Abstract
Seabirds are one of the most threatened groups of birds globally and, overall, their conservation status is deteriorating rapidly. Southern hemisphere countries are over-represented in the number of species of conservation concern yet long-term phenological data on seabirds in the southern hemisphere is limited. A better understanding of the implications of changes in the marine and terrestrial environments to seabird species is required in order to improve their management and conservation status. Here we conducted a meta-analysis of the phenological drivers and trends among southern hemisphere seabirds. Overall there was a general trend towards later phenological events over time (34 % of all data series, N = 47; 67 % of all significant trends), though this varied by taxa and location. The strongest trends towards later events were for seabirds breeding in Australia, the Laridae (gulls, noddies, terns) and migratory southern polar seabirds. In contrast, earlier phenologies were more often observed for the Spheniscidae (penguins) and for other seabirds breeding in the Antarctic and subantarctic. Phenological changes were most often associated with changes in oceanographic conditions, with sea-ice playing an important role for more southerly species. For some species in some locations, such as the Little Penguin Eudyptula minor in south-eastern Australia, warmer oceans projected under various climate change scenarios are expected to correspond to increased seabird productivity, manifested through earlier breeding, heavier chicks, an increased chance of double brooding, at least in the short-term.
Similar content being viewed by others
References
Ainley DG (2002) Adélie penguin bellwether of climate change. Columbia University Press, New York
Allen WJ, Helps FW, Molles LE (2011) Factors affecting breeding success of the Flea Bay white-flippered penguin (Eudyptula minor albosignata) colony. N Z J Ecol 35:199–208
Baduini CL, Hyrenbach KD, Coyle KO, Pinchuk A, Mendenhall V, Hunt GL (2001) Mass mortality of short-tailed shearwaters in the south-eastern Bering Sea during summer 1997. Fish Oceanogr 10:117–130
Barbraud C, Weimerskirch H (2006) Antarctic birds breed later in response to climate change. Proc Natl Acad Sci USA 103:6248–6251
Barlow ML, Dowding JE (2002) Breeding biology of Caspian terns (Sterna caspia) at a colony near Invercargill, New Zealand. Notornis 49(2):79–90
Baylis AMM, Zuur AF, Brickle P, Pistorius PA (2012) Climate as a driver of population variability in breeding Gentoo Penguins Pygoscelis papua at the Falkland Islands. Ibis 154:30–41
Boersma PD, Rebstock GA (2009) Intraclutch egg-size dimorphism in Magellanic Penguins (Spheniscus magellanicus): adaptation, constraint, or noise? Auk 126(2):335–340
Cannell B, Pollock K, Bradley S, Wooller R, Sherwin W, Sinclair J (2011) Augmenting mark-recapture with beach counts to estimate the abundance of little penguins on Penguin Island, Western Australia. Wildl Res 38:491–500. doi:10.1071/WR11042
Cannell BL, Chambers LE, Wooller RD, Bradley JS (2012) Poorer breeding by Little Penguins near Perth, Western Australia is correlated with above average sea surface temperatures and a stronger Leeuwin Current. Mar Freshw Res 63(10):914–925. doi: 10.1071/MF12139
Chambers LE, Devney CA, Congdon BC, Dunlop N, Woehler EJ, Dann P (2011) Observed and predicted effects of climate on Australian seabirds. Emu 111:235–251
Chambers LE, Keatley MR, Woehler EJ, Bergstrom DM (2013a) Antarctica. In: Schwartz MD (ed) Phenology: an integrative environmental science. Springer, Berlin
Chambers LE, Altwegg R, Barbraud C, Barnard P, Beaumont L, Crawford R, Durrant JM, Hughes L, Keatley MR, Low M, Morellato LPC, Poloczanska E, Ruoppolo V, Vansteels R, Woehler E, Wolfaardt A (2013b) Changes in Southern Hemisphere phenology. PLOS One (in press)
Cherubini G, Serra L, Baccetti N (1996) Primary moult, body mass and moult migration of Little Tern Sterna albifrons in northeast Italy. Ardea 84:99–114
