Acoustic recognition in macaroni penguins: an original signature system

Penguins use vocal signatures as cues to identify their kin in dense colonies. Experimental studies of four species in two genera have pointed out that vocal signatures depend on the breeding ecology of the birds. Penguins that have a meeting site for pair members and chicks (genus Pygoscelis), as in many seabirds, have a less complex vocal signature than penguins that have no nests (genus Aptenodytes). To investigate whether this pattern would extend to other nest-building penguins, we studied the vocal signature in a species of the genus Eudyptes, the macaroni penguin, E. chrysolophus. Temporal and spectral features of signatures were analysed to determine which were likely to encode individual identity. Using a methodology derived from the theory of information, we measured and compared the amount of information given by each of these parameters by means of a stereotypy index. We then tested their effective efficiency in playback experiments of modified calls. Like Aptenodytes species, the macaroni penguins used a double coding system that integrated information in both the temporal and spectral domains. The encoding was made through the tempo given by the successive syllables of the call and the harmonic content of the call. However, information was not complementary but was mostly repeated in both domains, and variables were unidimensional as in Pygoscelis signatures. These results point out an original and simple signature system in macaroni penguins. Although they support the hypothesis of simpler systems in nest-building species they also reveal more subtle differences within this category.     

Long-term breeding phenology shift in royal penguins

The Earth's climate is undergoing rapid warming, unprecedented in recent times, which is driving shifts in the distribution and phenology of many plants and animals. Quantifying changes in breeding phenology is important for understanding how populations respond to these changes. While data on shifts in phenology are common for Northern Hemisphere species (especially birds), there is a dearth of evidence from the Southern Hemisphere, and even fewer data available from the marine environment. Surface air temperatures at Macquarie Island have increased by 0.62°C during the 30-year study period (0.21°C decade(-1)) and royal penguins (Eudyptes schlegeli) commenced egg laying on average three days earlier in the 1990s than during the 1960s. This contrasts with other studies of Southern Ocean seabirds; five of nine species are now breeding on average 2.1 days later than during the 1950s. Despite the different direction of these trends, they can be explained by a single underlying mechanism: resource availability. There was a negative relationship between the Southern Annular Mode (SAM) and median laying date of royal penguins, such that low-productivity (low SAM) years delayed laying date. This accords with the observations of other seabird species from the Antarctic, where later laying dates were associated with lower sea ice and lower spring productivity. The unifying factor underpinning phenological trends in eastern Antarctica is therefore resource availability; as food becomes scarcer, birds breed later. These changes are not uniform across the region, however, with resource increases in the subantarctic and decreases in eastern Antarctica.     

Sex-biased disruptive behaviour in breeding crested penguins

Colonial breeding is common in seabirds, and may provide individuals with benefits such as increased protection from predators by joint defence, improved information exchange and enhanced access to mates. However, the presence of large numbers of individuals in breeding colonies may also lead to interference, especially where conspecific behaviour disrupts the normal chick-rearing routine. Using standardised video recordings, we describe and quantify for the first time such disruptive behaviour by conspecifics in penguins. This disruptive behaviour appeared to be common in chick-feeding Southern rockhopper penguins Eudyptes chrysocome and its occurrence did not differ significantly among the colony areas where observations were made. Females were commonly (77 % of 111 observation sessions) disrupted by other adults when attempting to feed chicks alone during the crèche stage. They consequently reduced the time spent with their chicks. Disrupted chicks compensated by begging more intensely when their female parents were present, and they did not eat significantly less often than undisrupted chicks. In contrast, disruptive behaviour towards chick-feeding males or pairs was never observed. This study supplements knowledge about a disruptive behaviour that appears to be common but for which the function remains unclear in penguins, as the intruders did not appear to gain any visible benefits.     

