Mate switching and copulation behaviour in King Penguins

Extra‐pair paternity (EPP) in monogamous birds may result from either extra‐pair copulations (EPCs) or mate switching. In this study of King Penguins in South Georgia, we observed no EPCs at all, an effect of very efficient mate guarding. Onshore males fast and need not divert attention to foraging or to defending nest or territory, as this species has neither. However, we found that mate switching was common. On average 38% (range: 29%–56%; three years pooled) of the birds established pair bonds with at least one initial partner before switching to the partner they bred with (i.e. the “pair mate”). Of the observed copulations of 44 studied females, 22% were with initial partners and 78% with the pair mate. This and the high proportion of mate switching suggest that roughly 10% of the females could have received sperm from males other than the pair mate. The average copulation frequency was 0.026 h^?1, resulting in an estimated 8.2 copulations per clutch (which consists of one egg). That more copulations than necessary for fertilisation occur suggests that males try to protect paternity by sperm competition, and that this is a result of the potential for EPP due to mate switching in King Penguins. All observed copulations except one took place between days 13 and 5, with the peak 7.5 days prior to egg‐laying. The birds found their pair mates (often not the same as in the previous year) on average about 10 days before egg‐laying, and always established themselves at the outskirts of the colony about 8 days before egg‐laying. Thus, most copulations occurred around the time the birds joined the colony. We suggest that it is adaptive to obtain a breeding spot early, because the colony will grow and pairs joining later will protect the offspring. Additionally, we suggest that early copulation outside the colony is adaptive because of the risk of failing to fertilise the egg when copulating among aggressive neighbours inside the dense colony. Based on these two arguments we suggest a “safe place hypothesis” to explain the early copulation peak in King Penguins.     

Fat King Penguins Are Less Steady on Their Feet

Returning to the shore after a feeding sojourn at sea, king penguins often undertake a relatively long terrestrial journey to the breeding colony carrying a heavy, mostly frontal, accumulation of fat along with food in the stomach for chick-provisioning. There they must survive a fasting period of up to a month in duration, during which their complete reliance on endogenous energy stores results in a dramatic loss in body mass. Our aim was to determine if the king penguin’s walking gait changes with variations in body mass. We investigated this by walking king penguins on a treadmill while instrumented with an acceleration data logger. The stride frequency, dynamic body acceleration (DBA) and posture of fat (pre-fasting; 13.2 kg) and slim (post fasting; 11 kg) king penguins were assessed while they walked at the same speed (1.4km/h) on a treadmill. Paired statistical tests indicated no evidence for a difference in dynamic body acceleration or stride frequency between the two body masses however there was substantially less variability in both leaning angle and the leaning amplitude of the body when the birds were slimmer. Furthermore, there was some evidence that the slimmer birds exhibited a decrease in waddling amplitude. We suggest the increase in variability of both leaning angle and amplitude, as well as a possibly greater variability in the waddling amplitude, is likely to result from the frontal fat accumulation when the birds are heavier, which may move the centre of mass anteriorly, resulting in a less stable upright posture. This study is the first to use accelerometry to better understand the gait of a species within a specific ecological context: the considerable body mass change exhibited by king penguins.     

Eye structure and foraging in King Penguins Aptenodytes patagonicus

Anterior eye structure and retinal visual fields were determined in King Penguins Aptenodytes patagonicus using keratometry and an ophthalmoscopic reflex technique. The cornea is relatively flat (radius 32.9 mm) and hence of low refractive power (10.2 dioptres in air) and this may be correlated with the amphibious nature of penguin vision. The large size of the eye and of the fully dilated pupil may be correlated with activity at low light levels. In air, the binocular field is long (vertical extent 180̀) and narrow (maximum width 29̀), with the bill placed approximately centrally—a topography found in a range of bird species which employ visual guidance of bill position when foraging. Upon immersion in water, the optical power of the cornea is abolished, with the effect that the monocular fields decrease and binocularity is lost. King Penguins have a pupil type which has not hitherto been recorded in birds. In daylight it contracts to a square-shaped pinhole but dilates to a large circular aperture in darkness. This change alters retinal illumination by 300-fold (2.5 log₁₀ units). When diving, this permits the retina to be pre-adapted to the low ambient light levels that the birds encounter upon reaching mesopelagic depths. These penguins also forage at depths where ambient light levels, even during the day, can fall below the equivalent of terrestrial starlight. Under these conditions, the birds must rely upon the detection of light from the photophores of their prey. In this they are aided by their absolutely large pupil size and broad cyclopean visual field.     

