Characteristics of tropical human-modified forests after 20 years of natural regeneration

Study plots

We chose two human-modified forests in Meinong District in Kaohsiung City, and one reference plot in the Nanjenshan Reserve in Pingtung County (Fig. 1). Both human-modified forests experienced negligible human disturbances since 1992. The reference primary forest, Nanjenshan Reserve, has been designated as a nature reserve since 1982.

The mean temperature in Meinong District is 24.0 °C (Central Weather Bureau 2014). The rainy season occurs from May to September. During this period, about 89% of the annual rainfall accumulated in the area. The lowland human-modified forests surrounding Meinong (295–650 m a.s.l.) are ecological buffer zones between human development and montane primary forests in the Central Mountain Range. In addition, mountains surrounding Meinong District shelter the human-disturbed forests from typhoon disturbances. Thus, exotic tropical timber species, such as those in the family of Dipterocarpaceae, were able to reach their natural heights of more than 30 m.

The first human-modified forest is an exotic species-poor plantation, Yellow Butterfly Valley (YBV; 120°35′33″E, 22°55′58″N). The area of YBV is 2805 ha (Chen 2013). YBV is a plantation where approximately 6 non-native timber and fruit tree species have been widely planted. Thus, the forest is relatively poor in its richness of non-native tree species. The name Yellow Butterfly Valley (YBV) is adopted by the local people referring to the yellow butterflies (Catopsilia pomona) which are attracted by the widely planted exotic tree, Senna siamea (Chen 2013). Based on our interviews with local farmers and researchers, YBV has experienced two intensive tree planting events. The first intensive period (from 1936 to 1945) was during the Japanese occupation. Two non-native timber trees, namely Senna siamea, and Tectona grandis, were extensively planted. The second intensive planting period was from 1949 to 1975, when the Taiwan Forestry Bureau enforced the rent afforestation policy. Fruit trees, including Mangifera indica, Litchi chinensis, Euphoria longana, and Bambusa spp., were commonly planted for afforestation and non-timber forest products. Based on land use policy amendment (Huang 2002) and local interviewees, logging activities eased around the late 1970s, reflecting the alteration of local economic activity. In 1992, some parts of YBV had additional plantations of Mangifera indica in order to receive governmental compensation for the Meinong reservoir plan (Meinung People’s Association 1994; Tsai et al. 2013). These Mangifera trees were not managed after planting because the reservoir construction plan was stopped by local people (Meinung People’s Association 1994). Thereafter, YBV has become a natural sightseeing attraction, especially for its yellow butterflies, with negligible human logging disturbances.

The other human-modified forest is an exotic species-rich arboretum, Shuanghsi Tropical Botanical Garden (STBG; 120°36′3″E, 22°56′10″N). STBG is adjacent to YBV and its area is 7.56 ha (Yang et al. 2010). STBG was originally known as the Meinong Twin Creek Arboretum which has high richness in exotic tree species. In 1935, 270 tree species were planted for the purpose of cultivating tropical non-native forest timber species (Yang et al. 2010). Chang (1970) found that majority of the originally planted species were not able to adapt to the environment in STBG, and by 1968 only 97 non-native species survived (Chang 1970). In 2008, the recorded non-native species in STBG was even lower, with only 75 non-native tree species (Yang et al. 2010). In 2008, the dominant (based on basal areas) non-native species in STBG included Swietenia macrophylla, Spathodea nilotica and Terminalia calamnsanai (Yang et al. 2010). Concurrently, more than 46 naturally recruited native tree species have been recorded, such as Schefflera octophylla, Ficus irisana, and Machilus zuihoensis (Yang et al. 2010). STBG was officially opened to public visitation in 1987 (Chuang 2013), and since then it has been jointly managed as a recreation park by the Taiwan Forestry Bureau and the local community (Chuang 2013).

