Trophic plasticity of a tropical seabird revealed through DNA metabarcoding and stable isotope analyses.

DNA metabarcoding and stable isotope analysis have significantly advanced our understanding of marine trophic ecology, aiding systematic research on foraging habits and species conservation. In this study, we employed these methods to analyse faecal and blood samples, respectively, to compare the trophic ecology of two Red-billed Tropicbird (Phaethonaethereus; Linnaeus, 1758) colonies on Mexican islands in the Pacific. Trophic patterns among different breeding stages were also examined at both colonies. Dietary analysis reveals a preference for epipelagic fish, cephalopods, and small crustaceans, with variations between colonies and breeding stages. Isotopic values (δ15N and δ13C) align with DNA metabarcoding results, with wider niches during incubation stages. Differences in diet are linked to environmental conditions and trophic plasticity among breeding stages, influenced by changing physiological requirements and prey availability. Variations in dietary profiles reflect contrasting environmental conditions affecting local prey availability.

High prevalence of haemosporidian parasites in Eurasian jays.

Avian haemosporidians are vector-borne parasites, infecting a great variety of birds. The order Passeriformes has the highest average infection probability; nevertheless, some common species of Passeriformes have been rather poorly studied. We investigated haemosporidians in one such species, the Eurasian jay Garrulus glandarius (Corvidae), from a forest population in Hesse, Central Germany. All individuals were infected with at least one haemosporidian genus (overall prevalence: 100%). The most common infection pattern was a mixed Haemoproteus and Leucocytozoon infection, whereas no Plasmodium infection was detected. Results on lineage diversity indicate a rather pronounced host-specificity of Haemoproteus and Leucocytozoon lineages infecting birds of the family Corvidae.

Nature 4.0: A networked sensor system for integrated biodiversity monitoring.

Ecosystem functions and services are severely threatened by unprecedented global loss in biodiversity. To counteract these trends, it is essential to develop systems to monitor changes in biodiversity for planning, evaluating, and implementing conservation and mitigation actions. However, the implementation of monitoring systems suffers from a trade-off between grain (i.e., the level of detail), extent (i.e., the number of study sites), and temporal repetition. Here, we present an applied and realized networked sensor system for integrated biodiversity monitoring in the Nature 4.0 project as a solution to these challenges, which considers plants and animals not only as targets of investigation, but also as parts of the modular sensor network by carrying sensors. Our networked sensor system consists of three main closely interlinked components with a modular structure: sensors, data transmission, and data storage, which are integrated into pipelines for automated biodiversity monitoring. We present our own real-world examples of applications, share our experiences in operating them, and provide our collected open data. Our flexible, low-cost, and open-source solutions can be applied for monitoring individual and multiple terrestrial plants and animals as well as their interactions. Ultimately, our system can also be applied to area-wide ecosystem mapping tasks, thereby providing an exemplary cost-efficient and powerful solution for biodiversity monitoring. Building upon our experiences in the Nature 4.0 project, we identified ten key challenges that need to be addressed to better understand and counteract the ongoing loss of biodiversity using networked sensor systems. To tackle these challenges, interdisciplinary collaboration, additional research, and practical solutions are necessary to enhance the capability and applicability of networked sensor systems for researchers and practitioners, ultimately further helping to ensure the sustainable management of ecosystems and the provision of ecosystem services.

Circadian gene variation in relation to breeding season and latitude in allochronic populations of two pelagic seabird species complexes.

Annual cues in the environment result in physiological changes that allow organisms to time reproduction during periods of optimal resource availability. Understanding how circadian rhythm genes sense these environmental cues and stimulate the appropriate physiological changes in response is important for determining the adaptability of species, especially in the advent of changing climate. A first step involves characterizing the environmental correlates of natural variation in these genes. Band-rumped and Leach's storm-petrels (Hydrobates spp.) are pelagic seabirds that breed across a wide range of latitudes. Importantly, some populations have undergone allochronic divergence, in which sympatric populations use the same breeding sites at different times of year. We investigated the relationship between variation in key functional regions of four genes that play an integral role in the cellular clock mechanism-Clock, Bmal1, Cry2 and Per2-with both breeding season and absolute latitude in these two species complexes. We discovered that allele frequencies in two genes, Clock and Bmal1, differed between seasonal populations in one archipelago, and also correlated with absolute latitude of breeding colonies. These results indicate that variation in these circadian rhythm genes may be involved in allochronic speciation, as well as adaptation to photoperiod at breeding locations.

