Receding ice drove parallel expansions in Southern Ocean penguins.

Climate shifts are key drivers of ecosystem change. Despite the critical importance of Antarctica and the Southern Ocean for global climate, the extent of climate-driven ecological change in this region remains controversial. In particular, the biological effects of changing sea ice conditions are poorly understood. We hypothesize that rapid postglacial reductions in sea ice drove biological shifts across multiple widespread Southern Ocean species. We test for demographic shifts driven by climate events over recent millennia by analyzing population genomic datasets spanning 3 penguin genera (Eudyptes, Pygoscelis, and Aptenodytes). Demographic analyses for multiple species (macaroni/royal, eastern rockhopper, Adélie, gentoo, king, and emperor) currently inhabiting southern coastlines affected by heavy sea ice conditions during the Last Glacial Maximum (LGM) yielded genetic signatures of near-simultaneous population expansions associated with postglacial warming. Populations of the ice-adapted emperor penguin are inferred to have expanded slightly earlier than those of species requiring ice-free terrain. These concerted high-latitude expansion events contrast with relatively stable or declining demographic histories inferred for 4 penguin species (northern rockhopper, western rockhopper, Fiordland crested, and Snares crested) that apparently persisted throughout the LGM in ice-free habitats. Limited genetic structure detected in all ice-affected species across the vast Southern Ocean may reflect both rapid postglacial colonization of subantarctic and Antarctic shores, in addition to recent genetic exchange among populations. Together, these analyses highlight dramatic, ecosystem-wide responses to past Southern Ocean climate change and suggest potential for further shifts as warming continues.

Dispersal in the sub-Antarctic: king penguins show remarkably little population genetic differentiation across their range.

BACKGROUND: Seabirds are important components of marine ecosystems, both as predators and as indicators of ecological change, being conspicuous and sensitive to changes in prey abundance. To determine whether fluctuations in population sizes are localised or indicative of large-scale ecosystem change, we must first understand population structure and dispersal. King penguins are long-lived seabirds that occupy a niche across the sub-Antarctic zone close to the Polar Front. Colonies have very different histories of exploitation, population recovery, and expansion. RESULTS: We investigated the genetic population structure and patterns of colonisation of king penguins across their current range using a dataset of 5154 unlinked, high-coverage single nucleotide polymorphisms generated via restriction site associated DNA sequencing (RADSeq). Despite breeding at a small number of discrete, geographically separate sites, we find only very slight genetic differentiation among colonies separated by thousands of kilometers of open-ocean, suggesting migration among islands and archipelagos may be common. Our results show that the South Georgia population is slightly differentiated from all other colonies and suggest that the recently founded Falkland Island colony is likely to have been established by migrants from the distant Crozet Islands rather than nearby colonies on South Georgia, possibly as a result of density-dependent processes. CONCLUSIONS: The observed subtle differentiation among king penguin colonies must be considered in future conservation planning and monitoring of the species, and demographic models that attempt to forecast extinction risk in response to large-scale climate change must take into account migration. It is possible that migration could buffer king penguins against some of the impacts of climate change where colonies appear panmictic, although it is unlikely to protect them completely given the widespread physical changes projected for their Southern Ocean foraging grounds. Overall, large-scale population genetic studies of marine predators across the Southern Ocean are revealing more interconnection and migration than previously supposed.

Transcriptome analysis in non-model species: a new method for the analysis of heterologous hybridization on microarrays.

BACKGROUND: Recent developments in high-throughput methods of analyzing transcriptomic profiles are promising for many areas of biology, including ecophysiology. However, although commercial microarrays are available for most common laboratory models, transcriptome analysis in non-traditional model species still remains a challenge. Indeed, the signal resulting from heterologous hybridization is low and difficult to interpret because of the weak complementarity between probe and target sequences, especially when no microarray dedicated to a genetically close species is available. RESULTS: We show here that transcriptome analysis in a species genetically distant from laboratory models is made possible by using MAXRS, a new method of analyzing heterologous hybridization on microarrays. This method takes advantage of the design of several commercial microarrays, with different probes targeting the same transcript. To illustrate and test this method, we analyzed the transcriptome of king penguin pectoralis muscle hybridized to Affymetrix chicken microarrays, two organisms separated by an evolutionary distance of approximately 100 million years. The differential gene expression observed between different physiological situations computed by MAXRS was confirmed by real-time PCR on 10 genes out of 11 tested. CONCLUSIONS: MAXRS appears to be an appropriate method for gene expression analysis under heterologous hybridization conditions.

