Migration phenology determines niche use of East Asian buntings (Emberizidae) during stopover

Migration phenology determines niche use of East Asian buntings (Emberizidae) during stopover Stopover niche utilization of birds during migration has not gained much attention so far, since the majority of the studies focuses on breeding or wintering areas. However, stopover sites are crucial for migratory birds. They are often used by a multitude of species, which could lead to increased competition. In this work, we investigated niche use of 8 migratory and closely related Emberiza bunting species at a stopover site in Far East Russia, situated on the poorly studied East Asian fly- way. We used bird ringing data to evaluate morphological similarity as well as niche overlap on the trophic, spatial, and temporal dimension. Bill morphology was used as a proxy for their trophic niche. We were able to prove that a majority of the species occupies well-defined stopover niches on at least one of the dimensions. Niche breadth and niche overlap differ between spring and autumn season with higher overlap found during spring. Morphological differences are mostly related to overall size and wing pointedness. The temporal dimension is most important for segre- gation among the studied species. Furthermore, all species seem to exhibit a rather strict and con- sistent phenological pattern. Their occurrence at the study site is highly correlated with their geo- graphic origin and the length of their migration route. We assume that buntings are able to use available resources opportunistically during stopover, while trying to follow a precise schedule in order to avoid competition and to ensure individual fitness. Key words: bird migration, Emberiza, habitat use, non-breeding, phenology, stopover. Introduction Those niches are shaped by competition with other species, resulting in segregation or resource partitioning (Pianka 1981). The niche con- Migratory flights are energetically costly (Wikelski et al. 2003). cept itself dates back to Grinnel (1917) and is now widely applied in Consequently, many migratory birds do need to replenish energy stores during migration at intermittent stopover sites (Klaassen 1996). bioecology and sociology (Popielarz and Neal 2007). Segregation can At such stopover sites, migrants often share space with other con- and be found on different dimensions (Pianka 1981): there can be tempo- heterospecific birds. How different species of stopover migrants share ral niches (for example, Carothers and Jaksic 1984; Kronfeld-Schor space has rarely been studied in detail (Kober and Bairlein 2009) and Dayan 2003; Castro-Arellano and Lacher 2009; Hayward and which is in particular so for Asian migrants. Ecological niche segrega- Slotow 2009), spatial niches (Hagen et al. 2007), trophic niches tion is a way different species may share a stopover site. (Dammhahn et al. 2015), acoustic niches (Henry and Wells 2010), or In general, an ecological niche is usually defined as the range in niches defined by light intensity (Gerrish et al. 2009). In many cases, a which a species can have positive population growth (Chase 2011). combination of different dimensions was found to be relevant (Pianka V C The Author(s) (2018). Published by Oxford University Press. 1 This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zoy016/4842010 by Ed 'DeepDyve' Gillespie user on 13 July 2018 2 Current Zoology, 2018, Vol. 0, No. 0 1973; Piet et al. 1999; Albrecht and Gotelli 2001; Gilbert et al. 2008; Table 1. Study species and number of trapped birds (including retraps), 2011–2016 (n ¼ 7642) Dennis and Hellberg 2010). The more species are included, the more dimensions have to be considered, on which species might segregate: English name Scientific name Number of trapped birds if species are similar on 1 dimension, dissimilarity on another dimen- sion should be implied (Schoener 1974). However, even species inhab- Spring Autumn Other iting an identical niche can coexist in highly structured food webs Yellow-breasted Bunting Emberiza aureola 119 50 (Leibold and McPeek 2006). This can be explained by stochastic Yellow-browed Bunting E. chrysophris 63 145 187 effects and might be driven by dispersal instead of competition—the Meadow Bunting E. cioides 20 0 basic assumption of the “neutral theory” (Leibold 2008). The debate Yellow-throated Bunting E. elegans 174 73 101 remains open whether niche partitioning, neutrality, or a synthesis of Chestnut-eared Bunting E. fucata 00 32 both is the key for species diversity (Mouillot 2007; Leibold 2008; Pine Bunting E. leucocephalos 119 24 Vergnon et al. 2009). In recent studies, both theories were included in Pallas’s Reed Bunting E. pallasi 53 181 647 Little Bunting E. pusilla 96 288 753 models explaining species diversity (Haegeman and Loreau 2011; Ai Rustic Bunting E. rustica 103 210 543 et al. 2013; Munoz et al. 2014). Chestnut Bunting E. rutila 663 67 Niches are highly dynamic on temporal and spatial scales, and can Common Reed Bunting E. schoeniclus 15 21 change between seasons—which might be especially true for most Black-faced Bunting E. spodocephala 578 959 1985 migratory birds, covering thousands of kilometres between breeding Tristram’s Bunting E. tristrami 93 15 grounds, stopover sites, and wintering areas twice a year (Bairlein Ochre-rumped Bunting E. yessoensis 4 51 108 et al. 2012). Niche utilization and segregation during breeding season Lapland Bunting Calcarius 00 1 is well described for many species of birds (e.g. Kosin ~ski and Winiecki lapponicus 2004; Kaboli et al. 2007; Laughlin et al. 2013). However, information Snow Bunting Plectrophenax 00 1 is scarce for stopover sites used during the long period of migration. nivalis Explanations for the coexistence of migrants and residents in those Individuals trapped using standard nets during spring (April–June 2013, areas are largely lacking (Salewski and Jones 2006), but see Bensusan 2015, 2016) and autumn (August–October 2013–2015) migration as well as et al. (2011). It has been shown that many migrants “track” their birds trapped during breeding season or with non-standard nets (“Other”) are niche, instead of switching it during the non-breeding season (Joseph shown separately. and Stockwell 2000; Nakazawa et al. 2004; Papes et al. 2012). On the other hand, changes in niche utilization between seasons have annual cycle will be crucial for their conservation (Newton 2004; been shown for migratory Sylvia warblers (Laube et al. 2015). Bairlein 2016). In this study, we analyze niche use and niche segre- Overlapping niches have been found during times of low food supply gation during stopover among a group of closely related bunting (Je ˛ drzejewski et al. 1989; Hasui et al. 2009) or superabundance of high quality food (Choi et al. 2017). Niche segregation at stopover species. In doing so, we want to prove the hypotheses listed below: sites can also be hampered under poor food conditions, when individ- 1. There are well-defined stopover niches—all species differ on at uals have to utilize a broader range of available niches (Kober and least 1 niche dimension. Bairlein 2009). In Uria murres, it was also found that sympatric spe- 2. Niche utilization and overlap differs between spring and autumn cies “widened” their niches during non-breeding season to avoid com- migration. petition (McFarlane Tranquilla et al. 2015). 3. The temporal dimension is the most important, since trophic Moreover, niche segregation may vary with season. Spring and spatial niches can be widened during stopover. migration of many bird species often differs from their autumn jour- 4. The occurrence of a species at the stopover site is linked to its neys and shows higher migration speed and a lower number of stop- geographic origin (latitude). overs (Schmaljohann et al. 2012; Nilsson et al. 2013). Also the time window, in which nocturnal migrants initiate their flights, is smaller during spring migration (Bolshakov et al. 2007; Schmaljohann et al. Materials and Methods 2011). These restrictions might also cause differences in niche use Data were collected within the Amur Bird Project, a standardized and niche overlap between seasons. bird-ringing scheme at Muraviovka Park (49 5508, 27 N, 127 4019, Past studies on niche use outside breeding season focused on 93 E) in Far East Russia (Heim et al. 2012; Heim and Smirenski 2013). waders (Davis and Smith 2001; Burger et al. 2007; Jing et al. 2007; Such ringing data were proven to be suitable for characterization of Kober and Bairlein 2009; Bocher et al. 2014) as well as penguins migration phenology (Knudsen et al. 2007). Birds were trapped during (Wilson 2010; Hinke et al. 2015) and seabirds (Young et al. 2010; spring (April–June) and autumn (August–October) migration 2011– Quillfeldt et al. 2013; McFarlane Tranquilla et al. 2015; Orben 2016. Additional individuals were ringed during breeding season et al. 2015; Quillfeldt et al. 2015), whereas studies on songbirds are 2013–2016. A total of 7,642 trapped individuals of 16 species were scarce (Bairlein 1983, 1992; Martinez-Meyer et al. 2004; Laube available for analysis (Table 1). All statistical analysis were carried out et al. 2015) and are virtually absent for the East Asian flyway (Yong using the program R version 3.2.4 (R Core Team 2016). et al. 2015). This flyway, however, holds the highest diversity of migratory birds, including numerous threatened species (Yong et al. Morphology 2015). The group of buntings (Emberizidae) has currently gained East Asian buntings show sexual size dimorphism, with males being global conservation interest caused by catastrophic declines of sev- bigger, longer winged and longer tailed (Nam et al. 2011). eral species of the genus Emberiza in Europe and Asia (Menz and Arlettaz 2012; Kamp et al. 2015; Edenius et al. 2017). Far East Therefore, 15 males and 15 females each were randomly selected for Russia is the diversity hotspot of this threatened genus (Pa ¨ ckert et al. each study species. To avoid ringer-specific differences, only individ- 2015). Knowledge of their specific needs and niches throughout the uals which have been measured by the first author were considered, Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zoy016/4842010 by Ed 'DeepDyve' Gillespie user on 13 July 2018 Heim et al.  