Diet composition of wild columbiform birds: next-generation sequencing of plant and metazoan DNA in faecal samples.

Accurate knowledge of a species' diets is fundamental to understand their ecological requirements. Next-generation sequencing technology has become a powerful and non-invasive tool for diet reconstruction through DNA metabarcoding. Here, we applied those methods on faecal samples of Common Woodpigeons Columba palumbus, European Turtle Doves Streptopelia turtur, and Stock Doves C. oenas to investigate their dietary composition. By applying primer pairs targeting both the ITS2 region of plant nuclear DNA and the mitochondrial COI region of metazoan DNA, we provide a complete picture of the food ingested and estimate the dietary overlap between the columbiform species during the breeding season. Animal DNA was present very rarely, and a diverse range of plants from the class Spermatopsida dominated the diet, with Asteraceae, Brassicaceae, Cucurbitaceae, Fabaceae, and Poaceae as the most frequently represented families. Generally, we detected a variability between species but also amongst individual samples. Plant species already known from previous studies, mainly visual analyses, could be confirmed for our individuals sampled in Germany and the Netherlands. Our molecular approach revealed new plant taxa, e.g. plants of the families Malvaceae for Woodpigeons, Lythraceae for Turtle Doves, and Pinaceae for Stock Doves, not found in previous studies using visual analyses. Although most of the plant species observed were of wild origin, the majority of cultivated plants found were present in higher frequencies of occurrence, suggesting that cultivated food items likely constitute an important part of the diet of the studied species. For Turtle Doves, a comparison with previous studies suggested regional differences, and that food items (historically) considered as important part of their diet, such as Fumitory Fumaria sp. and Chickweed Stellaria media, were missing in our samples. This indicates that regional variations as well as historic and current data on diet should be considered to plan tailored seed mixtures, which are currently proposed as an important management measure for conservation of the rapidly declining Turtle Dove.

Using Next-Generation Sequencing to Disentangle the Diet and Incidence of Intestinal Parasites of Falkland Flightless Steamer Duck Tachyeres brachypterus and Patagonian Crested Duck Lophonetta specularioides Sharing a South Atlantic Island.

Species overlapping in habitat use can cohabit depending on how they exploit resources. To understand segregation in resource use, an exhaustive knowledge of the diet is required. We aimed to disentangle the diet composition of the Falkland Flightless Steamer Duck Tachyeres brachypterus and the Patagonian Crested Duck Lophonetta specularioides sharing a coastal environment. Using DNA extracted from scats and Illumina sequencing, we generated a list of molecular operational taxonomic units. Both ducks consumed a variety of invertebrates, frequently overlapping in the taxa consumed. However, only the Falkland Flightless Steamer Ducks consumed fish, which might be indicative of dietary specialization and inter-specific segregation in the restricted space that these birds share. Moreover, the female and male Falkland Flightless Steamer Ducks consumed different fish prey, with almost one-third of the fish taxa being consumed by females only and another similar number consumed by males only. This result might suggest a case of intra-specific competition, triggering sexual segregation. Additionally, we detected parasitic Platyelminthes (Cestoda and Trematoda), with different frequencies of occurrence, probably related to the different diet compositions of the ducks. This study provides the necessary baseline for future investigations of the ecological segregation of these ducks.

Should I stay or should I fly? Migration phenology, individual-based migration decision and seasonal changes in foraging behaviour of Common Woodpigeons.

