Mutual Mate Choice for Colorful Traits in King Penguins

While studies of mate choice based on male color pattern are ubiquitous, studies of mate choice based on ornamental color traits in sexually monomorphic species are less common. We conducted manipulative field experiments on two color ornaments of king penguins (Aptenodytes patagonicus), the size of auricular patches of orange feathers and degree of UV reflectance from beak spots, to determine how the degree of ornamentation influenced pairing rate. In a reduction of auricular patch size, females paired significantly more quickly than males in both control and experimental samples. When this bias was taken into account statistically, pairing of individuals with reduced auricular patches was significantly delayed. We also reduced, but did not eliminate, UV reflectance from beak spots by applying a UV filter; no sex difference in pairing rate was evident in this experiment. Treated birds paired significantly more slowly than untreated control individuals, taking more than a week longer to pair on average than their unmanipulated counterparts, a result that was significant for males and approached significance for females. Our results may indicate mutual mate choice via UV reflectance of the beak spot. Given that this is a species where breeding is extremely slow and considerable investment by both males and females is required for successful reproduction, our results support the hypothesis that in such species, sexual selection might act on the same ornament in both sexes.     

Mutually honest? Physiological ‘qualities’ signalled by colour ornaments in monomorphic king penguins

Mate choice is expected to be important for the fitness of both sexes for species in which successful reproduction relies strongly on shared and substantial parental investment by males and females. Reciprocal selection may then favour the evolution of morphological signals providing mutual information on the condition/quality of tentative partners. However, because males and females often have differing physiological constraints, it is unclear which proximate physiological pathways guarantee the honesty of male and female signals in similarly ornamented species. We used the monomorphic king penguin (Aptenodytes patagonicus) as a model to investigate the physiological qualities signalled by colour and morphological ornaments known to be under sexual selection (coloration of the beak spots and size of auricular feather patches). In both sexes of this slow‐breeding seabird, we investigated the links between ornaments and multiple indices of individual quality; including body condition, immunity, stress and energy status. In both sexes, individual innate immunity, resting metabolic rate, and the ability to mount a stress response in answer to an acute disturbance (capture) were similarly signalled by various aspects of beak coloration or auricular patch size. However, we also reveal interesting and contrasting relationships between males and females in how ornaments may signal individual quality. Body condition and oxidative stress status were signalled by beak coloration, although in opposite directions for the sexes. Over an exhaustive set of physiological variables, several suggestive patterns indicated the conveyance of honest information about mate quality in this monomorphic species. However, sex‐specific patterns suggested that monomorphic ornaments may signal different information concerning body mass and oxidative balance of males and females, at least in king penguins.     

Establishment of the fatty acid profile of the brain of the king penguin (Aptenodytes patagonicus) at hatch: effects of a yolk that is naturally rich in n-3 polyunsaturates

Because the yolk lipids of the king penguin (Aptenodytes patagonicus) contain the highest concentrations of long-chain n-3 polyunsaturated fatty acids yet reported for an avian species, the consequences for the establishment of the brain's fatty acid profile in the embryo were investigated. To place the results in context, the fatty acid compositions of yolk lipid and brain phospholipid of the king penguin were compared with those from three other species of free-living birds. The proportions of docosahexaenoic acid (22:6n-3; DHA) in the total lipid of the initial yolks for the Canada goose (Branta canadensis), mallard (Anas platyrhynchos), moorhen (Gallinula chloropus), and king penguin were (% w/w of fatty acids) 1.0+/-0.1, 1.9+/-0.2, 3.3+/-0.1, and 5.9+/-0.2, respectively. The respective concentrations of DHA (% w/w of phospholipid fatty acids) in brains of the newly hatched chicks of these same species were 18.5+/-0.2, 19.6+/-0.7, 16.9+/-0.4, and 17.6+/-0.1. Thus, the natural interspecies diversity in yolk fatty acid profiles does not necessarily produce major differences in the DHA content of the developing brain. Only about 1% of the amount of DHA initially present in the yolk was recovered in the brain of the penguin at hatch. There was no preferential uptake of DHA from the yolk during development of the king penguin.     