Inter-Annual Variability of Fledgling Sex Ratio in King Penguins

As the number of breeding pairs depends on the adult sex ratio in a monogamous species with biparental care, investigating sex-ratio variability in natural populations is essential to understand population dynamics. Using 10 years of data (2000–2009) in a seasonally monogamous seabird, the king penguin (Aptenodytes patagonicus), we investigated the annual sex ratio at fledging, and the potential environmental causes for its variation. Over more than 4000 birds, the annual sex ratio at fledging was highly variable (ranging from 44.4% to 58.3% of males), and on average slightly biased towards males (51.6%). Yearly variation in sex-ratio bias was neither related to density within the colony, nor to global or local oceanographic conditions known to affect both the productivity and accessibility of penguin foraging areas. However, rising sea surface temperature coincided with an increase in fledging sex-ratio variability. Fledging sex ratio was also correlated with difference in body condition between male and female fledglings. When more males were produced in a given year, their body condition was higher (and reciprocally), suggesting that parents might adopt a sex-biased allocation strategy depending on yearly environmental conditions and/or that the effect of environmental parameters on chick condition and survival may be sex-dependent. The initial bias in sex ratio observed at the juvenile stage tended to return to 1∶1 equilibrium upon first breeding attempts, as would be expected from Fisher’s classic theory of offspring sex-ratio variation.     

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.     

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.     

Sex identification in King Penguins Aptenodytes patagonicus through morphological and acoustic cues

In the context of sexual selection, animals have developed a variety of cues conveying information about the sex of an individual to conspecifics. In many colonial seabird species, where females and males are monomorphic and do not show obvious differences in external morphology, acoustic cues are an important signal for individual and sex recognition. Here, we study the vocal and morphological sex dimorphism in the King Penguin Aptenodytes patagonicus, a colonial, monomorphic seabird for which our knowledge about the role of vocalizations and morphology in mate choice is very limited. Data were collected at Possession Island, Crozet Archipelago, in a breeding colony consisting of about 16 000 breeding pairs. Using measurements of six morphological features and analysing acoustic parameters of call recordings of adult individuals, we show that King Penguins can be sexed based on a single morphological measurement of the beak with an accuracy of 79%. We found a sex‐specific syntax in adult King Penguin calls that provided a 100% accurate method to distinguish between the sexes in our study population. To confirm the method at the species level, we analysed calls recorded from King Penguin adults in Kerguelen Island, 1300 km away from our study population and found the same accuracy of the sex‐specific syntax. This sex‐specific syllable arrangement is rare in non‐passerines and is a first step in understanding the mate choice process in this species. Furthermore, it offers a cost‐effective, non‐invasive technique for researchers to sex King Penguins in the field.     

Bluegill Coloration as a Sexual Ornament: Evidence From Ontogeny,Sexual Dichromatism,and Condition Dependence

In aquatic environments, visual communication is expected in animals that inhabit clear, shallow waters. Here, we investigate variation in the colorful traits of bluegills, Lepomis macrochirus, to elucidate their possible function. Bluegills use alternative mating tactics whereby males develop into one of two irreversible phenotypes termed parental and cuckolder. Parentals build and defend nests and care for offspring whereas cuckolders obtain matings by sneaking copulations. We hypothesized that bluegill coloration might function as a sexual ornament in parental males and that ornamental coloration might serve as an honest indicator of male quality. We predicted that coloration should be more pronounced in parental males than in females and immature males and should be more pronounced during the breeding season. We also predicted that males in better condition should be more intensely colored than fish in poor condition. To test our predictions, we sampled 510 bluegills during the breeding and post‐breeding seasons at nine lakes in southern Ontario, Canada, in 2007. We used reflectance spectrometry to quantify the coloration of five body regions, aged and sexed each fish, and calculated Fulton’s condition factor from morphological measurements. A separate experiment showed that color did not fade several minutes post capture, suggesting that coloration could be measured reliably and consistently. We found that color was influenced by maturity, sex, and season, in the predicted direction, for three body regions (breast, cheek, and opercular flap). We also found that color varied with the condition of males such that males in better condition were darker for the sexually dichromatic ventral and facial regions. Our findings therefore suggest that some colorful traits in bluegills may serve as condition‐dependent sexual signals during the breeding season. Our research contributes to a growing appreciation of the importance of visual signaling in aquatic environments.     

