TROPICS Vol. 22 (2) 59-66 Issued September 1, 2013

Brachystegia boehmii and floribunda facilitate the establishment of montane forest in woodland in northern

Tomohiro Fujita

Graduate School of Asian and African Area Studies, Kyoto University, Kyoto 606-8502, Japan * Corresponding author: [email protected]

ABSTRACT Sparse vegetation (i.e. savannah and woodland) interspersed with patchy forests (i.e. rain forest and montane forest) is typical of many tropical regions. Forest trees seldom establish adjacent to these sparsely vegetated areas because the adjacent vegetation is often more resistant to fire and water stress, and competition from grass species. However, these limiting factors may not apply under a closed crown due to a facilitative effect. Here the effect of a closed crown on the establishment of montane forest trees in miombo woodland in northern Malawi was determined. Environmental conditions, the number of saplings of montane forest trees and their regeneration mode were all studied. Result showed that grass cover is reduced and water stress can be ameliorated under a closed crown of Brachystegia boehmii and Brachystegia floribunda, which are the dominant trees of miombo woodland. Numerous montane forest saplings were found under the closed crown. These results indicate that a closed crown of B. boehmii and B. floribunda has a facilitative effect on the establishment of montane forest tree in miombo woodland.

Key words: , encroachment, fire, forest-savannah dynamics, montane forest tree

INTRODUCTION Witkowski 2008). In addition to the higher incidence of fires, the establishment of forest trees can also be limited by Savannah and woodland habitats interspersed with competition from grass species, water stress, and low closed-canopy forest are common in many tropical regions nutrient availability (Hoffmann 2000). (Hennenberg et al. 2006). Although major loss of forest These limiting factors, however, might not apply under area has occurred in these regions because of factors such a closed crown in savannah and woodland because of a as logging (Nepstad et al. 1999), recent studies have also facilitative effect (Hoffmann 1996, 2000). By providing documented the encroachment and expansion of forest into shade, a closed crown of savannah and woodland trees can more open vegetation types (Favier et al. 2004, Mitchard et suppress the growth of grass, leading to less frequent al. 2009, Bowman et al. 2010). Generally, forest trees occurrence of fires and less competitive conditions (Shararn seldom establish adjacent to these sparsely vegetated areas. et al. 2009). A closed crown can also improve water status Several factors can lead to the exclusion of forest trees from by reducing solar radiation (Gomez-Aparicio et al. 2005) such habitats. For example, frequent fires often exclude and by providing litter (Chambers 2001). Previous studies forest trees (Trapnell 1959, Hoffmann 2000, Shararn et al. have shown that forest trees become established under the 2009). At present, most fires in tropical regions are human- crown of savannah trees in many tropical savannah induced with a fire interval of 2–3 years (Campbell et al. ecosystems (Kellman and Miyanishi 1982, Bowman and 1996, Hoffmann 1996). Many forest trees are fire-sensitive Panton 1993, Hoffmann 1996, 2000, Shararn et al. 2009). (Trapnell 1959, Hoffmann 2000, Shararn et al. 2009), and This study focused on the role of woodland trees in the forest tree species can often expand into more open vegeta- establishment of forest trees in northern Malawi (southeast tion types under fire-exclusion conditions (Trapnell 1959, Africa). In south-central Africa, about 2.7 million km2 are Swaine et al. 1992, White et al. 2001). In habitats frequently covered with miombo woodland, which consists of disturbed by fire, the regeneration and persistence of sprouts leguminous species in three closely related genera: are essential for the establishment of trees (Bond and Brachystegia, Julbernardia, and Isoberlinia (, Midgley 2001). In many tropical forests, however, some subfamily Caesalpinioideae; Campbell et al. 1996). This species are incapable of sprouting even as mature trees region also contains patchy lowland rain forest, montane (Gould et al. 2002, Fensham et al. 2003, Mwavu and rain forest, and riparian forest, which all differ from 60 TROPICS Vol. 22 (2) Tomohiro Fujita miombo woodland in floristic composition and structure well-drained red and sandy clay loam. Most of the private (White et al. 2001). These vegetation communities within land area, with the exception of patchy montane forests, is the miombo woodland region should be considered 'forests' burnt at an interval of 2–3 years as a result of human because they have a closed canopy and sparse grass cover activity during the late dry