Ornithol Sci 15: 171 – 179 (2016)

ORIGINAL ARTICLE Dietary shift of White-cheeked 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 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 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 feeding, particularly for small 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,

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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. Three fecal sam- PCR with the M13F&M13R primer. The PCR condi- ples were lost during analysis thus the total number tions were as follows: an initial denaturation at 95°C of samples available for further analysis was 110. for 10 min, 35 cycles of denaturation at 94°C for 30 s; annealing at 55°C for 30 s; elongation at 72°C for 2) Prevalence of animal and vegetable diet in feces 1 min; and a final extension step at 72°C for 7 min. Dietary analyses were conducted on starling feces After the reactions, the amplified PCR products were identified by morphological and molecular methods. purified using an ExpinTM PCR SV Kit (GeneAll, Seeds in feces were identified by morphological cri- Seoul, Korea). Sequencing was conducted by a com- teria based on Lee et al. (2009). Animal matter was mercial sequencing service company (Macrogen, significantly more prevalent (71 of 110 samples; Seoul, Korea). Each sequence obtained was identi- 64.5%) in fecal samples than vegetable matter (36 of fied by BLASTN analysis in the GenBank database 110; 32.7%) during the entire period. Vegetable mat- and the BOLD-identification system (IDS) online ter was either not detected, or only detected at low workbench provided by the BOLD website (www. rates prior to mid-May, but increased to 68.1% by boldsystems.org) (Ratnasingham & Hebert 2007). the end of May and remained high until mid–June, whereas the detection rate of animal matter in the 3) Landscape analysis diet was high (>58.1%) throughout the entire study To determine the relationship between land-cover period (Fig. 2). Most seeds detected in feces were availability and starling feeding patterns, the percent- identified as mulberries. ages of relative area according to land-use type were calculated from four different study sites in the land- 3) Classification of animal diet by habitat scape sector within a 500 m radius. Feare (1984) Based on a BLASTN analysis, the animal matter explained that Common Starling Sturnus vulgaris identified in starling feces was categorized by habi- feeding nestlings mostly forage in boundary habitats tat into three types: terrestrial, aquatic and unclassi- within 500 m from their nest. Landscape analyses fied (Table 1, Fig. 3). Of 110 starling fecal samples were conducted using Arc-GIS 9.3 (ESRI), based on identified, 84 (76.4%) were successfully amplified a 2012 aerial photograph (downloaded from http:// by the Uni-Minibar_F1 & R1 primer pair to detect air.ngii.go.kr). the diet species. Excluding sequencing errors, fungal and other bird sequences, 37 different operational 4) Statistical analysis taxonomic units (OTU) were detected and identified The chi-square test was used to test for statistically by BLASTN analysis (Table 1). Nine different prey significant differences in feeding preferences before species (spiders, flies, moths, cicadas, and grasshop- and after irrigation. To reduce the approximation pers) living in terrestrial regions were detected. Most error, Pearson’s chi-square test with Yate’s continuity sequences were identified to genus, or to the family correction was selected. All statistical analyses were level, and were highly similar (>90%) to registered performed with R software (R Core Team 2013). cytochrome c oxidase subunit 1 (COI) sequences in GenBank. Eleven aquatic organisms OTUs were RESULTS detected in starling feces (Table 1). Pond Loach Misgurnus mizolepis, and diving beetle Philaccolus 1) Number of collected fecal samples sp. were identified to the species or genus levels. A total of 529 fecal samples were collected from Rotifers and algae, although not eaten directly by the WGS, JJ, YD and WB study sites during May, starlings, were also detected in feces allowing us June and July (Fig. 1). The largest number (n=53) to assume that starlings had foraged in an aquatic of samples was collected from WB, and the greatest habitat. Two OTUs, identified as Hemiptera sp. and

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Fig. 1. The number of fecal samples collected from four different study sites during the study period. (a) Total number of fecal samples collected, and (b) the number of samples identified as from Spodiopsar cineraceus. Samples were col- lected on the first day of the sampling periods. JJ, Jeungjwa; YD, Yundong; WGS, Wongusin; WB, Wonbanwol.