How slow breeding can be selected in seabirds: testing Lack's hypothesis.

The historical debate of the 1960s between group and individual selection hinged on how the slow breeding of seabirds could be explained. While this debate was settled by the ascendance of individual selection, championed by David Lack, explanations for slow breeding in seabirds remain to be tested. We examined the slowest breeding of these birds, the albatrosses and petrels (order Procellariiformes), using analyses that statistically controlled for variations in body size and phylogeny. Incubation and fledging periods appeared strongly correlated, but this turned out to be largely explained by phylogeny. Nonetheless, developmental and reproductive rates were associated with the distance to the foraging range, as predicted under the hypothesis of ecological constraints on breeding pairs, and these results were independent of body size and phylogeny. Slower breeding in these seabirds appeared associated with the rigors of farther pelagic feeding, as Lack originally hypothesized.

Mother Vocal Recognition in Antarctic Fur Seal Arctocephalus gazella Pups: A Two-Step Process.

In otariids, mother's recognition by pups is essential to their survival since females nurse exclusively their own young and can be very aggressive towards non-kin. Antarctic fur seal, Arctocephalus gazella, come ashore to breed and form dense colonies. During the 4-month lactation period, females alternate foraging trips at sea with suckling period ashore. On each return to the colony, females and pups first use vocalizations to find each other among several hundred conspecifics and olfaction is used as a final check. Such vocal identification has to be highly efficient. In this present study, we investigated the components of the individual vocal signature used by pups to identify their mothers by performing playback experiments on pups with synthetic signals. We thus tested the efficiency of this individual vocal signature by performing propagation tests and by testing pups at different playback distances. Pups use both amplitude and frequency modulations to identify their mother's voice, as well as the energy spectrum. Propagation tests showed that frequency modulations propagated reliably up to 64m, whereas amplitude modulations and spectral content greatly were highly degraded for distances over 8m. Playback on pups at different distances suggested that the individual identification is a two-step process: at long range, pups identified first the frequency modulation pattern of their mother's calls, and other components of the vocal signature at closer range. The individual vocal recognition system developed by Antarctic fur seals is well adapted to face the main constraint of finding kin in a crowd.

Color ornaments and territory position in king penguins.

King penguins exhibit mutual color ornamentation of feathers and beak color. They breed in dense colonies and produce a single chick every 2 years. Thus, males and females must choose partners carefully to be reproductively successful, and auricular patches of males and UV coloration of beak spots have been shown to influence mate choice. Position in the breeding colony is also important to reproductive success, with pairs on the edge of the colony less successful than those in the center. We studied the mutual ornaments, individual condition, and position of pairs in their breeding colony. Males were significantly larger than females in size, body mass, and auricular patch size. Within pairs, auricular patch size of males and females were significantly correlated, and male auricular patch size and body mass were significantly associated, suggesting a link between this ornament and male body condition. Moving from the edge to the center of the colony, pairs had larger yellow-orange auricular patches, indicating a link between this ornament and settlement in higher quality territories in the center of the colony. Pairs were also less brightly brown colored on the breast and less saturated in UV color of the beak spot. Since we observed pairs that were settling for egg laying, location in the colony may have reflected aspects of pair condition, rather than later jockeying for positioning using ornaments as signals of behavioral dominance.

Mother-lamb acoustic recognition in sheep: a frequency coding.

