Biodivers Conserv (2013) 22:1965–1989 DOI 10.1007/s10531-013-0521-5

ORIGINAL PAPER

Linking vegetation structure and organization: response of mixed- bird flocks to forest succession in subtropical China

Qiang Zhang • Richou Han • Zhongliang Huang • Fasheng Zou

Received: 18 June 2012 / Accepted: 21 June 2013 / Published online: 4 July 2013 Ó Springer Science+Business Media Dordrecht 2013

Abstract As forests undergo natural succession following artificial afforestation, their bird assemblages also change. However, interspecific avian social organization associated with forest succession has not been fully understood, particularly for mixed-species bird flocks. To disentangle how mixed-species flocks change as a function of local forest structure, we analyzed flock characteristics (particularly species richness, flocking fre- quency and propensity) and vegetation physiognomies along a presumed successional series (early, middle, and advanced) simultaneously in subtropical forests in southern China. As hypothesized, monthly point counts demonstrated that complexity of flocks increases with the progression of natural forest succession at a local scale. Advanced forests differed significantly from pioneering plantations with respect to vegetation structure, flock characteristics and constituents (especially for understory specialists). Importantly, forest succession affected flock patterns particularly in relation to the flocking propensity of regular species, and the frequency of nuclear species (Huet’s fulvetta Alcippe hueti), which in turn determined flocking occurrence at different successional stands. Canonical correspondence analysis indicated that understory flocking species (mainly Timaliidae babblers) were significantly associated with intact native canopy cover, com- plex DBH diversity, as well as high densities of dead trees and large trees, representing a maturity level of successional stands. Our study reveals that the effect of natural forest succession on mixed-species bird flocks is species-specific and guild-dependent. From a conservation perspective, despite a high proliferation of pine plantation in southern China, priority should be placed on protecting the advanced forest with a rich collection of understory flocking specialists.

Q. Zhang R. Han F. Zou (&) Guangdong Entomological Institute/South China Institute of Endangered , No. 105, XinGang West Road, Guangzhou 510260, China e-mail: [email protected] Q. Zhang e-mail: [email protected]

Z. Huang South China Botanical Garden, Chinese Academy of Science, Guangzhou 510650, China 123 1966 Biodivers Conserv (2013) 22:1965–1989

Keywords Flock characteristics Forest succession Mixed-species bird flock Nuclear species Southern China

Introduction

Most native subtropical forests in southern China have experienced severe exploitation and conversion to monocultures during the last century, leading to degradation and loss of biodiversity (Zhang et al. 2000; Liu et al. 2003). In these degraded sites, two contrasting processes of vegetation restoration are passive secondary succession and active refores- tation with native trees or timber plantations (Peng 2003). As forests undergo successional changes after major disturbance events, their bird assemblages also change (Dı´az et al. 2005; Barlow et al. 2007; Ding et al. 2008; Hingston and Grove 2010; Rey-Benayasa et al. 2010). Our understanding of interspecific avian organization associated with ecological vegetation succession is limited yet. Such information would be important because subtle changes in interactions between species of a region could have cascading effects on its avifauna (Terborgh et al. 2001; Sridhar and Sankar 2008). Mixed-species bird flocks represent a common social organization in forest bird com- munities worldwide, that provides foraging and anti-predation benefits (Moynihan 1962; Powell 1985; Greenberg 2000). Species richness, flocking frequency and flocking pro- pensity are representative indices used to characterize mixed-species flocks (Morse 1970; Munn and Terborgh 1979; Pomara et al. 2007). And flock characteristics mainly depended on environmental factor through species requirements (‘‘species co-dependency on envi- ronmental variables’’: Hutto 1994), and on mutualistic organization between species (‘‘interspecific interactions’’: Hino 1998). For example, in the Old World tropics, flocking species with specialized ecological traits (e.g. primary forest and understory microhabitat specialization) are more vulnerable to habitat disturbance, either through changes in fre- quency or in flocking propensity of the species (Lee et al. 2005; Sridhar and Sankar 2008; Peron and Crochet 2009); while, in the Neotropics, forest degradation increases the detectability of predators, and therefore reduce flocking propensity, which are mediated by mutual habitat dependencies or species-specific interactions within flocks (Latta and Wunderle 1996; Thiollay 1999). Furthermore, flocks become less cohesive after the dis- appearance or low occurrence of nuclear species in fragments of Atlantic forests (Maldonado-Coelho and Marini 2000, 2004). Thus, by altering vegetation structure and composition, the extent of secondary forest succession may influence the aggregation of flocks at different serial stages. Forest succession is a fundamental ecological process which can ameliorate stand conditions and microclimate factors, and change vegetation physiognomy and floristics (Shugart 1984; Guariguata and Ostertag 2001). Vegetation complexity has long been known as a significant factor influencing bird communities, including species composition, diversity, and local abundance (MacArthur and MacArthur 1961). In instances where bird species are associated with specific vegetation structure, it may be related to provision of specific resources such as invertebrates, seeds, fruits and nest sites or preferred micro- habitats for foraging (Wiens 1989; Helle and Mo¨nkko¨nen 1990). However, despite the fact that mixed-species flocks are a clearly defined subset of the local avifaunas, the ecological consequences of woodland structure on the occurrence and characteristics of flocks across successional stands is not well understood. Indeed, responses of flocks to advancing forest

