Bai et al. Avian Res (2017) 8:31 DOI 10.1186/s40657-017-0089-y Avian Research RESEARCH Open Access Bulbuls and crows provide complementary seed dispersal for China’s endangered trees Bing Bai1† , Ning Li2†, Xinhai Li3 and Changhu Lu4* Abstract Background: Diferent functional frugivores generally exhibit unequal contributions, both in terms of quantity (seed removal) and quality (seedling recruitment), to efective seed dispersal of plant species. However, variations in this dispersal pattern generated by frugivores across diferent regions are still unknown. Methods: In our study, we evaluated the contributions of two functional frugivore bird groups, the bulbuls (Pycnon‑ otidae) and crows (Corvidae), in both the seed removal and seedling recruitment of the endangered Chinese yew tree (Taxus chinensis) across three diferent geographical regions in eastern China. Results: The dominant crow species, Urocissa erythrorhyncha, was the most common disperser crow species at all sites, while the dominant bulbul species varied across the three sites. Furthermore, the two functional groups of dispersers diverged in the aspects of seed removal (quantity) and seedling recruitment pattern (quality). While bulbuls outperformed crows in seed removal (quantity), crows took more seeds to a safer site for seedlings (quality). Conclusions: Our results highlight the importance of variations in the efective seed dispersal patterns of diferent functional disperser groups across diferent regions in the conservation and management of endangered tree species. Keywords: Complementary seed dispersal, Efective seed dispersal, Seed removal, Seedling recruitment, Taxus chinensis Background is the key strategy for preventing endangered populations In tropical and temperate forests, more than 75% of from collapsing (Bascompte and Jordano 2007; Li et al. woody species depend on frugivores for primary or sec- 2015a; Razafndratsima and Dunham 2015). Te efec- ondary seed dispersal (Howe and Smallwood 1982). Seed tive dispersal pattern is often estimated as the number dispersal is important for determining the composition, of seed removal by frugivores (quantity) and the rela- diversity, and structure of plant communities (Nathan tive contribution of frugivores to seedling recruitment and Muller-Landau 2000; Levine and Murrell 2003), (quality) (Schupp 1993; Schupp et al. 2010). Operating which has important implications for the conservation under this view, most empirical studies have tradition- and management of endangered plants (Trakhtenbrot ally evaluated the role of dispersers in determining the et al. 2005). efective dispersal patterns of plant species based on the For the conservation of endangered feshy-fruited above two aspects (Carlo et al. 2013; Rey and Alcántara plants, it is important to explore how the plants form an 2014). However, the range of plant species always varies efective dispersal pattern across diferent regions, which across diferent regions, causing variations in the efec- tive disperser species and thus afecting the regenera- *Correspondence: [email protected] tion patterns of plant species at diferent sites. Terefore, †Bing Bai and Ning Li contributed equally to this work information on efective dispersal may be important for 4 Laboratory of Plant‑Animal Interactions, College of Forest Resources implementing efective conservation strategies for plant and Environment, Nanjing Forestry University, Nanjing 210037, China Full list of author information is available at the end of the article species (Burns 2002, 2003). Given the inherent difculty © The Author(s) 2017. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/ publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Bai et al. Avian Res (2017) 8:31 Page 2 of 6 in studying efective dispersal patterns across plant dis- Chongtou, Tongkeng: 2011 and 2012) at each site. tributional ranges, empirical evidence supporting the Observations were made with binoculars from a hideout contribution of disperser species in endangered plant located at least 25 m away from the trees. Each mother conservation remains limited. tree was observed for an 8-h period once a day during In this study, we assessed the contributions of two the seasons, with observations being terminated when no functional groups of bird species (bulbuls and crows) in more fruits remained on the mother trees. determining the efective dispersal patterns of Chinese For each bird that visited the mother tree, we recorded yew (Taxus chinensis (Rehder and E.H. Wilson) Rehder) the species and the number of fruits swallowed during across three regions in eastern China. Specifcally, we visits. If a group of conspecifc birds visited the tree, we investigated: (1) the variation in the foraging behavior only focused on the most visible individual (Altmann of bulbuls and crows on T. chinensis across regions, and 