The effects of introduced mice on seabirds breeding at sub-Antarctic Islands

Seabirds play keystone roles as apex predators in marine ecosystems and also influence the ecology of terrestrial ecosystems where they breed. Seabirds are among the most threatened group of birds - almost half of all seabird species are known or suspected to be experiencing population declines with 97 (28%) of the 346 species currently classed as globally threatened and at risk of extinction. Introduced predators at oceanic islands where many seabirds breed account for the largest proportion of population declines, more so than incidental fisheries bycatch or degradation of their breeding habitats. Since few oceanic islands have escaped invasion, the problem is widespread, with the prime culprits being introduced cats Felis catus, rats Rattus spp. and house mice Mus musculus which depredate adult birds, chicks and eggs. Rats were widely introduced to thousands of islands and their catastrophic effects on seabird populations have been well documented. Mice are estimated to have invaded more oceanic islands than any other alien predator, but until fairly recently they were considered to have little impact on seabird populations. This thesis focuses on seabirds breeding at two large oceanic islands - Marion Island (293 km2 ) in the south Indian Ocean and Gough Island (65 km2 ) in the south central Atlantic Ocean. Both islands have mice as the sole introduced mammal. Of relevance to this study, however, is that the density of burrow-nesting petrels is much higher on Gough Island because Marion Island’s petrel populations were greatly reduced by cats, which were introduced in 1948 and eradicated by 1991. In the early 2000s, researchers on Gough Island identified mouse predation as the most probable cause of the high chick mortality of at least three species of seabirds, including the endemic Tristan albatross Diomedea dabbenena. Further research concluded that mice can be devastating predators of seabirds on islands where they are the sole introduced mammal, because in the absence of competition and predation from larger introduced species, mice can attain very high population densities, and resort to attacking seabird chicks mainly in winter when there are few other food sources. In 2003, the first mouse-injured wandering albatross Diomedea exulans chicks were found on Marion Island and in 2009 the first attacks on summer-breeding albatross chicks were recorded, but incidents appeared to be infrequent. Although mouse predation had been identified as a potentially serious threat to seabirds at both islands, further evidence was required on how many seabird species were being affected and to quantify the impacts. Field observations suggested a noticeable increase in levels of mouse predation at both islands, yet there was still no direct evidence of mice depredating burrow-nesting petrels at Marion. In this thesis I assess the impacts of invasive mice at both islands and establish pre-eradication baseline estimates for the burrow-nesting petrel populations at Marion Island. Burrow-nesting petrels are the most abundant seabirds in the Southern Ocean, yet their populations are poorly known compared to surface-breeding albatrosses because they are difficult to survey accurately. Extrapolation from density estimates can lead to large error margins, but these can be reduced with the development of repeatable, island-specific survey methods for long-term monitoring. This forms the basis of Chapter 2, where I test the effect of sampling strategy (random transect or systematic survey) on population size estimates of three burrow-nesting petrel populations at Marion Island. Systematic, island-wide surveys were appropriate to estimate the population sizes of blue petrels Halobaena caerulea (strongly clustered distribution - Appendix 1) and white-chinned petrels Procellaria aequinoctialis (moderately clustered distribution - Appendix 2) and but for the very widely distributed great-winged petrels Pterodroma macroptera I counted burrows within random transects and extrapolated burrow densities by associated habitat attributes to generate island-wide estimates. The systematic surveys required more effort, but resulted in more accurate estimates for species with clustered distributions, whereas the random transects required less effort but resulted in broad estimates with wide error margins which limits the ability to detect changes over time. In Chapter 3, I investigate how burrow-nesting petrel populations on Marion Island have recovered since cats were eradicated in 1991. In theory, the removal of cats as the superpredator, combined with endogenous growth and the potential for immigration from nearby mouse-free Prince Edward Island, could have promoted a multi-fold increase in petrel numbers over the last two decades. To investigate this, I repeated a burrow-nesting petrel survey in the north-eastern sector of Marion Island originally conducted by Mike Schramm in 1979 and assessed how burrow densities have changed compared to densities at the peak of the cat-era. I found that burrow densities have increased by a modest 56% since 1979. The recovery of summer-breeding petrels decreased with decreasing body size, and winterbreeding species showed even smaller recoveries, which is similar to patterns of breeding success at Gough Island where mice are the major drivers of population declines among petrels. Mice are the likely cause of the limited recovery of burrowing petrels at Marion Island. To assess and document the impacts of invasive mice at both islands, I installed infra-red video cameras into burrows and assessed breeding success with regular burrow-scope nest inspections of study colony nests at both Gough and Marion Islands (Chapters 4 and 5). The results show that mice can be very effective predators of burrow-nesting petrel chicks and to a lesser extent, eggs. The breeding success for winter breeders were lower than for summer breeders at both islands, and among winter breeders most chick fatalities were of small chicks less than 14 days old. Fatal mouse attacks on small chicks were video recorded for six burrow-nesting petrel species and winter breeders had very high chick mortality rates (e.g. 82–100% on Gough Island). Since mouse depredation of seabird chicks was first identified as a problem in 2001, the frequency and severity of mouse predations appears to have escalated on Gough (Appendix 3), yet on Marion Island detected incidents remained infrequent until 2015, when mice attacked 4.0–4.6% of the large chicks of all three albatross species that fledge in autumn. Attacks started independently in small pockets all around the island’s 70 km coastline, separated by distances hundreds of times greater than mouse home ranges. Attacks have continued from 2016–2018 at varying rates on summer-breeding albatross fledglings, showing how mice alone may significantly affect threatened seabird species (Chapter 6). In summary, mice appear to be suppressing the productivity of burrow- and surface-nesting seabird populations at both islands and are very likely causing population declines, especially among winter breeding species. Fortunately, the removal of invasive mice from islands through aerial spreading of toxic bait is a viable option and the scientific and visual evidence collected during this thesis has contributed to the growing body of evidence needed to persuade funders and Governments to support eradication operations at both study islands

