Late-arriving barn swallows linked to population declines Sang-Don Lee a,⇑ , Elizabeth R. Ellwood b , Se-young Park a , Richard B. Primack b a Department of Environmental Science and Engineering, Ewha Womans University, Seoul 120-750, Republic of Korea b Department of Biology, Boston University, 5 Cummington Street, Boston, MA 02215, USA article info Article history: Received 3 May 2011 Accepted 16 May 2011 Available online 24 June 2011 Keywords: Barn swallows Climate change Phenology South Korea abstract Barn swallows (Hirundo rustica) are arriving later in the spring than they did 30–40 years ago at numer- ous sites in Korea. In some cases their arrival times are later by more than 1 month. This result is perplex- ing as spring activities of plants and animals are generally getting earlier due to warming temperatures. The first arrival dates of swallows are not related to temperature, suggesting that another factor is involved. On the basis of a questionnaire, a large majority of long-term observers are confident that there has been a moderate to severe decline in swallow populations at their field site over the study period. The greatest delays in arrival times are associated with sites with more severe reported declines in population size. Simulations using trapping data of large migratory bird populations from the United States, consist- ing of hundreds of individuals, suggest that severe population declines of 99% can result in delays of 10– 12 days in arrival times. In summary, our results suggest that the large delays in arrival time of Korean swallows are due, at least in part, to severe reductions of more than 99% in what were formerly very large populations. Significant delays in spring phenology over time during a period of climatic warming may indicate population decline, though alternative explanations, such as changes in range or migration path or changing number of broods per season, should also be investigated. Delays in first arrival data can pro- vide a valuable new tool to conservation biologists by indicating declines in a population that would otherwise go unnoticed. This can, in turn, lead to efforts by researchers to verify the dynamics of a pop- ulation and draw attention to the conservation needs of the species. Ó 2011 Elsevier Ltd. All rights reserved. 1. Introduction Climate change is already having a notable impact on ecosystems throughout the world (Parmesan, 2006; Rosenzweig et al., 2008; Vis- ser and Both, 2005). One of the most sensitive indicators of climate change is the earlier phenology of spring active species (Both et al., 2010; Gordo and Sanz, 2010; Van Buskirk et al., 2009). Plants are flowering earlier in the spring (Cleland et al., 2007; Primack et al., 2004), migratory birds are arriving earlier (Cotton, 2003; Sparks et al., 2005), and many animals are emerging earlier (Diamond et al., 2011; Parmesan, 2007). These earlier patterns of activity are of- ten strongly correlated with temperature in the late winter and spring, with earlier activity associated with warmer temperatures. Analyses show that the earlier activity over time is due to the overall warming trends that species are experiencing (Amano et al., 2010; Miller-Rushing and Primack, 2008; Parmesan and Yohe, 2003). In addition to these overall patterns, there are some striking exceptions. There are notable cases in which species are showing later phenologies in the spring despite warming temperatures (Doi, 2008; Gordo et al., 2005). In one well-documented case from Massachusetts, USA the first arrivals of certain bird species in the spring are getting later over time (Miller-Rushing et al., 2008). The later arrival in this case is due to a declining population size. With a declining population size, the range of arrival dates be- comes smaller over time, with both a later first arrival and an ear- lier last arrival over time. The challenges of using first arrival data in climate change research are well known, given that population size can affect the observation of first arrival (Sparks et al., 2001; Lehikoinen and Sparks, 2010). However, first arrival dates are often the only data available on phenology. In Japan and South Korea, a recent study documents a wide- spread later spring phenology of certain bird, insect, and an amphibian species at numerous sites across both countries (Pri- mack et al., 2009). A declining population size is considered to be a likely explanation, but only limited information from one site is available on changing population sizes of Korean barn swallows (Hirundo rustica)(Lee, 2009). This species is known to be declining in other parts of its range (Møller, 1989), although in Denmark the decline is associated with earlier arrival (Møller, 2008). It is not clear if changing population size is capable of causing such large shifts in spring phenology for these species. The barn 0006-3207/$ - see front matter Ó 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.biocon.2011.05.009 ⇑ Corresponding author. Tel.: +82 2 3277 3545; fax: +82 2 3277 3275. E-mail address: lsd@ewha.ac.kr (S.-D. Lee). Biological Conservation 144 (2011) 2182–2187 Contents lists available at ScienceDirect Biological Conservation journal homepage: www.elsevier.com/locate/biocon