Genetic isolation and divergence in sexual traits: evidence for the northern rockhopper penguin Eudyptes moseleyi being a sibling species

The taxonomic status of populations of rockhopper penguins (Eudyptes chrysocome) is still enigmatic. Northern populations differ from southern ones in breeding phenology, song characteristics and head ornaments used as mating signals. We conducted a molecular analysis using mitochondrial DNA sequencing to test if there is a gene flow barrier between northern (subtropical) populations and southern (subantarctic) populations in relation to the Subtropical Convergence, a major ecological boundary for marine organisms. Sequences of the control region and the ND2 gene were analysed in rockhopper penguins and in the macaroni penguin (Eudyptes chrysolophus), a closely related species. Genetic distances and phylogenetic analyses showed a clear split into three clades, two rockhopper clades and the macaroni penguin. Moreover, Theta(ST) and gene flow estimates also suggested genetic structuring within the northern rockhoppers. Our results add further support to the notion that the two rockhopper penguin taxa, often considered as two subspecies, can be recognized as two species E. chrysocome and E. moseleyi. The divergence in mating signals found between these two taxa seems to have occurred recently and relatively rapidly. Thus, the behavioural changes may have been enough to isolate these taxa without the need for morphological differentiation. The findings have important conservational implications, since E. moseleyi is far less abundant than E. chrysocome, but more populations may warrant an uplisting to endangered status if full species status should be recognized for more subpopulations.     

Speciation chronology of rockhopper penguins inferred from molecular, geological and palaeoceanographic data

Aim The Southern Ocean is split into several biogeographical provinces between convergence zones that separate watermasses of different temperatures. Recent molecular phylogenies have uncovered a strong phylogeographic structure among rockhopper penguin populations, Eudyptes chrysocome sensu lato, from different biogeographical provinces. These studies suggested a reclassification as three species in two major clades, corresponding, respectively, to warm, subtropical and cold sub‐Antarctic watermasses rather than to geographic proximity. Such a phylogeographic pattern, also observed in plants, invertebrates and fishes of the Southern Ocean, suggests that past changes in the positions of watermasses may have affected the evolutionary history of penguins. We calculated divergence times among various rockhopper penguin clades and calibrated these data with palaeomagmatic and palaeoceanographic events to generate a speciation chronology in rockhopper penguins. Location Southern Ocean. Methods Divergence times between populations were calculated using five distinct mitochondrial DNA loci, and assuming a molecular clock model as implemented in mdiv . The molecular evolution rate of rockhopper penguins was calibrated using the radiochronological age of St Paul Island and Amsterdam Island in the southern Indian Ocean. Separations within other clades were correlated with palaeoceanographic data using this calibrated rate. Results The split between the Atlantic and Indian populations of rockhopper penguins was dated as 0.25 Ma, using the date of emergence of St Paul and Amsterdam islands, and the divergence between sub‐Antarctic and subtropical rockhopper penguins was dated as c. 0.9 Ma (i.e. during the mid‐Pleistocene transition, a major change in the Earth’s climate cycles). Main conclusions The mid‐Pleistocene transition is known to have caused a major southward shift in watermasses in the Southern Ocean, thus changing the environment around the northernmost rockhopper penguin breeding sites. This ecological isolation of northernmost populations may have caused vicariant speciation, splitting the species into two major clades. After the emergence of St Paul and Amsterdam islands in the subtropical Indian Ocean 0.25 Ma, these islands were colonized by penguins from the subtropical Atlantic, 6000 km away, rather than by penguins from the sub‐Antarctic Indian Ocean, 5000 km closer.     

Aspects of the breeding biology of the southern rockhopper penguin <Emphasis Type="Italic">Eudyptes c. chrysocome</Emphasis> and new consideration on the intrinsic capacity of the A-egg

The rockhopper penguins Eudyptes chrysocome have recently been split into the northern E. moseleyi and the southern E. chrysocome rockhopper penguin. It is therefore crucial to have a comprehensive understanding of the biology of each species in order to develop appropriate conservation measures. We investigated the breeding biology of the southern rockhopper on New Island, in the western part of the Falklands Islands, by following the breeding attempt of 160 pairs during the 2006/2007 season and examining the effect of lay time and colony habitat on breeding success. Specifically, we compared survival and growth parameters between A- and B-eggs and chicks from non-manipulated and artificially manipulated nests to investigate why southern rockhopper penguins in the Falkland Islands are more able to fledge an A-egg (first laid) than conspecifics elsewhere. Breeding was highly synchronous, with no significant difference in the breeding success between early and late breeders or between pairs breeding in different habitats. We demonstrate for the first time that the A-egg produced by the southern rockhopper penguin has, when alone, the same theoretical intrinsic potential to lead to a fledged chick as the B-egg. In contrast, the hatching success and survival of the B-chick was similar when alone or in a two-egg clutch.     