Bunting stopover niche use 3 with few exceptions for single Chestnut Buntings Emberiza rutila, seasons in the relative abundance of the species and the habitats Ochre-rumped Buntings E. yessoensis, and Little Buntings E. pusilla. used. Null hypothesis (random distribution) was rejected if All measurements were taken as proposed by Eck et al. (2011): P< 0.05. Habitat use was compared between species with a cluster Wing length (Wmax), Wing pointedness (Kipp-Index), Tail length, analysis (Ward method based on Euclidean distances). Bill length (Bsk), Bill width (Bwp), and Bill depth (Bp). Birds were In 2013, an extreme flood event occurred, covering the flood- weighed with a precision to 0.1 g using an electronic weight plain completely with water for the first time since 30 years (Ecotone Pesola PPS200). As age determination was not always pos- (Sokolova 2015). Therefore, the conditions at the nets in the wet- sible, both adults and first-year birds were included in this study. A lands changed drastically, and mist-net sites in Habitat type B were principal component analysis (PCA) was used to investigate which completely drowned. Habitat use (abundance of trapped birds per morphological features contribute most to the interspecific variabil- habitat type) differed significantly between the flood year and the ity. All data were standardized using a log transformation, to mini- years without flood (v ¼ 159.89, df ¼ 5, P< 0.001). Therefore, we mize the effects of different units (Shao et al. 2016). In our first excluded the year 2013 for the analysis of habitat use. PCA, data were not size corrected to preserve the valuable informa- We adopted the approach Bairlein (1981) used to compute niche breadth, since we intend to describe the species-specific relative uti- tion of body size, which could act as an important factor for species segregation (Alatalo et al. 1986; Shao et al. 2016). In our second lization of the resources at the study site. For the analysis of niche PCA, data were size corrected by dividing all measures of length by overlap, we used the R package spaa (Zhang 2016) with the widely the cube root of lean body mass to analyze differences in shape used niche overlap measure based on Pianka (1973). Niche overlap (Winkler and Leisler 1992). Bill morphology was used as a proxy in phenology was computed based on the proportion of birds for the size of the feeding structure—which is usually correlated to trapped per calendar week during spring and autumn migration. We food characteristics (Schoener 1965, 1974). Similarity among spe- used a Pearson’s product moment correlation to investigate the rela- cies was described based on difference in wing, tail, and tarsus tionship between mean migration days during spring and autumn. length as well as bill morphology applying the method of Ricklefs Differences in phenology between years were tested with simple lin- and Cox (1977). We computed an index of overall similarity as well ear models (DayYear). Linear mixed-effects models (LMEs) were as an index of bill similarity accordingly. used to analyze the impact of different variables on migration tim- ing. This analysis was carried out with R package nlme (Pinheiro et al. 2016). The following variables were used to explain the Habitat and phenology dependent variable median migration day for spring and autumn There are known differences in migratory behavior among sexes— each: breeding latitude (southernmost, northernmost), wintering lat- especially during spring migration, when males often migrate ahead itude (southernmost, northernmost) and migration distance (length of the females (Schmaljohann et al. 2016). The occurrence of the so- of migration route calculated as difference between mean breeding called protandrous migration in East Asian buntings was shown by and wintering latitude). Information about distribution of bunting Nam et al. (2011) at a stopover site on the Korean Peninsula, and species was gathered from the BirdLife range maps (BirdLife was also found in Ortolan Bunting E. hortulana along the west end International 2017), see Supplementary Material 2. The application of the Asian continent (Yosef and Tryjanowski 2002). To allow for of LMEs allowed us to include year and species as random factors. inner-specific variation, we included all species where we had a suf- Significant variables were selected with help of “backward stepwise ficient sample size for both females and males in our study. We model selection” (Crawley 2013) using the Likelihood-ratio test included all species in the analysis with a sample size of n> 30 per (P< 0.05) and the Akaike information criterion (AIC)-values. season. For the analysis of habitat use and phenology we included Normal distribution and variance homogeneity of residuals was those periods, during which all nets were opened at exactly the same graphically tested with help of a normal probability plot (Crawley locations for the same time span. This was true for the spring sea- 2013). Goodness-of-fit statistics (R -values) for these models were sons in 2013, 2015, and 2016 from April to June and for the autumn computed with the help of the piecewiseSEM package (Lefcheck season during the years 2013–2015, when trapping was conducted 2015). Furthermore, we tested the differences in overall niche over- from the beginning of August until the end of October. A total of 17 lap regarding habitat use and phenology between spring and autumn nets with lengths of either 6 (n ¼ 4) or 12 m (n ¼ 13) was used. Each season with a Welch Two-sample t-test. Based on the available data, net was assigned to 1 of 6 different types of habitats, which form a we were able to evaluate the existence of stopover niches for 8 spe- gradient from the low wetlands to the forests on the river terrace. cies on 3 dimensions: morphology, space, and time. Habitat type A (reed) consists of reed stands with Phragmites aus- tralis and Carex spec. Habitat type B (willow1) is characterized by low willow thickets (for example, Salix miyabeana) and wet mead- Results ows. Habitat type C (willow2) is situated on the edge of the river Morphology terrace and includes larger willow bushes and trees (e.g. S. pierotii). Habitat type D (deciduous) is situated on the terrace, with poplar Complete morphometric data of 15 males and 15 females each were Populus tremula and bird cherry Prunus padus trees and raspberry available for 8 species (Supplementary Material 2). The results of Rubus idaeus in the understorey. Large Mongolian oak Quercus the PCA are shown in Table 2. When using the original data, the mongolica trees are characteristic for Habitat type E (oak), as well first principal component, explaining 53% of total variance, is nega- as a dense understorey with Artemisia spec. and Lespedeza bicolor. tively correlated with body mass and all other measurements, and A pine plantation with Pinus sylvestris forms Habitat type F (pine). therefore, stands for overall size. The second principal component, Habitats A–C are situated in the lowlands, and Habitats D–F on the explaining 17% of total variance, is positively correlated with tail terrace. The nets were not equally distributed among the habitat and wing length, whereas the third principal component explaining types, for details see Supplementary Material 1. v -tests were used 16% of total variance is positively correlated with wing pointedness. to evaluate whether the trapped buntings are randomly distributed PC1, PC2, and PC3 are depicted in Figure 1. After correcting for among the habitat types and whether there are differences between size, we found that the first and the second principal component are Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zoy016/4842010 by Ed 'DeepDyve' Gillespie user on 13 July 2018 4 Current Zoology, 2018, Vol. 0, No. 0 Figure 1. Principal components 1–3 for morphology of 8 bunting species using original data (upper line) and size-corrected data (lower line). The following spe- cies were included: Yellow-browed Bunting (chr), Yellow-throated Bunting (ele), Pallas’s Reed Bunting (pal), Little Bunting (pus), Rustic Bunting (rus), Chestnut Bunting (rut), Black-faced Bunting (spo) and Ochre-rumped Bunting (yes). correlated with wing length and wing pointedness, respectively, and 2013. This pattern still remains consistent when excluding the explaining 39% and 25% of total variance, whereas the third princi- superabundant Black-faced Bunting (Supplementary Material 4a). pal component is negatively correlated with bill and tarsus length In spring, most buntings were found in the pine plantation (30.4%, explaining 16% of variance. The PCA with the original data Habitat F) and in deciduous trees (22.3%, Habitat D). In autumn, explained more of the morphological variance than the PCA based the majority of the birds were trapped in small willow thickets on the size-corrected data. (40.5%, Habitat B) and oak forest with dense understorey (19.5%, A similarity index was computed for each of the species pairs. Habitat E) —see Supplementary Material 1. Almost all bunting spe- The morphologically