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Ornithol. Sci. 15(2): 171-179

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Ornithol. Sci. 15(2): 171-179 Ornithol Sci 15: 171 – 179 (2016) ORIGINAL ARTICLE Dietary shift of White-cheeked Starlings Spodiopsar cineraceus living in Korean village groves around rice paddy elds Sungbae JOO1,3, Jiwon KIM2, Chan-Ryul PARK2 and Sangkyu PARK3,# 1 Division of Basic Research, National Institute of Ecology, Seocheon, 33657, South Korea 2 Division of Forest Ecology, National Institute of Forest Science, Seoul, 02455, South Korea 3 Department of Biological Science, Ajou University, Suwon, 16499, South Korea ORNITHOLOGICAL Abstract We investigated the feeding preferences of the White-cheeked Starling Spodiopsar cineraceus in Korean village groves during the breeding season by means SCIENCE of a fecal dietary analysis using a non-invasive molecular approach. A total of 529 © The Ornithological Society fecal samples were collected from four different study sites, 113 of them (21.4% of of Japan 2016 all fecal samples) were identified as those of S. cineraceus. Analysis showed that the starling’s diet mostly consisted of animal matter (64.5%), but also contained veg- etable matter (32.7%). Terrestrial prey, such as insects and spiders, constituted the largest proportion (65.2%) of species in the diet, although aquatic organisms (26.1%) were also important. Most of the seeds detected in feces were of mulberries, with detection rates rising to 68.1% by the end of May and remaining high until mid-June. Our results suggest that higher water levels in paddy fields due to irrigation could potentially act as an impediment to bird feeding, particularly for small birds such as S. cineraceus and induce a dietary shift to terrestrial organisms from aquatic organisms. In addition, we suggest that human agricultural activities may influence the feeding activities of small bird species such as S. cineraceus in an agricultural ecosystem. Key words Agricultural ecosystem, Dietary analysis, Feces, Korean village grove, maeulsoop, Spodiopsar cineraceus, White-cheeked Starling Conserving biodiversity is one of the most impor- rural landscape. From an ecological perspective, tant issues worldwide. Traditional cultivation regimes maeulsoop play an important role in providing hab- in agricultural ecosystems enhance biodiversity in itat for local wildlife. For example, various birds, many areas (Balmford et al. 2001; Hughes et al. 2002; especially cavity nesters, select trees in maeulsoop Luetz & Bastein 2002). In particular, rice paddies as as breeding sites (Park et al. 2006). In addition, agricultural ecosystems are recognized as important maeulsoop can serve as habitat corridors or stepping wetland systems and serve as biodiversity nurser- stones, increasing landscape connectivity in land- ies (Kim et al. 2011). The importance of rice paddy scapes fragmented by human activities (Lee et al. fields as agricultural wetlands was formally empha- 2007). Because landscape connectivity is such a cru- sized at the 10th Ramsar Convention in Changwon, cial aspect of maintaining biodiversity, some studies Korea (Kim et al. 2011). have focused on their ecological roles in terms of Traditionally in Korea, village forests and groves landscape ecology (Turner 1989; Jordán et al. 2003; were created and conserved in order to compensate Koh 2011). However, few studies have been con- topographically weak areas, these important habi- ducted on the trophic relationships of birds living in tats are known locally as Maeulsoop (pronounced maeulsoop (Park & Lee 2010). má-ùl-soop) (Lee et al. 2007). Maeulsoop range in The White-cheeked Starling Spodiopsar cinera- size from isolated old trees to groves of various tree ceus (hereafter referred to as starling (s)) is a suitable types (coniferous, deciduous, mixed forest) and are avian study species for facilitating an understanding closely associated with paddy fields in the Korean of trophic relationships in an agricultural landscape. Starlings breed from early March to July, but particu- (Received 23 June 2015; Accepted 5 April 2016) larly during April and May in Korea. Many starlings # Corresponding author, E-mail: [email protected] nest in large trees in maeulsoop and use two different 171 S. JOO et al. habitats (forest and agricultural land) in which to for- very short period in our study sites. We prepared 24 age during their breeding season (Park et al. 2006). m2 (3.4×7 m) fecal collection traps using recycled During this same period, farmers irrigate their paddy polyester banners in order to collect fecal samples fields for rice transplantation. Such agricultural activ- without contamination from soil. The traps were set ities affect avian foraging and and may influence the beneath starling nests (n=3 in WGS, n=2 in JJ, n=1 foraging preferences of starlings (Park et al. 2006). in YD and n=2 in WB) and left in place overnight Therefore, monitoring the diet of starlings utilizing during the sampling periods. Fecal collection traps maeulsoop is important in understanding