Understanding the foraging behavior is essential for investigating seabird ecology and conservation, as well as monitoring the well-being of the marine environment. Breeding seabirds adopt diverse foraging strategies to maximize energy gains and cope with the intensified challenges of parenting and self-maintenance. Such trade-off may stem from the heterogeneity of food resources and the constraints of central place foraging. Nevertheless, abundant marine productivity could alleviate the energy limitation for seabirds, resulting in a consistent foraging approach. Here, we investigated the foraging strategy during the breeding season of a cryptic small-sized seabird, Swinhoe’s Storm-petrel (Hydrobates monorhis), in the Yellow Sea, a productive marginal sea of the Northwest Pacific. Using GPS tracking, we evaluated habitat preference, quantified the foraging strategy, and tested if environmental conditions and individual traits influence foraging trips. We found that Swinhoe’s Storm-petrels preferred nearshore areas with shallow water and engaged in primarily short foraging trips. Distinctive southeastward and southwestward strategies emerged when combining trip metrics, including foraging direction, duration, and maximum distance. The bathymetry, proximity to the coastline, and sea surface temperature differed in two foraging strategies. Foraging strategies exhibited flexibility between individuals, potentially explained by wing morphology, in which longer-winged birds are more likely to embark on longer-distance foraging trips. These findings highlight the impact of environmental factors and individual traits on seabirds’ foraging decisions in productive marginal sea ecosystems. Our study also provides valuable insights into the foraging ecology of this Asian endemic storm-petrel.
Arcilla, N., Choi, C.Y., Ozaki, K., Lepczyk, C.A., 2015. Invasive species and Pacific island bird conservation: a selective review of recent research featuring case studies of Swinhoe’s Storm-petrel and the Okinawa and Guam rail. J. Ornithol. 156, S199-S207.
Baduini, C.L., Hyrenbach, K.D., 2003. Biogeography of procellariiform foraging strategies: Does ocean productivity influence provisioning? Mar. Ornithol. 31, 101–112.
Ballance, L.T., Pitman, R.L., Fiedler, P.C., 2006. Oceanographic influences on seabirds and cetaceans of the eastern tropical Pacific: A review. Prog. Oceanogr. 69, 360–390.
Beal, M., Oppel, S., Handley, J., Pearmain, E.J., Morera-Pujol, V., Carneiro, A.P.B., et al., 2021. track2KBA: An R package for identifying important sites for biodiversity from tracking data. Methods Ecol. Evol. 12, 2372–2378.
Bolnick, D.I., Svanbäck, R., Fordyce, J.A., Yang, L.H., Davis, J.M., Hulsey, C.D., et al., 2003. individual specialization. Am. Nat. 161, 1–28.
Bolton, M., 2020. GPS tracking reveals highly consistent use of restricted foraging areas by European Storm-Petrels Hydrobates pelagicus breeding at the largest UK colony: Implications for conservation management. Bird Conserv. Int. 31, 35–52.
Bond, A.L., McClelland, G.T.W., Jones, I.L., Lavers, J.L., Kyser, T.K., 2010. Stable isotopes confirm community patterns in foraging among Hawaiian Procellariiformes. Waterbirds 33, 50–58.
Bretagnolle, V., 1993. Adaptive significance of seabird coloration: the case of Procellariiforms. Am. Nat. 142, 141–173.
Brooke, M., 2004. Albatrosses and Petrels across the World. Oxford University Press, Oxford.
Calenge, C., 2006. The package ‘adehabitat’ for the R software: A tool for the analysis of space and habitat use by animals. Ecol. Modell. 197, 516–519.
Choi, C.Y., Nam, H.Y., Park, J.G., Lee, K.G., 2011. Swinhoe’s Storm Petrels (Oceanodroma monohris) show no apparent sexual dimorphism in size and color. Ornithol. Sci. 10, 145–149.
Claustre, H., Maritorena, S., 2003. The many shades of Ocean Blue. Science 302, 1514–1515.
Clay, T.A., Joo, R., Weimerskirch, H., Phillips, R.A., den Ouden, O., Basille, M., et al., 2019a. Sex-specific effects of wind on the flight decisions of a sexually dimorphic soaring bird. J. Anim. Ecol. 89, 1811–1823.