season (September–December). in the understory, and are composed of evergreen and semi- The fire is set to clear foot paths because paths overgrown deciduous species that are not found in miombo woodland. by tall grass become difficult to traverse and dangerous due The vegetation dynamics between these forests and miombo to the presence of snakes. The montane forests are typically woodlands are unclear (White 1983). Some studies have less flammable due to the dense canopy that excludes suggested that miombo woodlands in wetter regions have grasses and maintains a more humid understory. Therefore, been maintained by human activity, particularly fire, and fire is unlikely to penetrate far into the forest. Few trees are that miombo woodlands can be replaced by forested harvested from this area of private land because it is located ecosystems when human activities are excluded (Lawton far from local villages. 1978, Kikula 1986). Although only a few studies have Data collection examined the establishment of forest tree species in miombo woodlands, a descriptive study showed that Four plots (50 m×50 m) were established on a moun- tropical forest tree seedlings grew under the crown of a tainous slope covered by miombo woodland (Fig. 1). The miombo woodland tree (Lawton 1978). The forest tree plots were located at least 100 m from the patchy montane seedlings might have become established via a facilitative forests. A fire break (1–1.5 m wide) was established for effect of the woodland tree. each plot in August 2009 to protect them from fire. The objective of this study was to show the role of the In each plot, all mature trees over 1 cm in diameter at facilitative effect provided by a closed crown of miombo breast height (DBH) were identified and measured. Each woodland trees on the establishment of forest trees in plot was subdivided into 100 contiguous quadrats (5× miombo woodland. The following specific predictions were 5 m). In each plot, 50 nonadjacent quadrats were selected tested: microenvironments under a closed crown of miombo for sampling, sequentially alternating the left and right woodland trees are mitigated (i.e., low grass cover and sides. The total number of sampled quadrats was 200 well-accumulated litter layer) to a greater extent than those (0.5 ha). found under sparse crowns and in treeless openings; more To characterise microhabitat conditions in each forest tree saplings are found under closedcrowns; and quadrat, the proportion of grass cover was estimated saplings of miombo woodland trees occur mainly in open visually in all quadrats (n＝200) using 5 % cover-class microhabitats and are established via sprouting. intervals. Litter mass was also determined because litter may positively affect seedling establishment through the amelioration of water stress (Facelli and Pickett 1991). MATERIALS AND METHODS Litter samples were collected in January 2010 (rainy season). In miombo woodland, most trees and are Study site deciduous, shedding their leaves during the late dry season The study was conducted from August 2009 to January (from August to October) (Chidumayo and Frost 1996). The 2010 on private land located in a rural zone that is managed sampling was conducted after the peak of leaf fall. Litter by the village of Ntchuka (10°58′S, 34°04′E) on the north mass was sampled in every fourth plot (n＝50). Litter was Vipya Plateau in northern Malawi. The region collected at the centre of each quadrat (50×50 cm) and predominantly consists of miombo woodland, although samples were dried at 80°C to a constant mass and then some circular montane rain forest patches exist on mountain weighed. crests (above approximately 1800 m a.s.l.) and mountainous To determine the effect of a closed crown on the slopes (1700–1800 m a.s.l.) (White et al. 2001). The size of pattern of sapling distribution, the crown cover of each these patches varies from about 100 m2 to several hectares. quadrat sampled was classified into one of three categories: The mean annual rainfall on the north Vipya Plateau open, intermediate, or dense. Open sites were defined as exceeds 1270 mm, which is distributed across a wet season quadrats lacking both standing trees and canopy cover over from December to April with a dry season from May to 5 cm in DBH. At intermediate sites, standing trees over November (Chapman 1970). The Vipya Plateau is underlain 5 cm in DBH formed a canopy that covered more than 0 % by undifferentiated basement complex rocks that are mainly and less than 75 % of the quadrat. At dense sites, standing gneisses (Chapman 1970). The soil of the study area is a trees over 5 cm in DBH formed a canopy that covered more Brachystegia boehmii and Brachystegia floribunda facilitate the establishment of montane forest trees in miombo woodland in northern Malawi 61

