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      Survival in macaroni penguins and the relative importance of different drivers: individual traits, predation pressure and environmental variability

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          Abstract

          1. Understanding the demographic response of free-living animal populations to different drivers is the first step towards reliable prediction of population trends.

          2. Penguins have exhibited dramatic declines in population size, and many studies have linked this to bottom-up processes altering the abundance of prey species. The effects of individual traits have been considered to a lesser extent, and top-down regulation through predation has been largely overlooked due to the difficulties in empirically measuring this at sea where it usually occurs.

          3. For 10 years (2003–2012), macaroni penguins ( Eudyptes chrysolophus) were marked with subcutaneous electronic transponder tags and re-encountered using an automated gateway system fitted at the entrance to the colony. We used multistate mark–recapture modelling to identify the different drivers influencing survival rates and a sensitivity analysis to assess their relative importance across different life stages.

          4. Survival rates were low and variable during the fledging year (mean = 0·33), increasing to much higher levels from age 1 onwards (mean = 0·89). We show that survival of macaroni penguins is driven by a combination of individual quality, top-down predation pressure and bottom-up environmental forces. The relative importance of these covariates was age specific. During the fledging year, survival rates were most sensitive to top-down predation pressure, followed by individual fledging mass, and finally bottom-up environmental effects. In contrast, birds older than 1 year showed a similar response to bottom-up environmental effects and top-down predation pressure.

          5. We infer from our results that macaroni penguins will most likely be negatively impacted by an increase in the local population size of giant petrels. Furthermore, this population is, at least in the short term, likely to be positively influenced by local warming. More broadly, our results highlight the importance of considering multiple causal effects across different life stages when examining the survival rates of seabirds.

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          Most cited references64

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          Cascading top-down effects of changing oceanic predator abundances.

          1. Top-down control can be an important determinant of ecosystem structure and function, but in oceanic ecosystems, where cascading effects of predator depletions, recoveries, and invasions could be significant, such effects had rarely been demonstrated until recently. 2. Here we synthesize the evidence for oceanic top-down control that has emerged over the last decade, focusing on large, high trophic-level predators inhabiting continental shelves, seas, and the open ocean. 3. In these ecosystems, where controlled manipulations are largely infeasible, 'pseudo-experimental' analyses of predator-prey interactions that treat independent predator populations as 'replicates', and temporal or spatial contrasts in predator populations and climate as 'treatments', are increasingly employed to help disentangle predator effects from environmental variation and noise. 4. Substantial reductions in marine mammals, sharks, and piscivorous fishes have led to mesopredator and invertebrate predator increases. Conversely, abundant oceanic predators have suppressed prey abundances. Predation has also inhibited recovery of depleted species, sometimes through predator-prey role reversals. Trophic cascades have been initiated by oceanic predators linking to neritic food webs, but seem inconsistent in the pelagic realm with effects often attenuating at plankton. 5. Top-down control is not uniformly strong in the ocean, and appears contingent on the intensity and nature of perturbations to predator abundances. Predator diversity may dampen cascading effects except where nonselective fisheries deplete entire predator functional groups. In other cases, simultaneous exploitation of predator and prey can inhibit prey responses. Explicit consideration of anthropogenic modifications to oceanic foodwebs should help inform predictions about trophic control. 6. Synthesis and applications. Oceanic top-down control can have important socio-economic, conservation, and management implications as mesopredators and invertebrates assume dominance, and recovery of overexploited predators is impaired. Continued research aimed at integrating across trophic levels is needed to understand and forecast the ecosystem effects of changing oceanic predator abundances, the relative strength of top-down and bottom-up control, and interactions with intensifying anthropogenic stressors such as climate change.
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            Emperor penguins and climate change.

