Breeding short-tailed shearwaters buffer local environmental variability in south-eastern Australia by foraging in Antarctic waters

Movement Ecology

John P. Y. Arnould¹  Maud Berlincourt¹ 

[1] School of Life and Environmental Sciences, Deakin University, Burwood 3125, VIC, Australia

关键词: Southern Ocean;    Geolocation;    Reproductive performance;    Foraging ecology;    Movement;    Procellariiforms;   

Others  :  1222607
DOI  :  10.1186/s40462-015-0044-7

 received in 2014-12-23, accepted in 2015-05-19,  发布年份 2015

【 摘 要 】

Background

Establishing patterns of movements of free-ranging animals in marine ecosystems is crucial for a better understanding of their feeding ecology, life history traits and conservation. As central place foragers, the habitat use of nesting seabirds is heavily influenced by the resources available within their foraging range. We tested the prediction that during years with lower resource availability, short-tailed shearwaters (Puffinus tenuirostris) provisioning chicks should increase their foraging effort, by extending their foraging range and/or duration, both when foraging in neritic (short trips) and distant oceanic waters (long trips). Using both GPS and geolocation data-loggers, at-sea movements and habitat use were investigated over three breeding seasons (2012–14) at two colonies in southeastern Australia.

Results

Most individuals performed daily short foraging trips over the study period and inter-annual variations observed in foraging parameters where mainly due to few individuals from Griffith Island, performing 2-day trips in 2014. When performing long foraging trips, this study showed that individuals from both colonies exploited similar zones in the Southern Ocean. The results of this study suggest that individuals could increase their foraging range while exploiting distant feeding zones, which could indicate that short-tailed shearwaters forage in Antarctic waters not only to maintain their body condition but may also do so to buffer against local environmental stochasticity. Lower breeding performances were associated with longer foraging trips to distant oceanic waters in 2013 and 2014 indicating they could mediate reductions in food availability around the breeding colonies by extending their foraging range in the Southern Ocean.

Conclusions

This study highlights the importance of foraging flexibility as a fundamental aspect of life history in coastal/pelagic marine central place foragers living in highly variable environments and how these foraging strategies are use to buffer this variability.