The different breeding strategies of penguins: A review

The 18 penguin species are exclusively and widely distributed in the Southern hemisphere, from the Equator to the Antarctic continent, and are thus submitted to various ecological constraints in their reproductive strategy. This results in a high variability in all aspects of the breeding biology of the different species. Although penguins appear primarily adapted for a marine existence, they remain dependent on land for breeding, rearing young, and moulting. Here we describe and compare the breeding cycle of all the penguin species, highlighting the characteristics of each species in terms of breeding range, population status, threats induced by environmental changes, duration of the different phases of the breeding cycle, mate fidelity, body mass, body height, egg mass and duration of egg formation. We also focus on the breeding cycle of the genus Aptenodytes, since it largely differs from the breeding cycle of most of the other penguin species.     

Potential for individual recognition in acoustic signals: a comparative study of two gulls with different nesting patterns

We test relationships between structure of acoustic signal used for individual recognition and nesting ecology among two gulls: the black-headed gull (Larus ridibundus), in which chicks remain in the nest, and the slender-billed gull (L. genei), in which chicks leave the nest after hatching to form crèches. A striking difference between both species is the presence of two fundamental frequencies in the slender-billed gull's call and only one in the black-headed gull's call. Our study shows that the potential for individuality coding is more important in the species where the offspring experiment the greatest constraints--due to their nesting pattern--to identify their parents.     

Reproductive performance of little penguins Eudyptula minor in relation to year, age, pair-bond duration, breeding date and individual quality

We measured breeding performance of little penguins Eudyptula minor at Phillip Island, Victoria, Australia, during a 21-year period. All birds considered in this paper (n=307) were of known age (2–22 y) and sex, and most were of known, or closely-estimated, pair-bond status (1–8 mates per bird; pair-bond durations 1–13 y). Breeding dates and breeding performance varied markedly from year to year; measures of annual performance were not associated with early breeding. Measures of individual breeding performance (clutch-size, hatching success, chick masses and productivity) were related to early laying, parental age, and duration of pair-bond. Dependence of breeding performance on parental age was curvilinear, levelling off at about 8 y of age. Productivity declined significantly among birds older than 8 y; this decline was not due to events in the last year of breeding ("terminal illness"). Breeding performance increased with duration of pair-bond at least through y 5. Early breeding was significantly related to age and duration of pair-bond. Most of these relationships were stronger among males than among females, and many of them were not significant when females were considered alone. After controlling for other factors, breeding performance varied significantly among birds, but autocorrelations were low and limited to intervals of one year. Parental quality (defined for birds studied in six or more years as the individual bird term in a GLM for productivity controlling for other factors) was not correlated with lifespan or other demographic parameters, but high-quality birds were less prone to change mates and burrows than low-quality birds. We know of no previous study in which simultaneous effects of laying date, age and pair-bond duration on breeding performance were measured, while controlling for year, individual quality and terminal illness.     

Increased survival and breeding performance of double breeders in little penguins Eudyptula minor,New Zealand: evidence for individual bird quality?

The little penguin Eudyptula minor is unique among penguin species in being able to fledge chicks from two clutches in one breeding season. Pairs laying two clutches in a given season make a higher reproductive investment, and may be rewarded by a higher reproductive success as they may raise twice as many chicks as pairs laying one clutch. The higher effort made by pairs laying two clutches could correlate negatively with survival, future reproductive performance or offspring survival, indicating a cost of reproduction. Conversely, a positive relationship between the number of clutches produced in a given breeding season and survival, future reproductive performance or offspring survival would indicate that birds laying two clutches belonged to a category of birds with higher fitness, compared to birds laying only one clutch in the season. In this study we used a long‐term data set taken from an increasing population of little penguins in Otago, SE New Zealand. We modelled the relationship between the number of clutches laid in a breeding season and survival probability, reproductive performance in the next breeding season and first year survival of offspring using capture‐recapture modelling.
Birds laying two clutches produced 1.7 times more fledglings during a breeding season than pairs laying one clutch. We found that birds laying two clutches had a higher probability of breeding in the following breeding season, a higher probability of laying two clutches in the following breeding season and a higher survival probability. There was no overall difference in post‐fledging survival between the young of birds producing one clutch and the young of birds producing two clutches. However, the survival of young of single clutch breeders declined with laying date, whereas the young of double clutch breeders had the same survival rate irrespective of laying date. For a subset of data with birds of known age, we found evidence that the probability of laying two clutches increased with age. However, there were also indications for differences among birds in the tendency to lay two clutches that could not be attributed to age. We tentatively interpret our results as evidence of quality difference among little penguin breeders.     