Crawford RJM, Dyer BM, Cooper J, Underhill LG (2006) Breeding numbers and success of Eudyptes penguins at Marion Island, and the influence of mass and time of arrival of adults. CCAMLR Sci 13:175–190
Croxall JP, Butchart SHM, Lascelles B, Stattersfield AJ, Sullivan B, Symes A, Taylor P (2012) Seabird conservation status, threats and priority actions: a global assessment. Bird Conserv Int 22:1–34
Cullen JM, Chambers LE, Coutin PC, Dann P (2009) Predicting the onset and success of breeding of Little Penguins, Eudyptula minor, on Phillip Island from ocean temperatures off south east Australia. Mar Ecol Prog Ser 378:269–278
Dann P, Chambers LE (2013) Ecological effects of climate change on Little Penguins Eudyptula minor and the potential economic impact on tourism. Clim Res (in press)
Dann P, Cullen JM (1990) Chapter 3. Survival, patterns of reproduction and lifetime reproductive success in little blue penguins (Eudyptula minor) in Victoria, Australia. In: Davis L, Darby J (eds) Penguin biology. Academic, San Diego, pp 63–84
Dunlop JN, Surman CA (2012) The role of foraging ecology in the contrasting responses of two dark terns to a changing ocean climate. Mar Ornithol 40:105–110
Durant JM, Hjermann DØ, Ottersen G, Stenseth NC (2007) Climate and the match or mismatch between predator requirements and resource availability. Clim Res 33:271–283
Durant JM, Crawford RJM, Wolfaardt AC, Agenbag CJ, Visagie J, Upfold L, Stenseth NC (2010) Influence of feeding conditions on breeding of African penguins—importance of adequate local food supplies. Mar Ecol Prog Ser 420:263–271
Emmerson L, Pike R, Southwell C (2011) Reproductive consequences of environment-driven variation in Adélie penguin breeding phenology. Mar Ecol Prog Ser 440:203–216
Fortescue M (1998) The marine and terrestrial ecology of a northern population of the Little Penguin, Eudyptula minor, from Bowen Island, Jervis Bay. PhD Thesis, University of Canberra
Hindell MA, Bradshaw CA, Brook BW, Fordham DA, Knowles K, Hull C, McMahon CR (2012) Long-term breeding phenology shift in royal penguins. Ecol Evol 2:1563–1571
Imber M, West JA, Cooper WJ (2003) Cook’s petrel (Pterodroma cookii): historic distribution, breeding biology and effects of predators. Notornis 50:221–230
Knox GA (2007) Biology of the southern ocean, 2nd edn. CRC, Boca Raton
Lynch HJ, Fagan WF, Naveen R, Trivelpiece SG, Trivelpiece WZ (2009) Timing of clutch initiation in Pygoscelis penguins on the Antarctic Peninsula: towards an improved understanding of off-peak census correction factors. CCAMLR Sci 16:149–165
Lynch HJ, Fagan WF, Naveen R, Trivelpiece SG, Trivelpiece WZ (2012) Differential advancement of breeding phenology in response to climate may alter staggered breeding among sympatric pygoscelid penguins. Mar Ecol Prog Ser 454:135–145
McCutcheon C, Dann P, Salton M, Renwick L, Gormley A, Arnould J (2011) Foraging range of Little Penguins during winter. Emu 111:321–329
McMahon C, Hindell MA (2009) Royal penguin phenology: Changes in the timing of egg-laying of a Sub-Antarctic predator in response to a changing marine environment. In: Stienin E, Ratcliffe N, Seys J, Jürgen T, Mees J, Dobbelaere I (eds) Seabird Group 10th International Conference VLIZ Special Publication 42. Communications of the Research Institute for Nature and Forest. Research Institute for Nature and Forest (INBM), Brussels, Belgium. Flanders Marine Institute (VLIZ) Oostende, Belgium, p 45
Mills JA, Yarrall JW, Bradford-Grieve JM, Uddstrom MJ, Renwick JA, Merilä J (2008) The impact of climate fluctuation on food availability and reproductive performance on the planktivorous red-billed gull Larus novaehollandiae scopulinus. J Anim Ecol 77:1129–1142
Paredes R, Zavalaga CB, Boness DJ (2002) Patterns of egg laying and breeding success in Humboldt penguins (Spheniscus humboldti) at Punta San Juan, Peru. Auk 119:244–250
Parker DE, Folland CK, Bevan AC, Ward MN, Jackson M, Maskerll K (1995) Marine surface data for analysis of climatic fluctuations on interannual-to-century time scales. In: Climate Research Committee (ed) National climate variability on decade-to-century time scales. National Academy Press, Washington DC, pp 241–252