【 授权许可】

   
2015 Berlincourt and Arnould; licensee BioMed Central.

【 图 表 】

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【 参考文献 】

• [1]Ashmole NP. Seabird ecology and the marine environment. In: Avian biology. Farner DS, King JR, editors. Academic Press, New York, N.Y., U.S.A.; 1971: p.223-86.
• [2]Hansen J, Martos P, Madirolas A. Relationship between spatial distribution of the Patagonian stock of Argentine anchovy, Engraulis anchoita, and sea temperatures during late spring to early summer. Fish Oceanogr. 2001; 10:193-206.
• [3]Weimerskirch H. Are seabirds foraging for unpredictable resources? Deep-Sea Res II Top Stud Oceanogr. 2007; 54:211-23.
• [4]Frederiksen M, Harris MP, Daunt F, Rothery P, Wanless S. Scale-dependent climate signals drive breeding phenology of three seabird species. Glob Chang Biol. 2004; 10:1214-21.
• [5]Lewis S, Gremillet D, Daunt F, Ryan PG, Crawford RJ, Wanless S. Using behavioural and state variables to identify proximate causes of population change in a seabird. Oecologia. 2006; 147:606-14.
• [6]Forcada J, Trathan P, Reid K, Murphy E. The effects of global climate variability in pup production of Antarctic fur seals. Ecology. 2005; 86:2408-17.
• [7]Burke CM, Montevecchi WA. The foraging decisions of a central place foraging seabird in response to fluctuations in local prey conditions. J Zool. 2009; 278:354-61.
• [8]Guinet C, Dubroca L, Lea MA, Goldsworthy S, Cherel Y, Duhamel G et al.. Spatial distribution of foraging in female Antarctic fur seals Arctocephalus gazella in relation to oceanographic variables: a scale-dependent approach using geographic information systems. MEPS. 2001; 219:251-64.
• [9]Orians GH, Pearson NE. On the theory of central place foraging. In: Analysis of ecological systems. Horn DJ, Stairs GR, Mitchell RD, editors. Ohio State University Press, Columbus; 1979: p.155-77.
• [10]Ydenberg R, Welham C, Schmid-Hempel R, Schmid-Hempel P, Beauchamp G. Time and energy constraints and the relationships between currencies in foraging theory. Behav Ecol. 1994; 5:28-34.
• [11]Furness RW, Camphuysen KCJ. Seabirds as monitors of the marine environment. ICES J Mar Sci. 1997; 54:726-37.
• [12]Péron C, Delord K, Phillips RA, Charbonnier Y, Marteau C, Louzao M et al.. Seasonal variation in oceanographic habitat and behaviour of white-chinned petrels Procellaria aequinoctialis from Kerguelen Island. MEPS. 2010; 416:267-84.
• [13]Lack D: Ecological adaptations for breeding in birds. London; 1968
• [14]Ricklefs RE. Seabird life history and the marine environment : some speculations. Colonial Waterbirds. 1990; 13:1-6.
• [15]Hamer KC, Hill JK, Scott I. Chick provisioning and parental attendance in Cory’s shearwaters: implication for nestling obesity. J Avian Biol. 1999; 30:309-15.
• [16]Baduini CL, Hyrenbach KD. Biogeography of procellariiform foraging strategies: does ocean productivity influence provisioning. Mar Ornithol. 2003; 31:101-12.
• [17]Congdon BC, Krockenberger AK, Smithers BV. Dual-foraging and co-ordinated provisioning in a tropical Procellariiform, the wedge-tailed shearwater. MEPS. 2005; 301:293-301.
• [18]Weimerskirch H. How can a pelagic seabird provision its chick when relying on a distant food resource ? Cyclic attendance at the colony, foraging decision and body condition in sooty shearwaters. J Anim Ecol. 1998; 67:99-109.
• [19]Chaurand T, Weimerskirch H. The regular alternation of short and long foraging trips in the blue petrel Halobaena caerulea : a previously undescribed strategy of food provisioning in a pelagic seabird. J Anim Ecol. 1994; 63:275-82.
• [20]Weimerskirch H, Chastel O, Ackermann L, Chaurand T, Cuenot-Chaillet F, Hindermeyer X et al.. Alternate long and short foraging trips in pelagic seabird parents. Anim Behav. 1994; 47:472-6.
• [21]Terauds A, Gales R. Provisioning strategies and growth patterns of Light-mantled Sooty Albatrosses Phoebetria palpebrata on Macquarie Island. Polar Biol. 2006; 29:917-26.
• [22]Granadeiro JP, Nunes M, Silva MC, Furness RW. Flexible foraging strategy of Cory’s shearwater, Calonectris diomedea, during the chick-rearing period. Anim Behav. 1998; 56:1169-76.
• [23]Hyrenbach KD, Fernandez P, Anderson DJ. Oceanographic habitats of two sympatric North Pacific albatrosses during the breeding season. MEPS. 2002; 233:283-301.
• [24]Smithers B, Peck D, Krockenberger A, Congdon B. Elevated sea-surface temperature, reduced provisioning and reproductive failure of wedge-tailed shearwaters (Puffinus pacificus) in the southern Great Barrier Reef, Australia. Mar Freshw Res. 2004; 54:973-7.
• [25]Weimerskirch H, Zimmermann L, Prince PA. Influence of environmental variability on breeding effort in a long-lived seabird, the yellow-nosed albatross. Behav Ecol. 2001; 12:22-30.
• [26]Skira IJ. The short-tailed shearwater: a review of its biology. Corella. 1991; 15:45-52.
