Superciliums in white-eared hummingbirds as badges of status signaling dominance
The role of badges as indicators of contest ability has been previously described. In hummingbirds, the exhibition of a badge is expected to save energy expenditure in agonistic interactions and to favor energy intake. Here, we investigate whether variable supercilium size in the white-eared hummingbird has a role in dominance status signaling. Firstly, 45 hummingbird males were captured and their superciliums were photographed to investigate variation in size and any possible allometric relationships. Secondly, 42 male birds were used to analyze whether the supercilium has a role in dominance status signaling in a dyadic contest. We found that supercilium size varied continuously but that despite variability between individuals, there was no relationship between supercilium size and body size. However, our dyad experiment indicated that birds with larger badges were able to make more visits to the feeders than individuals with smaller badges. We suggest a status signaling function of the supercilium.
KeywordsDominance Hylocharis leucotis Recognizing dominance Signal reliability Status badge
The most common means of resource-holding in animals is territoriality, that is, the basic behavior of a resident individual aimed at defending and excluding others from a specific area (Brown and Orians 1970). Prior to a territorial dispute, contesting individuals are often able to evaluate each other through the use of signals that are reflections of their inherent ability in a contest (Smith and Harper 1995; Rat et al. 2015). The signals used for either a context of intra-sexual competition for sexual resources (e.g., mates) or social competition for food resources involve similar traits, such as conspicuous displays, weaponry, aggressive behaviors, and costly signals (Tobias et al. 2012). These types of signals have been found in many avian species and include auditory cues and visual signals associated with plumage—e.g., the size of ornaments and both pigmented or structural plumage coloration—which prevent birds from engaging in costly contests with predictable outcomes (Rohwer 1975; Smith and Harper 2003; Senar 2006; Pryke 2013).
The conspicuous coloration patches in the plumage of many birds that are made up of different pigments, termed by convention “badges,” often reflect different individual health and condition (e.g., carotenoids) but mostly reflect social status (e.g., melanin-based colors) (Rohwer 1975; Senar 2006; Santos et al. 2011; Young et al. 2015). The role of badges as indicators of contest ability has been analyzed, above all, in bird species from temperate areas of the world via the evaluation of territorial performance of individuals exhibiting a gradient in the size and/or intensity in their badges (i.e., Møller 1987; Senar et al. 1993; Rémy et al. 2010; Quesada et al. 2013; Mercadante and Hill 2014). These studies have shown that larger and brighter badges (less dark) indicate better competitive abilities.
Generally, the maintenance and development of these visual signals are energetically costly, which makes them reliable signals (Zahavi 1975; Husak et al. 2015). Ornament production and maintenance have associated drawbacks: they may increase the risk of predation (Endler 1978; Stuart-Fox et al. 2003; Pascual and Senar 2014), reduce immune-competence (Ressel and Schall 1989; Dunlap and Schall 1995; Salvador et al. 1996; Calisi et al. 2008), and have social costs in the event of aggressive contests that are both physiologically expensive and time-consuming (Tibbetts and Dale 2004). Therefore, the ability to exhibit this type of signal may be an honest indicator of an individual’s health and its physical capabilities in a contest (Hamilton and Zuk 1982; Folstad and Karter 1992), particularly if these traits are more exaggerated in larger-than-average individuals (hyperallometric). This is because, according to indicator traits (Gould 1974; Petrie 1988, 1992), only males in overall good conditions will be able to invest relatively more on these traits with respect to body size (Álvarez et al. 2013). Disentangling these various factors is a challenge for the current signaling theory underlying that the evolution and maintenance of these badges are still poorly understood.
