Climate and human stressors on global penguin hotspots: Current assessments for future conservation.

As charismatic and iconic species, penguins can act as "ambassadors" or flagship species to promote the conservation of marine habitats in the Southern Hemisphere. Unfortunately, there is a lack of reliable, comprehensive, and systematic analysis aimed at compiling spatially explicit assessments of the multiple impacts that the world's 18 species of penguin are facing. We provide such an assessment by combining the available penguin occurrence information from Global Biodiversity Information Facility (>800,000 occurrences) with three main stressors: climate-driven environmental changes at sea, industrial fisheries, and human disturbances on land. Our analyses provide a quantitative assessment of how these impacts are unevenly distributed spatially within species' distribution ranges. Consequently, contrasting pressures are expected among species, and populations within species. The areas coinciding with the greatest impacts for penguins are the coast of Perú, the Patagonian Shelf, the Benguela upwelling region, and the Australian and New Zealand coasts. When weighting these potential stressors with species-specific vulnerabilities, Humboldt (Spheniscus humboldti), African (Spheniscus demersus), and Chinstrap penguin (Pygoscelis antarcticus) emerge as the species under the most pressure. Our approach explicitly differentiates between climate and human stressors, since the more achievable management of local anthropogenic stressors (e.g., fisheries and land-based threats) may provide a suitable means for facilitating cumulative impacts on penguins, especially where they may remain resilient to global processes such as climate change. Moreover, our study highlights some poorly represented species such as the Northern Rockhopper (Eudyptes moseleyi), Snares (Eudyptes robustus), and Erect-crested penguin (Eudyptes sclateri) that need internationally coordinated efforts for data acquisition and data sharing to understand their spatial distribution properly.

Eradicating an invasive mammal requires local elimination and reduced reinvasion from an urban source population.

Invasive mammal eradications are increasingly attempted across large, complex landscapes. Sequentially controlled management zones can be at risk of reinvasion from adjacent uncontrolled areas, and managers must weigh the relative benefits of ensuring complete elimination from a zone or minimizing reinvasion risk. This is complicated in urban areas, where habitat heterogeneity and a lack of baseline ecological knowledge increase uncertainty. We applied a spatial agent-based model to predict the reinvasion of a well-studied species, the brushtail possum (Trichosurus vulpecula), across an urban area onto a peninsula that is the site of an elimination campaign in Aotearoa New Zealand. We represented fine-scale urban habitat heterogeneity in a land cover layer and tested management scenarios that varied four factors: the density of possums remaining following an elimination attempt, the maintenance trap density on the peninsula, and effort expended toward preventing reinvasion by means of a high-density trap buffer at the peninsula isthmus or control of the source population adjacent to the peninsula. We found that achieving complete elimination on the peninsula was crucial to avoid rapid repopulation. The urban isthmus was predicted to act as a landscape barrier and restrict immigration onto the peninsula, but reliance on this barrier alone would fail to prevent repopulation. In combination, complete elimination, buffer zone, and source population control could reduce the probability of possum repopulation to near zero. Our findings support urban landscape barriers as one tool for sequential invasive mammal elimination but reaffirm that novel methods to expose residual individuals to control will be necessary to secure elimination in management zones. Work to characterize the urban ecology of many invasive mammals is still needed.

The importance of urban gardens in supporting children's biophilia.

Exposure to and connection with nature is increasingly recognized as providing significant well-being benefits for adults and children. Increasing numbers of children growing up in urban areas need access to nature to experience these benefits and develop a nature connection. Under the biophilia hypothesis, children should innately affiliate to nature. We investigated children's independent selection of spaces in their neighborhoods in relation to the biodiversity values of those spaces, in three New Zealand cities, using resource-selection analysis. Children did not preferentially use the more biodiverse areas in their neighborhoods. Private gardens and yards were the most preferred space, with the quality of these spaces the most important factor defining children's exposure to nature. Children's reliance on gardens and yards for nature experiences raises concerns for their development of a nature connection, given disparities in biodiversity values of private gardens in relation to socioeconomic status, and the decline in sizes of private gardens in newer urban developments.

Invasive mammal eradication on islands results in substantial conservation gains.