123 Biodivers Conserv (2013) 22:1965–1989 1967 serial stages over time vary widely, possibly because mechanisms are scale-dependent and species-specific (Croxall 1976; Maldonado-Coelho and Marini 2000; Kotagama and Goodale 2004). Therefore, the identification of preferred elements of vegetation physi- ognomy and their relationships to flock characteristics will advance our understanding and may inform avian conservation and forest management practices. The subtropical monsoon evergreen forests are important for their high biodiversity and critical role in watershed protection in southern China (Zhou et al. 2006, 2007). Unfor- tunately, these regional climax forests were severely damaged by large-scale deforestation and land use change during the 1960s. They now exhibit marked variability along suc- cessional gradients (temporal scale). In order to restore forest ecosystems, a large-scale reforestation and reclamation program (mainly Masson pine plantation) was launched in the late 1980s in Guangdong Province. During natural succession of forests in subtropical China, concern that bird assemblages change as species that inhabit newly disturbed plantations are progressively replaced by those favoring regional climax forests has been noted (Zhou 1986; Zhang et al. 2011; Zou et al. 2013). Due to the extensive proliferation of pine plantations and regeneration of mixed forests over time, it may be advantageous to study bird social organization response, such as mixed-species flocks to forest succession. In addition, characteristics of mixed-species flocks might be an effective ecological indi- cator of forest disturbance and restoration (Maldonado-Coelho and Marini 2004; Lee et al. 2005). In this study, we evaluate flock characteristics and vegetation structure in three habitat types, including Masson pine forest (PF), pine-broadleaved mixed forest (MF), and sub- tropical monsoon evergreen broadleaved forest (MEBF). These systems are well main- tained at Dinghushan Nature Reserve, and provide a controlled model for the study of changes in mixed-species flocks along a natural successional gradient (early, middle, and advanced stages). The specific objectives of this study were: (1) to determine differences in species richness, flocking frequency and propensity to form mixed-species flocks, among different successional stage forest stands; (2) to assess the role of nuclear species in maintaining the cohesion of flocks among different sites; and (3) to define specific structural components of forests that create bird habitats and promote flock organization.

Methods

Study area

The study was conducted in the Dinghushan Nature Reserve (DNR) in the mid-west of Guangdong, China (112°3003900–112°3304100E, 23°0902100–23°1103000N). DNR located west of the Pearl River Delta, is one of the most densely populated and industrialized areas in China. The reserve is hilly with an altitude varying locally between 100 and 700 m, with an area of 1155 ha. The region is characterized by typical subtropical monsoon climate, with an annual mean temperature of 21.4 °C and mean relative humidity of 80 %. The mean annual precipitation of 1,927 mm is distributed seasonally, with the rainy season from April to October and the dry season from November to March (Mo et al. 2006; Yan et al. 2009). Because of its geographical location and diverse vegetation types, the reserve is referred to as an ‘oasis of the Tropic of Cancer’ (Zhou et al. 2007). The nature reserve, the oldest in China, was established in 1956 with the objective of protecting southern sub- tropical monsoonal evergreen broadleaf forest. It is also an ‘Important Bird Area’ in China

