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.

Seabird mortality induced by land-based artificial lights.

Artificial lights at night cause high mortality of seabirds, one of the most endangered groups of birds globally. Fledglings of burrow-nesting seabirds, and to a lesser extent adults, are attracted to and then grounded (i.e., forced to land) by lights when they fly at night. We reviewed the current state of knowledge of seabird attraction to light to identify information gaps and propose measures to address the problem. Although species in families such as Alcidae and Anatidae can be grounded by artificial light, the most affected seabirds are petrels and shearwaters (Procellariiformes). At least 56 species of Procellariiformes, more than one-third of them (24) threatened, are subject to grounding by lights. Seabirds grounded by lights have been found worldwide, mainly on oceanic islands but also at some continental locations. Petrel breeding grounds confined to formerly uninhabited islands are particularly at risk from light pollution due to tourism and urban sprawl. Where it is impractical to ban external lights, rescue programs of grounded birds offer the most immediate and employed mitigation to reduce the rate of light-induced mortality and save thousands of birds every year. These programs also provide useful information for seabird management. However, these data are typically fragmentary, biased, and uncertain and can lead to inaccurate impact estimates and poor understanding of the phenomenon of seabird attraction to lights. We believe the most urgently needed actions to mitigate and understand light-induced mortality of seabirds are estimation of mortality and effects on populations; determination of threshold light levels and safe distances from light sources; documentation of the fate of rescued birds; improvement of rescue campaigns, particularly in terms of increasing recovery rates and level of care; and research on seabird-friendly lights to reduce attraction.

A novel spatio-temporal scale based on ocean currents unravels environmental drivers of reproductive timing in a marine predator.

Life-history strategies have evolved in response to predictable patterns of environmental features. In practice, linking life-history strategies and changes in environmental conditions requires comparable space-time scales between both processes, a difficult match in most marine system studies. We propose a novel spatio-temporal and dynamic scale to explore marine productivity patterns probably driving reproductive timing in the inshore little penguin (Eudyptula minor), based on monthly data on ocean circulation in the Southern Ocean, Australia. In contrast to what occurred when considering any other fixed scales, little penguin's highly variable laying date always occurred within the annual peak of ocean productivity that emerged from our newly defined dynamic scale. Additionally, local sea surface temperature seems to have triggered the onset of reproduction, acting as an environmental cue informing on marine productivity patterns at our dynamic scale. Chlorophyll-a patterns extracted from this scale revealed that environment factors in marine ecosystems affecting breeding decisions are related to a much wider region than foraging areas that are commonly used in current studies investigating the link between animals' life history and their environment. We suggest that marine productivity patterns may be more predictable than previously thought when environmental and biological data are examined at appropriate scales.

Environmental variability drives shifts in the foraging behaviour and reproductive success of an inshore seabird.

Marine animals forage in areas that aggregate prey to maximize their energy intake. However, these foraging 'hot spots' experience environmental variability, which can substantially alter prey availability. To survive and reproduce animals need to modify their foraging in response to these prey shifts. By monitoring their inter-annual foraging behaviours, we can understand which environmental variables affect their foraging efficiency, and can assess how they respond to environmental variability. Here, we monitored the foraging behaviour and isotopic niche of little penguins (Eudyptula minor), over 3 years (2008, 2011, and 2012) of climatic and prey variability within Port Phillip Bay, Australia. During drought (2008), penguins foraged in close proximity to the Yarra River outlet on a predominantly anchovy-based diet. In periods of heavy rainfall, when water depth in the largest tributary into the bay (Yarra River) was high, the total distance travelled, maximum distance travelled, distance to core-range, and size of core- and home-ranges of penguins increased significantly. This larger foraging range was associated with broad dietary diversity and high reproductive success. These results suggest the increased foraging range and dietary diversity of penguins were a means to maximize resource acquisition rather than a strategy to overcome local depletions in prey. Our results demonstrate the significance of the Yarra River in structuring predator-prey interactions in this enclosed bay, as well as the flexible foraging strategies of penguins in response to environmental variability. This plasticity is central to the survival of this small-ranging, resident seabird species.

Fine-scale spatial age segregation in the limited foraging area of an inshore seabird species, the little penguin.