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.     

Geographical variation in egg size dimorphism in rockhopper penguins

All crested penguins present a unique reversed hatching asynchrony: the larger second-laid egg (B-egg) hatches before the smaller first-laid egg (A-egg). Although both eggs often hatch, the A-chick generally dies of starvation within days after hatching. However, within rockhopper penguins, the population at the Falkland Islands is unique in that some birds manage to raise both chicks. Although it has been suggested that the egg size dimorphism between A- and B-eggs may explain how long both eggs and chicks survive, this hypothesis has never been explicitly tested. We expect that both eggs are retained longer in the less dimorphic clutches than in the more dimorphic ones. In this paper, we have compiled egg measurements for three rockhopper penguin species (Eudyptes chrysocome, E. filholi and E. moseleyi) in order to compare the intra-clutch egg size dimorphism among these species. Furthermore, we have collected new data to compare egg size dimorphism between two populations of E. chrysocome (Falkland Islands versus Staten Island). A-egg volumes are more variable between species and populations than B-egg volumes. E. chrysocome and especially the population from the Falkland Islands produces the largest A-eggs and the least dimorphic eggs. Nevertheless, as differences in A-egg volumes between species and between the populations of Falkland Islands and Staten Island are stronger and more significant than differences in egg dimorphism, we suggest that A-egg volume, more than egg dimorphism, could be one of the factors influencing the prevalence of twins. A large A-egg and/or reduced egg dimorphism is probably necessary to enable rockhopper penguins to raise two chicks, but other reasons may also be involved which enable them to keep both eggs and chicks.     

A northern rockhopper penguin unveils dispersion pathways in the Southern Ocean

We report the first record of a northern rockhopper penguin Eudyptes moseleyi on the Kerguelen Islands, Southern Indian Ocean. The penguin must have crossed the subtropical convergence to reach the island. This species was recently proved to be genetically different from the subantarctic eastern rockhopper penguin E. filholi that normally breeds on the Kerguelen Islands. The sequencing of a part of the mitochondrial control region shows that this bird may come from the population of Gough Island, 6,000 km away, in the south Atlantic Ocean. This finding confirms that the genetic isolation between these two penguin species is complete, although some individuals may sporadically disperse between the breeding sites. This first direct observation of a disperser from the Atlantic to the Indian Ocean also adds further support to a biogeographic dispersion pattern already suggested by phylogeographic patterns in other species from the Southern Ocean.     

Stable isotopes in southern rockhopper penguins: foraging areas and sexual differences in the non-breeding period

Southern rockhopper penguins (Eudyptes chrysocome chrysocome) have experienced severe population declines across their distribution area, potentially in response to bottom-up effects following elevated sea surface temperatures, changes in the food web and prey availability. We conducted stable isotope analysis to compare trophic levels and distribution patterns in the non-breeding period over three consecutive years, and between males and females, using egg membranes, blood cells and feathers of parent birds. Tissues representing the non-breeding season had lower ??¹³C values than prey sampled around the Falklands and red blood cells from breeding rockhopper penguins. In contrast, ??¹⁵N values were higher in red blood cells from the end of winter compared to those from the breeding season and compared to feathers. This indicated that rockhopper penguins left the Falkland Island area in the non-breeding season and foraged either around Burdwood Bank further south, or over the Patagonian Shelf. In winter, only males took more prey of higher trophic level than females. Inter-annual differences in isotopic values partly correlated with sea surface temperatures. However, as prey isotope samples were collected only in 1?year, inter-annual differences in penguin isotopic values may result from different foraging sites, different prey choice or different isotopic baseline values. Our study highlights the potential for stable isotope analyses to detect seasonal and gender-specific differences in foraging areas and trophic levels, while stressing the need for more sampling of isotopic baseline data.     

Morphological aspects of the heart of the northern rockhopper penguin (Eudyptes chrysocome moseleyi ): possible implication in diving behavior and ecology?