most similar species pairs are Pallas’s Reed cies were found in all kind of habitats (Supplementary Material 4b), Bunting and Little Bunting with a similarity index of 0.679, the with exception of the Ochre-rumped Bunting, in which 80% of the most dissimilar pair are Ochre-rumped Bunting and Yellow-browed birds were trapped in Habitat type A (reeds). Nevertheless, all spe- Bunting with a similarity index of 0.004 (Figure 2A, Supplementary cies were neither randomly distributed among the habitat types (v - Material 3). Part of this overall index is the similarity index of bill test, P< 0.001), nor among the total traps per habitat (v -test, morphology. The most similar index values were found for Ochre- P< 0.05). rumped Bunting and Yellow-throated Bunting; the most unlike pair In spring, the 6 studied species can be divided in 3 clusters in are Yellow-browed Bunting and Yellow-throated Bunting terms of their habitat use (Figure 3): (1) Low willow shrubs (pal), (Figure 2B, Supplementary Material 3). (2) species of higher willow shrubs and deciduous forest (ele, pus, rus, spo), and (3) species mainly found in the pine plantation (chr). Habitat In autumn, 8 species can be divided into 4 clusters: (1) reed and wet- Trapped buntings were not equally distributed among all habitats, land species (yes), (2) species of low willow thickets (pal, pus, spo), 2 2 neither in spring (v ¼ 39.588, df ¼ 5, P< 0.001) nor in autumn (v (3) forest species (ele, rus), and (4) species that occur in all habitats ¼ 11.833, df ¼ 5, P ¼ 0.037). Habitat types A–C in the lowlands (chr, rut). were most important in years without flood, while the buntings Habitat use differed significantly between spring and autumn shifted to the habitat types D–E on the terrace in the flood year season (v ¼ 115.25, df ¼ 5, P< 0.001). In spring, 31.8% of all Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zoy016/4842010 by Ed 'DeepDyve' Gillespie user on 13 July 2018 Heim et al.  Bunting stopover niche use 5 Table 2. PCA: Factor loadings of the first 3 principal components based on 9 morphological measurements for 8 bunting species Measurement Original data Size-corrected PC1 PC2 PC3 PC1 PC2 PC3 Wing length (Maximum chord) 0.365 0.362 0.280 0.473 0.315 0.216 th Length of 8 primary 0.346 0.412 0.281 0.481 0.284 0.215 Wing pointedness (Kipp-Index) 0.218 0.135 0.668 0.087 0.609 0.224 Tail length 0.110 0.629 0.400 0.360 0.417 0.211 Tarsus length 0.321 0.059 0.423 0.002 0.409 0.600 Bill length (Bill to skull) 0.340 0.341 0.178 0.289 0.008 0.629 Bill width (behind nostrils) 0.369 0.270 0.117 0.376 0.179 0.227 Bill height (behind nostrils) 0.383 0.295 0.049 0.428 0.276 0.081 Weight (lean body mass) 0.431 0.076 0.100 NA NA NA Proportion of variance 0.545 0.177 0.164 0.391 0.251 0.157 Cumulative proportion of variance 0.545 0.721 0.886 0.391 0.642 0.799 The highest loadings for each component are in bold. AB CD Figure 2. Similarity of 8 bunting species regarding (A) morphology and (B) bill morphology, as well as niche overlap regarding (C) habitat use and (D) phenology. Point size resembles similarity index/niche overlap (range: 0–1). For species abbreviations, see Figure 1. Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zoy016/4842010 by Ed 'DeepDyve' Gillespie user on 13 July 2018 6 Current Zoology, 2018, Vol. 0, No. 0 Figure 3. Cluster analysis based on habitat preferences of bunting species during spring (left) and autumn (right) migration. For species abbreviations, see Figure 1. whereas some Little, Yellow-browed and Black-faced Buntings Table 3. Relative niche breadth of 8 species of buntings regarding habitat use and phenology during spring and autumn migrate until the end of May or even the first days of June. Autumn migration starts at the beginning of August in Chestnut and Ochre- Species Habitat Phenology rumped Buntings, and ends in the second half of October with Pallas’s Reed Bunting being the latest species. The median date of Spring Autumn Spring Autumn their occurrences at the study site is given in Supplementary Material Yellow-browed Bunting chr 22.7 69.8 18.2 42.7 5. Significant differences in phenology between years were found for Yellow-throated Bunting ele 48.7 52.2 38.3 40.7 Yellow-throated Bunting (F ¼ 9.578, R ¼ 0.052, P¼ 0.002) and 1,172 Pallas’s Reed Bunting pal 39.6 27.1 24.1 15.1 Pallas’s Reed Bunting (F ¼ 8.149, R ¼ 0.138, P ¼ 0.006) during 1,51 Little Bunting pus 62.5 46.0 31.1 29.4 spring migration, and for Ochre-rumped Bunting (F ¼5.462, 1,49 Rustic Bunting rus 49.3 49.4 26.5 23.4 R ¼ 0.100, P ¼ 0.024) as well as Pallas’s Reed Bunting Chestnut Bunting rut NA 54.1 NA 44.1 Black-faced Bunting spo 84.5 58.3 44.6 38.0 (F ¼ 16.18, R ¼ 0.083, P< 0.001) during autumn migration. No 1,180 Ochre-rumped Bunting yes NA 14.4 NA 29.7 significant differences in phenology between years were found for the remaining species (Black-faced Bunting, Chestnut Bunting, Little Bunting, Rustic Bunting, and Yellow-browed Bunting). Phenology for buntings were trapped in the lowlands (Habitats A–C), and 68.2% the 5 most common species (n/year> 30) during autumn migrations on the terrace (Habitats D–F). In autumn, it was 61.5% and 36.5%, 2013, 2014, and 2015 is shown in Figure 4B. Occurrence during respectively. This is also true within species: in spring, 41% of all autumn migration is highly correlated with spring phenology Black-faced Buntings are trapped in lowlands and 59% on the ter- (Figure 5). The final LME to explain the median day of migration race, while in autumn 71% were found in the lowlands and 29% on reveals significant the variable northernmost wintering latitude for the terrace. The interspecific differences in habitat use are less pro- spring migration (R ¼ 0.73) with more southern wintering species nounced in spring than in autumn. passing late. In autumn, northernmost breeding latitude and migra- Relative habitat niche breadth differed among species and tion distance combined (R ¼ 0.81, see Supplementary Material 6) 2 2 between seasons (Table 3). Black-faced Buntings utilized a broader explained passage date (R ¼ 0.32 and R ¼ 0.02, respec- marg marg habitat niche during spring than during autumn, whereas Yellow- tively); with northern breeding birds passing late and species travelling browed Buntings occupied a narrow niche during spring and a long distances passing early. broad one in autumn. Ochre-rumped Buntings utilized the narrow- est niche during autumn migration, again highlighting their status as Niche overlap habitat specialists. The mean niche overlap in phenology is significantly higher in spring The niches of the studied species overlapped during both spring than in autumn (t¼3.003, df ¼ 32.623, P ¼ 0.005), which is also and autumn (Figure 2C, Supplementary Material 3). Highest the case for niche overlap in habitat use (t¼3.302, df ¼ 40.491, overlap was found between Black-faced Bunting, Little Bunting, P ¼ 0.002) (Figure 6, Supplementary Material 3). During spring and Pallas’s Reed Bunting, as well as between Rustic Bunting and migration, 6 out of 15 species pairs (40%) show an overlap value in Yellow-throated Bunting. The niches of Chestnut Bunting and phenology of <0.5 (<50% overlap). Thirty-three percent of all spe- Ochre-rumped Bunting during autumn migration showed least cies pairs are well separated regarding bill morphology, and 13% overlap with other species. use differential spatial niches. Sixty-six percent of all species pairs were separated on at least 1 dimension. During autumn migration, Phenology this is true for 80% (24 of 30 species pairs). In autumn, 63% differ There are pronounced differences in the timing of migration among on the temporal dimension, and 37% on the spatial dimension the 8 studied species (Figure 4A). Spring migration begins with (Figure 7). There is a significant correlation between niche breadth Pallas’s Reed Bunting as the earliest species to arrive at the study site, on the spatial and on the temporal dimension (Figure 8). Species Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zoy016/4842010 by Ed 'DeepDyve' Gillespie user on 13 July 2018 Heim et al.  Bunting stopover niche use 7 Figure 4A. Phenology during spring (left) and autumn (right) migration. The height of the box resembles sample size. For species abbreviations, see Figure 1. species situated at the very end of the morphological spectrum, that is, between the smallest species (Ochre-rumped Bunting) and the largest species (Yellow-browed Bunting). This is also true for bill morphology—only the 2 species with the weakest (Yellow-throated Bunting) and the heaviest bill (Yellow- browed Bunting) showed very low similarity. The extreme low value between the latter 2 species seems to be more a methodological bias (highlighting the ends of the spectrum) rather than a real difference. Since bill morphology was used as a proxy for the feeding structure and the tropic niche, it seems likely, that there are no major differen- ces in diet among the studied species. Buntings form mixed-species flocks, and they were often seen feeding together on the same resources at the study site (personal observations). All species are foraging on seed-bearing plants on or close to the ground. According to Byers et al. (1995), all Emberiza buntings switch their diet from invertebrates during the breeding season to a wide range Figure 4B. Inter-annual variability in autumn phenology for the 5 most com- of small seeds during the non-breeding season. In a study by Hasui mon bunting species (n/year> 30). The height of the box resembles sample et al. (2009), niche partitioning among 2 tropical bird species was size. Significant differences between years were only found for Pallas’s Reed Bunting. For species