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.     

The breeding biology and population dynamics of King Penguins Aptenodytes patagonica on the Crozet Islands

Among King Penguins Aptenodytes patagonica at Possession Island, one of the Crozet Islands, the length of the moult period, pre-laying period, incubating and brooding shifts were highly variable according to the year and to the stage of the breeding season. The moulting period was shorter in late breeders than in early breeders. Only half of the birds which successfully reared a chick bred the following cycle, but late in the season. Almost all these late breeders were unsuccessful. The reasons for the high variability in the breeding pattern observed in this species between years, as well as between colonies and between individuals are discussed. Breeding success was on average 30.6% and survival during the first year at sea could reach 50%. The survival of adult birds has increased during the past 10 years from 90.7% to 95.2% per annum. Despite an almost biennial breeding frequency and a very high rate of chick loss during the winter fast, the King Penguin population of Possession Island has doubled between 1966 and 1985 due to a high survival rate of adult and immature birds. The increase during the last decade in adult survival and in adult and chick condition suggests that the population increase could be the result of an improvement in food availability.     

Interrelationship Between Fractal Ornament and Multilevel Selection Theory

Interdisciplinarity is one of the features of modern science, defined as blurring the boundaries of disciplines and overcoming their limitations or excessive specialization by borrowing methods from one discipline into another, integrating different theoretical assumptions, and using the same concepts and terms. Often, theoretical knowledge of one discipline and technological advances of another are combined within an interdisciplinary science, and new branches or disciplines may also emerge. Biosemiotics, a field that arose at the crossroads of biology, semiotics, linguistics, and philosophy, enables scientists to borrow theoretical assumptions from semiotics and extend them to different biological theories. The latter applies especially to extended synthesis, wherein culture is viewed as one of the factors influencing evolution. In the present research, the semiotic system of Ukrainian folk ornament is analyzed through the theory of fractals, key features of which are recursion and self-similarity. As a result, an assumption is made about the fractal structure of culture and social life on a conceptual level. What follows is a discussion of how this assumption can contribute to the multilevel selection theory, one of the foundations of extended synthesis, which employs the concept of self-similarity at all levels of the biological hierarchy.     

Comparative fuel metabolism in Gentoo and King Penguins: adaptation to brief versus prolonged fasting

To compare fuel utilization in large birds adapted to brief or prolonged fasting, protein and lipid utilization were quantified in the Gentoo Penguin (Pygoscelis papua) and the King Penguin (Aptenodytes patagonica). The inshore feeder Gentoo Penguin fasts for only a few days in its colony, while King Penguin chicks starve for several months in the subantarctic winter and male King Penguins starve for 5–6 weeks at the beginning of their breeding cycle. After an initial decrease in both daily body mass loss and nitrogen excretion during the first days of food deprivation, these two parameters thereafter stabilized at low values. At that time, protein utilization accounted for 15% of total energy expenditure in Gentoo Penguins and only 6% in King Penguin chicks during winter, the remainder (85% and 94%, respectively) being provided by fat oxidation. Similar percentages in fuel metabolism as seen in chicks during winter were reached in fasting adult King Penguins and spring chicks. However, a seasonal adaptation occurs in fasting chicks because energy expenditure is lower during winter. As previously described in starved mammals, the effectiveness in protein sparing could be related to the initial adiposity of the birds: the larger the fat stores (about 9% and 30% in Gentoo Penguins and winter chicks of King Penguins, respectively), the longer the fast duration and the better the level of protein conservation.     

