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Dipterocarpaceae) Forest Ecology and Management 256 (2008) 375–383 Contents lists available at ScienceDirect Forest Ecology and Management journal homepage: www.elsevier.com/locate/foreco Density-dependent selfing and its effects on seed performance in a tropical canopy tree species, Shorea acuminata (Dipterocarpaceae) Yoko Naito a,1, Mamoru Kanzaki a, Hiroyoshi Iwata b, Kyoko Obayashi c, Soon Leong Lee d, Norwati Muhammad d, Toshinori Okuda e,2, Yoshihiko Tsumura f,* a Graduate School of Agriculture, Kyoto University, Kitashirakawa Oiwake, Sakyo, Kyoto 606-8502, Japan b National Agricultural Research Center, 3-1-1 Kannondai, Tsukuba, Ibaraki 305-8666, Japan c Graduate School of Agricultural Science, Tohoku University, Naruko-onsen, Osaki, Miyagi 989-6711, Japan d Forest Research Institute Malaysia, Kepong, Kuala Lumpur 52109, Malaysia e National Institute for Environmental Studies, 16-2 Onogawa, Tsukuba, Ibaraki 305-0053, Japan f Forestry and Forest Products Research Institute, 1 Matsunosato, Tsukuba, Ibaraki 305-8687, Japan ARTICLE INFO ABSTRACT Article history: In the conservation and management practices of natural forests, sound reproduction and regeneration Received 14 December 2007 form the basis of the maintenance and viability of the tree populations. To obtain and serve biological Received in revised form 14 April 2008 information for sustainable forest management, we investigated reproductive biology and inbreeding Accepted 14 April 2008 depression in seeds of an important dipterocarp tree species, Shorea acuminata (Dipterocarpaceae), by both field and laboratory experiments. Results of parental analysis of immature and mature seeds Keywords: showed that selfing rates varied greatly, from 7.6 to 88.4% among eight mother trees, and the mean Flowering phenology overall selfing rate was 38.3%. Observed outcrossing events within a 40-ha study plot were Germination Inbreeding depression predominantly (76.5%) short-distance events with a mating distance (md) 100 m. Since the selfing Pollen flow rate sharply decreased with increase in the number of flowering conspecifics (i.e., individuals of the same Seedling establishment species) within a 100-m radius from the mother trees, the local density of flowering conspecifics appears Seed mass to be the key factor determining the outcrossing rate in S. acuminata. However, the extremely high selfing rate (88.4%) observed for one tree could not be simply explained by the low local density of flowering conspecifics. Instead, differences in its flowering phenology (its flowering peaked ca. a week earlier than most of the other examined individuals) may have severely limited its receipt of pollen from other conspecifics, and thus promoted selfing. Since there were no significant differences in the proportion of selfed progeny between immature and mature seed stages, there was no evidence of selective abortion of selfed seeds during seed development. However, the seed mass of outcrossed progeny was heavier than that of selfed progeny, and heavier seeds showed higher success rates at germination and seedling establishment. These results suggest that inbreeding depression resulted in reductions in seed mass and may reduce the fitness of selfed seeds in S. acuminata. In addition, the outcrossing rate of S. acuminata was more sensitive to low local conspecific flowering-tree densities than that of a sympatric bee-pollinated dipterocarp species with greater pollination distances. These results suggest that the management of local adult-tree densities is important for avoiding selfing and inbreeding depression in future generations, especially in a species like S. acuminata with predominantly short-distance pollination. ß 2008 Elsevier B.V. All rights reserved. 1. Introduction of many valuable timber tree species (Symington, 2004). In recent decades, many of the dipterocarp species in this region have been Lowland tropical forests in Southeast Asia are dominated by threatened by logging and other human activities that have Dipterocarpaceae (Ashton, 1982), a well-known family consisting critically reduced the numbers of their individuals and popula- tions. Accordingly, the sustainable management of remnant dipterocarp populations has become increasingly important for * Corresponding author. Tel.: +81 29 829 8261; fax: +81 29 874 3720. their sustainable use and species conservation. However, present E-mail address: [email protected] (Y. Tsumura). selective logging systems applied in Southeast Asia are not 1 Watami Food Service Company Limited, 1-1-3 Haneda, Ota, Tokyo 144-0043, necessarily sustainable, partly because tree ecology has received Japan. 