Competition for food resources can result in spatial and dietary segregation among individuals from the same species. Few studies have looked at such segregations with the combined effect of sex and age in species with short foraging ranges. In this study we examined the 3D spatial use of the environment in a species with a limited foraging area. We equipped 26 little penguins (Eudyptula minor) of known age, sex, and breeding output with GPS (location) and accelerometer (body acceleration and dive depth) loggers. We obtained dietary niche information from the isotopic analysis of blood tissue. We controlled for confounding factors of foraging trip length and food availability by sampling adults at guard stage when parents usually make one-day trips. We observed a spatial segregation between old (>11 years old) and middle-aged penguins (between 5 and 11 years old) in the foraging area. Old penguins foraged closer to the shore, in shallower water. Despite observing age-specific spatial segregation, we found no differences in the diving effort and foraging efficiency between age classes and sexes. Birds appeared to target similar prey types, but showed age-specific variation in their isotopic niche width. We hypothesize that this age-specific segregation was primarily determined by a "cohort effect" that would lead individuals sharing a common life history (i.e. having fledged and dispersed around the same age) to forage preferentially together or to share similar foraging limitations.

Exploring subcolony differences in foraging and reproductive success: the influence of environmental conditions on a central place foraging seabird.

While differences in foraging and reproductive success are well studied between seabird colonies, they are less understood at a smaller subcolony scale. Working with little penguins (Eudyptula minor) at Phillip Island, Australia, we used an automated penguin monitoring system and performed regular nest checks at two subcolonies situated 2 km apart during the 2015/2016 breeding seasons. We examined whether foraging and reproductive success differed between subcolonies. We used satellite data to examine how sea surface temperature, as environmental pressure, in the foraging regions from each subcolony influenced their foraging performance. In the pre-laying and incubation breeding stages, the birds from one subcolony had a lower foraging success than birds from the other. However, this pattern was reversed between the subcolonies in the guard and post-guard stages. Breeding success data from the two subcolonies from 2004-2018 showed that reproductive success and mean egg-laying had a negative relationship with sea surface temperature. We highlighted that variation in foraging and reproductive success can arise in subcolonies, likely due to different responses to environmental conditions and prey availability. Differences at the subcolony level can help refine, develop and improve appropriate species management plans for conserving a range of colonial central place seabirds.

Unpacking the lifelong secrets of little penguins: individual quality, energy allocation, and stochasticity in defining fitness.

While the heterogeneity among individuals of a population is more and more documented, questions on the paths through which it arises, particularly whether it is linked to fixed heterogeneity or chance alone, are still widely debated. Here, we tested how individual quality, energy allocation trade-offs, and environmental stochasticity define individual fitness. To do so, we simultaneously investigated the contribution of 18 life-history traits to the fitness of breeding little penguins (Eudyptula minor), using a structural equation model. Fitness was highly variable amongst the 162 birds monitored over their entire lifespan. It increased with the individual penguin's ability to increase (a) the number of breeding events (i.e., living longer, breeding younger, breeding more often, and producing more second clutches) and (b) the breeding success per event through increased foraging performances (i.e., mass gained at sea). While all three processes (stochasticity, individual quality, and allocation trade-offs) affected fitness, interindividual variability in fitness was mainly driven by individual quality, birds consistently breeding earlier in the season and displaying higher foraging efficiency exhibiting higher fitness. Why some birds consistently can perform better at sea and breed earlier remains a question to investigate to understand how selection applies to these traits.

New and legacy persistent organic pollutants (POPs) in breeding seabirds from the East Antarctic.

Persistent organic pollutants (POPs) are pervasive and a significant threat to the environment worldwide. Yet, reports of POP levels in Antarctic seabirds based on blood are scarce, resulting in significant geographical gaps. Blood concentrations offer a snapshot of contamination within live populations, and have been used widely for Arctic and Northern Hemisphere seabird species but less so in Antarctica. This paper presents levels of legacy POPs (polychlorinated biphenyls (PCBs), organochlorine pesticides (OCPs) and polybrominated diphenyl ethers (PBDEs)) and novel brominated flame retardants (NBFRs) in the blood of five Antarctic seabird species breeding within Prydz Bay, East Antarctica. Legacy PCBs and OCPs were detected in all species sampled, with Adélie penguins showing comparatively high ∑PCB levels (61.1 ± 87.6 ng/g wet weight (ww)) compared to the four species of flying seabirds except the snow petrel (22.5 ± 15.5 ng/g ww), highlighting that legacy POPs are still present within Antarctic wildlife despite decades-long bans. Both PBDEs and NBFRs were detected in trace levels for all species and hexabromobenzene (HBB) was quantified in cape petrels (0.3 ± 0.2 ng/g ww) and snow petrels (0.2 ± 0.1 ng/g ww), comparable to concentrations found in Arctic seabirds. These results fill a significant data gap within the Antarctic region for POPs studies, representing a crucial step forward assessing the fate and impact of legacy POPs contamination in the Antarctic environment.

