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Trends in numbers of the Critically Endangered Chinese Crested Tern Thalasseus bernsteini and sympatrically nesting Greater Crested Tern T. bergii in the Matsu Archipelago, Taiwan



The Chinese Crested Tern Thalasseus bernsteini (CCT) is likely the most critically endangered seabird species in Asia. The Matsu, Penghu, Jiushan, and Wuzhishan Archipelagos along the China coastline, plus Yeonggwang County in South Korea, are the five areas where this species is currently confirmed to breed. According to census and historical data collected in the Matsu Archipelago from 2004 to 2017, there was an average of 10 ± 4 adult CCT individuals at the Matsu Islands Tern Refuge (MITR) during the breeding season. CCT nested only in association with Greater Crested Terns T. bergii (GCT) among seven protected islands in the MITR, and the numbers of observed breeding individuals of the two species were positively correlated (r = 0.59, P < 0.001). We used generalized linear models to examine the effects of chlorophyll-a concentrations in surrounding marine habitats, typhoon frequency, and in-season shifts in colony location on inter-annual variation in numbers of breeding individuals and productivity (chick:adult ratios) of both CCT and GCT at the MITR from 2004 to 2017. Average chlorophyll-a concentrations during July-August obtained from the MODIS satellite were positively correlated with the annual maximum number of GCT at the MITR, but not that of CCT. In addition, we found that nest abandonment events during early incubation at the mixed-species colonies were associated with in-season shifts in colony location and delayed nesting chronology, thereby extending nesting into the peak typhoon season during July and August. The effects of in-season colony shifts on nesting chronology and the additive effects of typhoons caused a significant decline in CCT breeding success during the study period. We propose more rigorous monitoring to ascertain the root causes of in-season colony shifts of terns and then determine possible solutions. Additionally, creating educational programmes to increase public awareness towards seabird conservation could prove beneficial.


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Adams, J., Takekawa, J. Y., Carter, H. R. and Yee, J. (2010) Factors influencing the at-sea distribution of Cassin’s Auklets (Ptychoramphus aleuticus) that breed in the Channel Islands, California. Auk 127: 503513.
Akaike, H. (1974) A new look at the statistical model identification, IEEE Trans. Autom. Control 19: 716723.
Arnold, J. M., Hatch, J. J. and Nisbet, I. C. (2004) Seasonal declines in reproductive success of the common tern Sterna hirundo: timing or parental quality? J. Avian Biol. 35: 3345.
BirdLife International (2017) Thalasseus bernsteini. (amended version published in 2016) The IUCN Red List of Threatened Species 2017: e.T22694585A118862671. Downloaded on 06 December 2017.
Bugoni, L., Sander, M. and Costa, E. S. (2007) Effects of the first southern Atlantic hurricane on Aatlantic Petrels (Pterodroma incerta). Wilson J. Ornithol. 119: 725729.
Burger, J. (1984) Colony stability in Least Terns. Condor 86: 6167.
Burnham, K. P. and Anderson, D. R. (2003) Model selection and multimodel inference: a practical information-theoretic approach. New York: Springer Science & Business Media.
Chan, S., Chen, S. H. and Yuan, H. W. (2010) International single species action plan for the conservation of the Chinese Crested Tern (Sterna bernsteini). Bonn, Germany: BirdLife International Asia Division/CMS Secretariat.
Chang, S. H. (2008) Studies on the ornithological resources and their ecotourism in Matsu region. Master’s thesis. National Taiwan Ocean University, Keelung, Taiwan. (In Chinese with English abstract).
Chen, S. H., Chang, S. H., Liu, Y., Chan, S., Fan, Z. Y., Chen, C. S., Yen, C. W. and Guo, D. S. (2009) A small population and severe threats: status of the critically endangered Chinese Crested Tern Sterna bernsteini. Oryx 43: 209212.