More than US$21 billion is spent annually on biodiversity conservation. Despite their importance for preventing or slowing extinctions and preserving biodiversity, conservation interventions are rarely assessed systematically for their global impact. Islands house a disproportionately higher amount of biodiversity compared with mainlands, much of which is highly threatened with extinction. Indeed, island species make up nearly two-thirds of recent extinctions. Islands therefore are critical targets of conservation. We used an extensive literature and database review paired with expert interviews to estimate the global benefits of an increasingly used conservation action to stem biodiversity loss: eradication of invasive mammals on islands. We found 236 native terrestrial insular faunal species (596 populations) that benefitted through positive demographic and/or distributional responses from 251 eradications of invasive mammals on 181 islands. Seven native species (eight populations) were negatively impacted by invasive mammal eradication. Four threatened species had their International Union for the Conservation of Nature (IUCN) Red List extinction-risk categories reduced as a direct result of invasive mammal eradication, and no species moved to a higher extinction-risk category. We predict that 107 highly threatened birds, mammals, and reptiles on the IUCN Red List-6% of all these highly threatened species-likely have benefitted from invasive mammal eradications on islands. Because monitoring of eradication outcomes is sporadic and limited, the impacts of global eradications are likely greater than we report here. Our results highlight the importance of invasive mammal eradication on islands for protecting the world's most imperiled fauna.

Pollution, habitat loss, fishing, and climate change as critical threats to penguins.

Cumulative human impacts across the world's oceans are considerable. We therefore examined a single model taxonomic group, the penguins (Spheniscidae), to explore how marine species and communities might be at risk of decline or extinction in the southern hemisphere. We sought to determine the most important threats to penguins and to suggest means to mitigate these threats. Our review has relevance to other taxonomic groups in the southern hemisphere and in northern latitudes, where human impacts are greater. Our review was based on an expert assessment and literature review of all 18 penguin species; 49 scientists contributed to the process. For each penguin species, we considered their range and distribution, population trends, and main anthropogenic threats over the past approximately 250 years. These threats were harvesting adults for oil, skin, and feathers and as bait for crab and rock lobster fisheries; harvesting of eggs; terrestrial habitat degradation; marine pollution; fisheries bycatch and resource competition; environmental variability and climate change; and toxic algal poisoning and disease. Habitat loss, pollution, and fishing, all factors humans can readily mitigate, remain the primary threats for penguin species. Their future resilience to further climate change impacts will almost certainly depend on addressing current threats to existing habitat degradation on land and at sea. We suggest protection of breeding habitat, linked to the designation of appropriately scaled marine reserves, including in the High Seas, will be critical for the future conservation of penguins. However, large-scale conservation zones are not always practical or politically feasible and other ecosystem-based management methods that include spatial zoning, bycatch mitigation, and robust harvest control must be developed to maintain marine biodiversity and ensure that ecosystem functioning is maintained across a variety of scales.

Consistent Site-Specific Foraging Behaviours of Yellow-eyed Penguins/Hoiho Breeding on Stewart Island, New Zealand.

The endangered yellow-eyed penguin/hoiho (Megadyptes antipodes) predominantly forages benthically within its mainland range and shows high foraging site fidelity. Identifying consistencies in foraging locations can allow effective conservation, especially when managing bycatch risk. This study investigated the at-sea distribution of penguins breeding on Stewart Island to explore site-specific foraging strategies and inform fisheries management. During the 2020/21 season, 19 adult breeding yellow-eyed penguins from Port Pegasus, Paterson Inlet, and Codfish Island were fitted with GPS-TDR dive loggers to track their movements and diving behaviours. A total of 25,696 dives were recorded across 91 foraging trips. Birds from Port Pegasus reached significantly greater depths, spent longer at the seafloor, and performed longer dives. They also had the smallest foraging distribution, with most activity concentrated inshore. Compared to Port Pegasus, foraging radii and trip lengths were twice as large for Paterson Inlet and four times larger at Codfish Island. Despite differences in available foraging habitat, considerable individual and intra-site consistency for preferred foraging locations was observed. Localised behaviour and inter-site differences in dive metrics suggest significant plasticity in foraging ecology across their mainland range; however, individual behaviour and preferred foraging locations were extremely predictable. Thus, risk of mortality from fisheries can be quantified and managed accordingly.

The role of allochrony in influencing interspecific differences in foraging distribution during the non-breeding season between two congeneric crested penguin species.