Poor transferability of species distribution models for a pelagic predator, the grey petrel, Indicates contrasting habitat preferences across ocean basins

Species distribution models (SDMs) are increasingly applied in conservation management to predict suitable habitat for poorly known populations. High predictive performance of SDMs is evident in validations performed within the model calibration area (interpolation), but few studies have assessed SDM transferability to novel areas (extrapolation), particularly across large spatial scales or pelagic ecosystems. We performed rigorous SDM validation tests on distribution data from three populations of a long-ranging marine predator, the grey petrel Procellaria cinerea , to assess model transferability across the Southern Hemisphere (25-65°S). Oceanographic data were combined with tracks of grey petrels from two remote sub-Antarctic islands (Antipodes and Kerguelen) using boosted regression trees to generate three SDMs: one for each island population, and a combined model. The predictive performance of these models was assessed using withheld tracking data from within the model calibration areas (interpolation), and from a third population, Marion Island (extrapolation). Predictive performance was assessed using k-fold cross validation and point biserial correlation. The two population-specific SDMs included the same predictor variables and suggested birds responded to the same broad-scale oceanographic influences. However, all model validation tests, including of the combined model, determined strong interpolation but weak extrapolation capabilities. These results indicate that habitat use reflects both its availability and bird preferences, such that the realized distribution patterns differ for each population. The spatial predictions by the three SDMs were compared with tracking data and fishing effort to demonstrate the conservation pitfalls of extrapolating SDMs outside calibration regions. This exercise revealed that SDM predictions would have led to an underestimate of overlap with fishing effort and potentially misinformed bycatch mitigation efforts. Although SDMs can elucidate potential distribution patterns relative to large-scale climatic and oceanographic conditions, knowledge of local habitat availability and preferences is necessary to understand and successfully predict region-specific realized distribution patterns

Agent based modelling helps in understanding the rules by which fibroblasts support keratinocyte colony formation