Migration is used by many species as a strategy to deal with a seasonally changing environment. For some species, migration patterns can vary across different or even within the same breeding area. The Common Woodpigeon Columba palumbus, an abundant and widespread Palearctic species, exhibits three migratory strategies (strictly migratory, partially migratory and resident) across its European breeding grounds. Based on ring recoveries and satellite tracking data, we investigated the migration and foraging behaviour of Woodpigeons breeding in Southwestern Europe (Portugal) and Central Europe (Germany). We found that individuals could be classified as residents (Portugal) or partial migrants (Germany), with migrating individuals following the European sector of the East Atlantic flyway, and mainly wintering in France. In addition to general data on migration phenology, we provide evidence for different migration strategies (migration of varying distances or resident behaviour), low wintering site fidelity and the use of multiple wintering sites. Furthermore, tracking data provided information on migratory behaviour in consecutive years, clearly showing that individuals may switch migratory strategies (resident vs. migrant) between years, i.e. are facultative partial migrants. While individuals from Portugal mainly stayed within a large park ('green urban area') year-round, Woodpigeons from the city of Giessen (Germany) regularly left the urban area to forage on surrounding farmland (with an average distance covered of 5.7 km), particularly from July to September. Overall, our results highlight the behavioural plasticity in Woodpigeons in terms of foraging and migration strategies within and amongst individuals as well as populations.

Genomic insights into the secondary aquatic transition of penguins.

Penguins lost the ability to fly more than 60 million years ago, subsequently evolving a hyper-specialized marine body plan. Within the framework of a genome-scale, fossil-inclusive phylogeny, we identify key geological events that shaped penguin diversification and genomic signatures consistent with widespread refugia/recolonization during major climate oscillations. We further identify a suite of genes potentially underpinning adaptations related to thermoregulation, oxygenation, diving, vision, diet, immunity and body size, which might have facilitated their remarkable secondary transition to an aquatic ecology. Our analyses indicate that penguins and their sister group (Procellariiformes) have the lowest evolutionary rates yet detected in birds. Together, these findings help improve our understanding of how penguins have transitioned to the marine environment, successfully colonizing some of the most extreme environments on Earth.

Austral birds offer insightful complementary models in ecology and evolution.

The Southern Hemisphere differs from the Northern Hemisphere in many aspects. However, most ecological and evolutionary research is conducted in the Northern Hemisphere and its conclusions are extrapolated to the entire globe. Therefore, unique organismal and evolutionary characteristics of the south are overlooked. We use ornithology to show the importance of including a southern perspective. We present examples of plumage pigmentation, brood-parasitic nestling ejection, flightlessness, female song, and female aggression modulated by progesterone as complementary models for investigating fundamental biological questions. More research in the Southern Hemisphere, together with increased cooperation among researchers across the hemispheres and within the Southern Hemisphere, will provide a greater global outlook into ecology and evolution.

Independent evolution of intermediate bill widths in a seabird clade.

Interspecific introgression can occur between species that evolve rapidly within an adaptive radiation. Pachyptila petrels differ in bill size and are characterised by incomplete reproductive isolation, leading to interspecific gene flow. Salvin's prion (Pachyptila salvini), whose bill width is intermediate between broad-billed (P. vittata) and Antarctic (P. desolata) prions, evolved through homoploid hybrid speciation. MacGillivray's prion (P. macgillivrayi), known from a single population on St Paul (Indian Ocean), has a bill width intermediate between salvini and vittata and could also be the product of interspecies introgression or hybrid speciation. Recently, another prion population phenotypically similar to macgillivrayi was discovered on Gough (Atlantic Ocean), where it breeds 3 months later than vittata. The similarity in bill width between the medium-billed birds on Gough and macgillivrayi suggest that they could be closely related. In this study, we used genetic and morphological data to infer the phylogenetic position and evolutionary history of P. macgillivrayi and the Gough medium-billed prion relative other Pachyptila taxa, to determine whether species with medium bill widths evolved through common ancestry or convergence. We found that Gough medium-billed prions belong to the same evolutionary lineage as macgillivrayi, representing a new population of MacGillivray's prion that originated through a colonisation event from St Paul. We show that macgillivrayi's medium bill width evolved through divergence (genetic drift) and independently from that of salvini, which evolved through hybridisation (gene flow). This represents the independent convergence towards a similarly medium-billed phenotype. The newly discovered MacGillivray's prion population on Gough is of utmost conservation relevance, as the relict macgillivrayi population in the Indian Ocean is very small.

Overlap between marine predators and proposed Marine Managed Areas on the Patagonian Shelf.