A method to assess population changes in king penguins: the use of a Geographical Information System to estimate area-population relationships

During the last decades, king penguin (Aptenodytes patagonicus) populations have been reported to increase throughout most of their breeding range. In this study, we compared the results obtained from direct counts of incubating king penguins with the results yielded by the estimation of the change in area occupied by breeding birds at the Ratmanoff king penguin colony at the Kerguelen Islands. The area of the colony was determined using a Geographical Information System with a georeferencing extension on aerial pictures taken in 1963, 1985 and 1998. Individual king penguin were counted on the same pictures or pictures taken on the same day. The overall population increase between 1963 and 1998 was 733% while the colony area increased by 677%. This study indicates that monitoring change in colony size is a good indicator for detecting and monitoring large population changes in king penguins, in particular for remote colonies. The discrepancy between the two results may be from two different kinds of bias. Firstly, there could be a possible error in the estimation of the area occupied by the colony resulting from the georeferencing of oblique pictures, and secondly, the density of king penguins may also change with population number. This method, which only requires high-altitude pictures, also reduces the possible disturbance to breeding made by low- to medium-altitude flights. Accepted: 7 February 2000     

Isolation and characterization of macaroni penguin (Eudyptes chrysolophus) microsatellite loci and their utility in other penguin species (Spheniscidae, AVES)

We report the characterization of 25 microsatellite loci isolated from the macaroni penguin (Eudyptes chrysolophus). Thirteen loci were arranged into four multiplex sets for future genetic studies of macaroni penguin populations. All 25 loci were tested separately in each of four other penguin species [Adélie penguin (Pygoscelis adeliae), chinstrap penguin (Pygoscelis antarctica), gentoo penguin (Pygoscelis papua) and king penguin (Aptenodytes patagonicus)]. Between eight and 12 loci were polymorphic per species. These loci are expected to be useful for studies of population genetic structure in a range of penguin species.     

Comparison of Color and Body Condition Between Early and Late Breeding King Penguins

Early breeding is associated with greater reproductive success in many species. In king penguins, Aptenodytes patagonicus , laying extends for 6 mo. Early breeders may fledge a single chick at best, but late breeders virtually never fledge a chick. For early and late breeders, we compared colored ornaments known to be important in mate choice: yellow–orange feathers of the breast and auricular areas, and an ultraviolet and yellow–orange beak spot. Our purpose was to discern differences between males and females in this highly sexually monomorphic species, as well as to discern whether colored ornaments are more important for the more successful early breeders (aspects of color were hue, chroma, and brightness). For this, we weighed and measured 130 penguins. Early males had greater reflectance of ultraviolet color from the beak spot than did early females and late breeders of both sexes, and the early males were heavier and in better condition than late breeding males or females. Late breeding females were the yellowest in breast hue, a trait that has been linked to immunocompetence. Within pairs, males and females were significantly correlated in body mass, but only early in the breeding season. We concluded that early in the breeding season when reproductive success was greatest, potential mates were not only more similar in body mass, but also that females may have chosen males that had brighter beak spots and were in better body condition.     

Mate Choice and Colored Beak Spots of King Penguins

The theory of sexual selection explains sexual dimorphisms in ornaments used in mate choice. Mutual mate choice is a form of sexual selection that might explain sexually monomorphic ornamental traits. Under mutual mate choice, both sexes select partners based on the same ornament. We tested the mutual mate choice hypothesis in a mutually ornamented seabird, the king penguin (Aptenodytes patagonicus), through observations of the pair formation process in the field. Penguins that were ready to mate formed displaying pairs at the edge of the colony. Some of these pairs moved into the breeding colony and produced an egg (definitive pairs), while other pairs separated and often switched to another potential partner (temporary pairs). Colored ornaments were quantified using color vision modeling. We predicted that birds would mate assortatively by their elaborate ornamental traits (specifically, colors of beak spots, auricular patches of feathers, and breast patch of feathers). We also predicted that definitive pairs would exhibit more elaborate ornaments than temporary pairs. The mutual mate choice hypothesis was supported by assortative pairing for color of the beak spots, but not for color or size of the auricular patches or for the color of the breast patch. An alternative hypothesis was also consistent with our results, that female choice for a male ornamental trait and superior female condition associated with the same trait produced assortative pairing patterns. More UV‐ and yellow‐colored beak spots for females in definitive than temporary pairs supported the female choice hypothesis over the mutual mate choice hypothesis, but previous experimental results from altered beak spot colors supported the latter. Evidence to date thus supports both the mutual mate choice and female choice hypotheses.     