Mechanisms promoting coexistence between closely related species are fundamental for maintaining species diversity. Mechanisms of niche differentiation include allochrony which offsets the peak timing of resource utilisation between species. Many studies focus on spatial and temporal niche partitioning during the breeding season, few have investigated the role allochrony plays in influencing interspecific segregation of foraging distribution and ecology between congeneric species during the non-breeding season. We investigated the non-breeding migrations of Snares (Eudyptes robustus) and Fiordland penguins (Eudyptes pachyrhynchus), closely related species breeding between 100-350 km apart whose migration phenology differs by two months. Using light geolocation tracking, we examined the degree of overlap given the observed allochrony and a hypothetical scenario where the species commence migration simultaneously. We found that Fiordland penguins migrated to the Sub-Antarctic Frontal Zone and Polar Frontal Zone in the austral autumn whereas Snares penguins disperse westwards staying north of the Sub-Tropical Front in the austral winter. Our results suggest that allochrony is likely to be at the root of segregation because the relative profitability of the different water masses that the penguins forage in changes seasonally which results in the two species utilising different areas over their core non-breeding periods. Furthermore, allochrony reduces relatively higher levels of spatiotemporal overlap during the departure and arrival periods, when the close proximity of the two species' colonies would cause the birds to congregate in similar areas, resulting in high interspecific competition just before the breeding season. Available evidence from other studies suggests that the shift in phenology between these species has arisen from adaptive radiation and phenological matching to the seasonality of local resource availability during the breeding season and reduced competitive overlap over the non-breeding season is likely to be an incidental outcome.

Lost in translation or deliberate falsification? Genetic analyses reveal erroneous museum data for historic penguin specimens.

Historic museum specimens are increasingly used to answer a wide variety of questions in scientific research. Nevertheless, the scientific value of these specimens depends on the authenticity of the data associated with them. Here we use individual-based genetic analyses to demonstrate erroneous locality information for archive specimens from the late nineteenth century. Specifically, using 10 microsatellite markers, we analysed 350 contemporary and 43 historic yellow-eyed penguin (Megadyptes antipodes) specimens from New Zealand's South Island and sub-Antarctic regions. Factorial correspondence analysis and an assignment test strongly suggest that eight of the historic specimens purportedly of sub-Antarctic origin were in fact collected from the South Island. Interestingly, all eight specimens were obtained by the same collector, and all are currently held in the same museum collection. Further inspection of the specimen labels and evaluation of sub-Antarctic voyages did not reveal whether the erroneous data are caused by incorrect labelling or whether deliberate falsification was at play. This study highlights a promising extension to the well-known applications of assignment tests in molecular ecology, which can complement methods that are currently being applied for error detection in specimen data. Our results also serve as a warning to all who use archive specimens to invest time in the verification of collection information.

Relict or colonizer? Extinction and range expansion of penguins in southern New Zealand.

Recent human expansion into the Pacific initiated a dramatic avian extinction crisis, and surviving taxa are typically interpreted as declining remnants of previously abundant populations. As a case in point, New Zealand's endangered yellow-eyed penguin (Megadyptes antipodes) is widely considered to have been more abundant and widespread in the past. By contrast, our genetic and morphological analyses of prehistoric, historic and modern penguin samples reveal that this species expanded its range to the New Zealand mainland only in the last few hundred years. This range expansion was apparently facilitated by the extinction of M. antipodes' previously unrecognized sister species following Polynesian settlement in New Zealand. Based on combined genetic and morphological data, we describe this new penguin species, the first known to have suffered human-mediated extinction. The range expansion of M. antipodes so soon after the extinction of its sister species supports a historic paradigmatic shift in New Zealand Polynesian culture. Additionally, such a dynamic biological response to human predation reveals a surprising and less recognized potential for species to have benefited from the extinction of their ecologically similar sister taxa and highlights the complexity of large-scale extinction events.

Multilocus assignment analyses reveal multiple units and rare migration events in the recently expanded yellow-eyed penguin (Megadyptes antipodes).

The identification of demographically independent populations and the recognition of management units have been greatly facilitated by the continuing advances in genetic tools. Managements units now play a key role in short-term conservation management programmes of declining species, but their importance in expanding populations receives comparatively little attention. The endangered yellow-eyed penguin (Megadyptes antipodes) expanded its range from the subantarctic to New Zealand's South Island a few hundred years ago and this new population now represents almost half of the species' total census size. This dramatic expansion attests to M. antipodes' high dispersal abilities and suggests the species is likely to constitute a single demographic population. Here we test this hypothesis of panmixia by investigating genetic differentiation and levels of gene flow among penguin breeding areas using 12 autosomal microsatellite loci along with mitochondrial control region sequence analyses for 350 individuals. Contrary to our hypothesis, however, the analyses reveal two genetically and geographically distinct assemblages: South Island vs. subantarctic populations. Using assignment tests, we recognize just two first-generation migrants between these populations (corresponding to a migration rate of < 2%), indicating that ongoing levels of long-distance migration are low. Furthermore, the South Island population has low genetic variability compared to the subantarctic population. These results suggest that the South Island population was founded by only a small number of individuals, and that subsequent levels of gene flow have remained low. The demographic independence of the two populations warrants their designation as distinct management units and conservation efforts should be adjusted accordingly to protect both populations.