Ewes of the domestic sheep ( Ovis aries ) display selective maternal investment by restricting care to their own offspring and rejecting alien young. This trait relies on individual recognition processes between ewes and lambs. Whereas identification at the udder is only olfactory, distance recognition is performed through visual and acoustic cues. We studied the effectiveness and modalities of mutual acoustic recognition between ewes and lambs by spectrographic analysis of their vocal signatures and by playbacks of modified calls in the field. Our results show that ewes and their lambs can recognize each other based solely on their calls. The coding of identity within the vocal signatures, previously unknown in sheep, is similar in lamb and ewe: it uses the mean frequency and the spectral energy distribution of the call, namely the timbre of the call. These results point out a simple signature system in sheep that uses only the frequency domain. This engenders a signal with low information content, as opposed to some highly social birds and mammal species that may integrate information both in the temporal and spectral domains. The simplicity of this system is linked to the roles played by vision and olfaction that corroborate the information brought by the vocal signature.

Why breed every other year? The case of albatrosses.

Albatrosses exhibit extremely low reproductive rates, each pair brooding only one egg and subsequent chick at a time. Furthermore, in several of the species, the majority of successful pairs breed only once every second year (termed 'biennial' breeding). Thus, on average, these latter species have an annual fecundity of about half an offspring per year, while other albatrosses produce an egg and chick every year. Using our 40-year bank of demographic data, we compared 12 species of albatrosses according to these two breeding strategies to examine potential causes of biennial breeding. Biennial breeding could be due to physiological constraints, larger animals breeding more slowly, or ecological constraints, more distant pelagic feeding trips being energetically costly, or both. We tested these hypotheses by looking for predicted associations between the duration of the rearing period, the distance to the oceanic feeding zone and breeding frequency. We also looked for associations of these variables with other life-history traits. Body size had a strong influence on the duration of the rearing period, but not on the distance that birds travelled to the feeding zone. Both the duration of the rearing period and distance to the feeding zone appeared to have direct influences on breeding frequency, as revealed by a path analysis, and thus both hypotheses to explain biennial breeding were supported. Finally, breeding frequency exhibited a strong trade-off with adult survival and age at maturity, indicating that slower breeders live through more breeding seasons, perhaps mitigating their lower annual reproductive output.

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.

Effect of sea-ice extent on adult survival of an Antarctic top predator: the snow petrel Pagodroma nivea.

The snow petrel Pagodroma nivea is an obligate associate of sea-ice and one of the most abundant seabird species of the Southern Ocean. Time- and sex-specific annual variation in adult survival was estimated using capture-mark-recapture of petrels nesting at Pétrels Island, Terre Adélie, 1981-1997. On the basis of a regression analysis, 44% of the variation was linked inversely to the latitudinal extent of sea-ice during winter (June) in the region offshore of the study colony, where this population is likely to spend the non-breeding season. Monthly sea-surface temperature anomalies tended to influence adult survival but the relationship was not statistically significant. Why sea-ice extent should have such a critical effect on this species is yet to be explained, but the relationship, in the context of environmental warming and the consequent potential loss of Antarctic sea-ice, is an important one for this species.

Eleven polymorphic microsatellite markers in Cory's shearwater, Calonectris diomedea, and cross-species amplification on threatened Procellariiformes.

For the first time, we describe 11 variable dinucleotide microsatellites and the conditions for multiplexing and simultaneous genotyping sets of loci in Cory's shearwater, Calonectris diomedea. Microsatellite variability was assessed in a colony from the Azores archipelago (Atlantic Ocean). Two to eight alleles were detected per locus, the mean gene diversity being 4.5. Cross-species amplification in three other seabirds (Diomedea exulans, Procellaria aequinoctialis and Bulweria bulwerii) revealed some variability at one, two and eight loci, respectively.

Individual odor recognition in birds: an endogenous olfactory signature on petrels' feathers?

