Observed and predicted effects of climate on Australian seabirds

Abstract Although there is growing evidence of climate warming, for many regions the broader effects of climate variation on marine top predators remains unknown owing to the difficulty in obtaining, for synthesis, long-term and short-term datasets on multiple species. In the Australian region, climatic and oceanographic variability and change have been shown to affect marine species, often with profound consequences. Many seabirds are apex predators for which changes in climatic and oceanic dynamics have driven range movements poleward, reduced breeding success and altered breeding timing for some species. Here we review the literature to assess and determine the vulnerability of Australian seabirds to variation and change in climate and identify which species and ecosystems may be more resilient to future climate warming. It is clear from this synthesis that not all Australian seabirds are affected similarly, with responses varying by species and location. In addition, the paucity of information on the distribution and biology of seabird prey, foraging patterns and movements of seabirds, and the ability of seabirds to switch between prey species or adjust timing of life-cycles make generalisations about potential effects of future climate change and adaptive capacity in seabirds difficult. This applies both within Australia and elsewhere, where data are similarly sparse.

[1]  P. Dann,et al.  Seabirds and Climate Change , 2009 .

[2]  K. Dugger,et al.  Competition among penguins and cetaceans reveals trophic cascades in the western Ross Sea, Antarctica. , 2006, Ecology.

[3]  N. Crooker,et al.  What is the International Heliophysical Year , 2004 .

[4]  Hermann Bondi,et al.  The good, the bad and the ugly , 1988, Nature.

[5]  M. Mcphaden,et al.  Genesis and evolution of the 1997-98 El Nino , 1999, Science.

[6]  M. Hebblewhite,et al.  Global Population Dynamics and Hot Spots of Response to Climate Change , 2009 .

[7]  L. Chambers The impact of climate on Little Penguin breeding success , 2004 .

[8]  T. Ohsumi,et al.  The Ocean in a High CO2 World. , 2004 .

[9]  Dp O'Brien Surface schooling behaviour of the coastal krill Nyctiphanes australis (Crustacea: Euphausiacea) off Tasmania, Australia , 1988 .

[10]  D. Costa,et al.  Foraging behaviour and habitat selection of the little penguin Eudyptula minor during early chick rearing in Bass Strait, Australia , 2008 .

[11]  H. Weimerskirch,et al.  Foraging strategy of a tropical seabird, the red- footed booby, in a dynamic marine environment , 2005 .

[12]  F. Daunt,et al.  IMPACTS OF CLIMATE CHANGE ON SEABIRDS , 2006 .

[13]  M. Lavín,et al.  SEABIRD ECOLOGY, EL NINO ANOMALIES, AND PREDICTION OF SARDINE FISHERIES IN THE GULF OF CALIFORNIA , 2004 .

[14]  B. Congdon,et al.  Day-to-day variation in sea-surface temperature reduces sooty tern Sterna fuscata foraging success on the Great Barrier Reef, Australia , 2007 .

[15]  C. Sharples,et al.  Indicative Mapping of Tasmanian Coastal Vulnerability to Climate Change and Sea-Level Rise: Explanatory Report (Second Edition) , 2006 .

[16]  F. Norman The effects of sheep on the breeding success and habitat of the short-tailed shearwater, puffinus tenuirostris (Temminck) , 1970 .

[17]  M. Edwards,et al.  Impact of climate change on marine pelagic phenology and trophic mismatch , 2004, Nature.

[18]  M. Roughan,et al.  A comparison of observed upwellingmechanisms off the east coast of Australia , 2002 .

[19]  M. Weston,et al.  The State of Australia's Birds 2003 , 2003 .

[20]  Y. Ropert‐Coudert,et al.  Impact of small-scale environmental perturbations on local marine food resources: a case study of a predator, the little penguin , 2009, Proceedings of the Royal Society B: Biological Sciences.

[21]  S. Garnett,et al.  The Action Plan for Australian Birds 2010 , 2011 .

[22]  K. Hulsman,et al.  The Breeding Biology of the Crested Tern Sterna bergii , 1986 .

[23]  H. Weimerskirch,et al.  Community structure across a large-scale ocean productivity gradient: Marine bird assemblages of the Southern Indian Ocean , 2007 .

[24]  B. Congdon,et al.  Sea surface temperature constrains wedge-tailed shearwater foraging success within breeding seasons , 2004 .