The role of individual variability on the predictive performance of machine learning applied to large bio-logging datasets.

Animal-borne tagging (bio-logging) generates large and complex datasets. In particular, accelerometer tags, which provide information on behaviour and energy expenditure of wild animals, produce high-resolution multi-dimensional data, and can be challenging to analyse. We tested the performance of commonly used artificial intelligence tools on datasets of increasing volume and dimensionality. By collecting bio-logging data across several sampling seasons, datasets are inherently characterized by inter-individual variability. Such information should be considered when predicting behaviour. We integrated both unsupervised and supervised machine learning approaches to predict behaviours in two penguin species. The classified behaviours obtained from the unsupervised approach Expectation Maximisation were used to train the supervised approach Random Forest. We assessed agreement between the approaches, the performance of Random Forest on unknown data and the implications for the calculation of energy expenditure. Consideration of behavioural variability resulted in high agreement (> 80%) in behavioural classifications and minimal differences in energy expenditure estimates. However, some outliers with < 70% of agreement, highlighted how behaviours characterized by signal similarity are confused. We advise the broad bio-logging community, approaching these large datasets, to be cautious when upscaling predictions, as this might lead to less accurate estimates of behaviour and energy expenditure.

Plasticity in foraging strategies of inshore birds: how Little Penguins maintain body reserves while feeding offspring.

Breeding animals face important time and energy constraints when caring for themselves and their offspring. For long-lived species, life-history theory predicts that parents should favor survival over current reproductive attempts, thus investing more into their own maintenance than the provisioning of their young. In seabirds, provisioning strategies may additionally be influenced by the distance between breeding sites and foraging areas, and offshore and inshore species should thus exhibit different strategies. Here, we examine the provisioning strategies of an inshore seabird using a long-term data set on more than 200 Little Penguins, Eudyptula minor. They alternated between two consecutive long and several short foraging trips all along chick rearing, a strategy almost never observed for inshore animals. Short trips allowed for regular provisioning of the chicks (high feeding frequency and larger meals), whereas long trips were performed when parent body mass was low and enabled them to rebuild their reserves, suggesting that adult body condition may be a key factor in initiating long trips. Inshore seabirds do use dual strategies of alternating short and long trips, but from our data, on a simpler and less flexible way than for offshore birds.

The consequences of chaos: Foraging activity of a marine predator remains impacted several days after the end of a storm.

As extreme weather is expected to become more frequent with global climate change, it is crucial to evaluate the capacity of species to respond to short-term and unpredictable events. Here, we examined the effect of a strong storm event during the chick-rearing stage of little penguins (Eudyptula minor) from a mega colony in southern Australia. We investigated how a 3-day storm affected the foraging behaviour of little penguins by comparing their foraging activities and body mass change before, during and after the storm event. As strong winds deepened the mixed layer in the birds' foraging zone during the storm, penguins increased their foraging trip duration, had a lower prey encounter rate and a lower body mass gain. The adverse effects on the foraging efficiency of little penguins continued several days after the storm ceased; even though the water column stratification had returned as before the storm, suggesting a prolonged effect of the storm event on the prey availability. Thus, short-term stochastic events can have an extended impact on the foraging efficiency of penguins. When occurring at a crucial stage of breeding, this may affect breeding success.

Making the most of the old age: Autumn breeding as an extra reproductive investment in older seabirds.