Clay, T.A., Oppel, S., Lavers, J.L., Phillips, R.A., Brooke, M. de L., 2019b. Divergent foraging strategies during incubation of an unusually wide-ranging seabird, the Murphy’s petrel. Mar. Biol. 166, 1–14.
Collins, S.M., Hedd, A., Fifield, D.A., Wilson, D.R., Montevecchi, W.A., 2022. Foraging paths of breeding Leach’s Storm-Petrels in relation to offshore oil platforms, Breeding Stage, and Year. Front. Mar. Sci. 9, 816659.
Cui, Z., 1993. Study on reproduction and migration of Ancient Murrelet. Chin. J. Zool. 28, 27-30. (In Chinese).
Cui, Z., 1998. Study on breeding and migration of Swinhoe’s Storm-Petrel. Chin. J. Zool. 33, 19-22. (In Chinese).
Dalgaard, P., 2008. Introductory Statistics with R, second ed. Springer, New York, NY, USA.
Davies, T.E., Carneiro, A.P.B., Tarzia, M., Wakefield, E., Hennicke, J.C., Frederiksen, M., et al., 2021. Multispecies tracking reveals a major seabird hotspot in the North Atlantic. Conserv. Lett. 14, 1–14.
De la Cruz, A., Pereira, J.M., Paiva, V.H., Ramos, J.A., Oliveira, N., Alonso, H., et al., 2023. Using long-term data series to design adequate protected areas that ensure the conservation of inconspicuous small petrel species. J. Appl. Ecol. 60, 2586–2601.
Dodge, S., Bohrer, G., Weinzierl, R., Davidson, S.C., Kays, R., Douglas, D., et al., 2013. The environmental-data automated track annotation (Env-DATA) system: linking animal tracks with environmental data. Mov. Ecol. 1, 1–14.
Gatt, M.C., Lago, P., Austad, M., Bonnet-Lebrun, A.S., Metzger, B.J., 2019. Pre-laying movements of Yelkouan Shearwaters (Puffinus yelkouan) in the Central Mediterranean. J. Ornithol. 160, 625–632.
Geen, G.R., Robinson, R.A., Baillie, S.R., 2019. Effects of tracking devices on individual birds - a review of the evidence. J. Avian Biol. 1–13.
Granadeiro, J.P., Nunes, M., Silva, M.C., Furness, R.W., 1998. Flexible foraging strategy of Cory’s shearwater, Calonectris diomedea, during the chick-rearing period. Anim. Behav. 56, 1169–1176.
Grémillet, D., Lewis, S., Drapeau, L., van der Lingen, C.D., Huggett, J.A., Coetzee, J.C., et al., 2008. Spatial match-mismatch in the Benguela upwelling zone: Should we expect chlorophyll and sea-surface temperature to predict marine predator distributions? J. Appl. Ecol. 45, 610–621.
Hays, G.C., Bailey, H., Bograd, S.J., Bowen, W.D., Campagna, C., Carmichael, R.H., et al., 2019. Translating marine animal tracking data into conservation policy and management. Trends Ecol. Evol. 34, 459–473.
Hedd, A., Pollet, I.L., Mauck, R.A., Burke, C.M., Mallory, M.L., McFarlane Tranquilla, L.A., et al., 2018. Foraging areas, offshore habitat use, and colony overlap by incubating Leach’s Storm-Petrels Oceanodroma leucorhoa in the northwest atlantic. PLoS One 13, 1–18.
Huang, X., Zhao, Y., Liu, Y., 2021. Using light-level geolocations to monitor incubation behavior of a cavity-nesting bird Apus apus pekinensis. Avian Res. 12, 1–6.
Jessopp, M., Arneill, G.E., Nykanen, M., Bennison, A., Rogan, E., 2020. Central place foraging drives niche partitioning in seabirds. Oikos 129, 1704–1713.
Johnson, D., 1980. The comparison of usage and availability measurements for evaluating resource preference. Ecology 61, 65–71.