A growing body of evidence indicates that odors are used in individual, sexual, and species recognition in vertebrates, and may be reliable signals of quality and compatibility. Petrels are seabirds that exhibit an acute sense of smell. During the breeding period, many species of petrels live in dense colonies on small oceanic islands and form pairs that use individual underground burrows. Mates alternate between parental duties and foraging trips at sea. Returning from the ocean at night (to avoid bird predators), petrels must find their nest burrow. Antarctic prions, Pachyptila desolata, are thought to identify their nest by recognizing their partner's odor, suggesting the existence of an individual odor signature. We used gas chromatography and mass spectrometry to analyze extracts obtained from the feathers of 13 birds. The chemical profile of a single bird was more similar to itself, from year to year, than to that of any other bird. The profile contained up to a hundred volatile lipids, but the odor signature may be based on the presence or absence of a few specific compounds. Our results show that the odor signature in Antarctic prions is probably endogenous, suggesting that in some species of petrels it may broadcast compatibility and quality of potential mates.

Ultraviolet reflecting photonic microstructures in the King Penguin beak.

King and emperor penguins (Aptenodytes patagonicus and Aptenodytes forsteri) are the only species of marine birds so far known to reflect ultraviolet (UV) light from their beaks. Unlike humans, most birds perceive UV light and several species communicate using the near UV spectrum. Indeed, UV reflectance in addition to the colour of songbird feathers has been recognized as an important signal when choosing a mate. The king penguin is endowed with several highly coloured ornaments, notably its beak horn and breast and auricular plumage, but only its beak reflects UV, a property considered to influence its sexual attraction. Because no avian UV-reflecting pigments have yet been identified, the origin of such reflections is probably structural. In an attempt to identify the structures that give rise to UV reflectance, we combined reflectance spectrophotometry and morphological analysis by both light and electron microscopy, after experimental removal of surface layers of the beak horn. Here, we characterize for the first time a multilayer reflector photonic microstructure that produces the UV reflections in the king penguin beak.

How to measure information carried by a modulated vocal signature?

Acoustic signaling systems that permit individual recognition are described in an increasing number of species. Evolutionary logic predicts that the efficiency of these signatures is related to the possibilities for confusion. To test this "signature adaptation" hypothesis, one needs a standardized method to estimate and compare the efficiency of different signatures. Beecher [Am. Zool. 22, 477-490 (1989)] developed such a method by comparing scalar parameters extracted from the signals. However, vocal signatures frequently consist in the evolution of one parameter against one other, which are not comparable through Beecher's method. Here we present a method to estimate the efficiency of modulated signatures. A signature's efficiency is given by its information capacity (Hm), derived from Shannon's information theory. The measure of Hm is based on an analysis of variance and uses the Euclidian distances between the signature's contours in the population. To validate our method, simulated datasets of modulated contours were used. The predicted efficiency of those signatures, estimated from Hm, was strongly correlated to its actual efficiency given by two classification methods: a discriminant analysis and a classification by human observers. Being also untied to sample size, Hm therefore allows comparing objectively vocal, but also visual and olfactory signatures.

Localisation of an acoustic signal in a noisy environment: the display call of the king penguin Aptenodytes patagonicus.

King penguin chicks identify their parents by an acoustic signal, the display call. This call consists of a succession of similar syllables. Each syllable has two harmonic series, strongly modulated in frequency and amplitude, with added beats of varying amplitude generated by a two-voice system. Previous work showed that only one syllable of the call is needed for the chick to identify the calling adult. Both the frequency modulation pattern of the syllable and the two-voice system play a role in the call identification. The syllabic organisation of the call, the harmonic structure and the amplitude modulations of the syllables apparently do not contribute to individual recognition. Are these acoustic features useless? To answer to this question, playback experiments were conducted using three categories of experimental signals: (i) signal with only the fundamental frequencies of the natural call, (ii) signal with the amplitude of each syllable kept at a constant level and (iii) signals with only one syllable, repeated or not. The responses of chicks to these experimental signals were compared to those obtained with the calls of their natural parents. We found that these acoustic features, while not directly implicated in the individual recognition process, help the chicks to better localise the signal of their parents. In addition, the redundant syllabic organisation of the call is a means of counteracting the masking effect of the background noise of the colony.

How does a fur seal mother recognize the voice of her pup? An experimental study of Arctocephalus tropicalis.

