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Global phenological insensitivity to shifting ocean temperatures among seabirds

DOI:10.1038/s41558-018-0115-z
Authors:
Katharine Keogan at HiDef Aerial Surveying
Katharine Keogan
  • HiDef Aerial Surveying
Francis Daunt at UK Centre for Ecology & Hydrology
Francis Daunt
Sarah Wanless
Sarah Wanless
Sarah Wanless
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Richard A. Phillips at British Antarctic Survey
Richard A. Phillips
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Abstract and Figures

Reproductive timing in many taxa plays a key role in determining breeding productivity ¹, and is often sensitive to climatic conditions ² . Current climate change may alter the timing of breeding at different rates across trophic levels, potentially resulting in temporal mismatch between the resource requirements of predators and their prey ³ . This is of particular concern for higher-trophic-level organisms, whose longer generation times confer a lower rate of evolutionary rescue than primary producers or consumers ⁴ . However, the disconnection between studies of ecological change in marine systems makes it difficult to detect general changes in the timing of reproduction ⁵ . Here, we use a comprehensive meta-analysis of 209 phenological time series from 145 breeding populations to show that, on average, seabird populations worldwide have not adjusted their breeding seasons over time (-0.020 days yr⁻¹) or in response to sea surface temperature (SST) (-0.272 days °C⁻¹) between 1952 and 2015. However, marked between-year variation in timing observed in resident species and some Pelecaniformes and Suliformes (cormorants, gannets and boobies) may imply that timing, in some cases, is affected by unmeasured environmental conditions. This limited temperature-mediated plasticity of reproductive timing in seabirds potentially makes these top predators highly vulnerable to future mismatch with lower-trophic-level resources ² .
SST trends and map of study sites included in the analyses a, Across-year temporal changes in mean SST in the three months prior to breeding across all biogeographic regions, represented by slopes between 1982 (when SST time series began) and 2015 for each site. Each point represents a slope, with positive slopes indicating warming and negative slopes indicating cooling. b, Standard deviation from the mean SST at each site during the same study period. A = polar, B = subpolar, C = temperate, D = subtropical, E = tropical. c, The full data set comprises 209 time series from 61 seabird species and across 64 locations, collected between 1952 and 2015. The data include slopes for 32 genera, 9 families and 5 orders (Sphenisciformes (6), Procellariiformes (15), Suliformes (3), Pelecaniformes (5), Charadriiformes (32)) and span all seven continents. The underrepresentation of tropical time series is due to a combination of a paucity of long-term data for these regions and the asynchronous nature of breeding in many tropical species, which diminishes the informativeness of measuring the annual phenological central tendency.
SST trends and map of study sites included in the analyses a, Across-year temporal changes in mean SST in the three months prior to breeding across all biogeographic regions, represented by slopes between 1982 (when SST time series began) and 2015 for each site. Each point represents a slope, with positive slopes indicating warming and negative slopes indicating cooling. b, Standard deviation from the mean SST at each site during the same study period. A = polar, B = subpolar, C = temperate, D = subtropical, E = tropical. c, The full data set comprises 209 time series from 61 seabird species and across 64 locations, collected between 1952 and 2015. The data include slopes for 32 genera, 9 families and 5 orders (Sphenisciformes (6), Procellariiformes (15), Suliformes (3), Pelecaniformes (5), Charadriiformes (32)) and span all seven continents. The underrepresentation of tropical time series is due to a combination of a paucity of long-term data for these regions and the asynchronous nature of breeding in many tropical species, which diminishes the informativeness of measuring the annual phenological central tendency.
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Mean and between-year variance in phenology separated by hemisphere a, Differences in latitudinal gradient between Northern and Southern Hemispheres, where each data point (grey or red) represents the median timing of breeding of a population. Lines (grey = lay date, red = hatch date) represent the delay in phenology approaching the poles in days lat⁻¹, and were estimated using values from Supplementary Table 1. b, Between-year standard deviation in mean timing for residents (red dots) and migrants (grey dots). Lines are plotted from the ecological model and represent the median lay date in the mean year of study of an average surface-feeding resident bird, weighing 800 g, in a region where there is no major upwelling system. Nonlinearity in the plot is due to back calculation from the log scale.