Fig. 1. Map of the study plots and montane forest patch. Miombo woodland surrounds the montane forest patch. than 75 % of the quadrat. The numbers of saplings was data violated the assumption of homoscedasticity. recorded in all sampling quadrats at all four plots. All tree Differences in the proportion of grass cover among crown species that occur mainly in montane forest and montane covers were compared by the nonparametric Steel–Dwass rain forest were considered montane forest trees and were multiple comparisons test. Tukey–Kramer multiple recorded (Friis 1992, White et al. 2001). As typical miombo comparison tests were used to detect differences in litter woodland trees, saplings of Brachystegia boehmii Taub. and mass and sapling density among crown covers. Within each Brachystegia floribunda Benth. (Fabaceae: Caesalpinioideae) tree group (montane forest tree and miombo woodland were recorded. These two species are the dominant trees in tree), differences in the abundance of each type of miombo woodland (White 1983) and are also the main regeneration mode (sprout-established or -established) components of the miombo woodland of this region. Within were compared using Mann–Whitney U-tests. All statistical each quadrat, all saplings of these species over 20 cm in analyses were conducted in R software ver. 2.12.2 (R height and less than 1 cm in DBH were counted. development core team 2011). To examine the mode of regeneration for saplings, root excavations were conducted in the quadrats of two of the four plots (n＝100). All saplings of the study species were RESULTS excavated, and their mode of regeneration was categorised Species composition and structure of standing trees as either seed-established or sprout-established. Seed- established saplings do not arise from lateral roots, lack the In total, 1031 individuals from 31 species of standing formation of any adventitious roots and have a tapering trees (DBH＞1 cm) were recorded in four plots (1 ha). root. Sprout-established saplings arise from lateral or Basal area (BA) was 26.0 m2 ha－1. The DBH distributions of adventitious roots. Identifying the mode of regeneration common tree species in the plots had right-skewed was not possible for six saplings at intermediate sites and distributions (Table 1), showing the typical "reverse J" eight saplings at open sites. shape. Brachystegia boehmii and Brachystegia floribunda were the dominant tree species, together accounting for Data analysis 40 % of the total BA. Monotes africanus, Uapaca kirkiana Data were checked for normality using the Kolmogorov- and Faurea speciosa were also common. All of these tree Smirnov test and for homoscedasticity using the Bartlett species are miombo woodland tree species. test. The data for the proportion of grass cover were Forty-six individuals from three montane forest tree analysed using nonparametric methods because these data species were observed in four plots: whyteana, are discrete values rather than being continuous and the melanophloeos and Syzygium guineense ssp. 62 TROPICS Vol. 22 (2) Tomohiro Fujita

Table 1. Summary of standing tree in study plots (1 ha).

－1 BA Mean DBH (cm) individuals ha 2 －1 Skewness (m ha ) (Min-Max) Top five species of BA Brachystegia floribunda 197 5.34 14.7 (1.0–41.5) 3.38 Brachystegia boehmii 137 5.04 16.8 (1.3–60.2) 4.07 Monotes africanus A. DC. (Dipterocarpaceae) 69 1.18 12.2 (1.6–29.3) 1.56 Uapaca kirkiana Muell. Arg. (Euphorbiaceae) 175 0.80 6.0 (1.0–25.4) 6.43 Faurea speciosa Welw. (Proteaceae) 83 0.77 8.6 (1.2–26.6) 3.24

Montane forest tree species Syzygium guineense ssp. afromontanum (Willd.) DC. (Myrtaceae) 16 0.04 3.9 (1.0–19.9) － (L.) Mez (Myrsinaceae) 27 0.02 2.9 (1.1–6.0) 1.88 (Hiern) F. () 3 0.00 1.9 (1.2–2.4) － A dash means that sample sizes are not enough for statistical test.

