Developing δ15N and δ13C isoscapes using whole blood from Magellanic penguins, Spheniscus magellanicus.

RATIONALE: Understanding the migration of marine animals is hindered by the limitations of traditional tracking methods. It is therefore crucial to develop alternative methods. Stable isotope-based tracking has proven useful for this task, although it requires detailed isoscapes in the focal area. Here, we present predator-based isoscapes of the coastal zone of the Patagonian Shelf Large Marine Ecosystem (PSLME), which offers a novel tool for geolocation. METHODS: Whole-blood samples from breeding Magellanic penguins nesting at 11 colonies were used to create δ15N and δ13C isoscapes. Isotopic values were assigned to random positions inside their corresponding foraging area. Spatial analysis and data interpolation resulted in δ15N and δ13C isoscapes for the coastal zone of the PSLME, which were validated through cross-validation. RESULTS: The isoscapes mean standard error ranged from 0.05 to 0.41 for δ15N and from 0.07 to 0.3 for δ13C, similar to the error range of the mass spectrometer used for measuring isotope ratios. Predictive surfaces reflected the latitudinal trends, with δ13C and δ15N values increasing northwards. δ13C values showed a strong latitudinal gradient, while δ15N values had two distinct domains, with higher values in the north. The error surface indicated the highest certainty within 130 km from the shore and within the reported Magellanic penguin foraging areas. CONCLUSIONS: Both isoscapes revealed strong spatial variation. The δ13C isoscape showed a latitudinal gradient, consistent with patterns in other oceans. The δ15N isoscape clearly separated northern and southern colonies, likely influenced by nitrogen sources. The error obtained fell within the measurement error ranges, adding credibility to the models.

Changing course: Relocating commercial tanker lanes significantly reduces threat of chronic oiling for a top marine predator.

A goal for conservation biologists is to show that policies enacted on behalf of an imperiled species results in direct benefits for it. In Argentina, tens of thousands of Magellanic penguins (Spheniscus magellanicus) were estimated to have died from chronic oil pollution each year through the early 1980s. From 1982 to 1990, surveys at sites along approximately 900 km of Chubut Province coastline found that >60 % of penguin carcasses had evidence of oiling in some years. In response to these findings, as well as pressure from non-governmental organizations and the public, provincial and federal authorities in Chubut moved the commercial tanker lanes 20 nautical miles farther offshore in 1997 and required oil tankers to have double hulls. During a second round of surveys in 2001, using most of the same sites as the first survey period, the number of dead and oiled penguins dropped effectively to zero. A policy change not only led to fewer oiled penguins, but also likely increased the survival of adult Magellanic penguins near some of their most significant breeding colonies in Argentina.

Aspergillosis in free-ranging Magellanic penguins.

We evaluated the mortality due to aspergillosis in free-ranging Magellanic penguins during their migration and the reproductive season. A total of 98 carcasses of penguins were collected along 370 km of coastline in Southern Brazil, between June 2017 and October 2019, and from reproductive colonies in Patagonian Argentina, in January 2019. All animals were necropsied, and only proven cases were computed. Aspergillosis was diagnosed in 2.5% of the penguins evaluated during their migration route. Our study, of the Southern coast of Brazil, is the first to demonstrate that aspergillosis is an important cause of mortality in free-ranging penguins. The implications of these findings in the One Health context are discussed.

We evaluated the mortality due to aspergillosis in free-ranging Magellanic penguins during their migration and the reproductive season. The mortality rate of penguins was 2.5% during their migration route. Our study is the first to demonstrate aspergillosis as an important cause of mortality in free-ranging penguins.

Metapopulation dynamics and foraging plasticity in a highly vagile seabird, the southern rockhopper penguin.