How do king penguins (Aptenodytes patagonicus apply the mathematical theory of information to communicate in windy conditions?

In the king penguin (Aptenodytes patagonicus), both pair members alternate in incubating and rearing their chick. Mates can recognize each other among thousands of other birds in the hubbub of the colony using only acoustic signalling: the display call. Large penguin colonies are found on sub-Antarctic islands where strong winds blow throughout the year. We have shown by experiments under natural conditions that the level of background noise increases in windy conditions and thus leads to a diminution of the signal-to-noise ratio. Moreover the emergence level of the signal revealed by entropy calculation is statistically weaker in windy conditions. To achieve breeding success, birds must continue communicating in spite of the significant decrease in the total amount of information that can be transmitted in windy situations. For the first time, to our knowledge, we have shown that a bird species takes into account the constraints imposed by wind on their acoustic communication. In windy conditions, birds try to maintain the efficiency of communication by increasing both the number of calls emitted and the number of syllables per call. This result conforms with predictions from the mathematical theory of communication: increased redundancy in a signal improves the probability of receiving a message in a noisy channel.     

A history of shifting fortunes for African penguins

Africa is home today to only a single breeding species of penguin, Spheniscus demersus (black‐footed penguin), which is endangered with extinction. Spheniscus demersus has been the only breeding species of penguin to share African coastlines with humans over the last 400 000 years. Interestingly, African penguin diversity was substantially higher before the evolution of archaic humans. The fossil record indicates that a diverse assemblage of penguin species inhabited the southern African coasts for much of the Neogene. Previous excavations have identified four distinct species in Early Pliocene coastal marine deposits. Here we extend this pattern of high diversity and report the oldest record of penguins from Africa. Seventeen penguin specimens were identified from the Saldanha Steel locality, revealing the presence of at least four distinct species in South Africa during the Miocene. The largest of these species reached the size of the extant Aptenodytes patagonicus (king penguin), whereas the smallest was approximately the size of the smallest extant penguin Eudyptula minor (little blue penguin). Recovery of Miocene penguin remains is in accordance with earlier predictions of multiple pre‐Pliocene colonizations of Africa and supports a higher level of ecological diversity amongst African penguins in the past. © 2013 The Linnean Society of London     

The ubiquity of avian ultraviolet plumage reflectance

Although several bird species have been shown to reflect ultraviolet (UV) light from their plumages, the incidence of UV reflectance, and therefore the potential for UV or UV-enhanced signals, across the avian tree of life is not known. In this study, we collected reflectance data from the plumages of 312 bird species representing 142 families. Our results demonstrate that all avian families possess plumages that reflect significant amounts of UV light. The ubiquity of UV reflectance indicates that all studies of avian behaviour, ecology and evolution involving plumage coloration would benefit from consideration of plumage reflectance in the UV portion of the electromagnetic spectrum. Additionally, we demonstrate the existence of cryptic UV plumage patches and cryptic dimorphism among birds.     

Sex Identification of Four Penguin Species Using Locus‐Specific PCR

Traditional methods for sex identification are not applicable to sexually monomorphic species, leading to difficulties in the management of their breeding programs. To identify sex in sexually monomorphic birds, molecular methods have been established. Two established primer pairs (2550F/2718R and p8/p2) amplify the CHD1 gene region from both the Z and W chromosomes. Here, we evaluated the use of these primers for sex identification in four sexually monomorphic penguin species: king penguins (Aptenodytes patagonicus), rockhopper penguins (Eudyptes chrysocome), gentoo penguins (Pygoscelis papua), and Magellanic penguins (Spheniscus magellanicus). For all species except rockhopper penguins, primer pair 2550F/2718R resulted in two distinct CHD1Z and CHD1W PCR bands, allowing for sex identification. For rockhopper penguins, only primer pair p8/p2 yielded different CHD1Z and CHD1W bands, which were faint and similar in size making them difficult to distinguish. As a result, we designed a new primer pair (PL/PR) that efficiently determined the gender of individuals from all four penguin species. Sequencing of the PCR products confirmed that they were from the CHD1 gene region. Primer pair PL/PR can be evaluated for use in sexing other penguin species, which will be crucial for the management of new penguin breeding programs. Zoo Biol 32:257–261, 2013. © 2012 Wiley Periodicals, Inc.     

Life cycle of the tick Ixodes uriae in penguin colonies: relationships with host breeding activity.