White plumage ornaments, however, have often been assumed to be inexpensive because their production requires neither pigment nor specialized feather structure (McGlothlin et al. 2007). Proposed mechanisms for maintaining the honesty of unpigmented signals have usually focused on various costs of maintaining the trait, such as greater risk of feather abrasion and breakage, colonization of keratinolytic bacteria, reduced attractiveness, or its role of inducing male–male aggression (Fitzpatrick 1998; Kose and Møller 1999; Török et al. 2003; McGlothlin et al. 2005; Justyn et al. 2017). But some studies have shown trade-offs between life history traits such as brood size (Gustafsson et al. 1995) and diet quality (McGlothlin et al. 2007) in the expression of white plumage patterns, which suggest a role as honest signals of individual quality.
Hummingbirds (Trochilidae) are endemic to the Americas and are the second most diverse family of birds in this continent (approximately 350 taxa). These small birds inhabit all types of environments (Schuchmann 1999) and are known for their agility in flight, high metabolism, iridescent plumage, and both anatomical and physiological adaptations to a specialized diet of nectar (Stiles 1981). Hummingbirds have physiologically demanding flying abilities, which is fueled by the energy obtained from the flowers they visit, while also having evolved due to their feeding strategies (Wagner 1946; Wolf et al. 1976; Stiles 1995; Altshuler et al. 2004). As a result, competition (through territorial behavior) for feeding territories between certain hummingbird species is frequent and plays an important role in determining the structure of their communities (as opposed to the trapliner behavior displayed by non-territorial hummingbirds in which an individual visits food sources on a regular repeatable sequence involving an specific route) (Feinsinger and Colwell 1978; Montgomerie and Gass 1981; Hixon et al. 1983; Dearborn 1998; Camfield 2006).
Dominance (both intra and interspecific interactions) in hummingbirds has been found to be associated with the individual physical state, sexual dimorphism, body size, wing disc chord loading, species identity (e.g., some species dominate others at floral patches or feeders) and territorial quality (Kodric-Brown and Brown 1978; Carpenter et al. 1993; Ornelas et al. 2002; Stiles et al. 2005; Németh and Moore 2012). These characteristics have been postulated and tested in hummingbird species at particular moments of their biological cycles such as migration and reproduction (i.e., Gass 1979; Ewald 1985). It has also been suggested that variation in behavioral profile or “personalities” may affect the establishment of dominance relationships and risk sensitivity, where previous research has found hummingbirds to show a steroid-correlated boldness scale (Goloff and Burch 2012; Chávez-Zichinelli et al. 2014). However, despite that male hummingbirds employ their iridescent plumage (visual signals) in a variety of contexts, including nuptial displays, aggressive sexual displays, and aggressive displays associated with nectar-centered feeding territoriality (Stiles 1982), the possible role of structural coloration (iridescent or not) and badges during territorial intra- and interspecific disputes has only rarely been examined (but see Ewald and Rohwer 1980). This is somewhat surprising, above all, if we note that non-iridescent signals such as the postocular lines—often white in color (hereafter referred as superciliums)—are common in hummingbirds. For example, 56 out of the 70 hummingbird species that occur in Mexico and North and Central America (Howell and Webb 1995) have some type of white spot or patch on their heads (males, females, and juveniles).
The white-eared hummingbird (Hylocharis leucotis) earns its common name from its supercilium (this patch is not iridescent, so it can be observed at all angles, not specific ones). As opposed to the trapliner behavior displayed by females, the males of this species establish feeding territories that they aggressively defend against conspecifics and other heterospecific small-sized hummingbird species (Lara 2006). When passively (e.g., territorial calls) or actively (e.g., chases and physical contacts) defending a territory, the supercilium is always visible, so that this signal is obvious to any intruders during a territorial contest (hence, we focus here only in males). In this study, dominance is defined as success in intraspecific contests, a synonym for resource-holding potential, i.e., individuals with the higher resource-holding potential (RHP) win disputes (Parker 1974). Thus, resource-holding potential reliably reflects male quality. Hence, we hypothesized that the supercilium could play a role in signaling to intruders an individual’s resource-holding potential, where individuals with larger-sized superciliums will tend to monopolize the available resources, i.e., pay more frequent visits to a food source, to the detriment of individuals with smaller-sized superciliums. However, many supposed ornaments that could be related to dominance may actually signal other qualities such as age or size (see Senar 2006 for a discussion), aspects that require consideration in signaling studies. The goals of our study were thus (1) to assess supercilium size variation in males captured in natural conditions and analyze its possible relationship with body size (allometry). This first approach allowed us to rule out possible allometric effects on supercilium size. Subsequently, (2) we used a manipulative approach to experimentally evaluate the role of supercilium size as a badge of status signaling dominance.