Mean and between-year variance in phenology separated by hemisphere a, Differences in latitudinal gradient between Northern and Southern Hemispheres, where each data point (grey or red) represents the median timing of breeding of a population. Lines (grey = lay date, red = hatch date) represent the delay in phenology approaching the poles in days lat⁻¹, and were estimated using values from Supplementary Table 1. b, Between-year standard deviation in mean timing for residents (red dots) and migrants (grey dots). Lines are plotted from the ecological model and represent the median lay date in the mean year of study of an average surface-feeding resident bird, weighing 800 g, in a region where there is no major upwelling system. Nonlinearity in the plot is due to back calculation from the log scale.
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Funnel plots of phenological trends in relation to year and SST a,b, Funnel plots in relation to year (a) and SST (b). Each point represents a slope estimate from the meta-analysis, with negative slopes indicating an advance and positive slopes indicating a delay, in phenological trends. Positioning of each point on the y axis indicates the precision (1/s.e.) of the estimate. Thus, points with higher precision are expected to converge on the true average response. Lines represent the posterior for the average response or intercept (black) and its 95% CI (dashed red) from the basic model (Supplementary Tables 3a and 5a). s.e., standard error.
Funnel plots of phenological trends in relation to year and SST a,b, Funnel plots in relation to year (a) and SST (b). Each point represents a slope estimate from the meta-analysis, with negative slopes indicating an advance and positive slopes indicating a delay, in phenological trends. Positioning of each point on the y axis indicates the precision (1/s.e.) of the estimate. Thus, points with higher precision are expected to converge on the true average response. Lines represent the posterior for the average response or intercept (black) and its 95% CI (dashed red) from the basic model (Supplementary Tables 3a and 5a). s.e., standard error.
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"Global phenological insensitivity to shifting ocean temperatures
among seabirds"
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... independently from the environment), such as phenology (Keogan et al., 2018;Youngflesh et al., 2018), include some interindividual variability in the trait(i.e breeding earlier in the case of phenology). ...
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Environmental drivers of phenology in seabirds
Thesis
  • Jan 2023
Timing of important events in animal lives, such as breeding and migration, is shifting globally due to human-induced environmental change. While considered important for population resilience, the mechanisms underlying these shifts are not well understood. In this thesis, I use experimental and observational approaches to test the effects of environmental variation on breeding phenology of two seabird species: black-legged kittiwakes (Rissa tridactyla) and thick-billed murres (Uria lomvia). I focus on the role of food supply, which is often the resource that limits life history allocation, and use a diverse set of tools, including long-term monitoring, endocrinology, and biologging. First, I test whether environmental effects on phenology carry over to influence subsequent phenology. Food supply during the breeding season affected both breeding phenology and subsequent migratory phenology, demonstrating that the timing of seasonal events can be interconnected across life-history stages. Second, I test whether food supply during the pre-breeding season advances the timing of reproduction through energy reserves in income breeders. Food supply affected female behaviour, endocrine and reproductive phenology without influencing nutritional status or body condition, suggesting that perceiving greater food supply can advance phenology of income breeders. Third, I test for sex-specific behavioural and endocrine responses to food supply in the pre-breeding season. Contrary to predictions from the literature, I found that male pituitary sensitivity peaked after females, which suggests males integrate synchronising cues to align with female timing of reproduction. Finally, I test for climate drivers of breeding phenology in two circumpolar seabirds in very different environmental contexts. I found that black-legged kittiwakes lay earlier after experiencing colder climate, likely via bottom-up effects of climate on food supply, while thick-billed murres lay earlier in when sea-ice out dates were earlier and thus granted earlier access to the breeding grounds. While breeding phenology can be simple