Fig. 2. Temporal variation in starling feeding preferences, shown as detection rates in feces on different sampling dates.

Goera sp., could not be assigned to categories as 65.2%, of the total number of species detected in they could only be identified to the Order level and the diet, whereas aquatic organisms accounted for because they exhibit habitat differences between only 26.1%. Aquatic organisms were detected at their larvae and adults. Based on the habitat categories, highest rate, 75%, in early May, but thereafter their terrestrial species comprised the largest proportion, detection rate decreased, whereas terrestrial organ-

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Table 1. List of 37 different operational taxonomic units detected from S. cineraceus feces. All sequences are grouped by habitat.

Sample BLASTN results ID Description Identities Gap Accession Terrestrial 1 Adoretus tenuimaculatus 126/127 (99%) 0/127 (0%) KC510117 2 Alulatettix qinlingensis 125/126 (99%) 0/126 (0%) EU414805 3 Arctosa kwangreungensis 114/126 (90%) 0/126 (0%) JN817181 4 Delia platura 127/127 (100%) 0/127 (0%) JX438027 5 Dichomeris punctipennella 101/127 (80%) 0/127 (0%) GU096435 6 Diptera sp. 119/127 (94%) 0/127 (0%) JQ344933 7 Dolomedes sulfureus 125/127 (98%) 0/127 (0%) JN817191 8 Eristalis arbustorum 126/127 (99%) 0/127 (0%) JN991982 9 Evarcha coreana 119/127 (94%) 0/127 (0%) JN817257 10 Gonodonta sp. 105/123 (85%) 0/123 (0%) JQ528276 11 Haloniscus sp. 106/127 (83%) 0/127 (0%) EU364609 12 Hebecnema fumosa 119/127 (94%) 0/127 (0%) FJ025616 13 Hydrotaea ignava 127/127 (100%) 0/127 (0%) JX438036 14 Hyla japonica 127/127 (100%) 0/127 (0%) HM439188 15 Macropsis notata 114/127 (90%) 0/127 (0%) JQ755806 16 Metaphire sp. 111/111 (100%) 0/111 (0%) AB543234 17 Micaria dives 116/127 (91%) 0/127 (0%) JN817228 18 Phoridae sp. 117/125 (94%) 0/125 (0%) HQ979184 19 Platypleura capensis 113/125 (90%) 0/125 (0%) FJ169015 20 Psithyristria sp. 114/125 (91%) 0/125 (0%) GQ527112 21 Scarabaeidae sp. 111/123 (90%) 0/123 (0%) KC136007 22 Tipula mutila 120/126 (95%) 0/126 (0%) JQ912042 23 Uroobovella australiensis 111/126 (88%) 0/126 (0%) JN992210 24 Xysticus concretus 126/126 (100%) 0/126 (0%) JN817252 Aquatic 25 Acanthamoeba castellanii 122/131 (93%) 0/131 (0%) U12386 26 Adineta gracilis 115/126 (91%) 0/126 (0%) EF173198 27 Adineta vaga 117/125 (94%) 0/125 (0%) GQ465621 28 Clytia sp. 100/132 (76%) 6/132 (4%) JQ716211 29 Clytia sp. 101/132 (77%) 6/132 (4%) JQ716205 30 Coccomyxa sp. 129/133 (97%) 0/133 (0%) HQ874522 31 Misgurnus mizolepis 127/127 (100%) 0/127 (0%) FJ197700 32 Nebela tincta 99/131 (76%) 4/131 (3%) JX682594 33 Philaccolus sp. 96/107 (90%) 0/107 (0%) FJ819699 34 Plocamium sp. 107/129 (83%) 0/129 (0%) JF271639 35 Pseudopedinella elastica 105/132 (80%) 0/132 (0%) FJ030896 Unclassified 36 Goera sp. 116/127 (91%) 0/127 (0%) JQ907723 37 Hemiptera sp. 117/127 (92%) 0/127 (0%) HQ978865 isms increased to 100% and retained a higher rate of DISCUSSION detection in feces than did aquatic organisms (Fig. 3). A chi-square test showed significant differences The primary goal of this study was to investigate in starling feeding preferences before and after irri- the feeding preferences of White-cheeked Starlings gation (χ2=39.9, 50.2, 72.0 and 116.8, P <0.001 in inhabiting Korean village groves during the breeding all tests). season. Our results showed that the foraging prefer-