[25]  J. Coulson,et al.  Measuring immigration and philopatry in seabirds; recruitment to Black‐legged Kittiwake colonies , 2007 .

[26]  A. Chiaradia,et al.  The diet of Little Penguins (Eudyptula minor) at Phillip Island, Victoria, in the absence of a major prey—Pilchard (Sardinops sagax) , 2003 .

[27]  I. Barnes-Keoghan,et al.  Climate and climate change in the sub-Antarctic , 2007 .

[28]  K. Hulsman Breeding success and mortality of terns at one tree island, great barrier reef , 1977 .

[29]  B. Congdon,et al.  Dual-foraging and co-ordinated provisioning in a tropical Procellariiform, the wedge-tailed shearwater , 2005 .

[30]  M. Turner,et al.  Vulnerability of island flora and fauna in theGreat Barrier Reef to climate change , 2007 .

[31]  N. Stenseth,et al.  Marine Birds and Climate Fluctuation in the North Atlantic , 2005 .

[32]  B. Moe,et al.  Developmental plasticity of physiology and morphology in diet-restricted European shag nestlings (Phalacrocorax aristotelis) , 2004, Journal of Experimental Biology.

[33]  John McLeay,et al.  THE PARLIAMENT OF THE COMMONWEALTH OF AUSTRALIA , 1965 .

[34]  D. Goodall,et al.  Australia?s Biodiversity and Climate Change , 2010 .

[35]  Henri Weimerskirch,et al.  Trends in bird and seal populations as indicators of a system shift in the Southern Ocean , 2003, Antarctic Science.

[36]  R. Erwin Breeding habitat use by colonially nesting waterbirds in two mid-atlantic US regions under different regimes of human disturbance , 1980 .

[37]  Carol A. Devney,et al.  Testing the efficacy of a boundary fence at an important tropical seabird breeding colony and key tourist destination. , 2009 .

[38]  P. Long,et al.  Inter-annual variations in breeding participation at four Western Australian colonies of the Wedge-tailed shearwater Puffinus pacificus , 2002 .

[39]  H. Weimerskirch,et al.  Relative influence of fisheries and climate on the demography of four albatross species , 2010 .

[40]  C. Surman,et al.  THE GOOD, THE BAD AND THE UGLY: ENSO-DRIVEN OCEANOGRAPHIC VARIABILITY AND ITS INFLUENCE ON SEABIRD DIET AND REPRODUCTIVE PERFORMANCE AT THE HOUTMAN ABROLHOS, EASTERN INDIAN OCEAN , 2009 .

[41]  E. Maier‐Reimer,et al.  Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms , 2005, Nature.

[42]  R. Schreiber,et al.  Effects of the 1982-83 El Niño – Southern Oscillation on Pacific Ocean bird populations , 1988 .

[43]  James O’Connor,et al.  The State of Australia ’ s Birds 2010 Islands and Birds , 2010 .

[44]  B. Worm,et al.  META-ANALYSIS OF COD-SHRIMP INTERACTIONS REVEALS TOP-DOWN CONTROL IN OCEANIC FOOD WEBS , 2003 .

[45]  A. Lorenz,et al.  Vulnerable taxa of European Plecoptera (Insecta) in the context of climate change , 2010, Biodiversity and Conservation.

[46]  M. Short,et al.  Cyclonic and anthropogenic influences on tern populations , 2009 .

[47]  J. Komdeur,et al.  Population size, breeding habitat and nest site distribution of little penguins (Eudyptula minor) on Montague Island, New South Wales , 2003 .

[48]  H. Weimerskirch,et al.  Seabird community structure in a coastal tropical environment: importance of natural factors and fish aggregating devices (FADs) , 2004 .

[49]  B. Raymond,et al.  Convergence or divergence : where do short-tailed shearwaters forage in the Southern Ocean ? , 2006 .

[50]  M. Short,et al.  Sensitivity of tropical seabirds to El Niño precursors. , 2009, Ecology.

[51]  N. Holbrook,et al.  El Nino – Southern Oscillation , 2009 .

[52]  Juha Merilä,et al.  The impact of climate fluctuation on food availability and reproductive performance of the planktivorous red-billed gull Larus novaehollandiae scopulinus. , 2008, The Journal of animal ecology.

[53]  D. Ainley,et al.  Variable responses of seabirds to change in marine climate: California Current, 1985-1994 , 2001 .

[54]  R. Feely,et al.  Ocean acidification: the other CO2 problem. , 2009, Annual review of marine science.