Population connectivity is driven by individual dispersal potential and modulated by natal philopatry. In seabirds, high vagility facilitates dispersal yet philopatry is also common, with foraging area overlap often correlated with population connectivity. We assess the interplay between these processes by studying past and current connectivity and foraging niche overlap among southern rockhopper penguin colonies of the coast of southern South America using genomic and stable isotope analyses. We found two distinct genetic clusters and detected low admixture between northern and southern colonies. Stable isotope analysis indicated niche variability between colonies, with Malvinas/Falklands colonies encompassing the species entire isotopic foraging niche, while the remaining colonies had smaller, nonoverlapping niches. A recently founded colony in continental Patagonia differed in isotopic niche width and position with Malvinas/Falklands colonies, its genetically identified founder population, suggesting the exploitation of novel foraging areas and/or prey items. Additionally, dispersing individuals found dead across the Patagonian shore in an unusual mortality event were also assigned to the northern cluster, suggesting northern individuals reach southern localities, but do not breed in these colonies. Facilitated by variability in foraging strategies, and especially during unfavorable conditions, the number of dispersing individuals may increase and enhance the probability of founding new colonies. Metapopulation demographic dynamics in seabirds should account for interannual variability in dispersal behavior and pay special attention to extreme climatic events, classically related to negative effects on population trends.

Food provisioning in Magellanic penguins as inferred from stable isotope ratios.

RATIONALE: Food provisioning is considered one of the main traits affecting offspring fitness. Differences in food provisioning between sexes, particularly in dimorphic species, could affect the amount and type of food provided, due to differences in the amount of food carried to the nest as a result of differential resources exploitation. Quantitative evidence for sexual differences in food provisioning by parents in penguins is scarce. The Magellanic penguin is moderately sexually dimorphic and breeds along a broad latitudinal range, with birds north and south of this range being essentially dietary specialists while those at intermediate latitudes consume a more diverse diet. METHODS: We used stable isotope analysis of carbon and nitrogen by isotope ratio mass spectrometry to examine if there was a differential parental contribution to chicks in ten Magellanic penguin colonies throughout its latitudinal breeding distribution. We used the heuristic Euclidean isotopic distance (ED) and individual isotope distances between the chicks and their parents as a proxy for diet similarity (the smaller the distance, the more similar the diet). RESULTS: The analysis showed that chicks tended to have a more similar diet to that of their male parent and that this pattern was more evident at colonies and in seasons where penguins had a more diverse diet, which could be explained by differences in diet between parents. Distance in δ15 N values, but not in δ13 C values, differed between both sexes and their chicks in all the pairs sampled, suggesting that δ15 N values drive the differences found in ED between chicks and their parents. CONCLUSIONS: We have developed an approach that provides the first assessment of the extent of differential food provisioning between male and female Magellanic penguins. Results suggest chicks have a diet more similar to that of their male parent, probably related to the higher trophic level of male penguin prey.

Blood-specific isotopic discrimination factors in the Magellanic penguin (Spheniscus magellanicus).

RATIONALE: The use of stable isotopes for ecological studies has increased exponentially in recent years. Isotopic trophic studies are based on the assumption that animals are what they eat plus a discrimination factor. The discrimination factor is affected by many variables and can be determined empirically. The Magellanic penguin is a highly abundant marine bird that plays a key role in the southern oceans. This study provides the first estimation of the Magellanic penguin blood discrimination factor for (13) C and (15) N. METHODS: A two and a half month feeding experiment was performed, in which ten captive penguins were fed their main natural prey (anchovy Engraulis anchoita). The discrimination factors were estimated by comparing anchovy δ(13) C and δ(15) N values (obtained with isotope ratio mass spectrometry using lipid-extracted and bulk anchovy muscle) with penguin blood δ(13) C and δ(15) N values. RESULTS: Penguin blood was shown to be enriched, compared with anchovies, for (13) C and (15) N. No changes were observed in the stable isotope ratios of anchovies and discrimination factors during the experiment. The overall discrimination factors were 0.93 ± 0.12 (bulk) and 0.41 ± 0.12 (lipid-free) for (13) C; and 2.81 ± 0.17 (bulk) and 2.31 ± 0.17 (lipid-free) for (15) N. CONCLUSIONS: Having an accurate discrimination factor for the studied species is key in any trophic or food web isotopic study. Comparisons of estimated diet-to-blood discrimination factors with published values of aquatic piscivore birds showed that the (13) C discrimination factor is particularly variable, and therefore ecologists should be cautious when using a surrogate value from other species. In this study, the Magellanic penguin discrimination factor of a tissue that does not require euthanasia was obtained, a fundamental input for trophic isotopic modeling of the species. Copyright © 2016 John Wiley & Sons, Ltd.