Study site and species
From February 2013 to March 2015, white-eared hummingbirds (Hylocharis leucotis) were studied in La Malinche National Park (LMNP), Tlaxcala, Mexico (19°14′N, 98°58′W, 3000 m a.s.l.). Ethical approval was received from the relevant local authorities (SEMARNAT, license number FAUT-0296). The vegetation in the study area consists mainly of a mosaic of pine forest and second-growth vegetation (Villers et al. 2006). These small hummingbirds (ca 3.1–3.4 g) are residents in LMNP, and both sexes feed throughout the year on a wide range of hummingbird-pollinated plants (Lara 2006). Males are highly territorial and are frequently observed defending clumps of flowers on firecracker bushes Bouvardia ternifolia (Rubiaceae), beardtongues Penstemon roseus (Lamiaceae), and pineapple sages Salvia elegans (Lamiaceae). Both sexes have a distinctive white line above and behind the eye (supercilium), and their pigmented underparts are whitish, heavily speckled with green, but males have a bluish violet iridescent forecrown and chin, and a glittering green throat (absents in females).
Natural variation in supercilium size
To evaluate variation in supercilium size in males, 45 hummingbirds were captured with mist nets in different areas of the LMNP, but most in areas where patches of flowering firecracker bushes, beardtongues, and pineapple sages abounded. We took the following measurements from each captured individual: (1) total length (mm), (2) bill length (mm), (3) tail length (mm), (4) wing chord (mm), and (5) weight (g; sensu Pyle 1997). Body measurements were taken using a digital caliper (Mitutoyo SC-6, ± 0.2 mm error) and a digital scale (US-SONIC-500, 0.1 g resolution).
After measurements, the superciliums (on the right and left sides of head) of each individual were laterally photographed twice with a digital camera (Sony Alpha SH0006) from a constant position and distance. The number of pixels per square millimeter (area) and 1 mm (linear) was calculated using a ruler to get the scale for each photograph using Adobe Photoshop CS6. This methodology is commonly used in studies of plumage color (Muck and Goymann 2011). The photographed birds were marked by clipping the fifth rectrice (to avoid pseudoreplication) and were then released back to sites from which they were captured. Time from capture to release for each bird was approximately 20 min.
We assessed the repeatability of supercilium area by comparing the size estimated from photographs 1 and 2 of only the left-side supercilium of each captured individual. These two samples turned out to be highly repeatable for the same individual (adjusted repeatability 0.92; confidence interval, CI 0.87—0.93, P < 0.0001; following Nakagawa and Schielzeth 2010).
In order to assess whether variation in supercilium size in males is allometrically determined, we performed major axis regressions between supercilium size and body measurements (MA regression; Sokal and Rohlf 2012). MA regressions were performed using the “smatr” package in R (Warton et al. 2012), which calculates allometric slopes between two continuous variables, as well as their 95% confidence intervals (CIs; upper CI-lower CI). A slope was considered to be significantly different from 1 if the confidence intervals excluded β = 1, and the associated P value was ≤ 0.05 (Álvarez et al. 2013).