2 Graduate School of Integrated Arts and Sciences, Hiroshima University, 1-7-1 limited consideration in the development of harvest–regeneration Kagamiyama, Higashi-Hiroshima 739-8521, Japan. protocols (see Sist et al., 2003). To reduce the gap between forest 0378-1127/$ – see front matter ß 2008 Elsevier B.V. All rights reserved. doi:10.1016/j.foreco.2008.04.031 376 Y. Naito et al. / Forest Ecology and Management 256 (2008) 375–383 exploitation practices and conservation requirements for mixed particular, the local flowering-tree density is likely to have dipterocarp forests, more biological and ecological information extremely strong effects on the reproduction of species that about dipterocarps needs to be acquired, and incorporated in depend on weak flyers (e.g., thrips) for pollination, and moderate effective forest management policies with a sound scientific basis. effects on species pollinated by strong flyers (e.g., bees). The In the conservation and management practices of natural sensitivity or robustness of the pollination system of different forests, sound reproduction and regeneration form the basis of the species can thus be assessed by comparing the effects of local maintenance and viability of the tree populations. Previous studies flowering-tree density on their mating patterns. We chose a thrip- on mating systems and pollination ecology have shown that pollinated dipterocarp species, Shorea acuminata Dyer to make a dipterocarps are predominantly outcrossing species (Bawa, 1998; comparison with the previous results of Neobalanocarpus heimii Tsumura et al., 2003) pollinated by insects (Appanah, 1979; (King) Ashton (Naito et al., 2005), a sympatric bee-pollinated Appanah and Chan, 1981; Bawa, 1998; Momose et al., 1998). For dipterocarp species in our study site to test the validity of the predominantly outcrossing species, the maintenance of high above speculation. outcrossing rates is crucial in order to avoid inbreeding depression Thus, exploring the natural variations in mating patterns, the in future generations. However, relatively low outcrossing rates causes of such variations, and the impact of inbreeding depression have been generally reported in secondary forests (i.e., forests may provide important knowledge for predicting potential threats which has re-grown after timber harvest) compared to those in associated with changes in pollination environments due to primary forests (i.e., undisturbed forests) for dipterocarp species human disturbance such as selective logging. In this study, we (e.g., Lee, 2000; Murawski et al., 1994b; Obayashi et al., 2002). sought to obtain information on the reproductive biology and Furthermore, large variations in their outcrossing rates have been inbreeding depression in a natural population of S. acuminata,an observed among individual trees, even within a single population important tropical timber tree species in Southeast Asia. More (e.g., Fukue et al., 2007; Lee et al., 2000; Lee et al., 2006; Murawski specifically, we sought to quantify key reproductive parameters and Bawa, 1994; Murawski et al., 1994a,b; Nagamitsu et al., 2001; (i.e., flowering phenology, selfing/outcrossing rates and mating Naito et al., 2005; Obayashi et al., 2002). These findings suggest patterns) and variations of the parameters in a S. acuminata that not only ecological differences at the forest-stand level, but population in a primary forest. We then addressed the following also the fine-scale heterogeneity in pollination environments, questions. (1) How does spatial and temporal isolation of flowering heavily affect outcrossing rates of dipterocarp individuals. affect selfing rates of individual trees? (2) Are there any differences Several ecological variables have been proposed as factors that in the relationships between selfing rates and the local flowering- may affect mating patterns in tree species, e.g., spatial isolation tree density between sympatric dipterocarp species with different (Fuchs et al., 2003; Oddou-Muratorio et al., 2006), flowering pollination systems? (3) Does inbreeding affect the survival of pre- phenology (Oddou-Muratorio et al., 2006), plant density (Fran- mature seed and seed mass as a result of selective abortion or ceschinelli and Bawa, 2000) and pollinator activity (Hirao et al., inbreeding depression? (5) If so, is the seed mass correlated with 2006). Among these factors, both temporal isolation (i.e., the performance of the progeny at germination and seedling differences in flowering phenology) and spatial isolation of establishment? Finally, we discuss the implications of the results flowering (low tree density) have been proposed as causes of of the study for forest management and conservation. the observed high selfing rates of dipterocarp individuals (Fukue et al., 2007; Obayashi et al., 2002). In fact, spatial isolation (low 2. Materials and methods conspecific tree densities) has increased selfing rates in some dipterocarp
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