The extrinsic and intrinsic factors affecting differing reproductive strategies among populations are central to understanding population and evolutionary ecology. To evaluate whether individual reproductive strategies responded to annual patterns in marine productivity and age-related processes in a seabird we used a long term (2003-2013), a continuous dataset on nest occupancy and attendance at the colony by little penguins (Eudyptula minor) at Phillip Island (Victoria, Australia). We found that concurrent with a secondary annual peak of marine productivity, a secondary peak in colony attendance and nest occupancy was observed in Autumn (out of the regular breeding season in spring/summer) with individuals showing mating-like behavior. Individuals attending this autumn peak averaged 2.5 years older than those individuals that exclusively bred during spring/summer. Rather than being a naïve response by younger and inexperienced birds misreading environmental cues, our data indicate that the autumn peak attendance is an earlier attempt to breed by older and more experienced penguins. Therefore, we provide strong support for the fundamental prediction of the life-history theory of increasing investment in reproduction with age to maximize lifetime fitness as future survival prospects diminish and experience increases.

Oceanic thermal structure mediates dive sequences in a foraging seabird.

Changes in marine ecosystems are easier to detect in upper-level predators, like seabirds, which integrate trophic interactions throughout the food web.Here, we examined whether diving parameters and complexity in the temporal organization of diving behavior of little penguins (Eudyptula minor) are influenced by sea surface temperature (SST), water stratification, and wind speed-three oceanographic features influencing prey abundance and distribution in the water column.Using fractal time series analysis, we found that foraging complexity, expressed as the degree of long-range correlations or memory in the dive series, was associated with SST and water stratification throughout the breeding season, but not with wind speed. Little penguins foraging in warmer/more-stratified waters exhibited greater determinism (memory) in foraging sequences, likely as a response to prey aggregations near the thermocline. They also showed higher foraging efficiency, performed more dives and dove to shallower depths than those foraging in colder/less-stratified waters.Reductions in the long-term memory of dive sequences, or in other words increases in behavioral stochasticity, may suggest different strategies concerning the exploration-exploitation trade-off under contrasting environmental conditions.

A baseline for POPs contamination in Australian seabirds: little penguins vs. short-tailed shearwaters.

While globally distributed throughout the world's ecosystems, there is little baseline information on persistent organic pollutants (POPs) in marine environments in Australia and, more broadly, the Southern Hemisphere. To fill this knowledge gap, we collected baseline information on POPs in migratory short-tailed shearwaters (Ardenna tenuirostris) from Fisher Island, Tasmania, and resident little penguins (Eudyptula minor) from Phillip Island, Victoria. Levels of polychlorinated biphenyls (PCBs), organochlorine pesticides (OCPs) and brominated flame retardants (BFRs) were determined from blood samples, with total contamination ranging 7.6-47.7 ng/g ww for short-tailed shearwaters and 0.12-46.9 ng/g ww for little penguins. In both species contamination followed the same pattern where PCBs>OCPs>BFRs. BFR levels included the presence of the novel flame retardant hexabromobenzene (HBB). These novel results of POPs in seabirds in southeast Australia provide important information on the local (penguins) and global (shearwaters) distribution of POPs in the marine environment.

Impact of small-scale environmental perturbations on local marine food resources: a case study of a predator, the little penguin.

Although the impact of environmental changes on the demographic parameters of top predators is well established, the mechanisms by which populations are affected remain poorly understood. Here, we show that a reduction in the thermal stratification of coastal water masses between 2005 and 2006 was associated with reduced foraging and breeding success of little penguins Eudyptula minor, major bio-indicators of the Bass Strait ecosystem in southern Australia. The foraging patterns of the penguins suggest that their prey disperse widely in poorly stratified waters, leading to reduced foraging efficiency and poor breeding success. Mixed water regimes resulting from storms are currently unusual during the breeding period of these birds, but are expected to become more frequent due to climate change.

Translating Marine Animal Tracking Data into Conservation Policy and Management.

There have been efforts around the globe to track individuals of many marine species and assess their movements and distribution, with the putative goal of supporting their conservation and management. Determining whether, and how, tracking data have been successfully applied to address real-world conservation issues is, however, difficult. Here, we compile a broad range of case studies from diverse marine taxa to show how tracking data have helped inform conservation policy and management, including reductions in fisheries bycatch and vessel strikes, and the design and administration of marine protected areas and important habitats. Using these examples, we highlight pathways through which the past and future investment in collecting animal tracking data might be better used to achieve tangible conservation benefits.

Seabird plastic ingestion differs among collection methods: Examples from the short-tailed shearwater.