A survey of the temporal pattern of population structure and feeding activity of the seabird tick Ixodes uriae was conducted for the first time in two host species colonies: King penguin (Aptenodytes patagonicus halli) and Macaroni penguin (Eudyptes chrysolophus chrysolophus). The life cycle of the tick was investigated over 3 years in a King penguin colony and 2 years in a Macaroni penguin colony at Possession Island (Crozet Archipelago). There was a marked seasonal feeding activity pattern of ticks in both host species, connected with the presence of birds during the breeding season. Although the King penguin colonies were occupied throughout the year by birds, the favourable period for engorgement was limited to 3.5-4.5 months, and almost all the ticks overwintered in the unengorged state. Consequently, I. uriae probably completed its life cycle over 3 years in King penguin colonies. In contrast, this life cycle could be shortened to 2 years in Macaroni penguin colonies, as a result of a different timetable of the presence of birds for breeding and moulting. The relationships between such plasticity and the host behaviour and subantarctic climatic conditions are discussed.     

Experimental stress during molt suggests the evolution of condition‐dependent and condition‐independent ornaments in the king penguin

Sexual selection and social selection are two important theories proposed for explaining the evolution of colorful ornamental traits in animals. Understanding signal honesty requires studying how environmental and physiological factors during development influence the showy nature of sexual and social ornaments. We experimentally manipulated physiological stress and immunity status during the molt in adult king penguins (Aptenodytes patagonicus), and studied the consequences of our treatments on colourful ornaments (yellow‐orange and UV beak spots and yellow‐orange auricular feather patches) known to be used in sexual and social contexts in this species. Whereas some ornamental features showed strong condition‐dependence (yellow auricular feather chroma, yellow and UV chroma of the beak), others were condition‐independent and remained highly correlated before and after the molt (auricular patch size and beak UV hue). Our study provides a rare examination of the links between ornament determinism and selection processes in the wild. We highlight the coexistence of ornaments costly to produce that may be honest signals used in mate choice, and ornaments for which honesty may be enforced by social mediation or rely on genetic constraints.     

Low MHC variation in the endangered Galápagos penguin (<Emphasis Type="Italic">Spheniscus mendiculus</Emphasis>)

The major histocompatibility complex (MHC) is one of the most polymorphic regions of the genome, likely due to balancing selection acting to maintain alleles over time. Lack of MHC variability has been attributed to factors such as genetic drift in small populations and relaxed selection pressure. The Galápagos penguin (Spheniscus mendiculus), endemic to the Galápagos Islands, is the only penguin that occurs on the equator. It relies upon cold, nutrient-rich upwellings and experiences severe population declines when ocean temperatures rise during El Niño events. These bottlenecks, occurring in an already small population, have likely resulted in reduced genetic diversity in this species. In this study, we used MHC class II exon 2 sequence data from a DRB1-like gene to characterize the amount of genetic variation at the MHC in 30 Galápagos penguins, as well as one Magellanic penguin (S. magellanicus) and two king penguins (Aptenodytes patagonicus), and compared it to that in five other penguin species for which published data exist. We found that the Galápagos penguin had the lowest MHC diversity (as measured by number of polymorphic sites and average divergence among alleles) of the eight penguin species studied. A phylogenetic analysis showed that Galápagos penguin MHC sequences are most closely related to Humboldt penguin (Spheniscus humboldti) sequences, its putative sister species based on other loci. An excess of non-synonymous mutations and a pattern of trans-specific evolution in the neighbor-joining tree suggest that selection is acting on the penguin MHC.     

King penguin demography since the last glaciation inferred from genome-wide data

How natural climate cycles, such as past glacial/interglacial patterns, have shaped species distributions at the high-latitude regions of the Southern Hemisphere is still largely unclear. Here, we show how the post-glacial warming following the Last Glacial Maximum (ca 18 000 years ago), allowed the (re)colonization of the fragmented sub-Antarctic habitat by an upper-level marine predator, the king penguin Aptenodytes patagonicus. Using restriction site-associated DNA sequencing and standard mitochondrial data, we tested the behaviour of subsets of anonymous nuclear loci in inferring past demography through coalescent-based and allele frequency spectrum analyses. Our results show that the king penguin population breeding on Crozet archipelago steeply increased in size, closely following the Holocene warming recorded in the Epica Dome C ice core. The following population growth can be explained by a threshold model in which the ecological requirements of this species (year-round ice-free habitat for breeding and access to a major source of food such as the Antarctic Polar Front) were met on Crozet soon after the Pleistocene/Holocene climatic transition.     