Creating proxies of extinct species: the bioethics of de-extinction.

In April 2013 the National Geographic magazine carried the cover title 'Reviving extinct species, we can, but should we?' suggesting that the technical challenges had been met, but some ethical concerns remained unresolved. Seven years later it is clear that this is not the case. Here we consider the technical scope, the uncertainties, and some of the bioethical issues raised by the future prospect of de-extinction. Biodiversity and welfare will not always align, and when a clash is unavoidable, a trade-off will be necessary, seeking the greatest overall value. De-extinction challenges our current conservation mind-set that seeks to preserve the species and population diversity that currently exists. But if we want to sustain and enhance a biodiverse natural world we might have to be forward looking and embrace the notion of bio-novelty by focussing more on ecosystem stability and resilience, rather than backward looking and seeking to try and recreate lost worlds.

Parasites Lost: Neglecting a Crucial Element in De-Extinction.

Bringing back iconic and beloved extinct species is a hot and intensely debated current topic. Yet, the parasites of de-extinction candidate species have remained largely overlooked in this debate. Here we point out the potentially far-reaching ecological impacts of bringing back extinct species without their parasites.

Effects of Warm Temperatures on Metabolic Rate and Evaporative Water Loss in Tuatara, a Cool-Climate Rhynchocephalian Survivor.

The thermal sensitivity of physiological rates is a key characteristic of organisms. For tuatara (Sphenodon punctatus), the last surviving member of the reptilian order Rhynchocephalia and an unusually cold-tolerant reptile, we aimed to clarify responses in indices of metabolic rate (oxygen consumption [[Formula: see text]] and carbon dioxide production [[Formula: see text]]) as well as rates of total evaporative water loss (TEWL) to temperatures at the warmer end of the known tolerated range; currently, patterns for metabolic rate are unclear above 25°C, and TEWL has not been measured above 25°C. We first established that metabolic rate was lowest during the photophase and then measured [Formula: see text], [Formula: see text], and TEWL at six temperatures (12°, 20°, 24°, 27°, 29°, and 30°C) during this phase. Consistent with our predictions, we found that mass-adjusted [Formula: see text], [Formula: see text], and TEWL increased at least 3.5-fold between 12° and 30°C (at 30°C, rates were 2.509 mL g-1 h-1, 2.001 mL g-1 h-1, and 1.829 mg-1 g-1 h-1, respectively). Temperature coefficients (Q10 values) for mass-adjusted [Formula: see text] and TEWL showed thermal dependence between 12° and 29°C but with a reduced increase or thermal independence between 29° and 30°C. There was no observed effect of egg incubation temperature (inferred sex) on the subsequent metabolic rates of juveniles. The respiratory exchange ratio implied a switch from carbohydrate metabolism at <22°C to lipid metabolism at >27°C. The rigorous measurement of [Formula: see text] and TEWL provides a basis for future studies to predict the thermal sensitivity of tuatara to human-mediated climate change.

Marathon penguins - Reasons and consequences of long-range dispersal in Fiordland penguins / Tawaki during the pre-moult period.

Migratory species often roam vast distances bringing them into contact with diverse conditions and threats that could play significant roles in their population dynamics. This is especially true if long-range travels occur within crucial stages of a species' annual life-cycle. Crested penguins, for example, usually disperse over several hundreds of kilometres after completing the energetically demanding breeding season and in preparation for the costly annual moult. A basic understanding of crested penguins' pre-moult dispersal is therefore paramount in order to be able to assess factors affecting individual survival. The Fiordland penguin, or Tawaki, the only crested penguin species breeding on the New Zealand mainland, is currently one of the least studied and rarest penguin species in the world. We successfully satellite tracked the pre-moult dispersal of 17 adult Tawaki from a single colony located in the species' northern breeding distribution. Over the course of 8-10 weeks the penguins travelled up to 2,500 km away from their breeding colony, covering total swimming distances of up to 6,800 km. During outbound travels all penguins headed south-west within a well-defined corridor before branching out towards two general trip destinations. Birds leaving in late November travelled towards the Subtropical Front some 800 km south of Tasmania, whereas penguins that left in December headed further towards the subantarctic front. Using K-select analysis we examined the influence of oceanographic factors on the penguins' dispersal. Water depth, surface current velocity and sea level anomalies had the greatest influence on penguin movements at the subantarctic Front, while sea surface temperature and chlorophyll a concentration were key for birds travelling to the subtropical front. We discuss our findings in the light of anthropogenic activities (or lack thereof) in the regions visited by the penguins as well as the potential consequences of Tawaki pre-moult dispersal for the species' breeding distribution on the New Zealand mainland.