Static (fixed-boundary) protected areas are key ocean conservation strategies, and marine higher predator distribution data can play a leading role toward identifying areas for conservation action. The Falkland Islands are a globally significant site for colonial breeding marine higher predators (i.e., seabirds and pinnipeds). However, overlap between marine predators and Falkland Islands proposed Marine Managed Areas (MMAs) has not been quantified. Hence, to provide information required to make informed decisions regarding the implementation of proposed MMAs, our aims were to objectively assess how the proposed MMA network overlaps with contemporary estimates of marine predator distribution. We collated tracking data (1999-2019) and used a combination of kernel density estimation and model-based predictions of spatial usage to quantify overlap between colonial breeding marine predators and proposed Falkland Islands MMAs. We also identified potential IUCN Key Biodiversity Areas (pKBAs) using (1) kernel density based methods originally designed to identify Important Bird and Biodiversity Areas (IBAs) and (2) habitat preference models. The proposed inshore MMA, which extends three nautical miles from the Falkland Islands, overlapped extensively with areas used by colonial breeding marine predators. This reflects breeding colonies being distributed throughout the Falklands archipelago, and use being high adjacent to colonies due to central-place foraging constraints. Up to 45% of pKBAs identified via kernel density estimation were located within the proposed MMAs. In particular, the proposed Jason Islands Group MMA overlapped with pKBAs for three marine predator species, suggesting it is a KBA hot spot. However, tracking data coverage was incomplete, which biased pKBAs identified using kernel density methods, to colonies tracked. Moreover, delineation of pKBA boundaries were sensitive to the choice of smoothing parameter used in kernel density estimation. Delineation based on habitat model predictions for both sampled and unsampled colonies provided less biased estimates, and revealed 72% of the Falkland Islands Conservation Zone was likely a KBA. However, it may not be practical to consider such a large area for fixed-boundary management. In the context of wide-ranging marine predators, emerging approaches such as dynamic ocean management could complement static management frameworks such as MMAs, and provide protection at relevant spatiotemporal scales.

How animals distribute themselves in space: energy landscapes of Antarctic avian predators.

BACKGROUND: Energy landscapes provide an approach to the mechanistic basis of spatial ecology and decision-making in animals. This is based on the quantification of the variation in the energy costs of movements through a given environment, as well as how these costs vary in time and for different animal populations. Organisms as diverse as fish, mammals, and birds will move in areas of the energy landscape that result in minimised costs and maximised energy gain. Recently, energy landscapes have been used to link energy gain and variable energy costs of foraging to breeding success, revealing their potential use for understanding demographic changes. METHODS: Using GPS-temperature-depth and tri-axial accelerometer loggers, stable isotope and molecular analyses of the diet, and leucocyte counts, we studied the response of gentoo (Pygoscelis papua) and chinstrap (Pygoscelis antarcticus) penguins to different energy landscapes and resources. We compared species and gentoo penguin populations with contrasting population trends. RESULTS: Between populations, gentoo penguins from Livingston Island (Antarctica), a site with positive population trends, foraged in energy landscape sectors that implied lower foraging costs per energy gained compared with those around New Island (Falkland/Malvinas Islands; sub-Antarctic), a breeding site with fluctuating energy costs of foraging, breeding success and populations. Between species, chinstrap penguins foraged in sectors of the energy landscape with lower foraging costs per bottom time, a proxy for energy gain. They also showed lower physiological stress, as revealed by leucocyte counts, and higher breeding success than gentoo penguins. In terms of diet, we found a flexible foraging ecology in gentoo penguins but a narrow foraging niche for chinstraps. CONCLUSIONS: The lower foraging costs incurred by the gentoo penguins from Livingston, may favour a higher breeding success that would explain the species' positive population trend in the Antarctic Peninsula. The lower foraging costs in chinstrap penguins may also explain their higher breeding success, compared to gentoos from Antarctica but not their negative population trend. Altogether, our results suggest a link between energy landscapes and breeding success mediated by the physiological condition.

Prevalence and genetic diversity of avian haemosporidian parasites in wild bird species of the order Columbiformes.