We compared the heart morphology of the small, deep-diving northern rockhopper penguin to the hearts of small, shallow-diving and large, deep-diving penguin species. The rockhopper penguin had a heart larger than expected for its body mass, and its heart weight/body weight was significantly greater than in the larger Adélie penguin. We found the rockhopper's right ventricle weight/heart weight to be significantly greater than this relationship in both the larger chinstrap and Adélie penguins. The relationship of the right to left ventricular weights in the rockhopper heart is not different to that of the large, deepest-diving emperor penguin. A larger heart in the rockhopper penguin might be related to its diving behavior and ecology if it contributes to diving efficiency during foraging by increasing lung perfusion during surface recovery. This would lead to decreased surface time. Accepted: 20 May 2000     

Potential for redistribution of post-moult habitat for Eudyptes penguins in the Southern Ocean under future climate conditions

Anthropogenic climate change is resulting in spatial redistributions of many species. We assessed the potential effects of climate change on an abundant and widely distributed group of diving birds, Eudyptes penguins, which are the main avian consumers in the Southern Ocean in terms of biomass consumption. Despite their abundance, several of these species have undergone population declines over the past century, potentially due to changing oceanography and prey availability over the important winter months. We used light-based geolocation tracking data for 485 individuals deployed between 2006 and 2020 across 10 of the major breeding locations for five taxa of Eudyptes penguins. We used boosted regression tree modelling to quantify post-moult habitat preference for southern rockhopper (E. chrysocome), eastern rockhopper (E. filholi), northern rockhopper (E. moseleyi) and macaroni/royal (E. chrysolophus and E. schlegeli) penguins. We then modelled their redistribution under two climate change scenarios, representative concentration pathways RCP4.5 and RCP8.5 (for the end of the century, 2071–2100). As climate forcings differ regionally, we quantified redistribution in the Atlantic, Central Indian, East Indian, West Pacific and East Pacific regions. We found sea surface temperature and sea surface height to be the most important predictors of current habitat for these penguins; physical features that are changing rapidly in the Southern Ocean. Our results indicated that the less severe RCP4.5 would lead to less habitat loss than the more severe RCP8.5. The five taxa of penguin may experience a general poleward redistribution of their preferred habitat, but with contrasting effects in the (i) change in total area of preferred habitat under climate change (ii) according to geographic region and (iii) the species (macaroni/royal vs. rockhopper populations). Our results provide further understanding on the regional impacts and vulnerability of species to climate change.     

A comprehensive demographic assessment of the endangered Fiordland crested penguin Eudyptes pachyrhynchus

ABSTRACT

Many species of Eudyptes penguin have shown substantial population declines and in response, there have been efforts to identify the key demographic parameters. Here, we present the demographic parameters of one of the least well known and the least abundant species of crested penguin, the endangered Fiordland crested penguin Eudyptes pachyrhynchus. A population study incorporating mark–recapture, nest occupancy and breeding success was conducted over 16 years at several sites in the northern half of the range of the species. Survival probabilities were calculated using standard Cormack–Jolly–Seber models and the Burnham Live and Dead model. The annual probability of true survival for banded birds and apparent survival for birds with transponders were both estimated at 89% during their adult years, which is similar to that reported for Eudyptes penguin species inhabiting more southerly latitudes. Annual juvenile survival was assessed for Fiordland crested penguins until their first return at 77%. The mean breeding success (0.61?±?0.02 chicks/pair) was higher than is observed for other crested penguin species, except the southern rockhopper penguin, which may be due to having lower A-egg ejection rates and higher rates of fledging two chicks per pair. Breeding success was related to the niche of predators present.     

Few genetic differences between Victorian and Western Australian blue penguins,Eudyptula minor

Abstract

Blue penguins, Eudyptula minor, breeding on Penguin Island, Western Australia are considerably larger than other blue penguins in Australia. If genetic isolation is the cause, it may have implications for the conservation status of some blue penguin populations. We compared the sequences of two mitochondrial gene regions (cytochrome‐b and the control region) from Western Australian blue penguins with other populations of blue penguins from Australia and New Zealand. We found few differences between sequences from Western Australia, Phillip Island, Victoria and Otago, New Zealand, although all three differed considerably from other New Zealand blue penguins. Sequences for the control region from the Western Australian blue penguins and 30 more birds breeding at various Australasian sites provided further support for two major clades within Eudyptula; an Australian clade (including Otago) and a New Zealand clade.     