the impact were also installed beneath starling roosts. Fecal of agricultural activities on birds. samples were collected from the traps in the early Advances in molecular analysis have allowed morning, thus all had been excreted during the previ- the identification of dietary components retrieved ous 24 hr. Fecal samples were placed in 2 ml Eppen- from stomach contents or feces with great accuracy dorf tubes and frozen in liquid nitrogen in the field (Deagle et al. 2010). Furthermore, the construction then transported to the laboratory for later analysis. of barcode libraries has helped in the identification The samples were stored at −80°C until extraction. of species based on very small samples including those of blood, muscle, and feathers (Yang et al. 2) DNA preparation, polymerase chain reaction 2010; Waugh et al. 2011). Especially, the use of non- (PCR) amplification, and sequencing invasive sampling, such as the use of feces, avoids Genomic DNA was extracted from feces using any ethical problems arising from previous method- the QIAamp DNA Stool Mini Kit (Qiagen, Valencia, ologies (such as stomach content analysis after kill- CA, USA) according to the manufacturer’s protocol, ing and dissecting, the use of neck-collars, or crop except for the lysis step. We added one or two 5 or stomach flushing) (Miller & McEwen 1995; Hull mm stainless steel beads (Qiagen) to allow sufficient 1999; Exnerova et al. 2003; Moorman et al. 2007). homogenization to occur during the lysis step and We investigated the feeding preferences of White- mixed by vortexing for 1 min or shaking using a cheeked Starlings inhabiting Korean village groves Mixer Mill (Retsch, Haan, Germany) at 20 Hz for during the breeding season, and identified their 1 min. To identify White-cheeked Starling feces, dietary components by means of a non-invasive, PCR amplifications were carried out using a bird- molecular examination of their feces. In addition, we specific primer pair (K_Bird_F1 & R1) targeting the describe the relationship between human agricultural mitochondrial cytochrome c oxidase subunit I (COI) activities and the starling’s diet shift. region (Joo & Park 2012). The region amplified by the newly designed primer pair had a length of MATERIALS AND METHODS approximately 226 bp and was located in the middle of the full-length COI barcoding region. For dietary 1) Study site and sample collection analysis from feces, we used a universal primer, Our study sites were located around Mt. Mai in Uni_Minibar_F1 & R1, designed for biodiversity Jinan, in the middle part of South Korea (35°47′30″ analysis of eukaryotes after identifying starling feces N, 127°25′49″ E). Based on previous research (Joo (Meusnier et al. 2008). In each PCR amplification, 1 & Park 2012), we selected four different maeul- µl of extracted DNA was added to 24 µl of the ampli- soop as study sites: Wongusin (WGS), Jeungjwa fication mixture, giving final concentrations of 1×Ex (JJ), Yundong (YD) and Wonbanwol (WB), as they Taq Buffer, 1.5 mM of MgCl2, 10 mM of dNTP mix, support many starlings. The study sites are mostly 0.2 µM of each primer, 0.1 M of BSA, and 1 U of more than two kilometers apart, ensuring statistical Ex Taq DNA polymerase (Takara, Shiga, Japan), in independence among the study sites. Fecal samples a final volume of 25 µl. PCR conditions were as fol- were collected bi-weekly during the starling breed- lows: an initial denaturation at 95°C for 2 min, five ing season from May to early July 2012. During cycles of denaturation at 95°C for 1 min; annealing the first investigation, May 3–5, none of the paddy at 46°C for 1 min; elongation at 72°C for 30 s, 45 fields at each site had been flooded. However, before cycles of denaturation at 95°C for 1 min; anneal- the second investigation, May 16–18, most paddy ing at 53°C for 1 min; elongation at 72°C for 30 s, fields flooded for rice transplantation and thereafter and a final extension step at 72°C for 5 min. After retained as temporary wetlands until the end of the the reactions, the amplified PCR products were puri- starling breeding season. Irrigation occurred during a fied using an ExpinTM Gel SV Kit (GeneAll, Seoul, 172 Dietary shift of White-cheeked Starlings in village groves Korea). The purified PCR products were inserted numbers of samples were collected from mid-May to into the pGEM®-T Easy Vector, according to the mid- June at most sites. The highest number of fecal manufacturer’s protocol (Promega, Madison, WI, samples was collected at JJ in early May. Species USA) and transformed into DH5α chemically com- identification based on a molecular approach indi- petent cells. The cells were plated in Luria-Bertani cated that 113 of the 529 samples (21.4% of all fecal agar+ampicillin medium with 40 μl X-gal solution samples) were from starlings (Fig. 1). The number of (2% w/v) for screening. After cloning, three to five starling feces per trap increased at most study sites white colonies were selected and amplified by colony until the end of May then declined.
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