            Variations in ocean-atmosphere coupling over time in the Southern Ocean have dominant effects on sea-ice extent and ecosystem structure, but the ultimate consequences of such environmental changes for large marine predators cannot be accurately predicted because of the absence of long-term data series on key demographic parameters. Here, we use the longest time series available on demographic parameters of an Antarctic large predator breeding on fast ice and relying on food resources from the Southern Ocean. We show that over the past 50 years, the population of emperor penguins (Aptenodytes forsteri) in Terre Adélie has declined by 50% because of a decrease in adult survival during the late 1970s. At this time there was a prolonged abnormally warm period with reduced sea-ice extent. Mortality rates increased when warm sea-surface temperatures occurred in the foraging area and when annual sea-ice extent was reduced, and were higher for males than for females. In contrast with survival, emperor penguins hatched fewer eggs when winter sea-ice was extended. These results indicate strong and contrasting effects of large-scale oceanographic processes and sea-ice extent on the demography of emperor penguins, and their potential high susceptibility to climate change.
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              The demographic impact of extreme events: stochastic weather drives survival and population dynamics in a long-lived seabird.

              1. Most scenarios for future climate change predict increased variability and thus increased frequency of extreme weather events. To predict impacts of climate change on wild populations, we need to understand whether this translates into increased variability in demographic parameters, which would lead to reduced population growth rates even without a change in mean parameter values. This requires robust estimates of temporal process variance, for example in survival, and identification of weather covariates linked to interannual variability. 2. The European shag Phalacrocorax aristotelis (L.) shows unusually large variability in population size, and large-scale mortality events have been linked to winter gales. We estimated first-year, second-year and adult survival based on 43 years of ringing and dead recovery data from the Isle of May, Scotland, using recent methods to quantify temporal process variance and identify aspects of winter weather linked to survival. 3. Survival was highly variable for all age groups, and for second-year and adult birds process variance declined strongly when the most extreme year was excluded. Survival in these age groups was low in winters with strong onshore winds and high rainfall. Variation in first-year survival was not related to winter weather, and process variance, although high, was less affected by extreme years. A stochastic population model showed that increasing process variance in survival would lead to reduced population growth rate and increasing probability of extinction. 4. As in other cormorants, shag plumage is only partially waterproof, presumably an adaptation to highly efficient underwater foraging. We speculate that this adaptation may make individuals vulnerable to rough winter weather, leading to boom-and-bust dynamics, where rapid population growth under favourable conditions allows recovery from periodic large-scale weather-related mortality. 5. Given that extreme weather events are predicted to become more frequent, species such as shags that are vulnerable to such events are likely to exhibit stronger reductions in population growth than would be expected from changes in mean climate. Vulnerability to extreme events thus needs to be accounted for when predicting the ecological impacts of climate change.
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                Author and article information

                Journal
                J Anim Ecol
                J Anim Ecol
                jane
                The Journal of Animal Ecology
                BlackWell Publishing Ltd (Oxford, UK )
                0021-8790
                1365-2656
                September 2014
                21 May 2014
                : 83
                : 5
                : 1057-1067
                Affiliations
                [1 ]British Antarctic Survey High Cross, Cambridge, CB3 0ET, UK
                [2 ]Institute of Biodiversity, Animal Health & Comparative Medicine, University of Glasgow Glasgow, G12 8QQ, UK
                [3 ]School of Environmental Sciences, University of Liverpool Liverpool, L69 3GP, UK
                Author notes
                Correspondence author. E-mail: catrsw@ 123456bas.ac.uk

                Handling Editor: Henri Weimerskirch

                Article
                10.1111/1365-2656.12229
                4284017
                24846695
                b92b0472-8009-4756-ae56-14b878874bdf
                © 2014 The Authors. Journal of Animal Ecology published by John Wiley & Sons Ltd on behalf of British Ecological Society.

                This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 15 August 2013
                : 31 March 2014
                Categories
                Demography

                Ecology
                bottom-up,demography,el niño/southern oscillation,fledging mass,giant petrel,intrinsic factors,predation,sea surface temperature,southern annular mode,top-down

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