Peacock L, Paulin M, Darby J (2000) Investigations into climate influence on population dynamics of yellow-eyed penguins Megadyptes antipodes. N Z J Zool 27:317–325
Perriman L, Steen H (2000) Blue penguin (Eudyptula minor) nest distribution and breeding success on Otago Peninsula, 1992 to 1998. N Z J Zool 27:269–275
Perriman L, Houston D, Steen H, Johannesen E (2000) Climate fluctuation effects on breeding of blue penguins (Eudyptula minor). N Z J Zool 27:261–267
Przybylo R, Sheldon BC, Merila J (2000) Climatic effects on breeding and morphology: evidence for phenotypic plasticity. J Anim Ecol 69:395–403
Ramos JA, Maul AM, Ayrton V, Bullock I, Hunter J, Bowler J, Castle G, Mileto R, Pacheco C (2002) Influence of local and large-scale weather events and timing of breeding on tropical roseate tern reproductive parameters. Mar Ecol Prog Ser 243:271–279
Ramos JA, Maul AM, Bowler J, Wood L, Threadgold R, Johnson S, Birch D, Walker S (2006) Annual variation in laying date and breeding success of Brown Noddies on Aride Island, Seychelles. Emu 106:81–86
Reilly PN, Cullen JM (1983) The Little Penguin Eudyptula minor in Victoria, IV: the moult. Emu 83:94–98
Reynolds RW, Smith TM (1994) Improved global sea surface temperature analysis using optimum interpolation. J Clim 7:929–948
Ropert-Couder Y, Cannell B, Kato A (2004) Temperature inside nest boxes of little penguins. Wildl Soc Bull 32:177–182
Sagar P, Miskelly C, Sagar J, Tennyson AJD (2003) Population size, breeding, and annual cycle of the New Zealand Antarctic tern (Sterna vittata bethunei) at the Snares Islands. Notornis 50:36–42
Saraux C, Le Bohec C, Durant JM, Viblanc VA, Gauthier-Clerc M, Beaune D, Park Y-H, Yoccoz NG, Stenseth NC, Le Maho Y (2011) Reliability of flipper-banded penguins as indicators of climate change. Nature 469:203–208
Stahel C, Gales R (1987) Little penguins: Fairy penguins in Australia. New South Wales University Press, Kensington
Surman CA, Nicholson LW (2009a) El Niño Southern Oscillation and the Leeuwin Current influence on seabird reproductive performance and diet at the Houtman Abrolhos. J R Soc West Aust 92:155–163
Surman CA, Nicholson LW (2009b) 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. Mar Ornithol 37:129–138
Surman CA, Nicholson LW, Santora JA (2012) Effects of climate variability on breeding phenology and performance of tropical seabirds in the eastern Indian Ocean. Mar Ecol Prog Ser 454:147–157
Sutherland DR, Dann P (2012) Improving the accuracy of population size estimates for burrowing seabirds. Ibis 154:488–498
Underhill L, Crawford R (1999) Season of moult of African penguins at Robben Island, South Africa, and its variation, 1988–1998. S Afr J Mar Sci 21:437–441
Watanuki Y, Ito M (2012) Climatic effects on breeding seabirds of the northern Japan Sea. Mar Ecol Prog Ser 454:105–307
Woehler EJ (2012) What do signals from seabirds tell us about the marine environment? In: Heuttmann F (ed) Protection of the three poles. Springer, Berlin, pp 218–225
Wolfaardt AC, Underhill LG, Visagie J (2009a) Breeding and moult phenology of African Penguins Spheniscus demersus at Dassen Island. Afr J Mar Sci 31:119–132
Wolfaardt A, Underhill L, Crawford R (2009b) Comparison of moult phenology of African penguins Spheniscus demersus at Robben and Dassen islands. Afr J Mar Sci 31:19–29
Acknowledgements
We wish to acknowledge countless students and volunteers who have helped to monitor the various Little Penguin colonies over the years and whose dedication has greatly enhanced our knowledge of this species. These include members of the Penguin Study Group (Phillip Island) and Earthcare St Kilda Inc. We are grateful to two anonymous reviewers for comments and suggestions on an earlier version of this manuscript.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Chambers, L.E., Dann, P., Cannell, B. et al. Climate as a driver of phenological change in southern seabirds. Int J Biometeorol 58, 603–612 (2014). https://doi.org/10.1007/s00484-013-0711-6
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00484-013-0711-6