[55]  K. Erikstad,et al.  The effect of climate on adult survival in five species of North Atlantic seabirds , 2005 .

[56]  J. Jahncke,et al.  Comparison of trends in abundance of guano-producing seabirds in Peru and Southern Africa , 1999 .

[57]  Peter Dann,et al.  Predicting onset and success of breeding in little penguins Eudyptula minor from ocean temperatures , 2009 .

[58]  B. Congdon,et al.  Elevated sea-surface temperature, reduced provisioning and reproductive failure of wedge-tailed shearwaters (Puffinus pacificus) in the southern Great Barrier Reef, Australia , 2003 .

[59]  H. Weimerskirch,et al.  Antarctic birds breed later in response to climate change. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[60]  S. Garnett The Action Plan for Australian Birds , 1992 .

[61]  D. Au,et al.  SEABIRD INTERACTIONS WITH DOLPHINS AND TUNA IN THE EASTERN TROPICAL PACIFIC , 1986 .

[62]  L. Ballance,et al.  Oceanographic influences on seabirds and cetaceans of the eastern tropical Pacific: A review , 2006 .

[63]  Jean-Marc Fromentin,et al.  Ecosystem oceanography for global change in fisheries. , 2008, Trends in ecology & evolution.

[64]  D. Nussey,et al.  The evolutionary ecology of individual phenotypic plasticity in wild populations , 2007, Journal of evolutionary biology.

[65]  Alistair J. Wilson,et al.  Timing is everything: flexible phenology and shifting selection in a colonial seabird. , 2009, The Journal of animal ecology.

[66]  J. Gee,et al.  Ecology (3rd edn) , 1991 .

[67]  James A. Rodgers,et al.  Set‐Back Distances to Protect Nesting Bird Colonies from Human Disturbance in Florida , 1995 .

[68]  A. Harfenist,et al.  Ocean climate and El Niño impacts on survival of Cassin's Auklets from upwelling and downwelling domains of British Columbia , 2005 .

[69]  Abigail M. Smith Bryozoans as southern sentinels of ocean acidification: a major role for a minor phylum , 2009 .

[70]  D. Grémillet,et al.  Shifts in phenotypic plasticity constrain the value of seabirds as ecological indicators of marine ecosystems. , 2010, Ecological applications : a publication of the Ecological Society of America.

[71]  E. Woehler,et al.  Antarctic penguin response to habitat change as Earth's troposphere reaches 2°C above preindustrial levels , 2010 .

[72]  H. Weimerskirch,et al.  Seabird associations with mesoscale eddies: the subtropical Indian Ocean , 2006 .

[73]  O. Hoegh‐Guldberg,et al.  Vulnerability of reef-building corals on the Great Barrier Reef to climate change , 2007 .

[74]  William A. Montevecchi,et al.  Interactive effects of food shortage and predation on breeding failure of black-legged kittiwakes: indirect effects of fisheries activities and implications for indicator species , 1997 .

[75]  E. Barrett Impact of climate , 1974, Nature.

[76]  A. Kitaysky,et al.  Climate change causes contrasting trends in reproductive performance of planktivorous and piscivorous alcids , 2000 .

[77]  S. Wanless,et al.  Spatial match–mismatch in the Benguela upwelling zone: should we expect chlorophyll and sea-surface temperature to predict marine predator distributions? , 2008 .

[78]  D. Ainley Seabird Responses To Climate Change , 2001 .

[79]  G. Nevitt,et al.  Sensory ecology on the high seas: the odor world of the procellariiform seabirds , 2008, Journal of Experimental Biology.

[80]  Dsewpc National Recovery Plan for the Abbott’s Booby (Papasula abbotti) , 2005 .

[81]  Peter Rothery,et al.  The role of industrial fisheries and oceanographic change in the decline of North Sea black‐legged kittiwakes , 2004 .

[82]  David Grémillet,et al.  Spatial ecology and conservation of seabirds facing global climate change: a review , 2009 .

[83]  G. N. Batianoff,et al.  Birds of Raine Island: Population Trends, Breeding Behaviour and Nesting Habitats , 2005 .

[84]  Hughes,et al.  Biological consequences of global warming: is the signal already apparent? , 2000, Trends in ecology & evolution.

[85]  C. S. St. Clair,et al.  Tufted puffin reproduction reveals ocean climate variability , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[86]  J. Ramos,et al.  Annual variation in laying date and breeding success of Brown Noddies on Aride Island, Seychelles , 2006 .