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Fig. 3. Animal species found in fecal samples during the study period classified according to their habitat. Feeding preferences are represented as a percentage of the detection rate in feces. The chi-square test was used to test differences in feeding preferences before and after irrigation. Because paddy fields irrigation around maeulsoop finished before May 16 at all study sites, we considered the first sampling period as before irrigation. *** P < 0.001. ences of starlings changed during the breeding sea- explained by an increase in the availability of mulber- son; they preferred animal matter over vegetable mat- ries in the forests and groves around the study sites. ter during the early phase of the breeding period, but However, it is possible that adult starlings prefer to then consumed both animal and vegetable matter dur- forage for animal matter during egg laying, molting, ing the later part of the breeding season. Terrestrial and chick rearing phases. Adult Lark Bunting, for organisms, such as insects, earthworms and spiders, example, select more acridids, dipterans, odonates, represented the largest proportion (65.2%) of the diet, and spiders for their offspring than for themselves compared with aquatic organisms at just 26.1%. The (Orians 1966; Wiens 1973). We assume that the pref- proportion of aquatic organisms in the diet declined erence of starlings for animal matter might help with until the end of May after irrigation, whereas the protein uptake, which is essential for maturation and detection rate of terrestrial organisms increased to growth of nestlings during the breeding season. 100%. We considered the possibility that irrigation Agricultural activities such as irrigation may affect might act as an impediment to starling feeding and avian foraging, particularly of those species that use may have induced their dietary shift from aquatic to paddy fields as feeding sites. Generally, paddy fields terrestrial organisms. are temporary wetlands during the period when rice The dietary shift detected in the White-cheeked seedlings are transplanted. During that term, paddy Starling may have been related to temporal varia- fields are interconnected with irrigation ponds and tion in food availability and to varying nutritional rivers by means of extensive canal networks and pro- needs (e.g., during egg laying and raising chicks). vide substitute habitats for a wide range of wetland A wide range of omnivorous bird species have very species such as fish and aquatic insects (Washitani different diets during their spring/summer breeding 2007). In our study area, most paddy fields were season and autumn/winter; for example Wiens (1973) flooded for transplantation in early May, which showed that both Horned Lark Eremophila alpestris increased the proportion of paddy fields as tempo- and Lark Bunting Calamospiza melanocorys fed pri- rary aquatic areas to 26.6% of the total area (Table marily on grasshoppers, weevils, and ants during the 2 and Figs. 4, 5). In addition, previous studies have breeding season, but switched to a diet dominated by shown that increases in aquatic insects after irriga- Compositae, Amaranthus spp., or grass seeds during tion and until after summer occur naturally because fall and winter. In our study of the White-cheeked paddy fields become seasonal wetlands (Saijo 2001; Starling, we found that starlings took both vegetable Bambaradeniya & Amerasinghe 2003; Yamazaki et and animal matter while breeding, but their propor- al. 2004). However, our results showed that despite tions in the diet varied considerably. The increase in increases in the abundance of potential prey in paddy the proportion of vegetable matter in the diet can be fields, the proportion of aquatic organisms taken by

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Table 2. Land-use composition of the four different study sites in landscape sectors within a 500 m radius.

