Overviews
My results reveal cryptic sexual dichromatism in both carotenoid-based and melanin-based traits that cannot be detected by the human visual system. The subsequent molting experiments demonstrated that the bill coloration of a bird was highly correlated with its physical conditions:
redder bills had higher immunocompetence and incurred lower levels of oxidative stress. A significant correlation was observed between a bird’s melanin-based plumage and oxidative stress levels, indicating that the black plumage may be a cue about the physical condition of a bird.
However, the insignificant female preference for redder males rejected the hypothesis that the bill coloration served as a sexually selected trait.
Although I did not discover the functions of both carotenoid-based and melanin-based traits in the Himalayan black bulbul, according to the communication theory, I suggest that both trait types can play a role in focal species communication.
From the summary of my results (Table 6.1), I found that not all sexually dichromatic characteristics, such as the tarsi, remige and tail, can reflect an individual bird’s immunocompetence or oxidative stress level. This may be because I examined only the “quality” of an individual bird in a limited number of aspects. Several types of the quality have been reported to be correlated with the coloration, including parental caring, nesting
sites or territory quality and social ranking or good genes (Dale 2006). In the current study, the sexually dichromatic parts that did not reflect individual bird’s physical conditions may serve as indicators of other dimensions of the quality to the birds.
My results suggest the role of carotenoid-based bared parts (such as the bill, eye rings, leg or wattle) in avian species. In contrast to feathers, the color of bared parts may change rapidly and may therefore reflect the short-term physical conditions of the bearer (e.g., Faivre et al. 2003b, Pérez-Rodríguez and Viñuela 2008, Rosenthal et al. 2012). Compared with studies on the plumage of birds, studies exploring the links between birds’ physical conditions and coloration of carotenoid-based bared parts are relatively scant. To my knowledge, the roles of the carotenoid-based bill have been studied in only four avian species: European blackbirds (Turdus merula, Faivre et al. 2003a, Faivre et al. 2003b), red-legged partridges (Alectoris rufa, Pérez-Rodríguez and Viñuela 2008), zebra finches (Taeniopygia guttata, Blount et al. 2003), and mallard ducks (Anas platyrhynchos, Peters et al. 2004). In these species, the bill coloration has been determined to be positively correlated with immunocompetence (Faivre et al. 2003b, Jawor and Breitwisch 2003, Mougeot et al. 2009, Peters et al. 2004). However, no study has examined the correlation between bill coloration and oxidative stress. My works provide another case that bill coloration was positively correlated with a bird‘s immunocompetence and negatively correlated with its oxidative stress level. Regarding the functions of the carotenoid-based bill, my results are not conclusive. The carotenoid-based bared parts are the sexually selected traits in the mentioned species. Nevertheless, a recent
comparative study revealed that carotenoid-based bill is highly common in species living in social groups during the nonbreeding season, and in species nesting in colonies; it is not related to either sexual dichromatism or sexual size dimorphism (Dey et al. 2015). The carotenoid-based bill was suggested to primarily evolve as a social signal. Although my results do not provide the function of the carotenoid-based bared parts, they indicated that the red bared parts alone may not be cues for female preference in Himalayan black bulbuls. Himalayan black bulbuls are socially monogamous, but they live in groups during non-breeding seasons; therefore, my results support the hypothesis proposed by Dey et al. (2015).
The concept of sexual selection being the major force producing conspicuous coloration in birds has been subjected to debate recently.
Dunn et al. (2015) suggested that natural selection is also attributable to evolution of diverse colorations. Because species with less sexually dichromatic traits may be under lower pressures of sexual selection (Andersson 1994), studying the functions of different pigmentations on less sexually dichromatic species can facilitate understanding the mechanism behind evolution of coloration in birds. To my knowledge, such studies have been conducted on only three less sexually dichromatic species: the great tits (Parus major), the blue tits (Parus caeruleus) (Delhey and Peters 2008), and the king penguins (Aptenodytes
patagonicus, Jouventin et al. 2005). Similar to Himalayan black bulbuls, all these species are sexually monomorphic in human visions but sexually dichromatic in avian visions (Delhey and Peters 2008). In all three
species, carotenoid-based ornaments serve as only quality signals
(reviewed in Delhey and Peters 2008, Viera et al. 2008), but not sexually selected traits. In great tits, the sexually selected trait is the area of melanin-based plumage on the breast (Delhey and Peters 2008, Norris 1990); whereas in blue tits, it is the UV plumage on the head (Delhey and Peters 2008, Hunt et al. 1999) as for the mutual sexually selected trait.
Moreover, in king penguins, it is the UV coloration in the colorful bill as for the mutual selected traits (Nolan et al. 2010). My results are similar to those of aforementioned studies mentioned: carotenoid-based ornaments are quality cues but might not solely serve as sexually selected traits.
However, so far I do not have further evidence revealing the mechanism associated with that causes the different functions of carotenoid-based ornaments in less sexual dichromatic avian species.