[87]  K. Baker,et al.  Marine Ecosystem Sensitivity to Climate Change , 1999 .

[88]  B. Sæther,et al.  A latitudinal gradient in climate effects on seabird demography: results from interspecific analyses , 2007, Global Change Biology.

[89]  S. Blaber,et al.  Seabird Breeding Populations on the Far Northern Great Barrier Reef, Australia: Trends and Influences , 1998 .

[90]  T. A. Walker The distribution, abundance and dispersal by seabirds of Pisonia grandis , 1991 .

[91]  C. Greene,et al.  Climate Drives Sea Change , 2007, Science.

[92]  P. Quillfeldt,et al.  Sea surface temperatures and behavioural buffering capacity in thin‐billed prions Pachyptila belcheri: breeding success, provisioning and chick begging , 2007 .

[93]  E. Murphy,et al.  Environmental Change and Antarctic Seabird Populations , 2002, Science.

[94]  S. Schneider,et al.  Fingerprints of global warming on wild animals and plants , 2003, Nature.

[95]  G. Ross,et al.  The Status of Australia's Seabirds , 1997 .

[96]  M. Clout,et al.  The invasion ecology of mammals: a global perspective , 2008 .

[97]  N. Aebischer,et al.  Parallel long-term trends across four marine trophic levels and weather , 1990, Nature.

[98]  S. Bograd,et al.  Marine ecosystems, climate and phenology: introduction , 2009 .

[99]  J. C. Andrews,et al.  Upwelling as a source of nutrients for the Great Barrier Reef ecosystems: a solution to Darwin's question? , 1982 .

[100]  M. Weston,et al.  Climate change and its impact on Australia's avifauna , 2005 .

[101]  A. Chiaradia,et al.  Plasticity in parental provisioning and chick growth in Little Penguins Eudyptula minor in years of high and low breeding success , 2006 .

[102]  N. Fechner,et al.  Climate and Vegetation Changes at Coringa-Herald National Nature Reserve, Coral Sea Islands, Australia1 , 2010 .

[103]  Elizabeth H. Sinclair,et al.  Climate change and control of the southeastern Bering Sea pelagic ecosystem , 2002 .

[104]  Marius N. Müller,et al.  Marine Climate Change in Australia Impacts and Adaptation Responses 2012 REPORT CARD Ocean acidification , 2012 .

[105]  S. Dupont,et al.  What meta-analysis can tell us about vulnerability of marine biodiversity to ocean acidification? , 2010 .

[106]  O. Hoegh‐Guldberg,et al.  Climate change and Australian marine life , 2007 .

[107]  D. Atkinson Marine Ecosystems and Climate Variation: The North Atlantic – A Comparative Perspective , 2006 .

[108]  Denis Réale,et al.  Genetic and plastic responses of a northern mammal to climate change , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[109]  Peter Dann,et al.  Distribution, Population Trends and Factors Influencing the Population Size of Little Penguins Eudyptula minor on Phillip Island, Victoria , 1991 .

[110]  J. Dunlop THE POPULATION DYNAMICS OF TROPICAL SEABIRDS ESTABLISHING FRONTIER COLONIES ON ISLANDS OFF SOUTH-WESTERN AUSTRALIA , 2009 .

[111]  William J. Sydeman,et al.  A review of human disturbance effects on nesting colonial waterbirds , 1999 .

[112]  Stephen J. Hawkins,et al.  Modelling patch dynamics on rocky shores using deterministic cellular automata , 2022 .

[113]  Henri Weimerskirch,et al.  Effects of climate variability on the temporal population dynamics of southern fulmars. , 2003, The Journal of animal ecology.

[114]  S. E. Townsend,et al.  Paradigm lost, or is top-down forcing no longer significant in the Antarctic marine ecosystem? , 2007, Antarctic Science.

[115]  P. Trathan,et al.  Penguin responses to climate change in the Southern Ocean , 2009 .

[116]  E. Murphy,et al.  Environmental forcing and Southern Ocean marine predator populations: effects of climate change and variability , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[117]  M. Caley,et al.  Plasticity of Noddy Parents and Offspring to Sea-Surface Temperature Anomalies , 2010, PloS one.

[118]  R. Schreiber,et al.  Central Pacific Seabirds and the El Ni�o Southern Oscillation: 1982 to 1983 Perspectives , 1984, Science.