Kays, R., Davidson, S.C., Berger, M., Bohrer, G., Fiedler, W., Flack, A., et al., 2021. The Movebank system for studying global animal movement and demography. Methods Ecol. Evol. 2021, 1–13.
Lago, P., Austad, M., Metzger, B.J., 2019. Partial migration in the Mediterranean Storm-Petrel (Hydrobates pelagicus melitensis). Mar. Ornithol. 47, 105–113.
Lascelles, B.G., Taylor, P.R., Miller, M.G.R., Dias, M.P., Oppel, S., Torres, L., et al., 2016. Applying global criteria to tracking data to define important areas for marine conservation. Divers. Distrib. 22, 422–431.
Liu, D., Wang, X., 1993. A preliminary study onring study of Streaked Shearwater and Swinhoe’s Storm-Petrel in coastal islands of Qingdao. Sichuan J. Zool. 12, 32-33. (In Chinese).
Liu, J.Y., 2013. Status of Marine Biodiversity of the China Seas. PLoS One 8, e50719.
Liu, K.K., Kang, C.K., Kobari, T., Liu, H., Rabouille, C., Fennel, K., 2014. Biogeochemistry and ecosystems of continental margins in the western North Pacific Ocean and their interactions and responses to external forcing - An overview and synthesis. Biogeosciences 11, 7061–7075.
Liu, Y., Jiang, G., 2013. Marine bird resources and their conservation status in the Yellow Sea in China. Bull. Biol. 48, 5-7. (In Chinese).
Ma, S., Liu, D., Tian, Y., Fu, C., Li, J., Ju, P., et al., 2021. Critical transitions and ecological resilience of large marine ecosystems in the Northwestern Pacific in response to global warming. Glob. Chang. Biol. 27, 5310–5328.
Matsumoto, S., Yamamoto, T., Kawabe, R., Ohshimo, S., Yoda, K., 2016. The Changjiang River discharge affects the distribution of foraging seabirds. Mar. Ecol. Prog. Ser. 555, 273–277.
Matsumoto, S., Yamamoto, T., Yamamoto, M., Zavalaga, C.B., Yoda, K., 2017. Sex-related differences in the foraging movement of streaked shearwaters Calonectris leucomelas breeding on Awashima Island in the sea of Japan. Ornithol. Sci. 16, 23–32.
Mauck, R.A., Pratte, I., Hedd, A., Pollet, I.L., Jones, P.L., Montevecchi, W.A., et al., 2023. Female and male Leach’s Storm-Petrels (Hydrobates leucorhous) pursue different foraging strategies during the incubation period. Ibis. 165, 161–178.
Mcnamara, J.M., Houston, A.I., 2008. Optimal annual routines : behavior in the context of physiology and ecology. Phil. Trans. R. Soc. B 363, 301–319.
Michelot, T.T., Langrock, R., Patterson, T.A., 2016. moveHMM: an R package for the statistical modelling of animal movement data using hidden Markov models. Methods Ecol. Evol. 7, 1308–1315.
Natsukawa, H., Sergio, F., 2022. Top predators as biodiversity indicators: A meta-analysis. Ecol. Lett. 25, 2062–2075.
Neves, V.C., Carroll, G., Schäfer, W.C., Hereward, H.F.R., Quillfeldt, P., 2023. Consistent foraging habitat use by a vulnerable breeding seabird highlights potential areas for protection in the mid-Atlantic Ocean. Mar. Ecol. Prog. Ser. 716, 107–121.
Ozsanlav-Harris, L., Griffin, L.R., Weegman, M.D., Cao, L., Hilton, G.M., Bearhop, S., 2022. Wearable reproductive trackers: quantifying a key life history event remotely. Anim. Biotelem. 10, 1–15.
Pante, E., Simon-Bouhet, B., 2013. marmap: A package for importing, plotting and analyzing bathymetric and topographic data in R. PLoS One 8, 6–9.
Phillips, J.A., Guilford, T., Fayet, A.L., 2023. How do resource distribution and taxonomy affect the use of dual foraging in seabirds? A review. Behav. Ecol. 34, 769–779.
Phillips, R.A., Lewis, S., González-solis, J., Daunt, F., 2017. Causes and consequences of individual variability and specialization in foraging and migration strategies of seabirds. Mar. Ecol. Progreess Ser. 578, 117–150.