Experiment: supercilium as a badge of status signaling dominance
After discarding potential allometric relationships between supercilium size and body measurements (see the “Results” section), we evaluated whether this badge has a role in signaling dominance status. Dominant individuals usually prevail over others and take a disproportionate share of available resources (Barnard 1984). Thus, here, we considered an individual to be dominant if it made a greater number of visits to a feeder during an experimental trial (Tiebout 1996). A total of 42 adult hummingbird males were captured in the field using mist nets (different individuals to those used for measuring badges). After capture, the males were measured following the protocol described above (including supercilium size). The birds were housed individually for 24 h in collapsible field cages (dimensions 1.5 × 2.0 × 1.5 m), which contained a perch and a feeder with 120 ml of 20% (by mass) sucrose solution. During this period, feeding by the birds was taken as evidence that they were acclimatized to the enclosure. Individuals that did not feed during the first hour of confinement were released and not used for experimental procedures. Prior to the trials, individuals were not fed for 20 min so that by the time of the experiment, they were presumably hungry.
An experimental trial consisted of placing two captured individuals for 60 min in a collapsible field cage with the characteristics described above, the only difference being the existence of two perches. During this period, a videocamera (Panasonic Camcorder model SDR-H4OP) recorded for both hummingbirds the latency of feeder visits, the number and duration of visits, and the number of agonistic displays (physical contact between the two birds). The great individual variation in the shape and size of the supercilium allowed us to distinguish the individuals used in each dyad and to be able to collect their data. We predicted that the greater the differences between contestants’ supercilium sizes, the more differences there would be in the magnitude of the evaluated variables. Based on variation across individuals, half of the male dyads (n = 11) had a specific supercilium-size difference ranging from 0 to 0.04 cm2 (similar contenders) and the remaining half from 0.05 to 0.17 cm2 (different contenders). Thus, the contests were classified into two types in terms of the differences in supercilium size between the contenders (contest type). For analyses, we use patch size differences (that vary continuously) among contenders. All subjects (N = 42) were used only once in the experiment and were subsequently released as per the protocol described above.
To assess the contribution of differences in supercilium size between contenders to the intensity of feeder use during the experimental trials, two statistical approaches were used. In the first approach, four separate regressions test each of the behavioral measures (dependent variables: differences in latency of visits, number of visits, duration of visits, and number of disputes between contenders) against difference in badge size (independent variable) and considering the contest type (contestants with similar or different badge size).
In the second approach, we used the R package “lme4” (Bates et al. 2014) to build five candidate generalized linear mixed-effects models (GLMMs), to be compared using an information theoretic approach (Burnham and Anderson 2002). All continuous variables were log10-transformed prior to analyses. Each candidate model included supercilium size differences among contenders as independent variable (predictor) and foraging and agonistic variables and contest type as dependent variables (response variables). Contest identity was included in the models as a random effect due to variation shown in supercilium size in each dyad. For each model, an Akaike weight (Akaike 1981) was calculated, which indicates its level of support (since Akaike weights sum to 1, models with Akaike weights approaching 1 receive the most support relative to other models). By summing Akaike weights of all models containing a particular variable, a measure of the relative “evidence of importance” for that predictor variable is produced (Burnham and Anderson 2002). However, this value of predictor importance does not indicate the magnitude or direction of the relationship between predictor and response variables. To provide such an understanding, we subsequently used model averaging to calculate the average parameter estimates based on all GLMM models in which the parameter appeared, weighted by their Akaike weights. The BMS package was used to calculate the posterior inclusion probability (PIP) and standardized posterior mean coefficient (PMC) for all dependent variables. The prior probability for the model was set using the default, which uses the median of the number of available parameters and draws from a normal distribution (of the number of possible parameters).
All statistical analyses were performed using the software R (R Development Core Team 2014).
Allometry of supercilium size
Slopes, 95% confidence intervals (CIs), R2, and P values obtained from MA regressions fitted between supercilium size (dependent variable) and six body-size measurements of white-eared hummingbird males
Lower CI, Upper CI
Supercilium size and dominance status signaling
Results from Bayesian model averaging analyses for parameters affected by the supercilium size difference among contenders
Number of visits
Duration of visits
Latency of visits
Number of disputes
Typically, the evolution of sexual traits and, in particular, their hyperallometric patterns, has been explained by sexual selection given the supposed advantages that they confer in mate selection or access to reproductive mates (Gould 1974; Petrie 1992; Kodric-Brown et al. 2006). However, the theory of social competence (Lyon and Montgomerie 2012) states that competition for limited resources—rather than for mates—may also promote the use of such elaborate traits. Our study demonstrated the lack of hyperallometry in supercilium size in white-eared hummingbird males. These results, along with the demonstration that differences in badge size between contestants affect the level of intraspecific dominance at a food source (feeder), suggest that superciliums may be used as a status signal in a context of social competence.