Diseases can play a role in species decline. Among them, haemosporidian parasites, vector-transmitted protozoan parasites, are known to constitute a risk for different avian species. However, the magnitude of haemosporidian infection in wild columbiform birds, including strongly decreasing European turtle doves, is largely unknown. We examined the prevalence and diversity of haemosporidian parasites Plasmodium, Leucocytozoon and subgenera Haemoproteus and Parahaemoproteus in six species of the order Columbiformes during breeding season and migration by applying nested PCR, one-step multiplex PCR assay and microscopy. We detected infections in 109 of the 259 screened individuals (42%), including 15 distinct haemosporidian mitochondrial cytochrome b lineages, representing five H. (Haemoproteus), two H. (Parahaemoproteus), five Leucocytozoon and three Plasmodium lineages. Five of these lineages have never been described before. We discriminated between single and mixed infections and determined host species-specific prevalence for each parasite genus. Observed differences among sampled host species are discussed with reference to behavioural characteristics, including nesting and migration strategy. Our results support previous suggestions that migratory birds have a higher prevalence and diversity of blood parasites than resident or short-distance migratory species. A phylogenetic reconstruction provided evidence for H. (Haemoproteus) as well as H. (Parahaemoproteus) infections in columbiform birds. Based on microscopic examination, we quantified parasitemia, indicating the probability of negative effects on the host. This study provides a large-scale baseline description of haemosporidian infections of wild birds belonging to the order Columbiformes sampled in the northern hemisphere. The results enable the monitoring of future changes in parasite transmission areas, distribution and diversity associated with global change, posing a potential risk for declining avian species as the European turtle dove.

Compound-specific stable isotope analyses in Falkland Islands seabirds reveal seasonal changes in trophic positions.

BACKGROUND: While nitrogen and carbon stable isotope values can reflect ecological segregation, prey choice and spatial distribution in seabirds, the interpretation of bulk stable isotope values is frequently hampered by a lack of isotopic baseline data. In this study, we used compound-specific isotope analyses of amino acids (CSIA-AA) to overcome this constraint and to study interspecific differences, seasonal and historical changes in trophic positions of five seabird species, three penguins and two petrels, from a sub-Antarctic seabird community. RESULTS: CSIA-AA allowed comparing trophic positions of seabirds with temperate and polar distributions. Gentoo and Magellanic penguins had the highest trophic positions during the breeding season (3.7 and 3.9), but decreased these (2.9 and 3.3) during the feed-up for moult. Intra-specific differences were also detected in Thin-billed prions, where carbon isotope values clearly separated individuals with polar and temperate distributions, both in the breeding and interbreeding periods. Thin-billed prions that foraged in polar waters had lower trophic positions (3.2) than conspecifics foraging in temperate waters (3.8). We further investigated historical changes by comparing museum samples with samples collected recently. Our pilot study suggests that Rockhopper penguins, Magellanic penguins and Thin-billed prions with temperate non-breeding distributions had retained their trophic levels over a 90-100 year period, while Gentoo penguins and Thin-billed prions with polar non-breeding distributions had decreased trophic levels compared to historical samples. In contrast, Wilson's storm-petrels had slightly increased trophic levels compared to samples taken in 1924-1930. CONCLUSIONS: We applied compound-specific stable isotope analyses across a range of contexts, from intra-specific comparisons between stages of the breeding cycle to inter-specific seabird community analysis that would not have been possible using bulk stable isotope analyses alone due to differences in isotopic baselines.

Author Correction: Important At-Sea Areas of Colonial Breeding Marine Predators on the Southern Patagonian Shelf.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

High-coverage genomes to elucidate the evolution of penguins.