1974; Breitbach et al. 2010). After feld study, we com- how this variation impacts their seed removal, and (2) the pared the visiting frequency and foraging amount per variation in the perching behavior of bulbuls and crows visit by each disperser species as a quantity pattern across across regions, and how this afects the birds’ contribu- diferent regions. Moreover, we used a machine-learning tion to seedling recruitment. algorithm, random forest model, to plot how bird visit- ing frequency, foraging amount per visit, bird species, Methods sites, and years infuence the numbers of seeds that were Species and study sites removed (R package RandomForest) (Breiman 2001). T. chinensis is a relic species that is endemic to China. Tis species is designated as “endangered” in the Interna- Perching by dominated bulbuls and crows across diferent tional Union for Conservation of Nature (IUCN) Red List regions and its contribution to the seedling recruitment (2013 version), and is ranked as a frst priority protected pattern species by the Chinese government (Tomas et al. 2013). We frst used 10 m × 10 m habitat cells to digitize the Te regeneration of the wild population of T. chinensis is three study sites. Overall, we set 100 sampling cells in not only limited by low pollination rates, seed-predator Shuangkeng, Chongtou, and Tongkeng, respectively. We pressure, and low seedling survival rates, but also limited then investigated the 1-year-old seedlings (H ≤ 10 cm) by diferent bird species (Li et al. 2015b). in each cell of each site to determine the suitable recruit- For our study, we selected three feld sites in eastern ment habitat for T. chinensis. China (Shuangkeng village in Anhui, Chongtou village For modeling the contributions of birds to seedling in Fujian, and Tongkeng village in Zhejiang) that had recruitment, we monitored the perching frequencies of dense populations of T. chinensis. Te Shuangkeng vil- two dominant species of bulbuls and crows during the lage [30°00′N, 117°18′E; 540 m above sea level (a.s.l.)] fruiting period, from late October to early December is located in the southern part of Anhui Province, and (Breitbach et al. 2010; Li et al. 2015a, 2016). Bird perching contains 35 individual trees, which are distributed in a was observed from high vantage points on the hills using human-modifed bamboo (Phyllostachys heterocycla) binoculars. Birds were selected randomly and tracked patch (Li et al. 2015a). Te Chongtou village (25°15′– in sessions that ended once visual contact was lost or if 25°35′N, 116°45′–116°57′E; 960 m a.s.l.) is situated in the focal bird could no longer be distinguished from the the Meihua Mountain National Nature Reserve in Fujian other conspecifcs. During the sessions, the habitat used Province, and contains the largest wild population of T. by birds and their position were recorded every 30 s (Bre- chinensis (approximately 490 adults) in eastern China, itbach et al. 2010; Spiegel and Nathan 2012). including 200 trees that are over 500 years old (Li et al. We used the function to perform univariate Kriging 2015b). Te Tongkeng village (30°00′N, 119°22′E; 553– models to interpolate seedling number and bird perch- 638 m a.s.l.) contains the largest natural population of ing frequency in the sampled habitat plot. The method T. chinensis in Zhejiang Province (approximately 109 used for spatial interpolation is the krige function in adults), including 34 trees that are more than 500 years the R package gstat. We tested the number of seed- old (Li et al. 2015a). lings in the habitat cells by a generalized mixed-effect model, in which the perching frequencies of the bird Seed removal by bulbuls and crows across diferent species and sites were the covariates, while the sur- regions vey year and their interaction term were the random For studying seed removal by bulbuls and crows across effects. Because the numbers of seedlings were count diferent regions, 10 aggregated mother trees were data, the function glmer in the R package lme4 was observed during two fruiting seasons (from late Octo- used to run the generalized mixed-effect model with a ber to early December; Shuangkeng: 2010 and 2011; Poisson link function. Bai et al. Avian Res (2017) 8:31 Page 3 of 6 Results More bulbul and crow species with high visiting frequen- Seed removal by bulbuls and crows across diferent cies were recorded at Chongtou. Te Red-billed Blue regions Magpie (Urocissa erythrorhyncha) was the most com- We performed 400 h of tree observations at each site. Five mon disperser species of crow at all sites. However, the bulbul species and four crow species were recorded that dominant bulbul species varied across the three sites. Te dispersed the seeds of T. chinensis. Te composition of Mountain Bulbul (Hypsipetes mcclellandii), Black Bulbul disperser species and visiting frequency were similar at (H.