In the subantarctic fur seal Arctocephalus tropicalis, mothers leave their pups during the rearing period to make long and frequent feeding trips to sea. When a female returns from the ocean, she has to find her pup among several hundred others. Taking into account both spectral and temporal domains, we investigated the individual vocal signature occurring in the 'female attraction call' used by pups to attract their mother. We calculated the intra- and inter-individual variability for each measured acoustic cue to isolate those likely to contain information about individual identity. We then tested these cues in playback experiments. Our results show that a female pays particular attention to the lower part of the signal spectrum, the fundamental frequency accompanied by its first two harmonics being sufficient to elicit reliable recognition. The spectral energy distribution is also important for the recognition process. Of the temporal features, frequency modulation appears to be a key component for individual recognition, whereas amplitude modulation is not implicated in the identification of the pup's voice by its mother. We discuss these results with respect to the constraints imposed on fur seals by a colonial way of life.

How mothers find their pups in a colony of Antarctic fur seals.

In Antarctic fur seals, Arctocephalus gazella, mothers must identify their own young among hundreds or even thousands of pups, if they are to invest in their own offspring and avoid misdirecting their parental care. When returning to their breeding colony from a foraging trip of several days at sea, mothers have to find and identify their young before suckling can occur. There appears to be little confusion about which pup belongs to a mother, and adoption is absent or rare. Using behavioral observations, we investigated the means by which female Antarctic fur seals identified their pups in a breeding colony of about 750 mother-pup pairs on Kerguelen Island. We evaluated the importance of vision, scent communication, vocalizations, and rendezvous locations as possible explanations of how mothers find their pups. Every pup that a mother examined, whether her own or not, exchanged naso-nasal inspection with her, suggesting a strong role for olfactory communication in individual recognition. Both mothers and pups called to each other, and mothers that searched for pups over a longer period gave more calls and encountered more pups. Thus, vocalizations may have been used to attract pups that might be offspring. Nursing usually occurred in the same place from the end of one maternal visit to the colony and the arrival at the beginning of the next visit, suggesting that nursing locations may serve as a meeting place, or rendezvous, for mothers and pups. These results suggest that finding pups is a two-stage process for females, in which pups for sampling are attracted by calls or examined at the previous nursing location, and then individual identification is made by olfactory cues.

Homing in pelagic birds: a pilot experiment with white-chinned petrels released in the open sea.

During the breeding period white-chinned petrels (Procellaria aequinoctialis) repeatedly perform long foraging trips in the open ocean from their breeding island, and are able to home with an astonishing precision. The orientation mechanisms involved are not yet known. By analogy with those used by desert ants moving in a similarly "featureless" environment, one can hypothesise that petrels may home using path-integration. We displaced 11 white-chinned petrels 725-785km from their burrows to the open sea, preventing them from using visual and magnetic route-based information. Three birds carried satellite transmitters. Our results showed that they can home rather efficiently in such conditions.

Evidence for nest-odour recognition in two species of diving petrel.

In nearly every procellariiform species, the sense of smell appears to be highly adapted for foraging at sea, but the sense of smell among the diving petrels is enigmatic. These birds forage at considerable depth and are not attracted to odour cues at sea. However, several procellariiform species have recently been shown to relocate their nesting burrows by scent, suggesting that these birds use an olfactory signature to identify the home burrow. We wanted to know whether diving petrels use smell in this way. We tested the common diving petrel Pelecanoides urinatrix and the South-Georgian diving petrel Pelecanoides georgicus to determine whether diving petrels were able to recognise their burrow by scent alone. To verify the efficacy of the method, we also tested a bird that is known to use olfaction for foraging and nest recognition, the thin-billed prion Pachyptila belcheri. In two-choice T-maze trials, we found that, for all species, individuals significantly preferred the odour of their own nest material to that of a conspecific. Our findings strongly suggest that an individual-specific odour provides an olfactory signature that allows burrowing petrels to recognize their own burrow. Since this ability seems to be well developed in diving petrels, our data further implicate a novel adaptation for olfaction in these two species that have been presumed to lack a well-developed sense of smell.