Forests 2014, 5, 715-743; doi:10.3390/f5040715 OPEN ACCESS forests ISSN 1999-4907 www.mdpi.com/journal/forests Article Understory Structure and Vascular Plant Diversity in Naturally Regenerated Deciduous Forests and Spruce Plantations on Similar Clear-Cuts: Implications for Forest Regeneration Strategy Selection ZhiQiang Fang 1,2, WeiKai Bao 1,*, XiaoLi Yan 1,2 and Xin Liu 1,2 1 Key Laboratory of Mountain Ecological Restoration and Bio-resource Utilization, Ecological Restoration Biodiversity Conservation Key Laboratory of Sichuan Province, Chengdu Institute of Biology, Chinese Academy of Sciences, Sichuan, Chengdu 610041, China; E-Mails: [email protected] (Z.Q.F.); [email protected] (X.L.Y.); [email protected] (X.L.) 2 University of Chinese Academy of Sciences, Beijing 100049, China * Author to whom correspondence should be addressed; E-Mail: [email protected]; Tel.: +86-28-8289-0528; Fax: +86-28-8522-2753. Received: 5 December 2013; in revised form: 21 March 2014 / Accepted: 31 March 2014 / Published: 15 April 2014 Abstract: The active effect of natural regeneration on understory vegetation and diversity on clear-cut forestlands, in contrast to conifer reforestation, is still controversial. Here we investigated differences in understory vegetation by comparing naturally regenerated deciduous forests (NR) and reforested spruce plantations (SP) aged 20–40 years on 12 similar clear-cuts of subalpine old-growth spruce-fir forests from the eastern Tibetan Plateau. We found that 283 of the 334 vascular plant species recorded were present in NR plots, while only 264 species occurred in SP plots. This was consistent with richer species, higher cover, and stem (or shoot) density of tree seedlings, shrubs, and ferns in the NR plots than in the SP plots. Moreover, understory plant diversity was limited under dense canopy cover, which occurred more frequently in the SP plots. Our findings implied that natural deciduous tree regeneration could better preserve understory vegetation and biodiversity than spruce reforestation after clear-cutting. This result further informed practices to reduce tree canopy cover for spruce plantations or to integrate natural regeneration and reforestation for clear-cuts in order to promote understory vegetation and species diversity conservation. Forests 2014, 5 716 Keywords: understory vegetation; plant diversity; natural regeneration; reforestation; spruce plantation; Tibetan Plateau; generalized linear mixed-effect models (GLMMs) 1. Introduction Species composition, diversity, and structure of understory vegetation are keys to providing complex structure and conserving indigenous floras within forests [1,2]. The understory can provide habitat and food for faunal communities [3], and act as a driver of nutrient cycling [4], stand productivity [4,5], and forest regeneration and succession [6–8]. Thus, the understory community and biodiversity are focal objectives for sustainable forest management, effective forest biodiversity conservation, and successful forest restoration [4,6,9]. However, the effects of different strategic applications for forest regeneration on understory vegetation and species diversity on clear-cuts remains controversial, advocating further study [9–12]. It is a challenge for forest managers to promote forest regeneration, while conserving indigenous biodiversity in a large area of clear-cut forestlands. Natural regeneration and conifer reforestation on clear-cuts are two major regeneration strategies that have been long employed in the northwestern Sichuan Province, China [13], and globally [14]. Natural regeneration without artificial reforestation often depends on remnant vegetation, its seed pool, and dispersals surrounding vegetation and involves the synchronous development of both native trees and other plant forms together with their abiotic environment. It usually leads to a mix of tree species and unevenly-aged individuals, which exhibit connectivity among their components and are self-organized into hierarchies and cycles [15,16]. In contrast to natural regeneration, artificial reforestation schemes are designed with targets for establishing overstory structure and satisfying production demands, and they often repress vegetation with the potential to hinder target tree growth. They are also designed to achieve a stand of individuals that are even-aged and regularly spaced. Thus, artificial reforestation efforts usually do not include activities that are conducive to developing understory biodiversity [14]. This is true depending on the extent to which a site is prepared for planting, which has not been addressed [11,12,17] up to now. A substantial body of research has compared species composition and diversity between coniferous plantations and naturally