abbreviations, see Figure 1. found only during periods of fruit scarcity. Moore and Yong (1991) found that migrants at stopover sites gained less weight when more birds were around. If food availability is a limiting factor, one would with a broad temporal niche occur in a broad range of habitats, and vice versa. There are pronounced differences between spring and expect high overlap, since migrants are known to use a wide range of available niches under such conditions (Kober and Bairlein 2009). autumn season within some species, irrespective of sample size. All in all, the studied species are in general not very distinct in mor- phology, which is likely caused by their close phylogenetic relation- Discussion ship (all 8 species belong to the same genetic clade, even within the genus Emberiza, Pa ¨ ckert et al. 2015). Morphology Overall size was found to be the most important factor in our PCA, and the size-corrected PCA explained less of the morphological var- Habitat iation among the studied species. Slight but well-pronounced differ- Most of the studied species occurred in all available habitat types. In ences in overall size can be an important factor for niche segregation spring, the habitats in the lowlands were found to be of lesser impor- (Alatalo et al. 1986). The observed variability in wing morphology, tance for the buntings. This can probably be explained by the fact especially wing pointedness, is likely linked to flight behavior and that they provide less food and shelter before the vegetation period, migration distance (Baldwin et al. 2010). However, these differences which usually starts after the majority of the buntings have migrated might not be relevant regarding niche use when species meet at the through. Therefore, it seems possible that there is much stronger stopover site. Some morphologically rather similar species showed competition for suitable habitats during spring migration. Reeds are high niche overlap in habitat use and phenology as well (for exam- not of great importance for the studied species during spring migra- ple, Little Bunting and Rustic Bunting). We found that morphologi- tion. However, it has to be noted that the only reed specialist spe- cally similar species do not avoid each other on the spatial or cies, the Ochre-rumped Bunting, was not trapped during spring temporal scale. Strong differences were only found between those migration in sufficient numbers for an inclusion in the analysis Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zoy016/4842010 by Ed 'DeepDyve' Gillespie user on 13 July 2018 8 Current Zoology, 2018, Vol. 0, No. 0 pal pal pal pal pal pal pal pal pal pal rus ru ru ru ru rus s s s s pus pus pus pus pus ele ele ele ele ele pus pus pus pus pus ele ele ele ele ele spo spo spo spo spo spo spo spo spo spo chr chr chr chr chr chr chr chr chr chr 2013: t =−8.699, df =28, R=−0.854, P<0.001 2015: t =−6.461, df =28, R=−0.774, P<0.001 105 110 115 120 125 130 135 median day (spring) Figure 5. Median dates of occurrence during spring and autumn migration are correlated. For species abbreviations, see Figure 1. Figure 6. Mean similarity indices and niche overlap values for all species pairs during spring (S) and autumn (A). (which is also true for Common Reed Bunting E. schoeniclus, among the studied species. This is especially true for autumn migra- another reed specialist). tion, when the mean niche overlap value is much lower than on any During autumn migration, however, the majority of the individ- other dimension (Figure 6). Differences in phenology between years uals and species prefer those habitats in the lowlands, while the for- were found for Yellow-throated Bunting and Pallas’s Reed Bunting ested parts on the river terrace are of lesser importance. This change during spring migration. This might be caused by the delayed start in habitat use was visible even within species, like for example, in of the ringing season especially in 2016. Yellow-throated and Black-faced Bunting. It can be assumed that the abundance of seed- Pallas’s Reed Buntings are the earliest to migrate, with some individ- bearing plants (for example, grasses) is probably higher in the open uals arriving already in March (personal observations), and there- lowlands than in more forested places. Reed beds and marsh vegeta- fore, the data might not cover the complete migration period. This tion are known for high arthropod availability in late summer and might also explain the interannual differences in phenology for autumn and their attractiveness to a variety of migrant bird species Pallas’s Reed Bunting during autumn migration. In some years, this during this season (Bairlein 1983). The observed patterns of habitat species is found until November and single birds might overwinter use might therefore reflect food availability or food preferences. in the area (personal observations). The differences in Ochre- Again, high overlap among species would in this case suggest limited rumped Bunting, however, could be explained with its low sample resources (Kober and Bairlein 2009; McFarlane Tranquilla et al. size—only 11 individuals were trapped in 2015. 2015). Extreme events, like the flood in 2013, can lead to shifts in All in all, interannual variation does not occur on a large scale, habitat use, and might therefore increase competition among species and we assume that the majority of the studied species seems to fol- at stopover sites. low a rather strict schedule during their migration. Similar results were found for buntings during spring migration at a stopover site Phenology on the Korean Peninsula, with interannual variation of mean arrival dates by 3 to maximum 10 days (Nam et al. 2011). Two of the In comparison with the trophic and spatial dimension, phenology was found to be most important for stopover niche separation studied species are not only migrants but also breed at Muraviovka Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zoy016/4842010 by Ed 'DeepDyve' Gillespie user on 13 July 2018 median day (autumn) 230 240 250 260 270 280 290 Heim et al.  Bunting stopover niche use 9 Figure 7. Number of species pairs (in percentage) separated for each niche dimension. A species pair was considered separated if the similarity index or the niche overlap was below 0.5 (<50% overlap). Ninety percent of all species pairs (n ¼ 30) were separated on at least one dimension. well (Francis and Cooke 1986; Gatter 2000). Arrival at breeding and stopover sites during spring migration is known to correlate with large-scale climatic indices (Stervander et al. 2005) and depends on temperature en route (Hu ¨ ppop and Winkel 2006; Tøttrup et al. 2010), conditions on the wintering grounds (Saino et al. 2004; Saino et al. 2007), or both (Tøttrup et al. 2008). In our study, however, the interannual variation was low, and the median differed only by a few days in most cases (Figure 4B). These small- scale differences might be caused by factors listed above, but the general phenological pattern and the chronological order of the studied species was found to be consistent. Precise timing of migra- tion regarding phenology, synchrony, and consistency can affect not only individual fitness, but also population dynamics and gene flow (Bauer et al. 2016). In our study system, with a comparably high number of closely related species, exact timing might be crucial to avoid competition at the stopover site. Niche overlap The mean niche overlap was found to be higher in spring than dur- ing autumn migration. This might be linked to fewer available habi- Figure 8. Correlation between relative niche breadth on spatial (habitat) and tat (shelter) and food, since bunting migration takes place before the temporal (phenology) dimension. Point diameter reflects sample size. For start of the vegetation period (see above). Another reason might be species abbreviations, see Figure 1. the difference in the length of the migration period (Figure 4A): the majority of the bunting species migrates during spring between mid- Park: Black-faced Bunting and Ochre-rumped Bunting. It is not pos- April and mid-May (30 days), whereas the main autumn passage sible to separate local and transient individuals, unless they are spans from mid-August to mid-October (60 days). This phenom- already ringed. Therefore, our analysis of their phenological niche enon is well known and probably related to strong time pressure to and the median day of occurrence might be biased by local breeding match breeding schedule (Nilsson et al. 2013), causing higher niche birds. This probably explains the comparatively high relative niche overlap on the temporal scale during spring. breadth for Black-faced Bunting during spring (Table 3). Furthermore, we showed that species with a broad temporal The main driver for the observed phenological pattern seems to niche occur in a broad range of habitats, and that there are pro- be the geographic position the birds originate from. This fits to the nounced differences between seasons. This is not a bias caused by observation, that migratory Passerines track their preferred climatic differences in sample size (Figure 7), but might rather reflect changes conditions (Go ´ mez et al. 2016). Furthermore, migration distance in food availability between habitat types within the course of a sea- was found to be important during autumn migration. Long-distance son. These changes probably force later or earlier arriving individu- migrants are the earliest species to migrate through the study site in autumn, while species with shorter routes occur later. These patterns als to utilize other resources and, therefore, switch the habitat. 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Migration phenology determines niche use of East Asian buntings (Emberizidae) during stopover