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(BirdLife International 2004), with 214 bird species identified and documented (Vaughan and Jones 1913; Liao 1982; Zhang et al. 2011). There are three dominant forest types in DNR: MEBF, MF and PF. They represent a sequence of successional stages from climax to pioneer vegetation communities, and have different land-use histories (Kong et al. 1993; Peng and Wang 1995). The advanced MEBF has been well protected from anthropogenic disturbance for more than 400 years by Buddhist monks, and is the representative forest of the lower subtropics in China. The rehabilitated MF has existed for 60 years and originated from a planted PF that was naturally colonized by broadleaf species. The pioneering PF was originally planted in the 1930s and has been under constant human disturbance, generally including harvesting of understory and litter (Wang et al. 1982; Peng and Wang 1995). For more detailed description of forests characteristics in DNR, refer to Zhang et al. (2011).

Observation of mixed-species bird flocks

A mixed-species flock is a roving group of individuals from at least two species, moving in concert and behaving cohesively while foraging, usually staying within 25 m of each another for at least 5 min (Powell 1979; Hutto 1987, 1994). Fieldwork was conducted monthly from March 2008 to February 2009. Six transects were established, two in each forest type, with each transect consisting of 10 sampling points at least 200 m from the next nearest point. Timed point counts (10 min) were used to estimate abundance of all species, including those in mixed-species flocks, intraspecific flocks, and solitary indi- viduals. Observations were initiated at sunrise and terminated before 11:00 in good weather (i.e. no precipitation or mist). To reduce the possibility of encountering a given individual or flock more than once, transects were not repeated during a survey period, and the 10 points of each transect were surveyed in the same day. At each 25 m radius plot, two people simultaneously counted all seen and heard during the 10 min. When a flock was visually detected, we determined the species composition, and the number of indi- viduals of each species. If possible, behavioral activities were also recorded (e.g. which birds ‘lead’ the flock and which ones ‘follow’, foraging substrates and behaviors). We calculated mean number of detections for each flocking species per 25 m radius plot. To verify independence of samples from each point, we compared mean detections of flocks recorded in the same point with flocks recorded in the whole transect, and found no significant differences (following Latta and Wunderle 1996).

Measurement of vegetation structure

To determine whether flock participation was associated with specific vegetation structure, the following variables were measured within a 5 m 9 5 m quadrat around the bird count points: (i) diameter at breast height/DBH and height of all tree species (woody plants with DBH [1 cm, defined as 1.3 m); (ii) percentage of tree canopy cover (CANCOV), using a spherical densitometer, following Lee et al. (2005); (iii) percentage of shrub cover (SHRUBCOV, woody plants with DBH\1 cm) and percent herb cover (HERBCOV, non- woody plants with height \1 m), visually estimated by two independent observers; (iv) abundance of dead trees (NTD); (v) leaf litter depth (LLD, average of 10 readings from 10 random locations using a ruler). For statistical purposes, the DBH distribution was assigned to one of five classes: 1 and 10 cm (D1–10), 10 and 20 cm (D10–20), 20 and 30 cm (D20–30), 30 and 40 cm (D30–40), and[40 cm (D [ 40). The surveys were conducted at least 10 m away from the birding transects, which were approximately 1 m wide on 123 Biodivers Conserv (2013) 22:1965–1989 1969 average. Although vegetation sampling plots were of 5 m 9 5 m quadrat, we assumed that they correctly reflect vegetation structure within the bird count points of 25 m radius.

Data analyses

Flock categories and characteristics

Based on previous research in DNR, flocking birds were categorized as ‘forest-dependent specialists,’ ‘forest generalists,’ and ‘non-forest species’, and then assigned to one of five habitat-use guilds, namely ‘canopy-foliage users,’ ‘bark-searching users,’ ‘mid-story generalists,’ ‘understory bird,’ and ‘shrub users’. Combining observations from all surveys at each sampling point (including intraspecific flocks, pairs and solitary individuals), flocking frequency and propensity for each species was estimated. Flocking frequency of a species was defined as the percentage of all mixed-species flocks across all habitats within which it was represented, while flocking propensity of a species as the percentage of individuals in flocks divided by the total number of foraging birds sighted in all point counts (Latta and Wunderle 1996; Thiollay 1999). Species with a flocking frequency of more than 25 % were considered regularly-flocking species. Nuclear species were defined as the most frequently encountered species across habitats (‘‘quantitative’’ criteria), dis- played intraspecifically gregariousness with high flocking propensity, and had loud con- tinuous vocal and active foraging behavior (‘‘qualitative’’ criteria) (Moynihan 1962; Latta and Wunderle 1996). In this study, 23 species occurred in at least three flocks from all forests (with more than 2 % flocking frequency), and were used in analyses of flocking propensity and species-environment relationship.