regenerated forests or secondary forests worldwide (for reviews see Brockerhoff et al., 2008; Bremer & Farley, 2010) [11,12]. However, results vary and are even contradictory. Reforested plantations might have similar, or significantly lower or higher, vascular plant species richness and diversity of understory vegetation in comparison with naturally regenerated forests [10–12,18–21]. Consequently, the effects remain unpredictable and differ according to the manner and intensity of disturbance from different regeneration pathways [11,12]. The conflicting results presented in the literature regarding species richness and understory vegetation structure are due to several inconsistent factors used when making comparisons: different historical origins of previous vegetation [12], distinct initial site condition [22,23], different successional stage or forest age [16,24,25], target tree identity and mixture [10,11], and site degradation intensity and management [11,12,14,22]. To reach reliable conclusions on the effects of different regeneration methods on understory vascular plant composition and diversity requires Forests 2014, 5 717 controlling variability among study sites. Moreover, it is also necessary to consider the sampling design and the accompanying statistical methodology. During sampling design and the investigation of species composition, different scales (stand, plot, and quadrats) have long been widely used by researchers. Recently, systematical sampling has become more popular [25,26]. Quadrats are often nested plots, and plots are often nested stands during the systematical sample process. However, these data are usually not independent [27,28] and may also be non-normal. These are troubling issues for many researchers who are used to applying independent tests in their studies. The generalized linear mixed-effect models (GLMMs) is an extension of generalized linear models (GLMs), including random effects to deal with correlated data structures, in particular, with clustered structures [28,29]. This model also provides a more flexible approach for non-normal data [30]. However, it has not been widely used in studies that utilize nested data to explore differences in understory vascular plant structure and biodiversity between naturally and artificially regenerated forests [29,31]. In the current study, we aimed to evaluate the understory community structure and plant composition over the same regeneration period in two stand types: naturally regenerated deciduous forest and planted spruce forest, originating from similar clear-cuts of old-growth spruce-fir forests in the eastern Tibetan Plateau. GLMMs were applied to explore the difference of understory vegetation between the two regenerating forests. We addressed three questions: (1) Which regeneration strategies result in higher vascular plant diversity in the forest understory: natural regeneration or spruce reforestation? (2) How do the vascular plant groups (tree seedlings, shrubs, ferns, forbs, and graminoids) differ in species composition, richness, and community structure between the understory of the two forests? (3) What are the differences in structures of the overstory and understory and their relationships between the two forests? We hypothesized that: (H1) The naturally regenerated forests would host higher species diversity compared to the planted spruce forests, with woody plant diversity being the key driver of the diversity difference; and (H2) the tree canopy structure of the two forests disparately influences the structure and species diversity of the understory. 2. Materials and Methods 2.1. Study Area This study was conducted in the Aba Tibetan and Qiang Autonomous Prefecture (30°35′ N–34°19′ N, 100°30′ E–104°27′ E), which is an area of approximately 80,000 km2 in the northwestern Sichuan Province, China. This region is located in the northeastern Hengduan Mountains region, a famous biodiversity hotspot known in China and worldwide. It is also part of the Southwestern National Forest Region in China [13]. The forested elevations range from 2400 m to 3900 m, and the climate is temperate with an annual rainfall of 800–1000 mm and a mean annual temperature of 6–10 °C. The frost-free period in this region is less than 100 days. Mountain brown soil (luvisols) is the major soil type [32,33]. The old-growth coniferous forests are dominated by one to three species of firs (Abies spp.), spruces (Picea spp.), or larches (Larix spp.). They are widely distributed in the subalpine region and harbor a very high biodiversity with over 6000 species of vascular plants [13]. There is large-scale clear-cut logging in the primary coniferous forests beginning in the 1960s and ending with the Natural Forest Forests 2014, 5 718 Protection Program in 1998.