King Penguins adjust foraging effort rather than diet when faced with poor foraging conditions

The links between foraging success, foraging effort and diet in a myctophid specialist seabird, the King Penguin Aptenodytes patagonicus, were investigated during seven breeding seasons using tracking and isotopic data. Despite the variable foraging conditions encountered by the birds, isotopic signatures (a proxy for diet) were invariable throughout the study. On the other hand, penguins stayed longer at sea when the foraging success indices (i.e. prey capture attempts per day and mass gained per day) were low. Although King Penguins can compensate for low prey capture rates by increasing foraging effort, their specialist diet during reproduction makes the species particularly sensitive to prey availability, with its conservation tightly linked to its main prey.     

Post-Fledging Dispersal of King Penguins (Aptenodytes patagonicus) from Two Breeding Sites in the South Atlantic

Most studies concerning the foraging ecology of marine vertebrates are limited to breeding adults, although other life history stages might comprise half the total population. For penguins, little is known about juvenile dispersal, a period when individuals may be susceptible to increased mortality given their naïve foraging behaviour. Therefore, we used satellite telemetry to study king penguin fledglings (n = 18) from two sites in the Southwest Atlantic in December 2007. The two sites differed with respect to climate and proximity to the Antarctic Polar Front (APF), a key oceanographic feature generally thought to be important for king penguin foraging success. Accordingly, birds from both sites foraged predominantly in the vicinity of the APF. Eight king penguins were tracked for periods greater than 120 days; seven of these (three from the Falkland Islands and four from South Georgia) migrated into the Pacific. Only one bird from the Falkland Islands moved into the Indian Ocean, visiting the northern limit of the winter pack-ice. Three others from the Falkland Islands migrated to the eastern coast of Tierra del Fuego before travelling south. Derived tracking parameters describing their migratory behaviour showed no significant differences between sites. Nevertheless, generalized linear habitat modelling revealed that juveniles from the Falkland Islands spent more time in comparatively shallow waters with low sea surface temperature, sea surface height and chlorophyll variability. Birds from South Georgia spent more time in deeper waters with low sea surface temperature and sea surface height, but high concentrations of chlorophyll. Our results indicate that inexperienced king penguins, irrespective of the location of their natal site in relation to the position of the APF, develop their foraging skills progressively over time, including specific adaptations to the environment around their prospective breeding site.     

Restoration of body mass in King Penguins after egg abandonment at a critical energy depletion stage: early vs late breeders

In fasting‐incubating seabirds, it has been proposed that egg abandonment and refeeding should be induced when a low body mass (BM) threshold is attained, thus ensuring adult survival at the expense of immediate breeding. In the context of life‐history trade‐offs in long‐lived birds, we have tested this hypothesis by comparing short‐term survival and restoration of BM in King Penguins Aptenodytes patagonicus that abandoned their egg to those that were relieved normally by their mate at the end of the first incubation shift. Since King Penguins have an extended laying period, the possible influence of seasonal factors was also examined by comparing early and late breeders. Forty incubating males were experimentally forced to fast until egg abandonment by preventing relief by the female. At egg abandonment of both early and late breeding males, BM was below the BM threshold, fasting duration was eight days (about 30%) longer than for relieved birds, and plasma uric acid level was elevated (signature of increased body protein catabolism, phase III of fasting). All abandoning birds survived and came back from sea at a BM similar to that of relieved penguins. The duration of the foraging trip of abandoning early breeders was the same as that of relieved birds, and some abandoning birds engaged in a new breeding attempt. Abandoning late breeders, however, made foraging trips twice as long as those of relieved males. This difference can be explained by time constraints rather than nutritional constraints, abandoning early breeders having enough time left in the breeding season to engage in a new breeding attempt in contrast to abandoning late breeders. These observations lend support to the suggestion that not only BM but also an internal clock intervene in the decision to engage in breeding or not. By preventing a lethal energy depletion ashore and by acting at a fasting stage where the capacity to restore BM at sea is unaffected, abandonment at a low body condition threshold plays a major role in the trade‐off between adult penguin survival and reproduction.     