Pinet, P., Jaquemet, S., Phillips, R.A., Le Corre, M., 2012. Sex-specific foraging strategies throughout the breeding season in a tropical, sexually monomorphic small petrel. Anim. Behav. 83, 979–989.
Pollet, I.L., Ronconi, R.A., Jonsen, I.D., Leonard, M.L., Taylor, P.D., Shutler, D., 2014. Foraging movements of Leach’s Storm-Petrels Oceanodroma leucorhoa during incubation. J. Avian Biol. 45, 305–314.
Poupart, T.A., Waugh, S.M., Kato, A., Arnould, J.P.Y., 2020. Foraging niche overlap during chick-rearing in the sexually dimorphic Westland petrel: Foraging behavior of Westland petrel. R. Soc. Open Sci. 7.
Pyke, G.H., 1984. Optimal foraging theory: a critical review. Annu. Rev. Ecol. Evol. Syst 15, 523–575.
Quillfeldt, P., Weimerskirch, H., Delord, K., Cherel, Y., 2020. Niche switching and leapfrog foraging: Movement ecology of sympatric petrels during the early breeding season. Mov. Ecol. 8, 8:23.
Ricklefs, R., 1990. Seabird life histories and the marine environment: Some speculations. Waterbirds 13, 1–6.
Riotte-Lambert, L., Matthiopoulos, J., 2020. Environmental predictability as a cause and consequence of animal movement. Trends Ecol. Evol. 35, 163–174.
Safi, K., Kranstauber, B., Weinzierl, R., Griffin, L., Rees, E.C., Cabot, D., et al., 2013. Flying with the wind: scale dependency of speed and direction measurements in modelling wind support in avian flight. Mov. Ecol. 1, 1–13.
Sai, D., 1993. A preliminary study on reproduction of white-fronted shearwater. Zool. Res. 2, 117+142+149+157.
Sato, F., Karino, K., Oshiro, A., Sugawa, H., Hirai, M., 2010. Breeding of Swinhoe’s Storm-Petrel Oceanodroma monorhis in the Kitsujima Islan, Kyoto, Japan. Mar. Ornithol. 38, 133–136.
Schwarz, J.F.L., Mews, S., DeRango, E.J., Langrock, R., Piedrahita, P., Paez-Rosas, D., et al., 2021. Individuality counts: A new comprehensive approach to foraging strategies of a tropical marine predator. Oecologia 195, 313–325.
Signer, J., Fieberg, J., Avgar, T., 2019. Animal movement tools (amt): R package for managing tracking data and conducting habitat selection analyses. Ecol. Evol. 9, 880–890.
Spear, L.B., Ainley, D.G., 2007. Storm-petrels of the Eastern Pacific Ocean: Species assembly and diversity along marine habitat gradients. Ornithol. Monogr. 62, 1–77.
Tinker, M.T., Costa, D.P., Estes, J.A., Wieringa, N., 2007. Individual dietary specialization and dive behavior in the California sea otter: Using archival time-depth data to detect alternative foraging strategies. Deep. Res. Part Ⅱ Top. Stud. Oceanogr. 54, 330–342.
Tyson, C.W., Jennings, S.L., Hoover, B.A., Miles, A., Shamoun-baranes, J., 2022. Energetic constraints drive sex-specific parental care in the monomorphic Leach’s Storm-Petrel Hydrobates leucorhous. J. Avian Biol. e02904.
Weimerskirch, H., 2007. Are seabirds foraging for unpredictable resources? Deep. Res. Part Ⅱ Top. Stud. Oceanogr. 54, 211–223.
Yamamoto, T., Takahashi, A., Oka, N., Iida, T., Katsumata, N., Sato, K., Trathan, P.N., 2011. Foraging areas of streaked shearwaters in relation to seasonal changes in the marine environment of the Northwestern Pacific: Inter-colony and sex-related differences. Mar. Ecol. Prog. Ser. 424, 191–204.
Zhou, W., Meng, W., Huang, Mingpan, Wei, F.W., 2020. A marine biodiversity plan for China and beyond. Science. 53, 2020–2022.