Current treatment of rectal cancer adapted to the individual patient

Preoperative radiochemotherapy and total mesorectal excision surgery is a recommended standard therapy for patients with locally advanced rectal cancer. However, some subgroups of patients benefit more than others from this approach. In order to avoid long-term complications of radiation and chemotherapy, efforts are being made to subdivide T3N0 stage using advanced imaging techniques, and to analyze prognostic factors that help to define subgroup risk patients. Long-course radiochemotherapy has the potential of downsizing the tumor before surgery and may increase the chance of sphincter preservation in some patients. Short-course radiotherapy (SCRT), on the other hand, is a practical schedule that better suits patients with intermediated risk tumors, located far from the anal margin. SCRT is also increasingly being used among patients with disseminated disease, before resection of the rectal tumor. Improvements in radiation technique, such as keeping the irradiation target below S2/S3 junction, and the use of IMRT, can reduce the toxicity associated with radiation, specially long-term small bowel toxicity.     

Corvids congregate to breeding colonies of a burrow‐nesting seabird

Egg predation is a major cause of reproductive failure among birds, and can compromise the viability of affected populations. Some egg predators aggregate near colonially breeding birds to exploit the seasonal increase of prey resources. We investigated spatial and temporal variations in the abundance of an egg predator (little raven Corvus mellori; Corvidae) to identify whether ravens aggregate spatially or temporally to coincide with any of three potential prey species: burrow‐nesting little penguin (Eudyptula minor; Spheniscidae), short‐tailed shearwater (Ardenna tenuirostris; Procellariidae), and surface‐nesting silver gull (Chroicocephalus novaehollandiae; Laridae). We derived spatially explicit density estimates of little ravens using distance sampling along line transects throughout a calendar year, which encompassed little penguin, short‐tailed shearwater and silver gull breeding and non‐breeding seasons. High raven abundance coincided temporally with penguin and gull egg laying periods but not with that of shearwaters. The spatial distribution of raven density corresponded with the little penguin colony but not with shearwater or gull colonies. Thus, the presence of little penguin eggs in burrows correlated strongly with little raven activity, and this implies that little ravens may have learnt to exploit the plentiful subsurface food resource of little penguin eggs. Corvid management may be required to maintain the viability of this socially and economically important penguin colony.     

Body temperature changes induced by huddling in breeding male emperor penguins

Huddling is the key energy-saving mechanism for emperor penguins to endure their 4-mo incubation fast during the Antarctic winter, but the underlying physiological mechanisms of this energy saving have remained elusive. The question is whether their deep body (core) temperature may drop in association with energy sparing, taking into account that successful egg incubation requires a temperature of about 36 degrees C and that ambient temperatures of up to 37.5 degrees C may be reached within tight huddles. Using data loggers implanted into five unrestrained breeding males, we present here the first data on body temperature changes throughout the breeding cycle of emperor penguins, with particular emphasis on huddling bouts. During the pairing period, core temperature decreased progressively from 37.5 +/- 0.4 degrees C to 36.5 +/- 0.3 degrees C, associated with a significant temperature drop of 0.5 +/- 0.3 degrees C during huddling. In case of egg loss, body temperature continued to decrease to 35.5 +/- 0.4 degrees C, with a further 0.9 degrees C decrease during huddling. By contrast, a constant core temperature of 36.9 +/- 0.2 degrees C was maintained during successful incubation, even during huddling, suggesting a trade-off between the demands for successful egg incubation and energy saving. However, such a limited drop in body temperature cannot explain the observed energy savings of breeding emperor penguins. Furthermore, we never observed any signs of hyperthermia in huddling birds that were exposed to ambient temperatures as high as above 35 degrees C. We suggest that the energy savings of huddling birds is due to a metabolic depression, the extent of which depends on a reduction of body surface areas exposed to cold.     