to observe—an empty nest one day, an egg the next—I conclude that this key event is connected to environmental variation in food supply through dynamic shifts in behaviour, movement, morphology, and physiology. ------------------------------ Le calendrier des événements importants de la vie des animaux, tels que la reproduction et la migration, change à l'échelle mondiale en raison des changements environnementaux induits par l'homme. Bien qu'ils soient considérés comme importants pour la résilience des populations, les mécanismes sous-jacents à ces changements sont encore mal compris. Dans cette thèse, j'utilise des approches expérimentales et observationnelles pour tester les effets des variations environnementales sur la phénologie de reproduction de deux espèces d'oiseaux marins : la mouette tridactyle (Rissa tridactyla) et le Guillemot de Brünnich (Uria lomvia). Je me concentre sur le rôle de l'approvisionnement alimentaire, qui est souvent la ressource qui limite l'investissement dans chacune des étapes du cycle de vie, et j'utilise des outils diversifiés, notamment la surveillance à long terme, l'endocrinologie et le biologging. Tout d'abord, je teste si les effets environnementaux sur la phénologie présente se répercutent sur la phénologie ultérieure. L'approvisionnement alimentaire pendant la saison de reproduction a affecté à la fois la phénologie de reproduction et la phénologie migratoire subséquente, démontrant que le moment des événements saisonniers peut être interconnecté à travers les étapes du cycle biologique. Deuxièmement, je teste si l'approvisionnement alimentaire pendant la saison de pré- reproduction avance le moment de la reproduction grâce aux réserves d'énergie acquise localement. L'approvisionnement alimentaire a affecté le comportement des femelles, la phénologie endocrinienne et reproductive sans influencer l'état nutritionnel ou l'état corporel, ce qui suggère que la perception d'un approvisionnement alimentaire plus important peut faire progresser la phénologie des animaux dépendants des ressources locales. Troisièmement, je teste les réponses comportementales et endocriniennes spécifiques au sexe à l'approvisionnement alimentaire pendant la saison précédant la reproduction. Contrairement aux prédictions de la littérature, j'ai découvert que la sensibilité hypophysaire des mâles atteignait un pic après celui des femelles, ce qui suggère que les mâles intègrent des signaux de synchronisation pour s'aligner sur le moment de la reproduction des femelles. Enfin, je teste les facteurs climatiques de la phénologie de reproduction chez deux oiseaux marins circumpolaires dans des contextes environnementaux très différents. J'ai découvert que les mouettes tridactyles pondaient plus tôt après avoir connu un climat plus froid, probablement en raison des effets ascendants du climat sur l'approvisionnement alimentaire, tandis que les guillemots de Brünnich pondaient plus tôt lorsque les dates de sortie de la glace de mer étaient plus précoces et permettaient ainsi un accès plus précoce au site de reproduction. 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Preprint
Full-text available
  • Feb 2023
Climate change and weather variability are having global impacts on the lives of organisms, particularly on high-trophic level predators such as pelagic seabirds. In the North Atlantic, migratory seabirds are expected to respond to climate variability by adjusting their seasonal events, including the timing of migration and arrival at the breeding site. The timing of these events may be influenced by large-scale atmospheric phenomena like the North Atlantic Oscillation (NAO) and the Atlantic Multi-decadal Oscillation (AMO). The White-tailed Tropicbird ( Phaethon lepturus ) is a wide-spread tropical migratory seabird breeding at its Atlantic northernmost edge of distribution range in Bermuda Islands (32° 17' 58'' N, 64° 47' 25'' W). Using data from eBird, an online database of bird observations where expert and amateur birdwatchers can report their sightings, we explored trends in Tropicbird first annual observation (proxy for bird arrival time) at the Bermuda breeding ground from 1953 to 2023. Specifically, we examined the relationship between the arrival time of the Tropicbird at its breeding site and the NAO and AMO. We show that the progressive early arrival at the breeding site (20–25 days in advance) of Tropicbirds over the last 70 years positively correlated with the NAO and AMO Indices. This suggests that this tropic seabird breeding in the North Atlantic may be responding to climate-induced changes affecting the Atlantic Ocean. Our findings highlight the fundamental contribution of citizen-science data for ecological long-term studies to understand animals' responses to a changing world.