Contrasting patterns of selection between MHC I and II across populations of Humboldt and Magellanic penguins.

The evolutionary and adaptive potential of populations or species facing an emerging infectious disease depends on their genetic diversity in genes, such as the major histocompatibility complex (MHC). In birds, MHC class I deals predominantly with intracellular infections (e.g., viruses) and MHC class II with extracellular infections (e.g., bacteria). Therefore, patterns of MHC I and II diversity may differ between species and across populations of species depending on the relative effect of local and global environmental selective pressures, genetic drift, and gene flow. We hypothesize that high gene flow among populations of Humboldt and Magellanic penguins limits local adaptation in MHC I and MHC II, and signatures of selection differ between markers, locations, and species. We evaluated the MHC I and II diversity using 454 next-generation sequencing of 100 Humboldt and 75 Magellanic penguins from seven different breeding colonies. Higher genetic diversity was observed in MHC I than MHC II for both species, explained by more than one MHC I loci identified. Large population sizes, high gene flow, and/or similar selection pressures maintain diversity but limit local adaptation in MHC I. A pattern of isolation by distance was observed for MHC II for Humboldt penguin suggesting local adaptation, mainly on the northernmost studied locality. Furthermore, trans-species alleles were found due to a recent speciation for the genus or convergent evolution. High MHC I and MHC II gene diversity described is extremely advantageous for the long-term survival of the species.

Molecular Epidemiology of Avian Malaria in Wild Breeding Colonies of Humboldt and Magellanic Penguins in South America.

Avian malaria is a disease caused by species of the genera Haemoproteus, Leucocytozoon, and Plasmodium. It affects hundreds of bird species, causing varied clinical signs depending on the susceptibility of the host species. Although high mortality has been reported in captive penguins, limited epidemiological studies have been conducted in wild colonies, and isolated records of avian malaria have been reported mostly from individuals referred to rehabilitation centers. For this epidemiological study, we obtained blood samples from 501 adult Humboldt and 360 adult Magellanic penguins from 13 colonies throughout South America. To identify malaria parasitaemia, we amplified the mtDNA cytochrome b for all three parasite genera. Avian malaria was absent in most of the analyzed colonies, with exception of the Punta San Juan Humboldt penguin colony, in Peru, where we detected at least two new Haemoproteus lineages in three positive samples, resulting in a prevalence of 0.6% for the species. The low prevalence of avian malaria detected in wild penguins could be due to two possible causes: A low incidence, with high morbidity and mortality in wild penguins or alternatively, penguins sampled in the chronic stage of the disease (during which parasitaemia in peripheral blood samples is unlikely) would be detected as false negatives.

N-dimensional animal energetic niches clarify behavioural options in a variable marine environment.

Animals respond to environmental variation by exhibiting a number of different behaviours and/or rates of activity, which result in corresponding variation in energy expenditure. Successful animals generally maximize efficiency or rate of energy gain through foraging. Quantification of all features that modulate energy expenditure can theoretically be modelled as an animal energetic niche or power envelope; with total power being represented by the vertical axis and n-dimensional horizontal axes representing extents of processes that affect energy expenditure. Such an energetic niche could be used to assess the energetic consequences of animals adopting particular behaviours under various environmental conditions. This value of this approach was tested by constructing a simple mechanistic energetics model based on data collected from recording devices deployed on 41 free-living Magellanic penguins (Spheniscus magellanicus), foraging from four different colonies in Argentina and consequently catching four different types of prey. Energy expenditure was calculated as a function of total distance swum underwater (horizontal axis 1) and maximum depth reached (horizontal axis 2). The resultant power envelope was invariant, irrespective of colony location, but penguins from the different colonies tended to use different areas of the envelope. The different colony solutions appeared to represent particular behavioural options for exploiting the available prey and demonstrate how penguins respond to environmental circumstance (prey distribution), the energetic consequences that this has for them, and how this affects the balance of energy acquisition through foraging and expenditure strategy.