My results indicate that several carotenoid-based and melanin-based parts were sexually dichromatic or informative. This suggests that
multiple ornaments as sexually selected traits in Himalayan black bulbuls.
Studies have revealed that females might choose a mate according to multiple sexual ornaments (Chaine and Lyon 2008, Doucet and Montgomerie 2003). The benefit of multiple sexual ornaments is that these traits provide females with different types of information at various stages of the mate choice process (Borgia 1995) or function as redundant signals to improve the accuracy of mate assessment (Johnstone 1994, Moller and Pomiankowski 1993). Furthermore, females can use diverse characteristics in different breeding seasons as the current environmental conditions vary (Chaine and Lyon 2008, Qvarnström et al. 2000). Like in Northern cardinals (Cardinalis cardinalis), females use several
carotenoid-based parts and the size of melanin-based masks
simultaneously to choose their mates (Jawor and Breitwisch 2004, Jawor et al. 2003).
Future perspectives Social signal testing
In my dissertation, I did not test whether carotenoid-based or melanin-based traits function as indicators of the social status of an individual or contain information about individual qualities that can be useful in their social interactions, such as hierarchy or aggressiveness.
Studies have suggested that both types of traits are functional in social interaction in several avian species (Jawor and Breitwisch 2003, Roulin et al. 2008). Because Himalayan black bulbuls live in groups during
nonbreeding seasons and exhibit strong aggressiveness when in captivity with other individuals (personal observation), it is imperative for this species to develop social signals reflecting their physical conditions and fighting ability to reduce conflicts in social interactions. Therefore, I suggest that future studies could examine the correlation between color variations and social ranking (or fighting ability) of both trait types in black bulbuls.
Testing the possibility of other signal traits
In addition to carotenoid-based and melanin-based colorations, other traits can signal an individual’s quality or be used for mate choice, such as song (Shutler and Weatherhead 1990) and UV coloration (Prum 2006).
I observed UV light reflection from the bill and tarsi in Himalayan black
bulbuls. This can also serve as a target for signaling in black bulbuls.
Apart of UV light, bird songs have also been proved to be quality signals in other species (e.g., Gil and Gahr 2002). The songs of
Himalayan black bulbul are simple and can be performed by both sexes (personal observation) in an acoustic range (from20Hz to 20KHz, Pytte et al. 2004); however, such songs have not been analyzed systematically before. Nevertheless, Himalayan black bulbuls have been reported to sing ultrasonic sound (singing range >20KHz, Li et al. 2011). Several avian species were reported to sing in the ultrasonic sound range, which was determined to be indicator of individual quality in amphibians (e.g., Arch et al. 2008). Testing whether the songs both in acoustic and ultrasonic ranges could be vital functions in the focal species is imperative.
References
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Table 6.1 The summary of my results
Item Sexual
dichromatism
Quality cues
Sexual selected cues
(by females) Carotenoid-based
traits
Bill x
Tarsus x x
Melanin-based traits
Back x x Belly x x Breast x
Forehead x x
Nape x x
Remige x x
Scapula x
Tail x
“ ” indicates “yes” to the question.
“x” indicated “no” to the question
Table S2.1 Two-way ANOVA of different melanin-based parts in skin specimens
Parts Variables Total brightness Chromauv
F p F p df: year-2, sex-1, sex*year-2
Year: indicating the years after making into skin specimens, including within 5yrs, 10yrs and 15yrs.
Bold type indicates statistic significant (Bonferroin adjusted p = 0.005).
Table S2.2 Two-way ANOVA of different melanin-based parts between live birds and skin specimens
Parts Total brightness Chromauv
Variables F p F p Item: live bird and specimen, df= 1
Sex: female and male, df= 1 Item*sex: df=2.
Bold type indicates statistic significant (Bonferroin adjusted p = 0.005).
Table S 4.1 Multiple regressions of female preference and male morphometrics.
Term Estimate Std Error t p Intercept -2219.97 1352.23 -1.64 0.13
Bill 425.68 479.23 0.89 0.39
Head -50.79 301.64 -0.17 0.87
Tarsus 418.40 453.18 0.92 0.38
Wing 30.12 18.58 1.62 0.13
Weight 7.82 7.14 1.09 0.30
Female preference : (the amount of time a female spent on the perch in front of the male* 100) / (total choice time)
Table S 5.1 Multiple regressions of female preference and male morphometrics.
Term Estimate Std Error t p Intercept -2219.97 1352.23 -1.64 0.13
Bill 425.68 479.23 0.89 0.39
Head -50.79 301.64 -0.17 0.87
Tarsus 418.40 453.18 0.92 0.38
Wing 30.12 18.58 1.62 0.13
Weight 7.82 7.14 1.09 0.30
Female preference: (the amount of time a female spent on the perch in front of the male* 100) / (total choice time)