The reference plot is within the Nanjenshan Reserve, namely Nanjenshan Plot I (NPI; 120°50′51″E, 22°04′54″N) (Fig. 1). Its elevation ranges from 224 to 275 m (Chao et al. 2010a). NPI was established in 1993 (2.1 ha in size) for the purpose of long-term ecological research (Chao et al. 2010a). The mean annual temperature is 22.7 °C and the mean annual rainfall is 3252 mm, without a dry season (Chao et al. 2010b). Tree census of NPI has been conducted every 7–9 years since its establishment (Chao et al. 2010a). The forest in NPI is a tropical lowland rainforest which was classified as a Ficus-Machilus zone (Hsieh et al. 2000). A more recent study categorizes the NPI forest as a tropical foothill evergreen broad-leaved forest, which is in a Dysoxylum–Machilus zone (Li et al. 2013). The major difference is that the Ficus–Machilus zone describes the overall lowland forests in Taiwan (Su 1984), whereas the Dysoxylum–Machilus zone is only the lowland forests confined to southern Taiwan (to the south of 23.2°N) (Li et al. 2013).

The reference primary forest is the least disturbed lowland tropical primary forest in Taiwan (Editorial Committee of the Flora of Taiwan 1994–2003), and it has long-term census records (Chao et al. 2010a). However, the reference forest is not a perfect control because it is located approximately 130 km away from the studied human-modified forests, and it has no dry season. Nevertheless, we adopted NPI as a reference forest for the following reasons: (1) There was no lowland primary forest in Meinong (Weng 2013). (2) Based on the vegetation classification scheme in Li et al. (2013), the potential tropical foothill evergreen broad-leaved forest in Taiwan is to the south of 23.2°N. Both Meinong District (22.9°N) and the Nanjenshan Reserve (22.1°N) are within the range. (3) All the three plots are relatively sheltered from the impacts of typhoon [a crucial disturbance type for vegetation in Taiwan (Lin et al. 2010)]. Therefore, although the reference plot was not perfect, it is able to give some insights into the forest structure and composition of potential primary forests. We did not intend to imply that the Nanjenshan forests would be the final successional forest for the two human-modified forests. Rather, the reference plot was used to provide a basal line for the comparison of diversity and regeneration status between the two human-modified forests.

Quadrat sampling

For each of the human-modified forest, 4 transects were set up in July 2013. The distance between transects was at least 90 m and each transect had 4 quadrats. Therefore, a total of 16 quadrats (each size 10 m × 5 m) were sampled in each of the study plots (Loo 2015). In order to minimize environmental variations, we placed transects with aspects of approximately 300° and slope angles <40°. The quadrats were set up along a human accessibility distance gradient (from trail/river side into forest interior) at 10 m intervals. Some quadrats (n = 5 out of 32) did not follow the 10 m interval rule as we attempted to avoid steep slopes (>40°), hill top, and forest light gaps. These heterogenetic microenvironments were not considered in our study (Loo 2015).

In the Nanjenshan primary forest, we selected 16 quadrats (at 10–15 m intervals), measuring 10 m × 5 m. These quadrats were confined to those located in aspects at approximately 300° and slope angles <40° in the Nanjenshan Plot I (Loo 2015).

Data collection

We conducted tree censuses of the human-modified forests in July and August 2013. We used tree census data of NPI conducted in 2008. Vegetation data, including tree species, height, and DBH (diameter at breast height), were collected for evaluating forest structure, diversity, and composition. All trees ≥1 cm DBH in the selected quadrats were measured. Plant identification and nomenclature were based on Flora of Taiwan (Editorial Committee of the Flora of Taiwan 1994–2003) with three exceptions. (1) Radermachera sinica was misspelled as Radermachia sinica in Li (1998). Our study used its correct name according to International Plant Names Index (2005). (2) Glochidion ovalifolium was not recorded in Flora of Taiwan. We followed the name of this species in Lu and Hsu (2003) and Hsu et al. (2006). (3) The familial classification of the recorded species were updated with APG IV system (The Angiosperm Phylogeny Group 2016).

Data analysis

Forest structure

Forest structures (frequency of height and size classes) of the three plots were quite similar (Fig. 2). However, overall stem densities were quite high in the human-modified forest plots (6162.5 and 5812.5 individual ha⁻¹; Table 1). The maximum canopy height in STBG was the tallest (30 m), while the maximum canopy height in NPI was the shortest (13.5 m). The high canopy height in STBG was attributed to the non-native timber species at the height class 4 (height >20 m), including Hevea brasiliensis, Sindora cochinchinensis, Swietenia macrophylla, and Tectona grandis. Notably, the quadrats in the primary forest (NPI) did not have any trees at the height class 4 (Fig. 2a). Although NPI had the shortest maximum canopy height, it had the largest tree size among the three forests (DBH = 121 cm, Bischofia javanica).