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Long-term changes in climate are affecting the abundance, distribution and phenology of species across all trophic levels. Short-term climate variability is also having a profound impact on species and trophic interactions. Crucially, species will experience long- and short-term variation simultaneously, and both are predicted to change, yet studies tend to focus on one of these temporal scales. Apex predators are sensitive to long-term climate-driven changes in prey populations and short-term effects of weather on prey availability, both of which could result in changes of diet. We investigated temporal trends and effects of long- and short-term environmental variability on chick diet composition in a North Sea population of European shags Phalacrocorax aristotelis between 1985 and 2014. The proportion of the principle prey, lesser sandeel Ammodytes marinus, declined from 0.99 (1985) to 0.51 (2014), and estimated sandeel size declined from 104.5mm to 92.0mm. Concurrently, diet diversification increased from 1.32 to 10.05 prey types year-1, including Pholidae, Callionymidae and Gadidae. The relative proportion of adult to juvenile sandeel was greater following low Sea Surface Temperatures in the previous year. In contrast, the Pholidae proportion and Prey Richness were higher following high Sea Surface Temperatures in the previous year. Within a season, the proportion of sandeel in the diet was lower on days with higher wind speeds. Crucially, our results showed that diet diversification was linked to trends in temperature. Thus, predicted changes in climate means and variability may have important implications on diet composition in the future, with potential consequences for population dynamics.
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  • Jun 2016
Differences in phenological responses to climate change among species can desynchronise ecological interactions and thereby threaten ecosystem function. To assess these threats, we must quantify the relative impact of climate change on species at different trophic levels. Here, we apply a Climate Sensitivity Profile approach to 10,003 terrestrial and aquatic phenological data sets, spatially matched to temperature and precipitation data, to quantify variation in climate sensitivity. The direction, magnitude and timing of climate sensitivity varied markedly among organisms within taxonomic and trophic groups. Despite this variability, we detected systematic variation in the direction and magnitude of phenological climate sensitivity. Secondary consumers showed consistently lower climate sensitivity than other groups. We used mid-century climate change projections to estimate that the timing of phenological events could change more for primary consumers than for species in other trophic levels (6.2 versus 2.5-2.9 days earlier on average), with substantial taxonomic variation (1.1-14.8 days earlier on average).
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Later at higher latitudes: large-scale variability in seabird breeding timing and synchronicity
Article
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  • May 2016
In seasonal environments, organisms are expected to optimally schedule reproduction within an annual range of environmental conditions. Latitudinal gradients generate a range of seasonality to which we can expect adaptations to have evolved, and can be used to explore drivers of timing strategies across species' distribution ranges. This study compares the timing of egg hatching in four seabird species (Atlantic puffin Fratercula arctica, black-legged kittiwake Rissa tridactyla, common guillemot Uria aalge, and Brünnich's guillemot U. lomvia) covering a subarctic to Arctic latitudinal gradient along the Norwegian coast to Svalbard (65-79°N). Hatching was significantly delayed by an estimated 1.7, 2.3, and 1.9 d per latitudinal degree for puffins, kittiwakes, and common guillemots, respectively, but was not delayed for Brünnich's guillemots. Hatching distributions revealed an increase in intra- Annual breeding synchronicity along a latitudinal gradient for kittiwakes only, whereas the two guillemots exhibited high hatching synchronicity at all colonies. We used this large-scale, multispecies timing data series to discuss constraints, adaptations, and mechanisms affecting breeding timing, a necessary step to recognize risks to populations and predict future ecosystem change.
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Responses of Marine Organisms to Climate Change across Oceans
Article
Full-text available
  • May 2016
Climate change is driving changes in the physical and chemical properties of the ocean that have consequences for marine ecosystems. Here, we review evidence for the responses of marine life to recent climate change across ocean regions, from tropical seas to polar oceans. We consider observed changes in calcification rates, demography, abundance, distribution and phenology of marine species. We draw on a database of observed climate change impacts on marine species, supplemented with evidence in the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. We discuss factors that limit or facilitate species’ responses, such as fishing pressure, the availability of prey, habitat, light and other resources, and dispersal by ocean currents. We find that general trends in species responses are consistent with expectations from climate change, including poleward and deeper distributional shifts, advances in spring phenology, declines in calcification and increases in the abundance of warm-water species. The volume and type of evidence of species responses to climate change is variable across ocean regions and taxonomic groups, with much evidence derived from the heavily-studied north Atlantic Ocean. Most investigations of marine biological impacts of climate change are of the impacts of changing temperature, with few observations of effects of changing oxygen, wave climate, precipitation (coastal waters) or ocean acidification. Observations of species responses that have been linked to anthropogenic climate change are widespread, but are still lacking for some taxonomic groups (e.g., phytoplankton, benthic invertebrates, marine mammals).