Population trends, breeding success and diet composition of gentoo Pygoscelis papua, magellanic Spheniscus magellanicus and rockhopper Eudyptes chrysocome penguins in the Falkland Islands. A review

Data on population size, breeding success and diet composition of gentoo (Pygoscelis papua), magellanic (Spheniscus magellanicus) and rockhopper (Eudyptes chrysocome) penguins, collected as part of the Falkland Island Seabird Monitoring Programme from 1986/1987 to 1998/1999, were analysed with regard to spatial and temporal variation, as well as potential interaction with local commercial fisheries. No significant population trends were detectable, mainly because of the short time-series and large spatial and inter-annual variation in the number of breeding pairs in the colonies monitored. However, the breeding success of all three penguin species has improved slightly over the last few years, indicating a potential for increasing populations in the near future. During the breeding season, all three penguin species preyed opportunistically on a mixture of fish, squid and crustaceans. Diet composition too showed a high degree of spatial and temporal variation. However, in all three penguin species studied, squid gradually disappeared from the diet over successive years, to be replaced by fish. Coincidentally, the commercial catches of the squid species Loligo gahi in Falkland Islands waters decreased and the by-catch of nototheniid fish increased. All three penguin species compete directly with the commercial fishing fleet for L. gahi; however, there may also be competition for Patagonian toothfish (Dissostichus eleginoides), hake (Merluccius sp.) and southern blue whiting (Micromesistius australis), because juveniles of these species were found regularly in penguin diets.     

New records of South American sea lion <Emphasis Type="Italic">Otaria flavescens</Emphasis> predation on southern rockhopper penguins <Emphasis Type="Italic">Eudyptes chrysocome</Emphasis> at Staten Island,Argentina

Predation by fur seals and sea lions has been identified, among others, as a potential cause of the declines in rockhopper penguin populations. Here, we report a multiple predation event of southern rockhopper penguins Eudyptes chrysocome by South American sub-adult male sea lions Otaria flavescens at Staten Island, Argentina. The sea lions attacked and preyed on penguins mostly using a wait and rush tactic at sea, but in some cases, penguins were also pursued on land. Although observations suggested that only a few sea lions are involved in predation, further research is necessary to elucidate the importance of this predation in the rate of population decline.     

Breeding ecology of the gentoo penguin <Emphasis Type="Italic">Pygoscelis papua</Emphasis> at Kerguelen Archipelago

The gentoo penguin (Pygoscelis papua) is one of the most widespread penguin species and has been proven to be highly plastic in many aspects of its ecology. However, data from their sub-Antarctic range suggest an unexplained decline of their populations over the last 10–20 years, stressing the need for additional knowledge on their breeding ecology and demography. The present study provides insights into the breeding ecology of the gentoo penguin at a major breeding site, Kerguelen Archipelago, over three breeding seasons (1987, 2002 and 2003). Similarly to other northern populations, gentoo penguins breeding at Kerguelen exhibited winter laying, slow provisioning rate, slow growth rate associated with an extended rearing period and relatively low breeding success compared to southern populations. Our study also revealed interannual differences in the timing of laying and growth parameters as well as unusual sex differences in parental investment. Despite their high plasticity, there are indications that gentoo penguins at the northern edge of their range might work at the upper limit of their capacities. Sub-Antarctic populations would, therefore, be more sensitive to environmental changes than more southerly ones and need to be closely monitored.     

Dynamics of antarctic penguin populations in relation to inter-annual variability in sea ice distribution

To investigate the role of sea ice cover on penguin populations we used principal component analysis to compare population variables of Adélie (Pygoscelis adeliae) and chinstrap (Pygoscelis antarctica) penguins breeding on Signy Island, South Orkney Islands with local (from direct observations) and regional (from remote sensing data) sea ice variables. Throughout the study period, the Adélie penguin population size remained stable, whereas that of chinstrap penguins decreased slightly. For neither species were there significant relationships between population size and breeding success, except for an apparent inverse density-dependent relationship between the number of Adélie breeding pairs and the number of eggs hatching. For both species, no general relationship was found between either population size or breeding success and the local sea ice conditions. However, the regional sea ice extent at a particular time prior to the start of the breeding season was related to the number of birds that arrived to breed. For both species, this period occurred before the sea ice reached its maximum extent and was slightly earlier for Adélie than for chinstrap penguins. These results suggest that sea ice conditions outside the breeding season may play an important role in penguin population processes.     