Fig. 2. Box plots showing the proportion of grass cover for the Fig. 3. Mean values of the proportion of litter mass for the three three site categories (open, intermediate and dense). See site categories (open, intermediate and dense canopy). text for site definitions. Maximum and minimum values Error bars are 1 standard error (SE). Different letters are respectively shown by the upper and lower ends of the indicate statistically significant differences at the P＜0.01 vertical bars; 75 % and 25 % quartiles are shown by the level among sites (Tukey–Kramer multiple comparisons upper and lower edges of the boxes, respectively; and the test). middle line represents the median value. Different letters indicate statistically significant differences between sites among the different categories of crown cover (Figs. 2 and at the P＜0.01 level (Steel–Dwass multiple comparisons test). 3). The lowest proportions of grass cover were found at dense sites (median＝12.5 %), followed by the intermediate afromontanum. These individuals were small, together sites (40 %) and the open sites (60 %). The proportion of accounting for less than 1 % of the total BA (Table 1). The grass cover differed significantly between sites (P＜0.01; presence or absence of fruiting of these montane trees has Steel–Dwass multiple comparisons test). The common been observed in this plot since 2009 and no individuals grass species in the study sites were Carex conferta Hochst. bore fruit until 2012. Therefore, one can speculate that ex A. Rich. (Cyperaceae), Cyperus nyassensis (Podlech) these montane forest trees had not reached the age of first Lye (Cyperaceae) and Hyparrhenia cymbaria (L.) Stapf birth and the saplings growing in the plot (see below) had (Poaceae). These grasses grew up to about 1.5 m at some of been transported from elsewhere. the open sites. At intermediate and open sites, visible signs of fire were observed before 2009, but few signs of fire Comparison of microenvironmental parameters among were noted at the dense sites. crown covers Litter mass was highest at the dense sites (mean±SE, Twenty-two quadrats were categorised as dense, 119 220.8±21.2 g) and gradually decreased at open sites (47.7 quadrats as intermediate and 59 quadrats as open sites. The ±10.5 g). Litter mass also differed significantly between tree species that comprised the closed crown at dense sites sites (P＜0.01; Tukey–Kramer multiple comparison tests). were mainly B. boehmii and B. floribunda. Litter accumulated to a depth of about 1–3 cm at dense The proportions of grass cover and litter mass varied sites. At open sites, however, less litter accumulated and Brachystegia boehmii and Brachystegia floribunda facilitate the establishment of montane forest trees in miombo woodland in northern Malawi 63

Table 2. List of montane forest tree sapling grown in sampling quadrats..

Family Species No. of sapling Life form Fruit type Fruit size (cm) Araliaceae Cussonia spicata Thunb. 1 Tree Drupe 0.6×0.6 Araliaceae Schefflera umbellifera (Sond.) 6 Tree Drupe unknown Ebenaceae Diospyros whyteana 6 Drupe 1.6×1.3 Icacinaceae Apodytes dimidiataE. Mey. 8 Tree Drupe 0.8×0.6 Myrtaceae Syzygium guineense ssp. afromontanum 127 Tree Berry 1.6×1.4 Rubiaceae Oxyanthus speciosus spp. stenocarpus (K. Schum.) Bridson 3 Shrub Berry 3.0×0.5 Rubiaceae Psydrax schimperiana(A. Rich.) Bridson 2 Tree Drupe unknown

Fig. 4. Mean sapling density of montane forest and miombo woodland trees for the three site categories (open, intermediate and dense canopy). Error bars are 1 SE. Different letters indicate statistically significant differences at the P＜0.01 level among sites (Tukey–Kramer multiple comparisons test). some quadrats were bare. 0.01; Tukey-Kramer multiple comparison tests). The mode of regeneration of montane forest and miombo Comparison of sapling density among canopy types woodland trees In total, 868 saplings of the study species (montane forest and miombo woodland trees) were found in the 200 The mode of regeneration of montane forest and quadrats (0.5 ha). Of these, 153 saplings were from seven miombo woodland tree saplings is shown in Table 3. For montane forest tree species. All seven of these montane montane forest trees, most saplings were seed-established; forest trees are animal-dispersed (Table 2). 89 % of montane forest tree saplings were seed-established The sapling density of montane forest and miombo and only 11 % were sprout-established. woodland trees observed within each crown type is shown In contrast, miombo woodland trees were mainly in Figure 4. The highest density of montane forest tree sprout-established. Ninety-three per cent of saplings at the saplings was found at the dense sites (Fig. 4A), 119 (78 % intermediate sites and 89 % of saplings at the open sites of the total) saplings occurred at the dense sites, 30 (20 %) were sprout-established. For the miombo woodland trees, saplings were detected at intermediate sites and only 4 (3 %) the number of sprout-established saplings was significantly saplings were found at open sites. The sapling density at higher than the number of seed-established saplings at dense sites differed significantly from that at intermediate intermediate sites (P＜0.01; Mann–Whitney U-test), open and at open sites (P＜0.01; Tukey–Kramer multiple sites (P＜0.01) and in total (P＜0.01). comparison tests). A different distribution pattern was observed for saplings of miombo woodland trees (Fig. 4B). The highest DISCUSSION density of miombo woodland tree saplings was observed at Establishment of montane forest trees in miombo woodland the open sites, 523 (73 % of the total) saplings of miombo woodland trees occurred at the open sites and 187 (26 %) Numerous montane forest tree saplings were found were found at the intermediate sites. Only 5 (1 %) saplings under a closed crown of B. boehmii and B. floribunda in of miombo woodland trees were found at the dense sites. miombo woodland (Fig. 4). Under the closed crown, the The sapling density at the open sites was significantly proportion of grass cover was reduced (Fig. 2) and litter had different from that at intermediate and at dense sites (P＜ accumulated (Fig. 3). Such conditions can reduce 64 TROPICS Vol. 22 (2) Tomohiro Fujita

Table 3. Number of seed- and sprout-established sapling of montane forest tree and miombo woodland tree.