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Abstract

Stopover niche utilization of birds during migration has not gained much attention so far, since the majority of the studies focuses on breeding or wintering areas. However, stopover sites are crucial for migratory birds. They are often used by a multitude of species, which could lead to increased competition. In this work, we investigated niche use of 8 migratory and closely related Emberiza bunting species at a stopover site in Far East Russia, situated on the poorly studied East Asian fly- way. We used bird ringing data to evaluate morphological similarity as well as niche overlap on the trophic, spatial, and temporal dimension. Bill morphology was used as a proxy for their trophic niche. We were able to prove that a majority of the species occupies well-defined stopover niches on at least one of the dimensions. Niche breadth and niche overlap differ between spring and autumn season with higher overlap found during spring. Morphological differences are mostly related to overall size and wing pointedness. The temporal dimension is most important for segre- gation among the studied species. Furthermore, all species seem to exhibit a rather strict and con- sistent phenological pattern. Their occurrence at the study site is highly correlated with their geo- graphic origin and the length of their migration route. We assume that buntings are able to use available resources opportunistically during stopover, while trying to follow a precise schedule in order to avoid competition and to ensure individual fitness. Key words: bird migration, Emberiza, habitat use, non-breeding, phenology, stopover. Introduction Those niches are shaped by competition with other species, resulting in segregation or resource partitioning (Pianka 1981). The niche con- Migratory flights are energetically costly (Wikelski et al. 2003). cept itself dates back to Grinnel (1917) and is now widely applied in Consequently, many migratory birds do need to replenish energy stores during migration at intermittent stopover sites (Klaassen 1996). bioecology and sociology (Popielarz and Neal 2007). Segregation can At such stopover sites, migrants often share space with other con- and be found on different dimensions (Pianka 1981): there can be tempo- heterospecific birds. How different species of stopover migrants share ral niches (for example, Carothers and Jaksic 1984; Kronfeld-Schor space has rarely been studied in detail (Kober and Bairlein 2009) and Dayan 2003; Castro-Arellano and Lacher 2009; Hayward and which is in particular so for Asian migrants. Ecological niche segrega- Slotow 2009), spatial niches (Hagen et al. 2007), trophic niches tion is a way different species may share a stopover site. (Dammhahn et al. 2015), acoustic niches (Henry and Wells 2010), or In general, an ecological niche is usually defined as the range in niches defined by light intensity (Gerrish et al. 2009). In many cases, a which a species can have positive population growth (Chase 2011). combination of different dimensions was found to be relevant (Pianka V C The Author(s) (2018). Published by Oxford University Press. 1 This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zoy016/4842010 by Ed 'DeepDyve' Gillespie user on 13 July 2018 2 Current Zoology, 2018, Vol. 0, No. 0 1973; Piet et al. 1999; Albrecht and Gotelli 2001; Gilbert et al. 2008; Table 1. Study species and number of trapped birds (including retraps), 2011–2016 (n ¼ 7642) Dennis and Hellberg 2010). The more species are included, the more dimensions have to be considered, on which species might segregate: English name Scientific name Number of trapped birds if species are similar on 1 dimension, dissimilarity on another dimen- sion should be implied (Schoener 1974). However, even species inhab- Spring Autumn Other iting an identical niche can coexist in highly structured food webs Yellow-breasted Bunting Emberiza aureola 119 50 (Leibold and McPeek 2006). This can be explained by stochastic Yellow-browed Bunting E. chrysophris 63 145 187 effects and might be driven by dispersal instead of competition—the Meadow Bunting E. cioides 20 0 basic assumption of the “neutral theory” (Leibold 2008). The debate Yellow-throated Bunting E. elegans 174 73 101 remains open whether niche partitioning, neutrality, or a synthesis of Chestnut-eared Bunting E. fucata 00 32 both is the key for species diversity (Mouillot 2007; Leibold 2008; Pine Bunting E. leucocephalos 119 24 Vergnon et al. 2009). In recent studies, both theories were included in Pallas’s Reed Bunting E. pallasi 53 181 647 Little Bunting E. pusilla 96 288 753 models explaining species diversity (Haegeman and Loreau 2011; Ai Rustic Bunting E. rustica 103 210 543 et al. 2013; Munoz et al. 2014). Chestnut Bunting E. rutila 663 67 Niches are highly dynamic on temporal and spatial scales, and can Common Reed Bunting E. schoeniclus 15 21 change between seasons—which might be especially true for most Black-faced Bunting E. spodocephala 578 959 1985 migratory birds, covering thousands of kilometres between breeding Tristram’s Bunting E. tristrami 93 15 grounds, stopover sites, and wintering areas twice a year (Bairlein Ochre-rumped Bunting E. yessoensis 4 51 108 et al. 2012). Niche utilization and segregation during breeding season Lapland Bunting Calcarius 00 1 is well described for many species of birds (e.g. Kosin ~ski and Winiecki lapponicus 2004; Kaboli et al. 2007; Laughlin et al. 2013). However, information Snow Bunting Plectrophenax 00 1 is scarce for stopover sites used during the long period of migration. nivalis Explanations for the coexistence of migrants and residents in those Individuals trapped using standard nets during spring (April–June 2013, areas are largely lacking (Salewski and Jones 2006), but see Bensusan 2015, 2016) and autumn (August–October 2013–2015) migration as well as et al. (2011). It has been shown that many migrants “track” their birds trapped during breeding season or with non-standard nets (“Other”) are niche, instead of switching it during the non-breeding season (Joseph shown separately. and Stockwell 2000; Nakazawa et al. 2004; Papes et al. 2012). On the other hand, changes in niche utilization between seasons have annual cycle will be crucial for their conservation (Newton 2004; been shown for migratory Sylvia warblers (Laube et al. 2015). Bairlein 2016). In this study, we analyze niche use and niche segre- Overlapping niches have been found during times of low food supply gation during stopover among a group of closely related bunting (Je ˛ drzejewski et al. 1989; Hasui et al. 2009) or superabundance of high quality food (Choi et al. 2017). Niche segregation at stopover species. In doing so, we want to prove the hypotheses listed below: sites can also be hampered under poor food conditions, when individ- 1. There are well-defined stopover niches—all species differ on at uals have to utilize a broader range of available niches (Kober and least 1 niche dimension. Bairlein 2009). In Uria murres, it was also found that sympatric spe- 2. Niche utilization and overlap differs between spring and autumn cies “widened” their niches during non-breeding season to avoid com- migration. petition (McFarlane Tranquilla et al. 2015). 3. The temporal dimension is the most important, since trophic Moreover, niche segregation may vary with season. Spring and spatial niches can be widened during stopover. migration of many bird species often differs from their autumn jour- 4. The occurrence of a species at the stopover site is linked to its neys and shows higher migration speed and a lower number of stop- geographic origin (latitude). overs (Schmaljohann et al. 2012; Nilsson et al. 2013). Also the time window, in which nocturnal migrants initiate their flights, is smaller during spring migration (Bolshakov et al. 2007; Schmaljohann et al. Materials and Methods 2011). These restrictions might also cause differences in niche use Data were collected within the Amur Bird Project, a standardized and niche overlap between seasons. bird-ringing scheme at Muraviovka Park (49 5508, 27 N, 127 4019, Past studies on niche use outside breeding season focused on 93 E) in Far East Russia (Heim et al. 2012; Heim and Smirenski 2013). waders (Davis and Smith 2001; Burger et al. 2007; Jing et al. 2007; Such ringing data were proven to be suitable for characterization of Kober and Bairlein 2009; Bocher et al. 2014) as well as penguins migration phenology (Knudsen et al. 2007). Birds were trapped during (Wilson 2010; Hinke et al. 2015) and seabirds (Young et al. 2010; spring (April–June) and autumn (August–October) migration 2011– Quillfeldt et al. 2013; McFarlane Tranquilla et al. 2015; Orben 2016. Additional individuals were ringed during breeding season et al. 2015; Quillfeldt et al. 2015), whereas studies on songbirds are 2013–2016. A total of 7,642 trapped individuals of 16 species were scarce (Bairlein 1983, 1992; Martinez-Meyer et al. 2004; Laube available for analysis (Table 1). All statistical analysis were carried out et al. 2015) and are virtually absent for the East Asian flyway (Yong using the program R version 3.2.4 (R Core Team 2016). et al. 2015). This flyway, however, holds the highest diversity of migratory birds, including numerous threatened species (Yong et al. Morphology 2015). The group of buntings (Emberizidae) has currently gained East Asian buntings show sexual size dimorphism, with males being global conservation interest caused by catastrophic declines of sev- bigger, longer winged and longer tailed (Nam et al. 2011). eral species of the genus Emberiza in Europe and Asia (Menz and Arlettaz 2012; Kamp et al. 2015; Edenius et al. 2017). Far East Therefore, 15 males and 15 females each were randomly selected for Russia is the diversity hotspot of this threatened genus (Pa ¨ ckert et al. each study species. To avoid ringer-specific differences, only individ- 2015). Knowledge of their specific needs and niches throughout the uals which have been measured by the first author were considered, Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zoy016/4842010 by Ed 'DeepDyve' Gillespie user on 13 July 2018 Heim et al.  