Chen, S. H., Fan, Z. Y., Chen, C. S. and Lu, Y. W. (2011) The breeding biology of Chinese Crested Terns in mixed species colonies in eastern China. Bird Conserv. Internatn. 21: 266273.
Chen, S. H., Fan, Z. Y., Chen, C. S., Lu, Y. W. and Wang, Z. D. (2010) A new breeding site of the critically endangered Chinese Crested Tern Sterna bernsteini in the Wuzhishan archipelago, eastern China. Forktail 26: 132133.
Chen, S. H., Fan, Z. Y., Roby, D. D., Lu, Y. W., Chen, C. S., Huang, Q., Cheng, L. J. and Zhu, J. (2015) Human harvest, climate change and their synergistic effects drove the Chinese Crested Tern to the brink of extinction. Glob. Ecol. Conserv. 4: 137145.
Collar, N. J., Andreev, A. V., Chan, S., Crosby, M. J., Subramanya, S. and Tobias, J. A. (2001) Threatened birds of Asia: The BirdLife International Red Data Book. Cambridge, UK: Birdlife International.
Crawford, R. J. M. (2003) Influence of food on numbers breeding, colony size and fidelity to localities of Swift Terns in South Africa’s Western Cape, 1987-2000. Waterbirds 26: 4453.
Devney, C. A., Short, M. and Congdon, B. C. (2009) Cyclonic and anthropogenic influences on tern populations. Wildlife Res. 36: 368378.
Domingo, A., Jiménez, S., Abreu, M., Forselledo, R. and Yates, O. (2017) Effectiveness of tori line use to reduce seabird bycatch in pelagic longline fishing. PLoS ONE 12: e0184465.
Erwin, R. M., Galli, J. and Burger, J. (1981) Colony site dynamics and habitat use in Atlantic coast seabirds. Auk 98: 550561.
Gochfeld, M. (1979) Breeding synchrony in black skimmers: colony vs. subcolonies. Waterbirds 2: 171177.
Gong, G. C., Chen, L. Y. L. and Liu, K. K. (1996) Chemical hydrography and chlorophyll a distribution in the East China Sea in summer: implications in nutrient dynamics. Cont. Shelf Res. 16: 15611590.
Gong, G. C., Wen, Y. H., Wang, B. W. and Liu, G. J. (2003) Seasonal variation of chlorophyll a concentration, primary production and environmental conditions in the subtropical East China Sea. Deep Sea Res. Part II Top. Stud. Oceanogr. 50: 12191236.
Grémillet, D., Lewis, S., Drapeau, L., van Der Lingen, C. D., Huggett, J. A., Coetzee, J. C. … and Ryan, P. G. (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: 610621.
Hatchwell, B. J. (1991) An experimental study of the effects of timing of breeding on the reproductive success of Common Guillemots (Uria aalge). J. Anim. Ecol. 60: 721736.
Hsieh, H. Y., Lo, W. T., Chen, H. H. and Meng, P. J. (2016) Larval fish assemblages and hydrographic characteristics in the coastal waters of southwestern Taiwan during non-and post-typhoon summers. Zool. Stud. 55: 117.
Jones, H. P. and Kress, S. W. (2012) A review of the world’s active seabird restoration projects. J. Wildlife Manage. 76: 29.
Kim, J. Y., Kang, Y. S., Oh, H. j., Suh, Y. S. and Hwang, J. D. (2005) Spatial distribution of early life stages of anchovy (Engraulis japonicus) and hairtail (Trichiurus lepturus) and their relationship with oceanographic features of the East China Sea during the 1997–1998 El Niño Event. Estuar. Coast. Shelf Sci. 63: 1321.
King, B., Hicks, J. and Cornelius, J. (1992) Population-changes, breeding cycles and breeding success over six years in a seabird colony at Michaelmas Cay, Queensland. Emu 92: 110.
Langham, N. and Hulsman, K. (1986) The breeding biology of the Crested Tern Sterna bergii. Emu 86: 2332.