Statistical analysis

Since flock participation respond to variation in habitat structure due to presence of more diverse microhabitats and foraging resources, we compared differences in vegetation variables among three forest stands. We quantified 18 vegetation attributes at each sam- pling quadrat, and grouped them into two categories: structural physiognomy and com- positional floristics. The former includes 14 variables: no. trees higher (NTH) and lower (NTS) than 10 m; no. trees samplings with DBH more (D [ 1) and less (D \ 1) than 1 cm; no. trees with five DBH classes (D1–10, D10–20, D20–30, D30–40, D [ 40); NTD; LLD; CANCOV; SHRUBCOV and HERBCOV. And the latter consists of tree species richness (TSR), proportion of broadleaf tree (PBT), and the Shannon-Wiener index for tree species diversity (H0 TS) and tree DBH diversity (H0 DBH). For flock characteristics, we analyzed species richness (mean number of flocking spe- cies), flock size (mean number of individuals), and total number of species (considering all flocks observed) present in each forest stand separately. The relative abundance of each guild was analyzed to determine forest-dependency and habitat-use of flocking birds. The flocking frequency and propensity were calculated by species-specific and habitat-depen- dent. Seasonal changes were based on temporal dynamic of species and individuals across 12 month, while flocking frequency and propensity were also analyzed separately between dry and rainy season. To determine if sampling effort (i.e., number of flocks and indi- viduals) was sufficient for each stand, we constructed a sample-based rarefaction analyses implemented with EcoSim7.0 (Gotelli and Entsminger 2006). For statistical corroboration, we tested for differences in all flock characteristics among three forests, followed by a multiple comparison test. 123 1970 Biodivers Conserv (2013) 22:1965–1989

In the analysis of the relationship between flocking species and existing explanatory variables, we constrained the ordination of a matrix of bird abundance by a direct gradient technique on vegetation variables in a second matrix using canonical correspondence anal- ysis (CCA). To improve the level of independence between explanatory variables, we ran a Pearson correlation on 18 physiognomic variables. The correlated variables (Pearson cor- relation coefficient [0.5) formed six groups and only the most biologically meaningful variable from each group was retained for subsequent analyses. These were CANCOV, HERBCOV, DEAD, NTH, D30–40, and H0 DBH. CCA can be represented by joint biplots of the species and site ordination scores in which quantitative environmental variables are depicted as arrows (distance and angle of species scores from the center point on the plot indicate strength of environmental preferences), and the most important variables load most highly on the first axis (Palmer 1993). The significance of the CCA ordination was assessed by Monte Carlo permutation test (with 499 randomizations). To optimize the representation of flocking species, axis scores were rescaled using inter-species distances and biplot-scaling. Data on flock characteristics and habitat variables were tested for normality using the Kolmogorov–Smirnov test and were log transformed to achieve a normal distribution, and then compared with One-way ANOVA (followed by Tukey test) or Independent sample t tests. Bivariate coefficients were calculated with Pearson correlation. Statistical analyses were conducted using the statistical package STATISTICA 7.1 (StatSoft 2007). Forward stepwise multivariate direct gradient analysis was performed using CCA in CANOCO 4.5 (ter Braak and Sˇmilauer 2002). All curves and columns were plotted using OriginPro8.SR3.

Results

Vegetation structure

Forest stands differed in vegetation structure across serial stages. Most physiognomic vari- ables increased with a natural successional gradient, except for D20–30, D10–20, HERBCOV and SHRUBCOV (Table 1). Advanced MEBF had greater canopy cover than other stands (F2,59 = 16.243, p \ 0.001), with a broad DBH distribution (large canopy emergents[40 cm DBH), and frequent interlayer plants (lianas and epiphytes). However, the understory shrub cover in MEBF was significantly lower than in other forest stands (F2,59 = 17.326, p \ 0.001). Rehabilitated MF was the most