Bunting stopover niche use 3 with few exceptions for single Chestnut Buntings Emberiza rutila, seasons in the relative abundance of the species and the habitats Ochre-rumped Buntings E. yessoensis, and Little Buntings E. pusilla. used. Null hypothesis (random distribution) was rejected if All measurements were taken as proposed by Eck et al. (2011): P< 0.05. Habitat use was compared between species with a cluster Wing length (Wmax), Wing pointedness (Kipp-Index), Tail length, analysis (Ward method based on Euclidean distances). Bill length (Bsk), Bill width (Bwp), and Bill depth (Bp). Birds were In 2013, an extreme flood event occurred, covering the flood- weighed with a precision to 0.1 g using an electronic weight plain completely with water for the first time since 30 years (Ecotone Pesola PPS200). As age determination was not always pos- (Sokolova 2015). Therefore, the conditions at the nets in the wet- sible, both adults and first-year birds were included in this study. A lands changed drastically, and mist-net sites in Habitat type B were principal component analysis (PCA) was used to investigate which completely drowned. Habitat use (abundance of trapped birds per morphological features contribute most to the interspecific variabil- habitat type) differed significantly between the flood year and the ity. All data were standardized using a log transformation, to mini- years without flood (v ¼ 159.89, df ¼ 5, P< 0.001). Therefore, we mize the effects of different units (Shao et al. 2016). In our first excluded the year 2013 for the analysis of habitat use. PCA, data were not size corrected to preserve the valuable informa- We adopted the approach Bairlein (1981) used to compute niche breadth, since we intend to describe the species-specific relative uti- tion of body size, which could act as an important factor for species segregation (Alatalo et al. 1986; Shao et al. 2016). In our second lization of the resources at the study site. For the analysis of niche PCA, data were size corrected by dividing all measures of length by overlap, we used the R package spaa (Zhang 2016) with the widely the cube root of lean body mass to analyze differences in shape used niche overlap measure based on Pianka (1973). Niche overlap (Winkler and Leisler 1992). Bill morphology was used as a proxy in phenology was computed based on the proportion of birds for the size of the feeding structure—which is usually correlated to trapped per calendar week during spring and autumn migration. We food characteristics (Schoener 1965, 1974). Similarity among spe- used a Pearson’s product moment correlation to investigate the rela- cies was described based on difference in wing, tail, and tarsus tionship between mean migration days during spring and autumn. length as well as bill morphology applying the method of Ricklefs Differences in phenology between years were tested with simple lin- and Cox (1977). We computed an index of overall similarity as well ear models (DayYear). Linear mixed-effects models (LMEs) were as an index of bill similarity accordingly. used to analyze the impact of different variables on migration tim- ing. This analysis was carried out with R package nlme (Pinheiro et al. 2016). The following variables were used to explain the Habitat and phenology dependent variable median migration day for spring and autumn There are known differences in migratory behavior among sexes— each: breeding latitude (southernmost, northernmost), wintering lat- especially during spring migration, when males often migrate ahead itude (southernmost, northernmost) and migration distance (length of the females (Schmaljohann et al. 2016). The occurrence of the so- of migration route calculated as difference between mean breeding called protandrous migration in East Asian buntings was shown by and wintering latitude). Information about distribution of bunting Nam et al. (2011) at a stopover site on the Korean Peninsula, and species was gathered from the BirdLife range maps (BirdLife was also found in Ortolan Bunting E. hortulana along the west end International 2017), see Supplementary Material 2. The application of the Asian continent (Yosef and Tryjanowski 2002). To allow for of LMEs allowed us to include year and species as random factors. inner-specific variation, we included all species where we had a suf- Significant variables were selected with help of “backward stepwise ficient sample size for both females and males in our study. We model selection” (Crawley 2013) using the Likelihood-ratio test included all species in the analysis with a sample size of n> 30 per (P< 0.05) and the Akaike information criterion (AIC)-values. season. For the analysis of habitat use and phenology we included Normal distribution and variance homogeneity of residuals was those periods, during which all nets were opened at exactly the same graphically tested with help of a normal probability plot (Crawley locations for the same time span. This was true for the spring sea- 2013). Goodness-of-fit statistics (R -values) for these models were sons in 2013, 2015, and 2016 from April to June and for the autumn computed with the help of the piecewiseSEM package (Lefcheck season during the years 2013–2015, when trapping was conducted 2015). Furthermore, we tested the differences in overall niche over- from the beginning of August until the end of October. A total of 17 lap regarding habitat use and phenology between spring and autumn nets with lengths of either 6 (n ¼ 4) or 12 m (n ¼ 13) was used. Each season with a Welch Two-sample t-test. Based on the available data, net was assigned to 1 of 6 different types of habitats, which form a we were able to evaluate the existence of stopover niches for 8 spe- gradient from the low wetlands to the forests on the river terrace. cies on 3 dimensions: morphology, space, and time. Habitat type A (reed) consists of reed stands with Phragmites aus- tralis and Carex spec. Habitat type B (willow1) is characterized by low willow thickets (for example, Salix miyabeana) and wet mead- Results ows. Habitat type C (willow2) is situated on the edge of the river Morphology terrace and includes larger willow bushes and trees (e.g. S. pierotii). Habitat type D (deciduous) is situated on the terrace, with poplar Complete morphometric data of 15 males and 15 females each were Populus tremula and bird cherry Prunus padus trees and raspberry available for 8 species (Supplementary Material 2). The results of Rubus idaeus in the understorey. Large Mongolian oak Quercus the PCA are shown in Table 2. When using the original data, the mongolica trees are characteristic for Habitat type E (oak), as well first principal component, explaining 53% of total variance, is nega- as a dense understorey with Artemisia spec. and Lespedeza bicolor. tively correlated with body mass and all other measurements, and A pine plantation with Pinus sylvestris forms Habitat type F (pine). therefore, stands for overall size. The second principal component, Habitats A–C are situated in the lowlands, and Habitats D–F on the explaining 17% of total variance, is positively correlated with tail terrace. The nets were not equally distributed among the habitat and wing length, whereas the third principal component explaining types, for details see Supplementary Material 1. v -tests were used 16% of total variance is positively correlated with wing pointedness. to evaluate whether the trapped buntings are randomly distributed PC1, PC2, and PC3 are depicted in Figure 1. After correcting for among the habitat types and whether there are differences between size, we found that the first and the second principal component are Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zoy016/4842010 by Ed 'DeepDyve' Gillespie user on 13 July 2018 4 Current Zoology, 2018, Vol. 0, No. 0 Figure 1. Principal components 1–3 for morphology of 8 bunting species using original data (upper line) and size-corrected data (lower line). The following spe- cies were included: Yellow-browed Bunting (chr), Yellow-throated Bunting (ele), Pallas’s Reed Bunting (pal), Little Bunting (pus), Rustic Bunting (rus), Chestnut Bunting (rut), Black-faced Bunting (spo) and Ochre-rumped Bunting (yes). correlated with wing length and wing pointedness, respectively, and 2013. This pattern still remains consistent when excluding the explaining 39% and 25% of total variance, whereas the third princi- superabundant Black-faced Bunting (Supplementary Material 4a). pal component is negatively correlated with bill and tarsus length In spring, most buntings were found in the pine plantation (30.4%, explaining 16% of variance. The PCA with the original data Habitat F) and in deciduous trees (22.3%, Habitat D). In autumn, explained more of the morphological variance than the PCA based the majority of the birds were trapped in small willow thickets on the size-corrected data. (40.5%, Habitat B) and oak forest with dense understorey (19.5%, A similarity index was computed for each of the species pairs. Habitat E) —see Supplementary Material 1. Almost all bunting spe- The morphologically most similar