colouration may change in less than 15 d: Faivre et al. 2003), we expected body condition to be more closely associated with bare part colouration than feather colouration. A recent study investigated whether bill and gape colourations are linked to quality indices in a North Pacific population of kittiwakes (Leclaire et al. 2011) and found that their colouration was correlated to quality indices (reproductive success, heterozygosity, antioxydant levels). To our knowledge, no such study has ever been conducted on puffin colouration.
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- Material and methods
This study first investigated whether puffins and kittiwakes, apparently monochromatic to a human eye, were also monochromatic when bird visual range and sensitivity were taken into account. Using bird vision, we did not detect any sexual dichromatism for the two species. In puffins, however, gape rosette size was sexually dimorphic, being larger in males. We then investigated whether the colouration of both puffins and kittiwakes is correlated with individual condition and thus had the potential to be used as social or secondary sexual signals. In puffins, birds in better condition had more chromatic and redder bills (both males and females), as well as more chromatic and more orange gape rosettes (females only). In kittiwakes, both males and females had brighter and redder gapes when in better condition. Lastly, as far as our exploratory analysis provided generalizable results it seems that yellow, orange, and red bare parts contained carotenoids in both species. Taken together, these results suggest that in these two species, bare part colouration has a signalling potential and may be subjected to mutual social and/or sexual selection. This hypo thesis deserves to be experimentally tested in the future.
Although dichromatism has traditionally been estimated through human vision, recent studies raise some concerns about the relevance of such scoring. Birds and humans have a different vision. Humans have three colour cones while birds have four, this additional cone enabling them to perceive UV wavelengths to which humans are blind (reviewed by Bennett and Cuthill 1994). Moreover, birds have oil droplets that enhance colour discrimination (Vorobyev 2003). In agreement with theses doubts con cerning human capacity to correctly evaluate bird dichromatism, a reassessment of bird dichromatism in passerine revealed high level of dichromatism when bird vision is taken into account (Eaton 2005, Håstad and Ödeen 2008). Nevertheless, studies including non passerine birds concludes that human capacity to detect bird dichromatism is acceptable when birds do not present any UV-reflecting colouration (Armenta et al. 2008, Seddon et al. 2010).
In kittiwakes, none of our analyses detected a sexual difference in colouration. Our study thus confirmed the results of a recent study conducted on tegument colouration (bill, tongue and gape), during chick rearing period, in an Alaska population of black-legged kittiwakes (Leclaire et al. 2011). It also extended the absence of dichromatism to all colour traits (i.e. tegument and plumage colouration) and to the incubation period. Our study on black-legged kittiwakes is performed with a mix of genetic and morphological sexing. Because in this species morphological sexing is unambiguous for small and large individuals (Barret et al. 1985, Jodice et al. 2000, Coulson 2009), we think the conclusions we provided are reliable.
For puffins, both visual modelling and calculation based on spectral shape showed that bill, gape and cheeks were monochromatic. For the orange legs, classic brightness, chroma and hue descriptors suggested a sexual dichromatism while visual models suggested a monochromatism. Differences in results can be explained by the fact that differences between male and female spectra occur in the long wavelength range. Although endowed with a tetrachromatic vision, birds have a relatively poor visual performance at the edges of their sensitivity domain, as shown by vision experiments in chicks (Osorio et al. 1999). Hence, our results confirm that both puffins and kittiwakes are fully monochromatic when taking into account bird visual system, a result that would not be ascertained without spectrophotometry.
Integument colouration has been shown to undergo rapid changes when bird condition varies (e.g. 15 d in blackbirds Turdus merula: Faivre et al. 2003, and much more quickly – 48 h – for the feet of the blue-footed bobby Sula nebouxii: Velando et al. 2006). Our work has been conducted during incubation. We cannot exclude that the level of monomorphism in bare parts would have been different if measured earlier in the season, before laying for example. More data are thus needed to ensure that monomorphism in bare parts is maintained all year round.