Indices	NPI	YBV	STBG
Basal area (m2 ha−1)	45.4	39.2	39.0
Density (stems ha−1)	4475.0	6162.5	5812.5
Density_saplings (stems ha−1)	3862.5	5550.0	5037.5
Density_native saplings (stems ha−1)	3862.5	4750.0	2525.0
Species richness	45	40	52
Species richness_saplings	39	38	47
Species richness_native saplings	39	33	34
Effective species number	22.7	22.0	22.8
Effective species number_saplings	19.3	20.4	19.9
Effective species number_native saplings	19.3	18.7	17.2
Evenness	0.50	0.55	0.44
Evenness_saplings	0.49	0.54	0.42
Evenness_native saplings	0.49	0.57	0.51

Indices based on species native to Taiwan were noted with “_native”. Indices based on DBH (diameter at breast height) size class 1: ≥1 and < 10 cm were denoted with “_saplings”. Abbreviations of study plots please refer to Fig. 1

All the study plots showed a similar proportion (86–90%) of saplings (size class 1; ≥1 and <10 cm; Fig. 2b). However, the proportion of native saplings was higher in YBV (86% out of 5550.0 sapling individuals ha⁻¹) than in STBG (50% out of 5037.5 sapling individuals ha⁻¹) (Fig. 3; Table 1), indicating a poor regeneration status of native sapling numbers in STBG.

Species diversity

In general, species diversity indices were similar for all the three plots (Table 1). Notably, when sampling efforts of individual numbers were standardized, STBG had a higher average number of native saplings and steeper slopes of rarefaction curve than YBV (Fig. 4a). For quadrat rarefaction curve, STBG also had a steeper slope for native sapling species than YBV (Fig. 4b).

Species importance values

Similarity indices

Structure, diversity, and composition status

The structure of the two human-modified forests was comparable to that of the primary forest. However, their species compositions, especially in terms of quantity (Table 3), were not. As such, comparing just the forest structure may result in a misleading conclusion about forest naturalness, as mature secondary forests and primary forests are indistinguishable by structure (Richards 1952; Chazdon 2014). However, compared with the primary forest plot, the human-modified forest plots had high stem densities (Table 1), suggesting that they were both in a developing stage. Their reverse J-shaped distribution of diameter classes (Fig. 2b) signified the potential of the human-modified forests to have a certain degree of natural regeneration.

Although the diversity indices seemed similar between the two human-modified forests (Table 1), patterns of rarefaction curves were different. In the 1970s, the diversities of non-native overstorey tree species differed for the two human-modified forests (about 97 exotic species in STBG and 6 exotic species in YBV). Even so, the two forests are adjacent to each other, and thus the capacity of native species pool should be similar. After abandoning the original management practices and allowing free competition for more than 20 years, their composition was converged in terms of the quality of native saplings species (S _s  = 75%), but not in quantity (IS _mo  = 49%) (Table 3). Notably, species richness of native saplings at STBG for an equivalent number of individuals is higher and with a steeper slope than that of YBV (Fig. 4a). The results demonstrated the potential for STBG to harbor more native species than YBV. In contrast, the overall richness of YBV leveled off faster than STBG (Fig. 4b), showing high species evenness but low potential to harbor more native species. Therefore, we propose that a species-rich plantation has a potential to harbor more native species if allowing more native individuals to grow.