The promiscuous reproductive system of hummingbirds (Stiles and Wolf 1979) seems to favor the use of multiple signals to females (Candolin 2003; Chaine et al. 2013). For example, these signals can serve as multiple messages that either indicate general mate quality or enable females that differ in mate preferences to choose the most suitable male (i.e., the iridescent plumage on cheeks and throat). Likewise, the function of these features as status signals of social communication, particularly in a intraspecific territorial context, has been previously demonstrated for both sexes in a number of different species (Wolf 1969; Ingles 1976; Stiles 1982; Bleiweiss 1985). However, to our knowledge, this is the first documented study of the use of non-iridescent plumage for status signaling in hummingbirds. More than 50 species of hummingbirds in Mexico and North and Central America exhibit superciliums (Howell and Webb 1995) and appear in both males and females in approximately 25% of these species. The practice of territorial defense in both sexes in several hummingbird species has been used as an evolutionary explanation for the iridescent coloration in monomorphic species (Wolf and Stiles 1970); thus, it is possible that this selective pressure may also be acting on non-iridescent structural colorations such as the supercilium.
The white-eared hummingbird males evaluated in our study showed an important variation in supercilium size (from 15 to 35 mm2), which was independent of body size. The adaptive significance of intraspecific variation in plumage characters has received much attention, and a large number of hypotheses have been advanced to explain the variation (e.g., Butcher and Rohwer 1989; Lank 2002; Fowlie and Krüger 2003). Here, we suggest that superciliums serve as badges and can be signals of intraspecific dominance when males are foraging. But, our data could not determine whether supercilium size changes with age (this would require a longitudinal study). However, given the lack of hyperallometry, it is possible that supercilium (badge) size may be related to individual quality characters for dominance status signaling such as body size (important in interspecific contests for nectar sources, e.g., Justino et al. 2012), body condition, and many other physiological factors. This relationship has been established in other birds such as the American yellow warbler Setophaga petechia (Studd and Robertson 1985), the house sparrow Passer domesticus (Møller 1987), and the Eurasian siskin Carduelis spinus (Senar et al. 1993). Here, we show that birds with larger badges were usually more dominant over the food resource than individuals with smaller badges (individuals with larger superciliums were more likely to visit the feeders), suggesting that white plumage patch exhibited in male white-eared hummingbirds may act as a badge of intraspecific dominance status. The small size and high metabolic rate of hummingbirds prevent them from surviving for long if energy expenditure exceeds income (Kodric-Brown and Brown 1978). Because physical conflict over limited resources (as occur in hummingbirds) can be costly in terms of both time and health (Chaine et al. 2013), the exhibition of a badge (i.e., supercilium) can save energy expenditure associated with competitive interactions and favor energy intake (individuals with larger badges are expected to have a better resource-holding potential); such savings can be highly beneficial in a species with such high metabolism.
Not all signals are honest (e.g., lures, sensory exploits, sensory traps) but when they are, this honesty is maintained by the cost of the signal (Zahavi 1975). Nutrients required to maintain the plumage pigment colors are different. For example, carotenoids are scarce in the environment and exclusively obtained from diet (Goodwin 1984), but melanins are synthesized from amino acids that are basic dietary components and usually not a limiting resource (Griffith et al. 2006). In this regard, the presence of white color patches on melanized body structures could be of particular importance because their size and brightness seem to be affected by rearing conditions, parasite infections, and diet quality (Kose and Møller 1999; Gustafsson et al. 1995; McGlothlin et al. 2007). Hummingbirds do not have different breeding and non-breeding plumages and molt only once per year. Because this process is stressful, birds usually molt during periods when there are neither breeding nor migrating (Williamson 2001). Likewise, parasite infection is common in hummingbirds not only in plumage but rather with gastrointestinal and blood presence and so far little known effects (Matta et al. 2014). Therefore, it is expected that if despite the extra cost involved in molting and parasites the size of a badge (i.e., supercilium) is maintained over time, then the honesty of the signal is reaffirmed, but studies are needed to prove it.