Pasteurella multocida infections in rockhopper penguins (Eudyptes chrysocome) from Campbell Island, New Zealand

During an investigation into the population decline of rockhopper penguins (Eudyptes chrysocome) on Campbell Island, New Zealand, avian cholera (Pasteurella multocida) was found in dead adults and chicks. An RNA enveloped virus was isolated from Ixodes uriae, a tick which commonly parasitizes rockhopper penguins on the island. It is not known whether this virus is virulent for penguins. No evidence was obtained to suggest that avian cholera was the principal cause for the decline in the rockhopper penguin population.     

The double vocal signature of crested penguins: is the identity coding system of rockhopper penguins Eudyptes chrysocome due to phylogeny or ecology?

Parent-offspring recognition systems are used in bird colonies to avoid misdirected parental care. In penguins, where the risk of confusion is particularly high, recognition is achieved by acoustic signals that constitute highly efficient vocal signatures. Comparisons between species from the Pygoscelis and Aptenodytes genera have revealed interspecific differences on the encoding of information within the signatures which correlate with the presence/absence of nests in the colonies. However a recent study of individual recognition in macaroni penguins Eudyptes chrysolophus revealed diversity within nest-building species. This paper investigates whether the original and intermediate signature system found in macaroni penguins is shared by another species of Eudyptes , the rockhopper penguin E. chrysocome . Vocal signatures of rockhopper penguins were analysed and compared to macaroni penguins'. We used a methodology derived from the theory of information to determine which parameters of the call were likely to encode individual identity. Playbacks of modified calls in the field complemented the analyses, and parent-chick reunions were compared between the two species. Our results reveal a similar double signature system within the Eudyptes genus, which integrates information simultaneously from the temporal and spectral domains. This double encoding is made through the tempo given by the successive syllables of the call and the harmonic content of the call. While it confirms the hypothesis that signatures are simpler in nest-building species, this result reveals differences in the efficacies of signatures within this category. This suggests that other parameters such as the mean distance recognition should be considered to account for the differences in the encoding of the vocal signatures and in their resulting efficacies.     

Energy requirements for growth and maintenance in macaroni and rockhopper Penguins

Summary Energy requirements for growth and maintenance of macaroni and rockhopper penguin chicks at Marion Island, southern Indian Ocean, were estimated from rates of oxygen consumption and body composition analysis. Mass-specific energy expenditures of both species increased to levels 1.5 times that of hatchlings within 14–21 days of hatching and subsequently decreased. Lipid was initially accumulated slowly but the rate of accumulation increased after 30 days of age when male parents joined the females in feeding the chicks. Lipid, however, decreased markedly after 45 days of age and was presumably metabolized. Protein was laid down throughout the growth period, but doubled its initial rate of accumulation between 22 and 35 days of age. Thereafter the rate decreased until independence. Daily energy requirements of macaroni and rockhopper penguins increased from 417 and 211 kJ d^-1, respectively, in the first week after hatching to peaks of 1540 and 1170 kJ d^-1 about halfway through the growth period before decreasing until independence. Total energy requirement for growth and maintenance was estimated to be 76200 kJ for macaroni penguins and 59400 kJ for rockhopper penguins, of which growth energy comprised 38% and 28%, respectively. Based on the energy requirements and population data, macaroni and rockhopper penguin chicks at Marion Island consume an estimated 4200 and 700 t of food, respectively, each year.     

Both natural selection and isolation by distance explain phenotypic divergence in bill size and body mass between South Australian little penguin colonies

Morphological variation between populations of the same species can arise as a response to genetic variation, local environmental conditions, or a combination of both. In this study, I examined small‐scale geographic variation in bill size and body mass in little penguins (Eudyptula minor) across five breeding colonies in South Australia separated by <150 km. To help understand patterns driving the differences, I investigated these variations in relation to environmental parameters (air temperature, sea surface temperature, and water depth) and geographic distances between the colonies. I found substantial morphological variation among the colonies for body mass and bill measurements (except bill length). Colonies further located from each other showed greater morphological divergence overall than adjacent colonies. In addition, phenotypic traits were somewhat correlated to environmental parameters. Birds at colonies surrounded by hotter sea surface temperatures were heavier with longer and larger bills. Birds with larger and longer bills were also found at colonies surrounded by shallower waters. Overall, the results suggest that both environmental factors (natural selection) and interpopulation distances (isolation by distance) are causes of phenotypic differentiation between South Australian little penguin colonies.     

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