In comparative analyses, monochromatism is often interpreted as a low level of sexual selection and the share of common ornaments in males and females is often assumed to be the result of a genetic correlation between male and female ornaments when ornaments are not too costly (Lande 1980, Kraaijeveld et al. 2007). However monochromatism might alternatively suggest that sexual or social selection is equally high in both sexes. For instance mutual inter and intra sexual selection has been suggested correlatively or demonstrated experimentally in other seabird species, like crested auklets Aethia cristatella (Jones and Hunter 1993), yellow-eyed penguins Megadyptes antipodes (Massaro et al. 2003), great back-backed gull Larus marinus (Kristiansen et al. 2006), blue-footed bobbies Sula nebouxii (Torres and Velando 2005) or king penguins Aptenodytes patagonicus (Nolan et al. 2010). For kittiwakes and puffins, the hypothesis of mutual sexual selection is suggested by our results showing a correlation between bare part colouration and body condition in both sexes.
In puffins, two results nonetheless also suggested a potential difference between males and females. First, we found that gape rosette size was sexually dimorphic, being about 20% larger in males. This may reflect a stronger sexual or social selection on this trait if ornament size signals male quality. Second, we found a stronger association between gape rosette colouration and body condition in females than in males. This condition dependence is particularly interesting and can be explained by the fact that under good conditions all individuals may be able to present large signals and that under harsher reproductive conditions, only the good quality individuals may be able to present developed such signals (Van Noordwik et al. 1986, Doutrelant et al. 2008, Morales et al. 2008, Midamegbe et al. 2013). When coloration was measured, reproductive conditions have been harsher for females than male because females had just finished investing in egg laying. Egg laying can be extremely costly for females (Visser and Lessells 2001, Hanssen et al. 2005, De Heij et al. 2006). In agreement, females presented a lower body condition than males at the time of measurements (condition respectively varied from −32 to 63 in males and −72 to 27 in females: Fig. 2). So, this might explain why we found a relationship in females, but not in males.
It is highly interesting that in puffins, female gape rosette colouration was linked to body condition. As suggested by correlative (Boulet et al. 2010, Huchard et al. 2010) and experimental studies (Roulin et al. 2000, 2001, Smiseth and Amundsen 2000, Siefferman and Hill 2005, Doutrelant et al. 2008), colouration of female ornaments can be highly informative for males. Female colouration could predict maternal investment in eggs, as shown in lesser black-backed gulls (Larus fuscus:Blount et al. 2002) or blue tits (Midamegbe et al. 2013). In lesser black-backed gulls for instance, females with duller carotenoid-based integument colouration (bill, eye ring, gape flange and legs) produce clutches which exhibit a strong decline in yolk carotenoid levels over the laying sequence (Blount et al. 2002). During incubation, carotenoid-based colouration can indicate to males female potential capacity to support laying costs (Visser and Lessells 2001, Hanssen et al. 2005, De Heij et al. 2006) and thus to further invest in chicks.
A last argument in favour of the hypothesis that bare part colour traits have the potential to be sexually or socially selected in the two species is that they seem at least partially constituted by carotenoids. Although we sampled one individual per species, we can reasonably assume that this individual is representative of its species and that if carotenoids are detected in one, they are present in the other individuals of the same species as well (even if different carotenoids may vary in proportion among sampled individuals). Carotenoids are interesting in the context of sexual selection for at least the two following reasons. 1) They cannot be synthesized de novo by animals; they must be acquired by food intake and they may reveal individual capacity to acquire food and assimilate the nutrients. 2) They are concurrently needed by the signalling, immune and detoxification systems (Lozano 1994, Olson and Owens 1998, Von Schantz et al. 1999, Møller et al. 2000, Blount et al. 2003, Faivre et al. 2003, Mcgraw and Ardia 2003) although arguments against the antioxidant function of carotenoids in adults can be found in other studies (Costantini 2008, Vinkler and Albrecht 2010). In addition, they are protected from oxidation by vitamins (e.g. C, E, A) and enzymes with antioxidant powers. Hence, carotenoid based colouration might signal the availability of other non-pigmentary antioxidant molecules that might protect carotenoids from free radical attacks (Hartley and Kennedy 2004, Bertrand et al. 2006, Navarro et al. 2010).
To conclude, our results show a full monochromatism in puffins and kittiwakes colouration and suggest that mutual sexual selection might act on both kittiwakes and puffins bare part colourations. Bare part colourations are linked to estimators of condition in both sexes and seem to be based on carotenoids. Further descriptive investigation is required on samples coming from several individuals to confirm the carotenoid basis of the bare part colorations we studied here. In addition, experimental studies are needed to test the function of these colourations and the respective role of intra and intersexual and social selection in the evolution of these signals.