The most common type of agonistic interaction in territorial species occurs when an animal displaces an opponent and forces it to move away (i.e., Paton and Caryl 1986). However, due to the inherent costs of disputes, contestants can use their opponent’s traits or features to avoid fights and aggressive interaction (Smith and Harper 2003). A number of studies have demonstrated that this occurs in several bird species, mainly because sex and age are usually associated with different plumage colorations (the dominant birds typically have darker or blacker patches), and birds learn to associate coloration with the degree of dominance of a given individual (Krebs and Davies 1987; Whitfield 1987). Plumage thus becomes, indirectly, a status signal (i.e., Senar et al. 1993; Smith and Harper 2003; Quesada et al. 2013). Our study revealed that individuals with larger superciliums showed an increased resource-holding ability (number of visits to the feeder) compared to intraspecific contestants with small badges. These results suggest that individuals are able to assess the difference in status of an opponent on the basis of their relative supercilium sizes; thus, plumage will determine the outcome of any encounter (Whitfield 1987).
It has been suggested that status signals should be selected above all in species with unstable group composition or in species where contests are usually between individuals with no previous social contact, as in these cases, the cost of status assessment would be lessened whenever two individuals confront each other (Rohwer 1982; Senar et al. 1990; Vedder et al. 2010). For example, high-quality sites are often visited by many conspecific and heterospecific hummingbird species so that familiarity between individuals may be low and hence the exhibition of reliable badges beneficial. In this respect, the males of most northern temperate hummingbird species (and several tropical species) defend their territories by sitting on exposed perches in the open, thereby providing visual signals to scare away potential intruders (Skutch 1940; Pitelka 1942).
Given that our data show that supercilium size was not related to body size, it is possible that other factors may explain why individuals with larger badges forage more in captivity. For example, Chávez-Zichinelli et al. (2014) showed that testosterone (T) levels seem to influence foraging preferences in male white-eared hummingbirds and that individuals with higher levels of T make quicker and more frequent visits to flowers with variable rewards—and behave consistently as risk-prone foragers—than males with low T levels. These findings suggest that behavioral profiles or personalities of the birds used in the dyadic contest could influence our results. In this context, we predicted that individuals with larger badges should show higher levels of steroids and have higher levels of boldness and intraspecific dominance. Such a study could help us to understand the possible relationship between steroid hormones, badge size, and the signaling of dominance status in hummingbirds, a topic heretofore unexplored.
In short, we showed that white-eared hummingbird males with larger superciliums had enhanced access to the food resource than males with smaller superciliums: more visits to a feeder than their adversaries suggests a role for superciliums in dominance status signaling. Further future studies might seek to apply experimental manipulation, either artificially modifying the size or presence of this trait in individuals within a dyadic contest, to verify the status signaling function of supercilium.
We would like to thank M. J. Pérez-Crespo and V. Mendiola for their assistance in the field and their logistical support. To Mike Lockwood for the revision of the manuscript in English. Pietro K. Maruyama and three anonymous reviewers provided useful comments on previous versions of the manuscript. Permission to conduct our fieldwork was granted by the Mexican government (SEMARNAT, FAUT-0296). This work constitutes partial fulfillment of JMG’s doctorate at the Universidad Autónoma de Tlaxcala.
The Consejo Nacional de Ciencia y Tecnología (CONACYT: 365006/248109) provided the first author with financial support in the form of a scholarship. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Compliance with ethical standards
Conflict of interest
The authors declare that they have no competing interests.
All experiments comply with the current Mexican laws.
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