BACKGROUND: Penguins (Sphenisciformes) are a remarkable order of flightless wing-propelled diving seabirds distributed widely across the southern hemisphere. They share a volant common ancestor with Procellariiformes close to the Cretaceous-Paleogene boundary (66 million years ago) and subsequently lost the ability to fly but enhanced their diving capabilities. With ∼20 species among 6 genera, penguins range from the tropical Galápagos Islands to the oceanic temperate forests of New Zealand, the rocky coastlines of the sub-Antarctic islands, and the sea ice around Antarctica. To inhabit such diverse and extreme environments, penguins evolved many physiological and morphological adaptations. However, they are also highly sensitive to climate change. Therefore, penguins provide an exciting target system for understanding the evolutionary processes of speciation, adaptation, and demography. Genomic data are an emerging resource for addressing questions about such processes. RESULTS: Here we present a novel dataset of 19 high-coverage genomes that, together with 2 previously published genomes, encompass all extant penguin species. We also present a well-supported phylogeny to clarify the relationships among penguins. In contrast to recent studies, our results demonstrate that the genus Aptenodytes is basal and sister to all other extant penguin genera, providing intriguing new insights into the adaptation of penguins to Antarctica. As such, our dataset provides a novel resource for understanding the evolutionary history of penguins as a clade, as well as the fine-scale relationships of individual penguin lineages. Against this background, we introduce a major consortium of international scientists dedicated to studying these genomes. Moreover, we highlight emerging issues regarding ensuring legal and respectful indigenous consultation, particularly for genomic data originating from New Zealand Taonga species. CONCLUSIONS: We believe that our dataset and project will be important for understanding evolution, increasing cultural heritage and guiding the conservation of this iconic southern hemisphere species assemblage.

Important At-Sea Areas of Colonial Breeding Marine Predators on the Southern Patagonian Shelf.

The Patagonian Shelf Large Marine Ecosystem supports high levels of biodiversity and endemism and is one of the most productive marine ecosystems in the world. Despite the important role marine predators play in structuring the ecosystems, areas of high diversity where multiple predators congregate remains poorly known on the Patagonian Shelf. Here, we used biotelemetry and biologging tags to track the movements of six seabird species and three pinniped species breeding at the Falkland Islands. Using Generalized Additive Models, we then modelled these animals' use of space as functions of dynamic and static environmental indices that described their habitat. Based on these models, we mapped the predicted distribution of animals from both sampled and unsampled colonies and thereby identified areas where multiple species were likely to overlap at sea. Maximum foraging trip distance ranged from 79 to 1,325 km. However, most of the 1,891 foraging trips by 686 animals were restricted to the Patagonian Shelf and shelf slope, which highlighted a preference for these habitats. Of the seven candidate explanatory covariates used to predict distribution, distance from the colony was retained in models for all species and negatively affected the probability of occurrence. Predicted overlap among species was highest on the Patagonian Shelf around the Falkland Islands and the Burdwood Bank. The predicted area of overlap is consistent with areas that are also important habitat for marine predators migrating from distant breeding locations. Our findings provide comprehensive multi-species predictions for some of the largest marine predator populations on the Patagonian Shelf, which will contribute to future marine spatial planning initiatives. Crucially, our findings highlight that spatially explicit conservation measures are likely to benefit multiple species, while threats are likely to impact multiple species.

Additive Traits Lead to Feeding Advantage and Reproductive Isolation, Promoting Homoploid Hybrid Speciation.

Speciation through homoploid hybridization (HHS) is considered extremely rare in animals. This is mainly because the establishment of reproductive isolation as a product of hybridization is uncommon. Additionally, many traits are underpinned by polygeny and/or incomplete dominance, where the hybrid phenotype is an additive blend of parental characteristics. Phenotypically intermediate hybrids are usually at a fitness disadvantage compared with parental species and tend to vanish through backcrossing with parental population(s). It is therefore unknown whether the additive nature of hybrid traits in itself could lead successfully to HHS. Using a multi-marker genetic data set and a meta-analysis of diet and morphology, we investigated a potential case of HHS in the prions (Pachyptila spp.), seabirds distinguished by their bills, prey choice, and timing of breeding. Using approximate Bayesian computation, we show that the medium-billed Salvin's prion (Pachyptila salvini) could be a hybrid between the narrow-billed Antarctic prion (Pachyptila desolata) and broad-billed prion (Pachyptila vittata). Remarkably, P. salvini's intermediate bill width has given it a feeding advantage with respect to the other Pachyptila species, allowing it to consume a broader range of prey, potentially increasing its fitness. Available metadata showed that P. salvini is also intermediate in breeding phenology and, with no overlap in breeding times, it is effectively reproductively isolated from either parental species through allochrony. These results provide evidence for a case of HHS in nature, and show for the first time that additivity of divergent parental traits alone can lead directly to increased hybrid fitness and reproductive isolation.