Phage endolysins are adapted to specific hosts and are evolutionarily dynamic

Endolysins are produced by (bacterio)phages to rapidly degrade the bacterial cell wall and release new viral particles. Despite sharing a common function, endolysins present in phages that infect a specific bacterial species can be highly diverse and vary in types, number, and organization of their catalytic and cell wall binding domains. While much is now known about the biochemistry of phage endolysins, far less is known about the implication of their diversity on phage–host adaptation and evolution. Using CRISPR-Cas9 genome editing, we could genetically exchange a subset of different endolysin genes into distinct lactococcal phage genomes. Regardless of the type and biochemical properties of these endolysins, fitness costs associated to their genetic exchange were marginal if both recipient and donor phages were infecting the same bacterial strain, but gradually increased when taking place between phage that infect different strains or bacterial species. From an evolutionary perspective, we observed that endolysins could be naturally exchanged by homologous recombination between phages coinfecting a same bacterial strain. Furthermore, phage endolysins could adapt to their new phage/host environment by acquiring adaptative mutations. These observations highlight the remarkable ability of phage lytic systems to recombine and adapt and, therefore, explain their large diversity and mosaicism. It also indicates that evolution should be considered to act on functional modules rather than on bacteriophages themselves. Furthermore, the extensive degree of evolvability observed for phage endolysins offers new perspectives for their engineering as antimicrobial agents.

Endolysins are produced by bacteriophages to degrade the host cell wall and release new particles, but the implications of their diversity on phage-host adaptation and evolution is unknown. This study uses CRISPR-Cas9 genome editing to reveal novel insights into bacteriophage endolysin diversity and phage-bacteria interactions as well as into endolysin adaptation towards a new bacterial host.     

Diving behaviour and energetics in breeding little penguins (Eudyptula minor)

We present data on the diving behaviour and the energetics of breeding little penguins in Tasmania, Australia. Using an 18 m long still water canal in conjunction with respirometry, we determined the energy requirements while diving. Using electronic devices measuring dive depth or swimming speed, we investigated the foraging behaviour at sea. Cost of Transport was calculated to be minimal at the speed the birds prefer at sea (1.8 m/s) and averaged 11.1 J/kg/m (power requirements at that speed: 20.0 W/kg). Metabolic rate of little penguins resting in water was found to be 8.5 W/kg. The externally-attached devices had no significant influence on the energy expenditure.
Foraging trips can be divided into four distinct phases with different diving behaviours. A mean of 500 dives was executed per foraging trip lasting about 18 hours with 60% of this time being spent swimming. The total distance travelled averaged 73 km per day, although foraging range was about 12km. Mean swimming speed of little penguins at sea was 1.8 m/s, maximum swimming speed was 3.3 m/s. More than 50% of all dives had maxima not exceeding 2 m. Maximum depth reached was 27 m. Mean dive duration was 21 s. There were inter-sex differences in diving behaviour as well as changes in foraging behaviour over the breeding period. Aerobic dive limits (ADL) in the wild were estimated between 42 and 50 s. From the swim canal experiments we derived an ADL of 44 s. Total oxygen stores were calculated to be 45 ml O₂/kg. Only 2% of all dives exceeded the ADL. FMRs at sea were calculated to be between 1280 and 1500 kJ/kg/d according to chick size. The yearly food requirements of a breeding little penguin amount to 114 kg.     