Despite the increase of literature on seabird plastic ingestion in recent years, few studies have assessed how plastic loads vary according to different sampling methods. Most studies use necropsies of seabirds with a natural cause of death, e.g. beached or predated, to determine plastic loads and monitor marine debris. Sampling naturally dead seabirds may be biased as they have perished because of their intrinsic factors, e.g. poor body condition, high parasite loads, sickness or predation, affecting estimates of plastic loads. However, seabirds killed accidentally may be more representative of the population. Here, we used the short-tailed shearwater Ardenna tenuirostris to test different sampling methods: naturally beached fledglings and accidentally road-killed fledglings after being attracted and grounded by artificial lights. We compared plastic load, body condition, and feeding strategies (through using feathers' δ13C and δ15N isotope niche) between beached and road-killed fledglings. Beached birds showed higher plastic loads, poorer body condition and reduced isotopic variability, suggesting that this group is not a representative subsample of the whole cohort of the fledgling population. Our results might have implications for long-term monitoring programs of seabird plastic ingestion. Monitoring plastic debris through beached birds could overestimate plastic ingestion by the entire population. We encourage the establishment of refined monitoring programs using fledglings grounded by light pollution if available. These samples focus on known cohorts from the same population. The fledgling plastic loads are transferred from parents during parental feeding, accumulating during the chick-rearing period. Thus, these fledglings provide a higher and valuable temporal resolution, which is more useful and informative than unknown life history of beached birds.

Penguin colony attendance under artificial lights for ecotourism.

Wildlife watching is an emerging ecotourism activity around the world. In Australia and New Zealand, night viewing of little penguins attracts hundreds of thousands of visitors per year. As penguins start coming ashore after sunset, artificial lighting is essential to allow visitors to view them in the dark. This alteration of the nightscape warrants investigation for any potential effects of artificial lighting on penguin behavior. We experimentally tested how penguins respond to different light wavelengths (colors) and intensities to examine effects on the colony attendance behavior at two sites on Phillip Island, Australia. At one site, nocturnal artificial illumination has been used for penguin viewing for decades, whereas at the other site, the only light is from the natural night sky. Light intensity did not affect colony attendance behaviors of penguins at the artificially lit site, probably due to penguin habituation to lights. At the not previously lit site, penguins preferred lit paths over dark paths to reach their nests. Thus, artificial light might enhance penguin vision at night and consequently it might reduce predation risk and energetic costs of locomotion through obstacle and path detection. Although penguins are faithful to their path, they can be drawn to artificial lights at small spatial scale, so light pollution could attract penguins to undesirable lit areas. When artificial lighting is required, we recommend keeping lighting as dim and time-restricted as possible to mitigate any negative effects on the behavior of penguins and their natural habitat.

Moving in the Anthropocene: Global reductions in terrestrial mammalian movements.

Animal movement is fundamental for ecosystem functioning and species survival, yet the effects of the anthropogenic footprint on animal movements have not been estimated across species. Using a unique GPS-tracking database of 803 individuals across 57 species, we found that movements of mammals in areas with a comparatively high human footprint were on average one-half to one-third the extent of their movements in areas with a low human footprint. We attribute this reduction to behavioral changes of individual animals and to the exclusion of species with long-range movements from areas with higher human impact. Global loss of vagility alters a key ecological trait of animals that affects not only population persistence but also ecosystem processes such as predator-prey interactions, nutrient cycling, and disease transmission.

Climate impacts on global hot spots of marine biodiversity.

Human activities drive environmental changes at scales that could potentially cause ecosystem collapses in the marine environment. We combined information on marine biodiversity with spatial assessments of the impacts of climate change to identify the key areas to prioritize for the conservation of global marine biodiversity. This process identified six marine regions of exceptional biodiversity based on global distributions of 1729 species of fish, 124 marine mammals, and 330 seabirds. Overall, these hot spots of marine biodiversity coincide with areas most severely affected by global warming. In particular, these marine biodiversity hot spots have undergone local to regional increasing water temperatures, slowing current circulation, and decreasing primary productivity. Furthermore, when we overlapped these hot spots with available industrial fishery data, albeit coarser than our estimates of climate impacts, they suggest a worrying coincidence whereby the world's richest areas for marine biodiversity are also those areas mostly affected by both climate change and industrial fishing. In light of these findings, we offer an adaptable framework for determining local to regional areas of special concern for the conservation of marine biodiversity. This has exposed the need for finer-scaled fishery data to assist in the management of global fisheries if the accumulative, but potentially preventable, effect of fishing on climate change impacts is to be minimized within areas prioritized for marine biodiversity conservation.