species pairs are Pallas’s Reed cies were found in all kind of habitats (Supplementary Material 4b), Bunting and Little Bunting with a similarity index of 0.679, the with exception of the Ochre-rumped Bunting, in which 80% of the most dissimilar pair are Ochre-rumped Bunting and Yellow-browed birds were trapped in Habitat type A (reeds). Nevertheless, all spe- Bunting with a similarity index of 0.004 (Figure 2A, Supplementary cies were neither randomly distributed among the habitat types (v - Material 3). Part of this overall index is the similarity index of bill test, P< 0.001), nor among the total traps per habitat (v -test, morphology. The most similar index values were found for Ochre- P< 0.05). rumped Bunting and Yellow-throated Bunting; the most unlike pair In spring, the 6 studied species can be divided in 3 clusters in are Yellow-browed Bunting and Yellow-throated Bunting terms of their habitat use (Figure 3): (1) Low willow shrubs (pal), (Figure 2B, Supplementary Material 3). (2) species of higher willow shrubs and deciduous forest (ele, pus, rus, spo), and (3) species mainly found in the pine plantation (chr). Habitat In autumn, 8 species can be divided into 4 clusters: (1) reed and wet- Trapped buntings were not equally distributed among all habitats, land species (yes), (2) species of low willow thickets (pal, pus, spo), 2 2 neither in spring (v ¼ 39.588, df ¼ 5, P< 0.001) nor in autumn (v (3) forest species (ele, rus), and (4) species that occur in all habitats ¼ 11.833, df ¼ 5, P ¼ 0.037). Habitat types A–C in the lowlands (chr, rut). were most important in years without flood, while the buntings Habitat use differed significantly between spring and autumn shifted to the habitat types D–E on the terrace in the flood year season (v ¼ 115.25, df ¼ 5, P< 0.001). In spring, 31.8% of all Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zoy016/4842010 by Ed 'DeepDyve' Gillespie user on 13 July 2018 Heim et al.  Bunting stopover niche use 5 Table 2. PCA: Factor loadings of the first 3 principal components based on 9 morphological measurements for 8 bunting species Measurement Original data Size-corrected PC1 PC2 PC3 PC1 PC2 PC3 Wing length (Maximum chord) 0.365 0.362 0.280 0.473 0.315 0.216 th Length of 8 primary 0.346 0.412 0.281 0.481 0.284 0.215 Wing pointedness (Kipp-Index) 0.218 0.135 0.668 0.087 0.609 0.224 Tail length 0.110 0.629 0.400 0.360 0.417 0.211 Tarsus length 0.321 0.059 0.423 0.002 0.409 0.600 Bill length (Bill to skull) 0.340 0.341 0.178 0.289 0.008 0.629 Bill width (behind nostrils) 0.369 0.270 0.117 0.376 0.179 0.227 Bill height (behind nostrils) 0.383 0.295 0.049 0.428 0.276 0.081 Weight (lean body mass) 0.431 0.076 0.100 NA NA NA Proportion of variance 0.545 0.177 0.164 0.391 0.251 0.157 Cumulative proportion of variance 0.545 0.721 0.886 0.391 0.642 0.799 The highest loadings for each component are in bold. AB CD Figure 2. Similarity of 8 bunting species regarding (A) morphology and (B) bill morphology, as well as niche overlap regarding (C) habitat use and (D) phenology. Point size resembles similarity index/niche overlap (range: 0–1). For species abbreviations, see Figure 1. Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zoy016/4842010 by Ed 'DeepDyve' Gillespie user on 13 July 2018 6 Current Zoology, 2018, Vol. 0, No. 0 Figure 3. Cluster analysis based on habitat preferences of bunting species during spring (left) and autumn (right) migration. For species abbreviations, see Figure 1. whereas some Little, Yellow-browed and Black-faced Buntings Table 3. Relative niche breadth of 8 species of buntings regarding habitat use and phenology during spring and autumn migrate until the end of May or even the first days of June. Autumn migration starts at the beginning of August in Chestnut and Ochre- Species Habitat Phenology rumped Buntings, and ends in the second half of October with Pallas’s Reed Bunting being the latest species. The median date of Spring Autumn Spring Autumn their occurrences at the study site is given in Supplementary Material Yellow-browed Bunting chr 22.7 69.8 18.2 42.7 5. Significant differences in phenology between years were found for Yellow-throated Bunting ele 48.7 52.2 38.3 40.7 Yellow-throated Bunting (F ¼ 9.578, R ¼ 0.052, P¼ 0.002) and 1,172 Pallas’s Reed Bunting pal 39.6 27.1 24.1 15.1 Pallas’s Reed Bunting (F ¼ 8.149, R ¼ 0.138, P ¼ 0.006) during 1,51 Little Bunting pus 62.5 46.0 31.1 29.4 spring migration, and for Ochre-rumped Bunting (F ¼5.462, 1,49 Rustic Bunting rus 49.3 49.4 26.5 23.4 R ¼ 0.100, P ¼ 0.024) as well as Pallas’s Reed Bunting Chestnut Bunting rut NA 54.1 NA 44.1 Black-faced Bunting spo 84.5 58.3 44.6 38.0 (F ¼ 16.18, R ¼ 0.083, P< 0.001) during autumn migration. No 1,180 Ochre-rumped Bunting yes NA 14.4 NA 29.7 significant differences in phenology between years were found for the remaining species (Black-faced Bunting, Chestnut Bunting, Little Bunting, Rustic Bunting, and Yellow-browed Bunting). Phenology for buntings were trapped in the lowlands (Habitats A–C), and 68.2% the 5 most common species (n/year> 30) during autumn migrations on the terrace (Habitats D–F). In autumn, it was 61.5% and 36.5%, 2013, 2014, and 2015 is shown in Figure 4B. Occurrence during respectively. This is also true within species: in spring, 41% of all autumn migration is highly correlated with spring phenology Black-faced Buntings are trapped in lowlands and 59% on the ter- (Figure 5). The final LME to explain the median day of migration race, while in autumn 71% were found in the lowlands and 29% on reveals significant the variable northernmost wintering latitude for the terrace. The interspecific differences in habitat use are less pro- spring migration (R ¼ 0.73) with more southern wintering species nounced in spring than in autumn. passing late. In autumn, northernmost breeding latitude and migra- Relative habitat niche breadth differed among species and tion distance combined (R ¼ 0.81, see Supplementary Material 6) 2 2 between seasons (Table 3). Black-faced Buntings utilized a broader explained passage date (R ¼ 0.32 and R ¼ 0.02, respec- marg marg habitat niche during spring than during autumn, whereas Yellow- tively); with northern breeding birds passing late and species travelling browed Buntings occupied a narrow niche during spring and a long distances passing early. broad one in autumn. Ochre-rumped Buntings utilized the narrow- est niche during autumn migration, again highlighting their status as Niche overlap habitat specialists. The mean niche overlap in phenology is significantly higher in spring The niches of the studied species overlapped during both spring than in autumn (t¼3.003, df ¼ 32.623, P ¼ 0.005), which is also and autumn (Figure 2C, Supplementary Material 3). Highest the case for niche overlap in habitat use (t¼3.302, df ¼ 40.491, overlap was found between Black-faced Bunting, Little Bunting, P ¼ 0.002) (Figure 6, Supplementary Material 3). During spring and Pallas’s Reed Bunting, as well as between Rustic Bunting and migration, 6 out of 15 species pairs (40%) show an overlap value in Yellow-throated Bunting. The niches of Chestnut Bunting and phenology of <0.5 (<50% overlap). Thirty-three percent of all spe- Ochre-rumped Bunting during autumn migration showed least cies pairs are well separated regarding bill morphology, and 13% overlap with other species. use differential spatial niches. Sixty-six percent of all species pairs were separated on at least 1 dimension. During autumn migration, Phenology this is true for 80% (24 of 30 species pairs). In autumn, 63% differ There are pronounced differences in the timing of migration among on the temporal dimension, and 37% on the spatial dimension the 8 studied species (Figure 4A). Spring migration begins with (Figure 7). There is a significant correlation between niche breadth Pallas’s Reed Bunting as the earliest species to arrive at the study site, on the spatial and on the temporal dimension (Figure 8). Species Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zoy016/4842010 by Ed 'DeepDyve' Gillespie user on 13 July 2018 Heim et al.  Bunting stopover niche use 7 Figure 4A. Phenology during spring (left) and autumn (right) migration. The height of the box resembles sample size. For species abbreviations, see Figure 1. species situated at the very end of the morphological spectrum, that is, between the smallest species (Ochre-rumped Bunting) and the largest species (Yellow-browed Bunting). This is also true for bill morphology—only the 2 species with the weakest (Yellow-throated Bunting) and the heaviest bill (Yellow- browed Bunting) showed very low similarity. The extreme low value between the latter 2 species seems to be more a methodological bias (highlighting the ends of the spectrum) rather than a real difference. Since bill morphology was used as a proxy for the feeding structure and the tropic niche, it seems likely, that there are no major differen- ces in diet among the studied species. Buntings form mixed-species flocks, and they were often seen feeding together on the same resources at the study site (personal observations). All species are foraging on seed-bearing plants on or close to the ground. According to Byers et al. (1995), all Emberiza buntings switch their diet from invertebrates during the breeding season to a wide range Figure 4B. Inter-annual variability in autumn phenology for the 5 most com- of small seeds during the non-breeding season. In a study by Hasui mon bunting species (n/year> 30). The height of the box resembles sample et al. (2009), niche partitioning among 2 tropical bird species was size. Significant differences between years were only found for Pallas’s Reed Bunting. For species abbreviations, see