• [27]Einoder L, Goldsworthy SD. Foraging flights of short-tailed shearwaters (Puffinus tenuirostris) from Althorpe Island: assessing their use of neritic waters. Trans R Soc S Aust. 2005; 129:209-16.
• [28]Cherel Y, Hobson K, Weimerskirch H. Using stable isotopes to study resource acquisition and allocation in procellariiform seabirds. Oecologia. 2005; 145:533-40.
• [29]Einoder L, Page B, Goldsworthy S, De Little S, Bradshaw C. Exploitation of distant Antarctic waters and close neritic waters by short tailed shearwaters breeding in South Australia. Austral Ecology. 2011; 36:461-75.
• [30]Connan M, Mayzaud P, Hobson K, Weimerskirch H, Cherel Y. Food and feeding ecology of the Tasmanian short-tailed shearwater (Puffinus tenuirostris, Temminck): insights from three complementary methods. Journal of Oceanography, Research and Data; 2010.
• [31]Weimerskirch H, Cherel Y. Feeding ecology of short-tailed shearwaters: breeding in Tasmania and foraging in the Antarctic? MEPS. 1998; 167:261-74.
• [32]Klomp NI, Schultz MA. Short-tailed shearwaters breeding in Australia forage in Antarctic waters. MEPS. 2000; 194:307-10.
• [33]Raymond B, Shaffer SA, Sokolov S, Woehler EJ, Costa DP, Einoder L et al.. Shearwater foraging in the Southern Ocean: the roles of prey availability and winds. PLoS One. 2010; 5: Article ID e10960
• [34]Cleeland JB, Lea MA, Hindell MA. Use of the Southern Ocean by breeding Short-tailed shearwaters (Puffinus tenuirostris). J Exp Mar Biol Ecol. 2014; 450:109-17.
• [35]Einoder LD, Page B, Goldsworthy SD. Feeding strategies of the short-tailed shearwater vary by year and sea-surface temperature but do not affect breeding success. Condor. 2013; 115:777-87.
• [36]Sandery PA, Kämpf J. Winter-spring flushing of Bass Strait, south-eastern Australia: a numerical modelling study. Estuar Coast Shelf Sci. 2005; 63:23-31.
• [37]Gibbs C. Oceanography of Bass Strait: implications for the food supply of little penguins Eudyptula minor. Emu. 1992; 91:395-401.
• [38]Gill P. Ecological linkages within the Bonney Upwelling blue whale feeding area. Deakin University, School of Life and Sciences; 2004.
• [39]Butler A, Althaus F, Furlani D, Ridgway K. Assessment of the conservation values of the Bonney upwelling area: a component of the Commonwealth Marine Conservation Assessment Program 2002–2004: report to the Environment Australia, CSIRO Marine Research. 2002. Available from. http://www. environment.gov.au/system/files/resources/b3606df9-3fc5-48a6-a836-685337001578/files/conservation-assessment-bonney.pdf webcite
• [40]Collins M, Cullen J, Dann P. Seasonal and annual foraging movements of little penguins from Phillip Island, Victoria. Wildl Res. 1999; 26:705-21.
• [41]Fullagar PJ, Heyligers PC. Gabo Island Shearwater Surveys, 1995 and 1996. 1996.
• [42]Bowker GM. Griffiths Island. Corella. 1980; 4:104-6.
• [43]Phillips RA, Xavier JC, Croxall JP, Burger A. Effects of satellite transmitters on albatrosses and petrels. Auk. 2003; 120:1082-90.
• [44]Nieblas AE, Sloyan BM, Hobday AJ, Coleman R, Richardson AJ. Variability of biological production in low wind-forced regional upwelling systems: a case study off southeastern Australia. Limnol Oceanogr. 2009; 54:1548-58.
• [45]Ashok K, Guan Z, Yamagata T. Influence of the Indian Ocean Dipole on the Australian winter rainfall. Geophys Res Lett. 2003; 30:1821.
• [46]Sumner MD. trip: spatial analysis of animal track data. R package version 1.1-12. 2012.
• [47]Calenge C. The package “adehabitat” for the R software: a tool for the analysis of space and habitat use by animals. Ecol Model. 2006; 197:516-9.
• [48]McConnell B, Chambers C, Fedak M. Foraging ecology of southern elephant seals in relation to the bathymetry and productivity of the Southern Ocean. Antarct Sci. 1992; 4:393-8.
• [49]Wood A, Naef-Daenzer B, Prince P, Croxall J. Quantifying habitat use in satellite-tracked pelagic seabirds: application of kernel estimation to albatross locations. J Avian Biol. 2000; 31:278-86.
• [50]Wakefield ED, Bodey TW, Bearhop S, Blackburn J, Colhoun K, Davies R et al.. Space partitioning without territoriality in gannets. Science. 2013; 341:68-70.
• [51]Phillips R, Silk J, Croxall J, Afanasyev V, Briggs D. Accuracy of geolocation estimates for flying seabirds. Mar Ecol Prog Ser. 2004; 266:265-72.
• [52]Shaffer SA, Tremblay Y, Awkerman JA, Henry RW, Teo SL, Anderson DJ et al.. Comparison of light-and SST-based geolocation with satellite telemetry in free-ranging albatrosses. Mar Biol. 2005; 147:833-43.
• [53]Ekstrom P. Error measures for template-fit geolocation based on light. Deep-Sea Res II Top Stud Oceanogr. 2007; 54:392-403.
• [54]Sumner MD, Wotherspoon SJ, Hindell MA. Bayesian estimation of animal movement from archival and satellite tags. PLoS One. 2009; 4: Article ID e7324
• [55]Thiebot J-B, Pinaud D. Quantitative method to estimate species habitat use from light-based geolocation data. Endanger Species Res. 2010; 10:341-53.