Le Corre, M., Jaeger, A., Pinet, P., Kappes, M. A., Weimerskirch, H., Catry, T., Ramos, J. A., Russell, J. C., Shah, N. and Jaquemet, S. (2012) Tracking seabirds to identify potential Marine Protected Areas in the tropical western Indian Ocean. Biol. Conserv. 156: 8393.
Liu, Y., Guo, D. S., Qiao, Y. L., Zhang, E. and Cai, B. F. (2009) Regional extirpation of the critically endangered Chinese Crested Tern (Thalasseus bernsteini) from the Shandong coast, China? Waterbirds 32: 597599.
Martinez-Abrain, A., Oro, D., Forero, M. G. and Conesa, D. (2003) Modeling temporal and spatial colony-site dynamics in a long-lived seabird. Popul. Ecol. 45: 133139.
McLeay, L. J., Page, B. and Goldsworthy, S. D. (2017) But first, are you experienced? The consequences of timing, age, and adult condition on reproductive performance in Greater Crested Terns Thalasseus bergii. Mar. Ornithol. 45: 205215.
McLeay, L. J., Page, B., Goldsworthy, S. D., Paton, D. C., Teixeira, C., Burch, P. and Ward, T. (2010) Foraging behaviour and habitat use of a short-ranging seabird, the Crested Tern. Mar. Ecol. Prog. Ser. 411: 271283.
Monaghan, P. and Nager, R. G. (1997) Why don’t birds lay more eggs? Trends Ecol. Evol. 12: 270274.
QGIS Development Team (2017) QGIS Geographic Information System. Open Source Geospatial Foundation Project.
R Core Team (2017) R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing,
Regular, P. M., Hedd, A., Montevecchi, W. A., Robertson, G. J., Storey, A. E. and Walsh, C. J. (2014) Why timing is everything: energetic costs and reproductive consequences of resource mismatch for a chick-rearing seabird. Ecosphere 5: 113.
Song, S. K., Lee, S. W., Lee, Y. K., Lee, S. Y., Kim, C. H., Choi, S. S., Shin, H. C., Park, J. Y., Lee, J. H. and Kim, W. Y. (2017) First report and breeding record of the Chinese Crested Tern Thalasseus bernsteini on the Korean Peninsula. J. Asia Pac. Biodivers. 10: 250253
Suryan, R. M., Santora, J. A. and Sydeman, W. J. (2012) New approach for using remotely sensed chlorophyll a to identify seabird hotspots. Mar. Ecol. Prog. Ser. 451: 213225.
Tasker, M. L., Jones, P. H., Dixon, T. and Blake, B. F. (1984) Counting seabirds at sea from ships: a review of methods employed and a suggestion for a standardized approach. Auk 101: 567577.
Tayefeh, F. H., Zakaria, M., Mohamadi, H., Amini, H. and Ghasemi, S. (2015) Segregation in timing of breeding reduces inter-specific competition in tern species on the Persian Gulf Islands. Podoces 10: 2734.
Velarde, E., Ezcurra, E., Horn, M. H. and Patton, R. T. (2015) Warm oceanographic anomalies and fishing pressure drive seabird nesting north. Sci. Adv. 1: e1400210.
Visser, J. M. and Peterson, G. W. (1994) Breeding populations and colony site dynamics of seabirds nesting in Louisiana. Waterbirds 17: 146152.
Votier, S. C., Bearhop, S., Witt, M. J., Inger, R., Thompson, D. and Newton, J. (2010) Individual responses of seabirds to commercial fisheries revealed using GPS tracking, stable isotopes and vessel monitoring systems. J. Appl. Ecol. 47: 487497.
Walter, C. (1984) Fish prey remains in Swift Tern and Hartlaub’s Gull pellets at Possession-Island, off Namibia. Ostrich 55: 166167.
Wiley, J. W. and Wunderle, J. M. Jr. (1993) The effects of hurricanes on birds, with special reference to Caribbean islands. Bird Conserv. Internatn. 3: 319349.


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