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Importance of Plant and Bird Traits on the Seed Removal Pattern Of Li et al. Ecological Processes (2020) 9:43 https://doi.org/10.1186/s13717-020-00253-6 LETTER Open Access Importance of plant and bird traits on the seed removal pattern of endangered trees across different forest patches in southeast China Ning Li1* , Shuai Zhang2, Yuan-Hao Ren1 and Zheng Wang2 Abstract Seed removal by birds has been recognized as an important part of seed dispersal process in patchy forest areas; however, few studies have focused on the contribution of both plant and bird traits to seed removal. In this study, field data of seed removal for Taxus chinensis was combined with the data of bird and plant traits for analysis. The relevant traits of plants and birds that influenced T. chinensis–bird interaction were identified in a remnant patchy forest in yew ecological garden, Fujian Province, southeast China. Twenty bird species were found to forage and remove the seeds of T. chinensis. The number of bird species varied in different forest patches; however, their contribution to seed removal showed no significant differences. Both bird and plant traits were found to affect seed removal. The seed removal rate was positively affected by bird traits, such as foraging frequency and wing length, but decreased with body weight. The plant traits, such as number of fruits, tree height, canopy density, and crown width, which are related to safe shelter and food resource conditions, increased the seed removal rate. Our results underline the functional importance of bird and plant traits in the seed removal from endangered trees in patchy forests. Therefore, future conservation strategies should prioritize and recognize the role of both plant and bird traits in seed dispersal in remnant patchy forests. Keywords: Seed removal, Bird trait, Plant trait, Hypsipetes leucocephalus, Patchy forest Introduction habitat specialist, thus disrupting seed dispersal Habitat fragmentation is one of the most important fac- service (Bregman et al. 2016; Donoso et al. 2016; tors responsible for the decline of biodiversity and dis- Schupp et al. 2017). ruption of ecological functions (Taubert et al. 2018; Liu Seed removal is an important aspect of seed dispersal; et al. 2019; Peters et al. 2019). In remnant habitat it is performed by different frugivorous bird species patches, most of the ecological functions (pollination, based on their functional traits (Farwig et al. 2017; seed dispersal) are not only disrupted by loss of species, Schupp et al. 2017). Both bird and plant traits could but also affected by remnant patch size and quality affect seed removal pattern in a fragmented habitat (Bomfim et al. 2018; Emer et al. 2018). Small size and (Schupp et al. 2017). Morphological and behavioral traits low quality of remnant habitat patches cannot accom- of bird species could shape their role in seed removal modate the persistence of large-bodied species and pattern (Pérez-Méndez et al. 2015; Li et al. 2019). Large- bodied species are generally recognized as keystone spe- cies owing to their huge requirement for food resources * Correspondence: [email protected] 1Institute of Applied Ecology, Nanjing Xiaozhuang University, Nanjing (Marjakangas et al. 2020). Most importantly, food selec- 211171, Jiangsu, China tion by birds always affects the seed removal pattern of Full list of author information is available at the end of the article © The Author(s). 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. Li et al. Ecological Processes (2020) 9:43 Page 2 of 6 plant species. When birds treat fruits as their main food, leaved forest patch, we quantified the frequency of bird the regeneration ability of plants in a patchy forest be- visits to mature T. chinensis trees and number of foraged comes similar to the one in a natural forest (Sasal and and removed seeds. Ten individuals were selected, with Morales 2013; Schupp et al. 2017). Plant traits also affect two individuals distributed in bamboo patch, four in seed removal in fragmented remnant habitat (Dehling mixed bamboo and broad-leaved patch, and four in ever- et al. 2016), for instance, large trees could be easily lo- green broad-leaved forest patch. We observed the for- cated by bird species, thus affecting bird foraging behav- aging behavior of birds from the opposite mountain ior (Cousens et al. 2015). A high number of available slopes, at a distance of approximately 50 m using a tele- fruits attracts birds and affects their food selection (Li scope (Leica 70, Leica Microsystems GMBH, Mannheim, et