Figure 1. found only during periods of fruit scarcity. Moore and Yong (1991) found that migrants at stopover sites gained less weight when more birds were around. If food availability is a limiting factor, one would with a broad temporal niche occur in a broad range of habitats, and vice versa. There are pronounced differences between spring and expect high overlap, since migrants are known to use a wide range of available niches under such conditions (Kober and Bairlein 2009). autumn season within some species, irrespective of sample size. All in all, the studied species are in general not very distinct in mor- phology, which is likely caused by their close phylogenetic relation- Discussion ship (all 8 species belong to the same genetic clade, even within the genus Emberiza, Pa ¨ ckert et al. 2015). Morphology Overall size was found to be the most important factor in our PCA, and the size-corrected PCA explained less of the morphological var- Habitat iation among the studied species. Slight but well-pronounced differ- Most of the studied species occurred in all available habitat types. In ences in overall size can be an important factor for niche segregation spring, the habitats in the lowlands were found to be of lesser impor- (Alatalo et al. 1986). The observed variability in wing morphology, tance for the buntings. This can probably be explained by the fact especially wing pointedness, is likely linked to flight behavior and that they provide less food and shelter before the vegetation period, migration distance (Baldwin et al. 2010). However, these differences which usually starts after the majority of the buntings have migrated might not be relevant regarding niche use when species meet at the through. Therefore, it seems possible that there is much stronger stopover site. Some morphologically rather similar species showed competition for suitable habitats during spring migration. Reeds are high niche overlap in habitat use and phenology as well (for exam- not of great importance for the studied species during spring migra- ple, Little Bunting and Rustic Bunting). We found that morphologi- tion. However, it has to be noted that the only reed specialist spe- cally similar species do not avoid each other on the spatial or cies, the Ochre-rumped Bunting, was not trapped during spring temporal scale. Strong differences were only found between those migration in sufficient numbers for an inclusion in the analysis Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zoy016/4842010 by Ed 'DeepDyve' Gillespie user on 13 July 2018 8 Current Zoology, 2018, Vol. 0, No. 0 pal pal pal pal pal pal pal pal pal pal rus ru ru ru ru rus s s s s pus pus pus pus pus ele ele ele ele ele pus pus pus pus pus ele ele ele ele ele spo spo spo spo spo spo spo spo spo spo chr chr chr chr chr chr chr chr chr chr 2013: t =−8.699, df =28, R=−0.854, P<0.001 2015: t =−6.461, df =28, R=−0.774, P<0.001 105 110 115 120 125 130 135 median day (spring) Figure 5. Median dates of occurrence during spring and autumn migration are correlated. For species abbreviations, see Figure 1. Figure 6. Mean similarity indices and niche overlap values for all species pairs during spring (S) and autumn (A). (which is also true for Common Reed Bunting E. schoeniclus, among the studied species. This is especially true for autumn migra- another reed specialist). tion, when the mean niche overlap value is much lower than on any During autumn migration, however, the majority of the individ- other dimension (Figure 6). Differences in phenology between years uals and species prefer those habitats in the lowlands, while the for- were found for Yellow-throated Bunting and Pallas’s Reed Bunting ested parts on the river terrace are of lesser importance. This change during spring migration. This might be caused by the delayed start in habitat use was visible even within species, like for example, in of the ringing season especially in 2016. Yellow-throated and Black-faced Bunting. It can be assumed that the abundance of seed- Pallas’s Reed Buntings are the earliest to migrate, with some individ- bearing plants (for example, grasses) is probably higher in the open uals arriving already in March (personal observations), and there- lowlands than in more forested places. Reed beds and marsh vegeta- fore, the data might not cover the complete migration period. This tion are known for high arthropod availability in late summer and might also explain the interannual differences in phenology for autumn and their attractiveness to a variety of migrant bird species Pallas’s Reed Bunting during autumn migration. In some years, this during this season (Bairlein 1983). The observed patterns of habitat species is found until November and single birds might overwinter use might therefore reflect food availability or food preferences. in the area (personal observations). The differences in Ochre- Again, high overlap among species would in this case suggest limited rumped Bunting, however, could be explained with its low sample resources (Kober and Bairlein 2009; McFarlane Tranquilla et al. size—only 11 individuals were trapped in 2015. 2015). Extreme events, like the flood in 2013, can lead to shifts in All in all, interannual variation does not occur on a large scale, habitat use, and might therefore increase competition among species and we assume that the majority of the studied species seems to fol- at stopover sites. low a rather strict schedule during their migration. Similar results were found for buntings during spring migration at a stopover site Phenology on the Korean Peninsula, with interannual variation of mean arrival dates by 3 to maximum 10 days (Nam et al. 2011). Two of the In comparison with the trophic and spatial dimension, phenology was found to be most important for stopover niche separation studied species are not only migrants but also breed at Muraviovka Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zoy016/4842010 by Ed 'DeepDyve' Gillespie user on 13 July 2018 median day (autumn) 230 240 250 260 270 280 290 Heim et al.  Bunting stopover niche use 9 Figure 7. Number of species pairs (in percentage) separated for each niche dimension. A species pair was considered separated if the similarity index or the niche overlap was below 0.5 (<50% overlap). Ninety percent of all species pairs (n ¼ 30) were separated on at least one dimension. well (Francis and Cooke 1986; Gatter 2000). Arrival at breeding and stopover sites during spring migration is known to correlate with large-scale climatic indices (Stervander et al. 2005) and depends on temperature en route (Hu ¨ ppop and Winkel 2006; Tøttrup et al. 2010), conditions on the wintering grounds (Saino et al. 2004; Saino et al. 2007), or both (Tøttrup et al. 2008). In our study, however, the interannual variation was low, and the median differed only by a few days in most cases (Figure 4B). These small- scale differences might be caused by factors listed above, but the general phenological pattern and the chronological order of the studied species was found to be consistent. Precise timing of migra- tion regarding phenology, synchrony, and consistency can affect not only individual fitness, but also population dynamics and gene flow (Bauer et al. 2016). In our study system, with a comparably high number of closely related species, exact timing might be crucial to avoid competition at the stopover site. Niche overlap The mean niche overlap was found to be higher in spring than dur- ing autumn migration. This might be linked to fewer available habi- Figure 8. Correlation between relative niche breadth on spatial (habitat) and tat (shelter) and food, since bunting migration takes place before the temporal (phenology) dimension. Point diameter reflects sample size. For start of the vegetation period (see above). Another reason might be species abbreviations, see Figure 1. the difference in the length of the migration period (Figure 4A): the majority of the bunting species migrates during spring between mid- Park: Black-faced Bunting and Ochre-rumped Bunting. It is not pos- April and mid-May (30 days), whereas the main autumn passage sible to separate local and transient individuals, unless they are spans from mid-August to mid-October (60 days). This phenom- already ringed. Therefore, our analysis of their phenological niche enon is well known and probably related to strong time pressure to and the median day of occurrence might be biased by local breeding match breeding schedule (Nilsson et al. 2013), causing higher niche birds. This probably explains the comparatively high relative niche overlap on the temporal scale during spring. breadth for Black-faced Bunting during spring (Table 3). Furthermore, we showed that species with a broad temporal The main driver for the observed phenological pattern seems to niche occur in a broad range of habitats, and that there are pro- be the geographic position the birds originate from. This fits to the nounced differences between seasons. This is not a bias caused by observation, that migratory Passerines track their preferred climatic differences in sample size (Figure 7), but might rather reflect changes conditions (Go ´ mez et al. 2016). Furthermore, migration distance in food availability between habitat types within the course of a sea- was found to be important during autumn migration. Long-distance son. These changes probably force later or earlier arriving individu- migrants are the earliest species to migrate through the study site in autumn, while species with shorter routes occur later. These patterns als to utilize other resources and, therefore, switch the habitat. 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