Area (%) Land use type JJ YD WGS WB Average Terrestrial area Rice paddy field 29.7 20.7 25.2 17.1 23.2 Field (Other crops) 10.9 22.5 8.8 25.6 17.0 Ginseng (Plantation) 2.0 18.9 6.1 3.0 7.5 Forest and groves 24.0 7.2 41.7 16.6 22.4 Grassland 17.0 10.7 8.3 5.0 10.3 Total 83.8 80.1 90.2 67.2 80.3 Aquatic area River 10.1 1.7 0.7 1.1 3.4 Others Residential, traffic areas and so on 6.2 18.2 9.1 31.7 16.3

Fig. 4. The change in rice paddy fields to aquatic areas following flooding of the four different study sites in landscape sectors within a 500 m radius. The two land-cover maps for each maeulsoop represent before and after paddy field irrigation. starlings decreased during May, whereas the pro- feeding their nestlings mostly use boundary habitats portion of terrestrial organisms taken increased to for foraging within 500 m of their nests and paddy 100% (Fig. 3). Rainwater puddles can be important fields are a major (23.2% on average) land-use type habitats for aquatic organisms and small omnivorous in the total land-use composition within our study birds such as starlings (mean body size, 24 cm) can area. In addition, most terrestrial prey detected in this also access paddy fields prior to irrigation (Lee et al. study were spiders, flies, moths, cicadas, and grass- 2000). However, rising water levels in paddy fields hoppers. It is difficult to determine whether these resulting from irrigation may interfere with avian for- species increased rapidly during the starling breeding aging and act as an impediment to feeding for small season; therefore, we have assumed that the dietary birds such as the starlings. White-cheeked Starlings shift we observed resulted from changes in the paddy

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Fig. 5. Comparison of rice paddy fields before (top) and after (bottom) irrigation.

field environment caused by irrigation. ACKNOWLEDGMENTS The reproductive success of avian nestlings may be related to the availability of potential prey pro- This research was supported by the Basic Science Research vided by adults (Martine 1995), and parent birds Program (no. 2009-0073291 and 2009-0068335) of the may fly longer distances to utilize suitable habitats National Research Foundation of Korea and the “Coopera- tive Research Program for Agriculture Science & Technology when nearby landscapes are insufficient for forag- Development (Project No. PJ00919828)” Rural Development ing (Frey-Roos et al. 1995; Bruun & Smith 2003). Administration, Republic of Korea. Although flooded paddy fields may support tempo- rary increases in prey abundance such as aquatic REFERENCES insects and fishes, it may be difficult for starlings to use irrigated rice fields as foraging habitats because Balmford A, Moore JL, Brooks T, Burgess N, Hansen of their higher water levels. This may result in par- LA, Williams P & Rahbek C (2001) Conservation ents increasing their flight distances and this raising conflicts across Africa. Science 291: 2616–2619. doi: their energetic costs (Bruun & Smith 2003). 10.1126/science.291.5513.2616. Understanding the trophic relationships among liv- Bambaradeniya CNB & Amerasinghe FP (2003) Biodi- ing organisms is essential when attempting to explain versity associated with the rice field agroecosystem the ecological importance of the maeulsoop-related in Asian countries: A brief review. Working Paper 63. agricultural landscape. Our results show that White- International Water Management Institute, Colombo. Bruun M & Smith HG (2003) Landscape composition cheeked Starlings living in maeulsoop undergo a affects habitat use and foraging flight distances in dietary shift during the breeding season. Human agri- breeding European starlings. Biol Conserv 114: 179– cultural activities may significantly affect the forag- 187. doi: 0.1016/S0006-3207 (03)00021-1. ing behavior of small bird species such as starlings in Deagle BE, Chiaradia A, McInnes J & Jarman SN agricultural ecosystems. To clarify how such agricul- (2010) Pyrosequencing faecal DNA to determine diet tural activities affect avian foraging, it is necessary of little penguins: Is what goes in what comes out? to investigate changes in the feeding preferences of Conserv Genet 11: 2039–2048. doi: 10.1007/s10592- other bird species using paddies as feeding sites. In 010-0096-6. addition, applying our molecular strategy using avian Exnerova A, Stys P, Kristin A, Volf O & Pudil M (2003) feces is a convenient and non-invasive way to con- Birds as predators of true bugs (Heteroptera) in dif- duct avian dietary analyses and to help understand ferent habitats. Biologia 58: 253–264. avian trophic relationships. Feare CJ (1984) The Starling. Oxford University Press, Oxford. Frey-Roos F, Brodmann PA & Reyer H (1995) Rela-

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