al. 2019). Although several studies on seed dispersal Germany). The birds that visited a mother tree were ob- have already reported on such a trait approach for un- served from landing to leaving. Observations lasted 8 h derstanding the role of bird and plant traits in seed dis- per day during the fruiting seasons of T. chinensis, from persal, the combined effects of plant and bird traits on late October to early December, accounting for 58 days the pattern of seed removal in fragmented remnant habi- annually from 2018 to 2019. We identified and counted tat patchy forests remain largely unknown. the frugivorous bird species (Mackinnon et al. 2000), Taxus chinensis (Pilger) Rehd. is an endemic gymno- and recorded the number of seeds removed. sperm in China; it is on the endangered species list and is legally protected in China. The wild population of T. Effects of bird and plant traits on seed removal across chinensis regenerates poorly owing to low fecundity, different patches high levels of seed predation, weak competitive ability of We selected two behavioral traits (foraging frequency seedlings, and scarcity of microhabitats for recruitment. and foraging type, swallowing and pecking) and five It is widely distributed in eastern China; however, most morphological traits (bill length, body length, body of the wild populations are patchily distributed, and their weight, wing length, tail length, and tarsus length) to in- seeds are dispersed by avian frugivores (Li et al. 2019). vestigate the effects of bird traits on seed dispersal. Data In this study, we combined the field study of seed re- on body weight were obtained by capturing 10 individ- moval from T. chinensis with that of bird and plant traits uals of each species in the zoological garden of Nanjing and analyzed the results. With the analysis, we aim to and measuring their body weight using electronic scale. identify the relevant traits of plants and birds that influ- To obtain the other four morphological traits of the ence the seed removal pattern of T. chinensis in a local bird species, we measured five males and five fe- remnant patchy forest. males of each bird species using the specimens preserved in the Museum of Nanjing Xiaozhuang University. We Materials and methods used the mean value of each trait for analyses. Further- Study site more, we compared five morphological traits of frugivor- The study was conducted in a yew ecological garden ous bird species using ANOVA test after the data were (elevation 895–1218 m a.s.l., slope gradient 27°), located log-transformed to approximate normality; size effects in the southern experimental area of the Meihua Moun- were removed in all cases using the residuals from the tain National Nature Reserve (25° 15′–25° 35′ N; 116° regressions on body length (snout–vent length, SVL). 45′–116° 57′ E) in the west part of Fujian Province, Five traits of each mature tree (tree girth, tree height, China. This site has the largest natural population of T. fruit amount, canopy density, and crown width) were chinensis in China (approximately 490 adults, distributed also measured (Fang et al. 2009). in the evergreen broadleaf forest), including 200 trees To determine the role of bird and plant traits in seed that are older than 500 years. A national forest garden of removal, we first compared mean foraging frequency 15 ha was established by the government in 2003 to pro- and mean foraging amounts of each bird species. A seed tect these endangered trees; owing to their long-term dispersal interaction was built based on foraging fre- human use, the vegetation around the forest garden is quency of birds. We also used ANOVA test to compare highly fragmented. The remnant evergreen broad-leaved mean foraging frequency and mean foraging amounts forest patch interlaced with bamboo patches and mixed among three forest patches. The number of seed re- bamboo and broad-leaved patches to form a fragmented moval events in the habitats was explained by the gener- forest. The most important tree species in the remnant alized liner mixed model (GLMM), where bird trait was evergreen broad-leaved forest is T. chinensis (Fig. 1). a factor and study years and their interaction term the random factors. We used the glmer function in the lme4 Seed removal across different patches R package Ver. 3.1.2 for the analysis. Since the number To compare seed removal across bamboo patch, mixed of seed removal events is a count data, the models were bamboo and broad-leaved patch, and evergreen broad- fitted with a Poisson distribution.
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