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Predicting when climate-driven phenotypic change affects population dynamics
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Species' responses to climate change are variable and diverse, yet our understanding of how different responses (e.g. physiological, behavioural, demographic) relate and how they affect the parameters most relevant for conservation (e.g. population persistence) is lacking. Despite this, studies that observe changes in one type of response typically assume that effects on population dynamics will occur, perhaps fallaciously. We use a hierarchical framework to explain and test when impacts of climate on traits (e.g. phenology) affect demographic rates (e.g. reproduction) and in turn population dynamics. Using this conceptual framework, we distinguish four mechanisms that can prevent lower-level responses from impacting population dynamics. Testable hypotheses were identified from the literature that suggest life-history and ecological characteristics which could predict when these mechanisms are likely to be important. A quantitative example on birds illustrates how, even with limited data and without fully-parameterized population models, new insights can be gained; differences among species in the impacts of climate-driven phenological changes on population growth were not explained by the number of broods or density dependence. Our approach helps to predict the types of species in which climate sensitivities of phenotypic traits have strong demographic and population consequences, which is crucial for conservation prioritization of data-deficient species.
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Climate change and marine vertebrates
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  • Nov 2015
Climate change impacts on vertebrates have consequences for marine ecosystem structures and services. We review marine fish, mammal, turtle, and seabird responses to climate change and discuss their potential for adaptation. Direct and indirect responses are demonstrated from every ocean. Because of variation in research foci, observed responses differ among taxonomic groups (redistributions for fish, phenology for seabirds). Mechanisms of change are (i) direct physiological responses and (ii) climate-mediated predator-prey interactions. Regional-scale variation in climate-demographic functions makes range-wide population dynamics challenging to predict. The nexus of metabolism relative to ecosystem productivity and food webs appears key to predicting future effects on marine vertebrates. Integration of climate, oceanographic, ecosystem, and population models that incorporate evolutionary processes is needed to prioritize the climate-related conservation needs for these species.
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Seabird systematics and distribution: A review of current knowledge
Chapter
  • Jan 2001
This review of systematics and distribution will be restricted to the groups of birds traditionally considered as seabirds. These groups are the Sphenisciformes, Procellariiformes, Pelecaniformes, and certain families among the Charadriiformes (Table 3.1). And I begin by explaining the significance of the restriction. While all species among the Sphenisciformes (penguins) and Procellariiformes (albatrosses, petrels, shearwaters, fulmars, and allies) are seabirds, this is not universally true for members of the other two orders. Among the Pelecaniformes, tropicbirds, frigatebirds, and boobies are exclusively seabirds. On the other hand, the various species of cormorant, anhinga (= darter), and pelican can be strict seabirds, or freshwater birds, or are able to thrive in both environments. But at least all members of the order are waterbirds. That is not true of the Charadriiformes, an order which comprises some 200 species of shorebirds plus five groups considered to be primarily seabirds, namely, the gulls, terns, skuas, skimmers, and auks. Of these, the auks and skuas are strict seabirds while different species of gull, tern, and skimmer are variously associated with the sea, or with freshwater, or with estuaries.
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Circumpolar analysis of the Adélie Penguin reveals the importance of environmental variability in phenological mismatch
Article
Evidence of climate change-driven shifts in plant and animal phenology have raised concerns that certain trophic interactions may be increasingly mismatched in time, resulting in declines in reproductive success. Given the constraints imposed by extreme seasonality at high latitudes and the rapid shifts in phenology seen in the Arctic, we would also expect Antarctic species to be highly vulnerable to climate change-driven phenological mismatches with their environment. However, few studies have assessed the impacts of phenological change in Antarctica. Using the largest database of phytoplankton phenology, sea-ice phenology, and Adélie penguin breeding phenology and breeding success assembled to date, we find that while a temporal match between penguin breeding phenology and optimal environmental conditions sets an upper limit on breeding success, only a weak relationship to the mean exists. Despite previous work suggesting that divergent trends in Adélie penguin breeding phenology are apparent across the Antarctic continent, we find no such trends. Furthermore, we find no trend in the magnitude of phenological mismatch, suggesting that mismatch is driven by interannual variability in environmental conditions rather than climate change-driven trends, as observed in other systems. We propose several criteria necessary for a species to experience a strong climate change-driven phenological mismatch, of which several may be violated by this system. This article is protected by copyright. All rights reserved.
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