[119]  M. Hindell,et al.  Shearwater Foraging in the Southern Ocean: The Roles of Prey Availability and Winds , 2010, PloS one.

[120]  S. Jacobs,et al.  Freshening of the Ross Sea During the Late 20th Century , 2002, Science.

[121]  J. Cornelius,et al.  Population Changes, Breeding Cycles and Breeding Success over Six Years in a Seabird Colony at Michaelmas Cay, Queensland , 1992 .

[122]  A. Russo,et al.  Effects of environmental variables on recruitment of anchovy in the Adriatic Sea , 2006 .

[123]  F. Norman Notes on the breeding of the Pied Cormorant near Werribee, Victoria, in 1971, 1972 and 1973 , 1974 .

[124]  Mark Trinder,et al.  Oil pollution and climate have wide-scale impacts on seabird demographics. , 2005, Ecology letters.

[125]  M. Peterz,et al.  Cyclones and pelagic seabird movements , 1984 .

[126]  Hugh P. Possingham,et al.  Effects of climate‐driven primary production change on marine food webs: implications for fisheries and conservation , 2010 .

[127]  Kung-Sik Chan,et al.  Ecological Effects of Climate Fluctuations , 2002, Science.

[128]  Darren R. Peck,et al.  Colony-specific foraging behaviour and co-ordinated divergence of chick development in the wedge-tailed shearwater Puffinus pacificus , 2005 .

[129]  S. Wanless,et al.  Environmental forcing on life history strategies: Evidence for multi-trophic level responses at ocean basin scales , 2009 .

[130]  A. Hedd,et al.  Seabird nestling diets reflect latitudinal temperature-dependent variation in availability of key zooplankton prey populations , 2009 .

[131]  O. Hoegh‐Guldberg,et al.  Ecological responses to recent climate change , 2002, Nature.

[132]  C. Grimes Fishery Production and the Mississippi River Discharge , 2001 .

[133]  H. Heatwole,et al.  Long-Term Population Trends of Seabirds on the Swain Reefs, Great Barrier Reef , 1997 .

[134]  HighWire Press Philosophical Transactions of the Royal Society of London , 1781, The London Medical Journal.

[135]  K. Erikstad,et al.  Seabird life histories and climatic fluctuations: a phylogenetic‐comparative time series analysis of North Atlantic seabirds , 2008 .

[136]  K. Frank,et al.  The ups and downs of trophic control in continental shelf ecosystems. , 2007, Trends in ecology & evolution.

[137]  K. Hyrenbach,et al.  Top-down and bottom-up factors affecting seabird population trends in the California current system (1985-2006) , 2010 .

[138]  Rebecca L. Lewison,et al.  Understanding impacts of fisheries bycatch on marine megafauna , 2004 .

[139]  S. Wanless,et al.  Spatial match-mismatch across four trophic levels of the Benguela upwelling zone during an ecosystem shift. , 2008 .

[140]  Laird A. Henkel Effect of water clarity on the distribution of marine birds in nearshore waters of Monterey Bay, California , 2006 .

[141]  T. L. Adams The time to act is now. , 1989, Wisconsin medical journal.

[142]  P. Dann,et al.  Population regulation in Little Penguins (Eudyptula minor): the role of intraspecific competition for nesting sites and food during breeding , 2006 .

[143]  J. Ramos,et al.  Influence of local and large-scale weather events and timing of breeding on tropical roseate tern reproductive parameters , 2002 .

[144]  R. Wooller,et al.  The Breeding Biology of the Lesser Noddy on Pelsaert Island, Western Australia , 1995 .

[145]  M. Eriksson Prey detectability for fish-eating birds in relation to fish density and water transparency , 1985 .

[146]  P. Manow ‚The Good, the Bad, and the Ugly‘ , 2002 .

[147]  A. Dunn,et al.  NATIONAL RECOVERY PLAN FOR THE CHRISTMAS ISLAND FRIGATEBIRD Fregata andrewsi , 2004 .

[148]  R. Veit,et al.  Apex marine predator declines ninety percent in association with changing oceanic climate , 1997 .

[149]  R. Wal,et al.  Invasive plant suppresses charismatic seabird - the construction of attitudes towards biodiversity management options. , 2007 .

[150]  Paul Marshall,et al.  Vulnerability of seabirds on the Great Barrier Reefto climate change , 2007 .