Dense n (%) Intermediate n (%) Open n (%) Total n (%) Montane forest tree Seed-established sapling 57 (92) 14 (78) 0 71 (89) Sprout-established sapling 5 (8) 4 (22) 0 9 (11) p＜0.05 p＝0.31 － p＝0.11 Miombo woodland tree Seed-established sapling 0 (0) 1 (1) 29 (8) 30 (6) Sprout-established sapling 1 (100) 102 (93) 336 (89) 410 (90) － p＜0.01 p＜0.01 p＜0.01 6 sapling at intermediate and 8 sapling at open sites of miombo woodland tree can not be identified their regeneration mode.Within each tree groups (montane forest tree and miombo woodland tree), differences in the abundance of each type of regeneration mode (seed- versus sprout-established) were compared using Mann-Whitney U-tests. flammability and competition with grass and ameliorate fate of seedlings. water status (Hennenberg et al. 2006, Shararn et al. 2009). This study has shown that a closed canopy of B. These results indicate that a closed crown of B. boehmii and boehmii and B. floribunda can have a positive effect on the B. floribunda has a facilitative effect on the establishment establishment of montane forest trees in miombo woodland. of montane forest trees in miombo woodland. Similar However, the presence of a closed canopy can also have a facilitative effects have been reported in successional negative effect. For example, a thick litter layer can act as a processes (Slocum 2001, Yoshihara et al. 2010) and in the physical barrier to seed germination (Hoffmann 1996). The process of riparian forest tree encroachment into savannah closed crown can also have a cost in terms of height growth (Shararn et al. 2009). (Gomez-Aparicio et al. 2005). Future studies should dissect Hennenberg et al. (2006) reported that fires can occur both the positive and negative effects of a closed crown. frequently with high grass cover, but rarely with low grass The observation that the highest sapling density of cover. In this study, little sign of the dense sites having montane forest trees was observed at dense sites is a experienced fire was noted. Suppressed fire occurrence is reflection of not only microhabitat amelioration but also the crucial for the survival of montane forest trees because they spatial pattern of seed dispersal. All of the montane forest have a low resistance to fire (Trapnell 1959, Lawton 1978, tree saplings growing in the miombo woodland were from Kikula 1986). In Africa, including this region, fire- animal-dispersed species and likely play an important exclusion experiments have resulted in closed forest stands role in their seed dispersal (Dowsett-Lemaire 1988, Fujita (i.e., Swaine et al. 1992, White et al. 2001). unpublished data). Alcántara et al. (2000) showed that seed Low grass cover beneath the closed crown might also deposition for -dispersed species under a dense foliage reduce competition for seedlings. Several studies in tropical crown is higher than under a sparse foliage crown and in regions have shown that competition with grasses reduces open spaces. seedling survival and growth (Holl 2002, Shararn et al. Establishment pattern of miombo woodland tree species 2006). Other authors have suggested that reduced radiation In contrast to montane forest tree species, saplings of (Gomez-Aparicio et al. 2005) and accumulated litter miombo woodland trees primarily occurred at open sites (Chambers 2001) under a closed crown ameliorate the (Fig. 4B). Fire can take occur frequently at open sites due water status of seedlings. At dense sites in this study, the to the high proportion of grass cover (Fig. 2). Visible signs microenvironmental conditions included lower levels of of recent fires were observed at many of the open sites. The direct solar radiation (see data collection) and deeper high sprouting ability of miombo woodland trees can enable accumulations of litter. Therefore, the water status beneath their establishment in such microhabitats. This was the closed crown may be mitigated for montane forest trees. supported by the observation that 89 % of miombo Future studies should quantitatively examine the woodland saplings at open sites were sprout-established. In microclimatic factors (i.e., radiation, air temperature, habitats frequently disturbed by fire, the regeneration and evapotranspiration, soil moisture) and their effects on the persistence of sprouts are essential for the establishment Brachystegia boehmii and Brachystegia floribunda facilitate the establishment of montane forest trees in miombo woodland in northern Malawi 65 process (Bond and Midgley 2001). in the Australian monsoon tropics? 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