De-extinction and Barriers to the Application of New Conservation Tools.

Decades of globally coordinated work in conservation have failed to slow the loss of biodiversity. To do better-even if that means nothing more than failing less spectacularly-bolder thinking is necessary. One of the first possible conservation applications of synthetic biology to be debated is the use of genetic tools to resurrect once-extinct species. Since the currency of conservation is biodiversity and the discipline of conservation biology was formed around the prevention of species extinctions, the prospect of reversing extinctions might have been expected to generate unreserved enthusiasm. But it was not universal acclaim that greeted the coming-out party for "de-extinction" that was the TEDx conference and accompanying National Geographic feature in 2013. Why the concern, the skepticism, even the hostility among many conservationists about the idea of restoring lost species? And how does this professional concern relate to public perception and support for conservation? This essay explores the barriers to the acceptance of risky new genomic-based conservation tools by considering five key areas and associated questions that could be addressed in relation to any new conservation tool. I illustrate these using the specific example of de-extinction, and in doing so, I consider whether de-extinction would necessarily be the best first point of engagement between conservation biology and synthetic biology.

Evidence for high inter-generational individual quality in yellow-eyed penguins.

Longitudinal studies focusing on lifetime reproductive success (LRS) have been used to measure individual breeding performance and identify commonalities among successful breeders. By extending the focus to subsequent generations we identify a proportion of high-quality individuals that contribute disproportionately to the population over multiple generations. We used 23 years of yellow-eyed penguin (Megadyptes antipodes) breeding data from one breeding area to identify the proportion of individual birds that raised successful breeders, which in turn raised offspring. We explored which life-history components influenced LRS, as this knowledge would enable conservation resources to be focused on high-performing individuals in this endangered population. From 2,147 birds marked as chicks, 370 (17.2%) survived to adulthood and recruited to their natal location, of which 219 (10.2%) fledged offspring: 124 (56.6%) of the 219 birds produced offspring that recruited as breeders. Only 102 birds (4.8% of 2,147) fledged first-generation offspring that in turn fledged offspring (second-generation offspring, or grand-offspring). We found that ∼25% of the birds that survived to breed had above-average LRS as well as above-average numbers of grand-offspring, and were more likely to have produced first-generation chicks that recruited and also produced above-average numbers of second-generation chicks. Our findings suggest that there is a core of "super-breeders" that contribute disproportionately to the population over successive generations. Lifespan and age-at-first-breeding were correlated with LRS. We suggest that traits of birds relating to longevity, health (e.g., immunocompetence) and fitness could be examined to identify potential links with high LRS and inter-generational fecundity. "Super-breeders" appear to consistently achieve high LRS and long lifespans in a stochastic environment, demonstrating greater resilience in the face of extreme events.

Is Reintroduction Biology an Effective Applied Science?

Reintroduction biology is a field of scientific research that aims to inform translocations of endangered species. We review two decades of published literature to evaluate whether reintroduction science is evolving in its decision-support role, as called for by advocates of evidence-based conservation. Reintroduction research increasingly addresses a priori hypotheses, but remains largely focused on short-term population establishment. Similarly, studies that directly assist decisions by explicitly comparing alternative management actions remain a minority. A small set of case studies demonstrate full integration of research in the reintroduction decision process. We encourage the use of tools that embed research in decision-making, particularly the explicit consideration of multiple management alternatives because this is the crux of any management decisions.

Spending limited resources on de-extinction could lead to net biodiversity loss.

There is contentious debate surrounding the merits of de-extinction as a biodiversity conservation tool. Here, we use extant analogues to predict conservation actions for potential de-extinction candidate species from New Zealand and the Australian state of New South Wales, and use a prioritization protocol to predict the impacts of reintroducing and maintaining populations of these species on conservation of extant threatened species. Even using the optimistic assumptions that resurrection of species is externally sponsored, and that actions for resurrected species can share costs with extant analogue species, public funding for conservation of resurrected species would lead to fewer extant species that could be conserved, suggesting net biodiversity loss. If full costs of establishment and maintenance for resurrected species populations were publicly funded, there could be substantial sacrifices in extant species conservation. If conservation of resurrected species populations could be fully externally sponsored, there could be benefits to extant threatened species. However, such benefits would be outweighed by opportunity costs, assuming such discretionary money could directly fund conservation of extant species. Potential sacrifices in conservation of extant species should be a crucial consideration in deciding whether to invest in de-extinction or focus our efforts on extant species.