Background: Autologous keratincoytes are routinely expanded using irradiated mouse fibroblasts and bovine serum for clinical use. With growing concerns about the safety of these xenobiotic materials, it is desirable to culture keratinocytes in media without animal derived products. An improved understanding of epithelial/mesenchymal interactions could assist in this. Methodology/Principal Findings: A keratincyte/fibroblast o-culture model was developed by extending an agent-based keratinocyte colony formation model to include the response of keratinocytes to both fibroblasts and serum. The model was validated by comparison of the in virtuo and in vitro multicellular behaviour of keratinocytes and fibroblasts in single and co-culture in Greens medium. To test the robustness of the model, several properties of the fibroblasts were changed to investigate their influence on the multicellular morphogenesis of keratinocyes and fibroblasts. The model was then used to generate hypotheses to explore the interactions of both proliferative and growth arrested fibroblasts with keratinocytes. The key predictions arising from the model which were confirmed by in vitro experiments were that 1) the ratio of fibroblasts to keratinocytes would critically influence keratinocyte colony expansion, 2) this ratio needed to be optimum at the beginning of the co-culture, 3) proliferative fibroblasts would be more effective than irradiated cells in expanding keratinocytes and 4) in the presence of an adequate number of fibroblasts, keratinocyte expansion would be independent of serum. Conclusions: A closely associated computational and biological approach is a powerful tool for understanding complex biological systems such as the interactions between keratinocytes and fibroblasts. The key outcome of this study is the finding that the early addition of a critical ratio of proliferative fibroblasts can give rapid keratinocyte expansion without the use of irradiated mouse fibroblasts and bovine serum

Poor Transferability of Species Distribution Models for a Pelagic Predator, the Grey Petrel, Indicates Contrasting Habitat Preferences across Ocean Basins

Species distribution models (SDMs) are increasingly applied in conservation management to predict suitable habitat for poorly known populations. High predictive performance of SDMs is evident in validations performed within the model calibration area (interpolation), but few studies have assessed SDM transferability to novel areas (extrapolation), particularly across large spatial scales or pelagic ecosystems. We performed rigorous SDM validation tests on distribution data from three populations of a long-ranging marine predator, the grey petrel Procellaria cinerea, to assess model transferability across the Southern Hemisphere (25-65°S). Oceanographic data were combined with tracks of grey petrels from two remote sub-Antarctic islands (Antipodes and Kerguelen) using boosted regression trees to generate three SDMs: one for each island population, and a combined model. The predictive performance of these models was assessed using withheld tracking data from within the model calibration areas (interpolation), and from a third population, Marion Island (extrapolation). Predictive performance was assessed using k-fold cross validation and point biserial correlation. The two population-specific SDMs included the same predictor variables and suggested birds responded to the same broad-scale oceanographic influences. However, all model validation tests, including of the combined model, determined strong interpolation but weak extrapolation capabilities. These results indicate that habitat use reflects both its availability and bird preferences, such that the realized distribution patterns differ for each population. The spatial predictions by the three SDMs were compared with tracking data and fishing effort to demonstrate the conservation pitfalls of extrapolating SDMs outside calibration regions. This exercise revealed that SDM predictions would have led to an underestimate of overlap with fishing effort and potentially misinformed bycatch mitigation efforts. Although SDMs can elucidate potential distribution patterns relative to large-scale climatic and oceanographic conditions, knowledge of local habitat availability and preferences is necessary to understand and successfully predict region-specific realized distribution patterns

Global political responsibility for the conservation of albatrosses and large petrels

Migratory marine species cross political borders and enter the high seas, where the lack of an effective global management framework for biodiversity leaves them vulnerable to threats. Here, we combine 10,108 tracks from 5775 individual birds at 87 sites with data on breeding population sizes to estimate the relative year-round importance of national jurisdictions and high seas areas for 39 species of albatrosses and large petrels. Populations from every country made extensive use of the high seas, indicating the stake each country has in the management of biodiversity in international waters. We quantified the links among national populations of these threatened seabirds and the regional fisheries management organizations (RFMOs) which regulate fishing in the high seas. This work makes explicit the relative responsibilities that each country and RFMO has for the management of shared biodiversity, providing invaluable information for the conservation and management of migratory species in the marine realm

Independent evolution of intermediate bill widths in a seabird clade

16 pages, 5 figures, 5 tables, supplementary information https://doi.org/10.1007/s00438-021-01845-3.-- Availability of data and material: DNA sequences: GenBank accession numbers are provided in Table 1. All data are available in the manuscript or in the Supplementary information fileInterspecific 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 smallOpen Access funding enabled and organized by Projekt DEAL. PQ, JFM, TLC and LC were supported by the Deutsche Forschungsgemeinschaft (Germany), Heisenberg program (grant number DFG, Qu 148-5 to P.Q.). Logistical and financial support was obtained from the South African Department of Environmental Affairs, through the South African National Antarctic Programme. LDS was supported by a Rutherford Discovery Fellowship from the Royal Society of New ZealandWith the institutional support of the ‘Severo Ochoa Centre of Excellence’ accreditation (CEX2019-000928-S)Peer reviewe