• [56]Jonsen ID, Flemming JM, Myers RA. Robust state-space modeling of animal movement data. Ecology. 2005; 86:2874-80.
• [57]Phillips RA, Silk JR, Croxall JP, Afanasyev V. Year-round distribution of white-chinned petrels from South Georgia: relationships with oceanography and fisheries. Biol Conserv. 2006; 129:336-47.
• [58]R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria; 2013.
• [59]Paiva VH, Geraldes P, Ramirez I, Meirinho A, Garthe S, Ramos JA. Foraging plasticity in a pelagic seabird species along a marine productivity gradient. MEPS. 2010; 398:259-74.
• [60]Quillfeldt P, Strange IJ, Masello JF. Sea surface temperatures and behavioural buffering capacity in thin-billed prions Pachyptila belcheri: breeding success, provisioning and chick begging. J Avian Biol. 2007; 38:298-308.
• [61]Welcker J, Harding AMA, Karnovsky NJ, Steen H, Strøm H, Gabrielsen GW. Flexibility in the bimodal foraging strategy of a high Arctic alcid, the little auk Alle alle. J Avian Biol. 2009; 40:388-99.
• [62]Oka N, Maruyama N, Skira I. Chick growth and mortality of short-tailed shearwaters in comparison with sooty shearwaters, as a possible index of fluctuations of Australian krill abundance. Polar Biol. 1987; 1:166-74.
• [63]Gibbens J, Arnould JPY. Interannual variation in pup production and the timing of breeding in benthic foraging Australian fur seals. Marine Mammal Science. 2009; 25:573-87.
• [64]Ridgway KR. Long-term trend and decadal variability of the southward penetration of the East Australian Current. Geophys Res Lett. 2007; 34:1-5.
• [65]Poloczanska E, Babcock R, Butler A, Hobday A, Hoegh-Guldberg O, Kunz T et al.. Climate change and Australian marine life. Oceanogr Mar Biol. 2007; 45:407-78.
• [66]Carey MJ, Phillips RA, Silk JRD, Shaffer SA. Trans-equatorial migration of Short-tailed Shearwaters revealed by geolocators. Emu. 2014; 114:352-9.
• [67]Nicol S. Krill, currents, and sea ice: Euphausia superba and its changing environment. Bioscience. 2006; 56:111-20.
• [68]Pakhomov E, Perissinotto R, McQuaid C. Prey composition and daily rations of myctophid fishes in the Southern Ocean. Marine Ecology Progress Series Oldendorf. 1996; 134:1-14.
• [69]Pakhomov E, McQuaid C. Distribution of surface zooplankton and seabirds across the Southern Ocean. Polar Biol. 1996; 16:271-86.
• [70]Nicol S, Pauly T, Bindoff NL, Wright S, Thiele D, Hosie GW et al.. Ocean circulation off east Antarctica affects ecosystem structure and sea-ice extent. Nature. 2000; 406:504-7.
• [71]Reid K, Croxall JP. Environmental response of upper trophic-level predators reveals a system change in an Antarctic marine ecosystem. Proc R Soc Lond B Biol Sci. 2001; 268:377-84.
• [72]Woehler EJ, Raymond B, Watts DJ. Decadal-scale seabird assemblages in Prydz Bay, East Antarctica. MEPS. 2003; 251:299-310.
• [73]Woehler EJ, Raymond B, Boyle A, Stafford A. Seabird assemblages observed during the BROKE-West survey of the Antarctic coastline (30°E–80°E), January–March 2006. Deep-Sea Res II Top Stud Oceanogr. 2010; 57:982-91.
• [74]Atkinson A, Siegel V, Pakhomov E, Rothery P. Long-term decline in krill stock and increase in salps within the Southern Ocean. Nature. 2004; 432:100-3.
• [75]Hill KL, Rintoul SR, Coleman R, Ridgway KR. Wind forced low frequency variability of the East Australia Current. Geophys Res Lett. 2008;35.
• [76]Hobday AJ, Pecl GT. Identification of global marine hotspots: sentinels for change and vanguards for adaptation action. Rev Fish Biol Fish. 2013; 24:415-25.
• [77]Ridgway K, Hill K. The East Australian Current. In: Poloczanska ES, Hobday AJ, Richardson AJ, editors. A marine climate change impacts and adaptation report card for Australia 2009. NCCARF Publication 05/09; 2009
• [78]Brown CJ, Fulton EA, Hobday AJ, Matear RJ, Possingham HP, Bulman C et al.. Effects of climate-driven primary production change on marine food webs: implications for fisheries and conservation. Glob Chang Biol. 2010; 16:1194-212.
• [79]Schofield O, Ducklow HW, Martinson DG, Meredith MP, Moline MA, Fraser WR. How do polar marine ecosystems respond to rapid climate change? Science. 2010; 328:1520-3.
• [80]Trivelpiece WZ, Hinke JT, Miller AK, Reiss CS, Trivelpiece SG, Watters GM. Variability in krill biomass links harvesting and climate warming to penguin population changes in Antarctica. Proc Natl Acad Sci U S A. 2011; 108:7625-8.
• [81]Bradley J, Cox J, Nicholson L, Wooller R, Hamer K, Hill J. Parental influence upon the provisioning schedules of nestling Short-Tailed Shearwaters Puffinus tenuirostris. J Avian Biol. 2000; 31:522-6.
• [82]Orsi AH, Whitworth T, Nowlin WD. On the meridional extent and fronts of the Antarctic Circumpolar Current. Deep-Sea Res I Oceanogr Res Pap. 1995; 42:641-73.
• [83]Park YH, Charriaud E, Fieux M. Thermohaline structure of the Antarctic surface water/winter water in the Indian sector of the Southern Ocean. J Mar Syst. 1998; 17:5-23.