Responses of king penguin Aptenodytes patagonicus adults and chicks to two food‐related odours

Increasing evidence suggests that penguins are sensitive to dimethyl sulphide (DMS), a scented airborne compound that a variety of marine animals use to find productive areas of the ocean where prey is likely to be found. Here we present data showing that king penguins Aptenodytes patagonicus are also sensitive to DMS. We deployed DMS on a lake near a king penguin colony at Ratmanoff beach in the Kerguelen archipelago. We also presented DMS to ‘sleeping’ adults on the beach. On the lake, penguins responded to the DMS deployments by swimming more, while on the beach, penguins twitched their heads and woke up more for the DMS than for the control presentations. Interestingly, penguins did not respond to cod liver oil deployments on the lake; mirroring at‐sea studies of other penguins. Although at‐sea studies are needed to confirm that king penguins use DMS as a surface cue that informs them of productivity under the water, this study is an important first step in understanding how these birds locate prey over significant distances.     

Diurnal sleep depth changes in the king penguin (<Emphasis Type="Italic">Aptenodytes patagonicus</Emphasis>)

Avian sleep quality depends on its depth (deeper sleep being of better quality). In king penguins (Aptenodytes patagonica), sleep may be disturbed by congeners passing in the sleeper's vicinity. As king penguin activity is increased in the morning, sleep disturbances are more likely to occur during this time period. One might therefore assume that afternoon sleepers (AS) sleep more profoundly than morning sleepers (MS). To test this hypothesis, we examined the diurnal variations in sleep depth of king penguins sleeping in resting sites adjacent to the colony of 'La Baie du Marin' (Crozet Archipelago). We measured the bodily tactile arousal threshold at the upper back level. The arousal threshold in AS was twice as high as in MS. This study demonstrates for the first time that sleep depth changes according to time of day in a diurnal wild bird. We postulate that diurnal sleep depth is increased due to decreased congener movements close to the sleeping penguin.     

Ultraviolet reflectance by the cere of raptors

Ultraviolet (UV) signals have been shown to play key roles in social and sexual signalling in birds. Using a spectrophotometer, we analysed the colour of the cere (skin above the beak) of a diurnal raptor, the Montagu's harrier (Circus pygargus), and show that it reflects in the UV part of the spectrum. The cere is a well-known sexual signal in raptors, with carotenoid based pigmentation being indicative of quality. We thus hypothesized that UV reflectance also signals quality. Accordingly, we found that in our sample of wild males, the location of the UV peak was related to the orangeness of cere and correlated with male body mass and condition (mass corrected for size). Also, males with brighter UV were mated to females that laid earlier, as expected if UV reflectance relates to a male's quality and attractiveness. Future studies should investigate the relationships between UV reflectance and carotenoid pigmentation of cere, and test how UV reflectance influences mate choice.     

Superoxide activates a GDP-sensitive proton conductance in skeletal muscle mitochondria from king penguin (Aptenodytes patagonicus)

We present the partial nucleotide sequence of the avian uncoupling protein (avUCP) gene from king penguin (Aptenodytes patagonicus), showing that the protein is 88-92% identical to chicken (Gallus gallus), turkey (Meleagris gallopavo), and hummingbird (Eupetomena macroura). We show that superoxide activates the proton conductance of mitochondria isolated from king penguin skeletal muscle. GDP abolishes the superoxide-activated proton conductance, indicating that it is mediated via avUCP. In the absence of superoxide there is no GDP-sensitive component of the proton conductance from penguin muscle mitochondria demonstrating that avUCP plays no role in the basal proton leak.     

Ornamental colors reveal age in the king penguin

We investigated whether delayed plumage maturation occurred in king penguins (Aptenodytes patagonicus). Therefore we examined the relationships between age and sex on spectral properties and size of two colored plumage patches and a UV-reflective beak spot, using known-age cohorts. Unlike the colored patch on the breast, we found age differences in ear and beak coloration. These results suggest that head ornaments in king penguins could signal sexual maturity or social status. No sex differences were found in the intensity of colored ornaments, which can result from mutual mate choice or genetic correlation between sexes. Size of colored patches did not relate to age or sex.