Expanding Sexual Selection Gradients; A Synthetic Refinement of Sexual Selection Theory

Sexual selection is usually modeled as fitness differences that are mediated through variation in the number of mates obtained (variance in mating success, V_MS). Nevertheless, empirical studies increasingly posit sexual selection even when V_MS is low or does not contribute to variance in fitness, as is the case in females of many species. In these contexts, evolution by sexual selection is only plausible if it is mediated through variation in mate quality (V_MQ) rather than exclusively through variation in the number of mates (V_MS). However, we lack a formal theoretical foundation for sexual selection in these cases. Here, I argue the need for an explicit, formal treatment of how V_MQ may result in sexual selection. Building upon the conceptually powerful framework of sexual selection gradients, I propose a graphical heuristic model that aims to serve as a foundation for future formal models. I close by discussing the implications of this perspective for sexual selection research in general, with particular attention to predictions that the model generates for the action of sexual selection on female traits.     

The Relationship between Sexual Selection and Sexual Conflict

Evolutionary conflicts of interest arise whenever genetically different individuals interact and their routes to fitness maximization differ. Sexual selection favors traits that increase an individual’s competitiveness to acquire mates and fertilizations. Sexual conflict occurs if an individual of sex A’s relative fitness would increase if it had a “tool” that could alter what an individual of sex B does (including the parental genes transferred), at a cost to B’s fitness. This definition clarifies several issues: Conflict is very common and, although it extends outside traits under sexual selection, sexual selection is a ready source of sexual conflict. Sexual conflict and sexual selection should not be presented as alternative explanations for trait evolution. Conflict is closely linked to the concept of a lag load, which is context-dependent and sex-specific. This makes it possible to ask if one sex can “win.” We expect higher population fitness if females win.Many published studies ask if sexual selection or sexual conflict drives the evolution of key reproductive traits (e.g., mate choice). Here we argue that this is an inappropriate question. By analogy, G. Evelyn Hutchinson (1965) coined the phrase “the ecological theatre and the evolutionary play” to capture how factors that influence the birth, death, and reproduction of individuals (studied by ecologists) determine which individuals reproduce, and “sets the stage” for the selective forces that drive evolutionary trajectories (studied by evolutionary biologists). The more modern concept of “eco-evolutionary feedback” (Schoener 2011) emphasizes that selection changes the character of the actors over time, altering their ecological interactions. No one would sensibly ask whether one or the other shapes the natural world, when obviously both interact to determine the outcome.So why have sexual conflict and sexual selection sometimes been elevated to alternate explanations? This approach is often associated with an assumption that sexual conflict affects traits under direct selection, favoring traits that alter the likelihood of a potential mate agreeing or refusing to mate because it affects the bearer’s immediate reproductive output, whereas “traditional” sexual selection is assumed to favor traits that are under indirect selection because they increase offspring fitness. These “traditional” models are sometimes described as “mutualistic” (e.g., Pizzari and Snook 2003; Rice et al. 2006), although this term appears to be used only when contrasting them with sexual conflict models. The investigators of the original models never describe them as “mutualistic,” which is hardly surprising given that some males are rejected by females.In this review, we first define sexual conflict and sexual selection. We then describe how the notion of a “lag load” can reveal which sex currently has greater “power” in a sexual conflict over a specific resource. Next, we discuss why sexual conflict and sexual selection are sometimes implicitly (or explicitly) presented as alternative explanations for sexual traits (usually female mate choice/resistance). To illustrate the problems with the assumptions made to take this stance, we present a “toy model” of snake mating behavior based on a study by Shine et al. (2005). We show that empirical predictions about the mating behavior that will be observed if females seek to minimize direct cost of mating or to obtain indirect genetic benefits were overly simplistic. This allows us to make the wider point that whom a female is willing to mate with and how often she mates are often related questions. Finally, we discuss the effect of sexual conflict on population fitness.     

Sexual Selection in the Three-Spined Stickleback

The purpose of this study was to seek evidence for the influence of sexual selection on both male and female three-spined sticklebacks, a species in which the ♂ alone has parental responsibilities. We studied the intrasexual relationships of ♂♂ and ♀♀ prior to courtship, and the intrasexual and intersexual relationships of both sexes during courtship. Results demonstrated that both ♂♂ and ♀♀ compete intrasexually, and suggested that both sexes are discriminative in mate selection. These results are compatible with Trivers' (1972) model of the role of parental investment in sexual selection.