Senescent cells as a source of inflammatory factors for tumor progression

Cellular senescence, which is associated with aging, is a process by which cells enter a state of permanent cell cycle arrest, therefore constituting a potent tumor suppressive mechanism. Recent studies show that, despite the beneficial effects of cellular senescence, senescent cells can also exert harmful effects on the tissue microenvironment. The most significant of these effects is the acquisition of a senescent-associated secretory phenotype (SASP), which entails a striking increase in the secretion of pro-inflammatory cytokines. Here, we summarize our knowledge of the SASP and the impact it has on tissue microenvironments and ability to stimulate tumor progression

Global assessment of marine plastic exposure risk for oceanic birds

Plastic pollution is distributed patchily around the world’s oceans. Likewise, marine organisms that are vulnerable to plastic ingestion or entanglement have uneven distributions. Understanding where wildlife encounters plastic is crucial for targeting research and mitigation. Oceanic seabirds, particularly petrels, frequently ingest plastic, are highly threatened, and cover vast distances during foraging and migration. However, the spatial overlap between petrels and plastics is poorly understood. Here we combine marine plastic density estimates with individual movement data for 7137 birds of 77 petrel species to estimate relative exposure risk. We identify high exposure risk areas in the Mediterranean and Black seas, and the northeast Pacific, northwest Pacific, South Atlantic and southwest Indian oceans. Plastic exposure risk varies greatly among species and populations, and between breeding and non-breeding seasons. Exposure risk is disproportionately high for Threatened species. Outside the Mediterranean and Black seas, exposure risk is highest in the high seas and Exclusive Economic Zones (EEZs) of the USA, Japan, and the UK. Birds generally had higher plastic exposure risk outside the EEZ of the country where they breed. We identify conservation and research priorities, and highlight that international collaboration is key to addressing the impacts of marine plastic on wide-ranging species

Global assessment of marine plastic exposure risk for oceanic birds

Plastic pollution is distributed patchily around the world’s oceans. Likewise, marine organisms that are vulnerable to plastic ingestion or entanglement have uneven distributions. Understanding where wildlife encounters plastic is crucial for targeting research and mitigation. Oceanic seabirds, particularly petrels, frequently ingest plastic, are highly threatened, and cover vast distances during foraging and migration. However, the spatial overlap between petrels and plastics is poorly understood. Here we combine marine plastic density estimates with individual movement data for 7137 birds of 77 petrel species to estimate relative exposure risk. We identify high exposure risk areas in the Mediterranean and Black seas, and the northeast Pacific, northwest Pacific, South Atlantic and southwest Indian oceans. Plastic exposure risk varies greatly among species and populations, and between breeding and non-breeding seasons. Exposure risk is disproportionately high for Threatened species. Outside the Mediterranean and Black seas, exposure risk is highest in the high seas and Exclusive Economic Zones (EEZs) of the USA, Japan, and the UK. Birds generally had higher plastic exposure risk outside the EEZ of the country where they breed. We identify conservation and research priorities, and highlight that international collaboration is key to addressing the impacts of marine plastic on wide-ranging species

Intertidal foraging by Tristan Thrushes

We report that some 10% of Tristan Thrushes Turdus eremita on the coast at Inaccessible Island feed extensively on marine invertebrates (mainly crustaceans), despite lacking functional salt glands. Such birds regularly drink from freshwater springs that are common along the coast, but thrushes also forage along the coast at nearby Nightingale Island where there is little freshwater. One individual was observed feeding on stranded by-the-windsailors Velella velella. This appears to be only the second record of a passerine feeding on a cnidarian. These records further emphasise the resourcefulness of island birds in general, and the Tristan Thrush in particular, to exploit a wide range of food resources.Keywords: Turdus eremita, isopods, amphipods, Lepas, Velell