Sex‐specific lateralization during aggressive interactions in breeding king penguins

Brain and behavioral asymmetries (termed "lateralization"; e.g., preferential eye‐use) have been mostly described in controlled laboratory conditions, although striking similarities of hemispheric brain control for specific behaviors have also been shown in the wild. Visual lateralization may provide ecological advantages by allowing complementary roles played by the left–right lateral and frontal visual field in distant or close motion detection of predators or other threats. In this study, we tested for lateralization in aggressive behavior in wild king penguins (Aptenodytes patagonicus), seabirds breeding in a context of strong colonial aggressiveness, and subject to on‐land‐based predation of their egg or chick. We show that males initiated more agonistic interactions when a congener was located in their right frontal visual field and in their left lateral visual field. The results obtained in females were the exact opposite for each subdivision of their visual fields. Complementary lateralization in male and female penguins may be part of a more general phenomenon, allowing partners to coordinate their behavior during reproduction. This may be especially true during the period of courtship, during which these seasonally monogamous and monomorphic seabirds engage in mutual mate choice based on a complex and ritualized display of ornaments located on the left and right lateral sides of the head. Those results open exciting questions as to whether hemispheric control of aggression is a commonly selected phenotypic trait across colonial seabirds.     

Testing habitat copying in breeding habitat selection in a species adapted to variable environments

The habitat copying hypothesis states that animals use the reproductive performance of conspecifics to evaluate habitat quality and choose their future breeding site. We used data from Audouin's Gull Larus audouinii (1992–2003), a species adapted to unpredictable environments, to analyse subcolony (as patch) choice within a colony (small spatial scale). We also assessed the suitability of alternative hypotheses to the habitat copying hypothesis. The probability of subcolonies being reoccupied annually increased with their size (as number of nests), which suggests the existence of group adherence effects. Subcolony growth rate was related to its average reproductive success (or patch reproductive success) in the previous year: the higher the reproductive success in a colony, the higher the probability of growth the following year. However, this last result was obtained without considering the effect of colony size on the response variable because colony size is related to it. Therefore, results suggest at the population level that in this system habitat copying might either be one of the strategies used by the species in selecting its breeding habitat, or one of the possible strategies operating alone. The other strategies are group adherence mechanisms, and also the effect of conspecific attraction. At the individual level we failed to find evidence of habitat copying and only the previous success of an individual affected its fidelity to a subcolony. The importance of the lack of environmental predictability in the system is discussed, as predictability is a prerequisite of habitat copying.     

Population dynamics in a long-lived seabird: I. Impact of breeding activity on survival and breeding probability in unbanded king penguins

Understanding the trade-off between current reproductive effort, future survival and future breeding attempts is crucial for demographic analyses and life history studies. We investigated this trade-off in a population of king penguins (Aptenodytes patagonicus) marked individually with transponders using multistate capture-recapture models. This colonial seabird species has a low annual proportion of non-breeders (13%), despite a breeding cycle which lasts over 1 year. To draw inferences about the consequences of non-breeding, we tested for an effect of reproductive activity on survival and on the probability of subsequent breeding. We found that birds non-breeding in year t show the same survival rate as breeders (two-states analysis: breeding and non-breeding). However, breeders had a lower probability of breeding again the following year. This negative phenotypic correlation suggests the existence of reproductive costs affecting future breeding probability, but it might also be strengthened by late arrival for courtship in year t. A three-state analysis including breeding success revealed that failed breeders in year t have a lower probability to reproduce successfully in year t + 1 than non-breeders in year t, providing some evidence for the existence of reproductive costs. Moreover, successful breeders showed higher survival probability. This positive phenotypic correlation between current reproduction and subsequent survival supports the hypothesis of an heterogeneity in individual quality. Males breeding in year t had a lower probability to breed again in year t + 1 than females, suggesting higher reproductive costs for this sex. Such additional costs might be due to higher male parental investment in the final phase of chick-rearing, which also delays the arrival of males in year t + 1, and decreases their breeding probability. Our study is the first to explore the breeding biology and the demography of penguins without the disturbance of flipper-bands.