The differences in native sapling diversity patterns are likely to be due to their original overstorey species composition (Parrotta 1995; Heinrichs et al. 2016). Previous studies have found that some exotic overstorey trees may hinder the regeneration of native saplings, whereas some may catalyze it (e.g., Parrotta 1995). Although we currently do not know which exotic species in our study forests had positive or negative effects on native sapling regenerations, we propose that the original overstorey diversity can be a crucial factor for natural regeneration. This is compared with the possible influences of a monoculture exotic species plantation. In a monoculture exotic species plantation, its effects on native saplings would be relatively monotonic, either negative (inhibition or competition), neutral, or positive (facilitation). However, in an exotic species-rich plantation, the overall effect is a combination of any possible inhibition, competition, or facilitation effects from the overstorey composition. Thus, it is likely that at the forest-level, a higher diversity of native saplings can be observed in a species-rich plantation than in a species-poor plantation. In other words, a diverse species overstorey (such as arboreta and agroforestry sites) may be able to support and nurse more native species.

Although our sample size is not large, we found that all the curves had leveled off (Fig. 4). This means that we have reached an asymptotic richness and dominant species have been sampled (Gotelli and Colwell 2001). Moreover, the top 20 species accounted for more than 78% of the IV (Table 2), suggesting that those non-recorded species are likely to be rare species. For example, some native species in YBV and STBG were not recorded in the selected quadrats in NPI but they were recorded in the census data in 2000 and in 2008 in the Nanjenshan Plot I. These species are: Machilus japonica var. kusanoi, Machilus zuihoensis, Ficus irisana, Ficus superba, Ficus virgata, Morus australis, and Champereia manillana. They all have low relative density in Nanjenshan Plot I (<1% relative density (RD); Chao 2001; Chao et al. 2010a). Thus, a small sample size can influence the composition results, but such an influence would be mainly on rare species.

Management implications for native species

It is important for managers to be aware of the regeneration status of native species in human-modified forests as this determines the structure and composition of future communities (Chazdon 2014). The recruitment of native species in human-modified forests are likely to be from the surrounding remnant secondary forests, or the dispersal of seeds from other areas by wind or small animals (Parrotta 1995). Chazdon (1998) proposes that human-modified forests can be a biodiversity cornucopia. The on-going regeneration of native species found in the two human-modified forests supports the concept. Our results show that both YBV and STBG harbored species of the Ficus-Machilus vegetation type, which was once widespread in the lowland areas of Taiwan (Editorial Committee of the Flora of Taiwan 1994–2003). The diagnostic species for lowland tropical forests of Taiwan (Chiou et al. 2009; Li et al. 2013) can also be found in the two human-modified forests, including Dendrocnide meyeniana, Champereia manillana, Bischofia javanica, and Ficus irisana. The results demonstrate that these human-modified forests are acting as refuges for the remnant native biodiversity.

Remarkably, two taxa (Litsea akoensis var. chitouchiaoensis and Glochidion ovalifolium) recorded in YBV and STBG are rare and endemic species to central and southern Taiwan (Editorial Committee of the Flora of Taiwan 1994–2003; Hsu et al. 2006). The type specimen of Litsea akoensis var. chitouchiaoensis was collected in Chitouchiao village, which is adjacent to STBG and YBV (Liao 1982; Editorial Committee of the Flora of Taiwan 1994–2003). Glochidion ovalifolium was recorded only in the Chiayi County (Hsu et al. 2006), and its southern distribution in YBV was first documented by our study. These findings further support the conservation values of human-modified forests as biodiversity refuges, especially when primary forests are not available in the surrounding locality.

Although forests of YBV and STBG may not develop into the same type of forests as NPI, the comparison between the primary forest and the human-modified forests could provide some insights into conservation decision making. For example, the density of native saplings is still relatively low in STBG (Table 1). As there are no remnant primary forests within close proximity to Meinong (Weng 2013), it is critical to develop a list of species suitable for reintroduction to the area. After examining the species composition in NPI and their distribution range in Taiwan (based on Editorial Committee of the Flora of Taiwan 1994–2003), we have identified some possible native species for reintroduction. For example, we can introduce Michelia compressa, Ardisia sieboldii, and Ilex rotunda (the dominant species listed in Chiou et al. 2009; Li et al. 2013) to assist the recovery of YBV and STBG forests toward primary species composition. Other species, such as Dysoxylum hongkongense in NPI, are confined in the Hungchun Peninsula which would not be suitable for Meinong area. Without active management practices, the current dominance of some pioneers, such as Melanolepis multiglandulosa, Ficus septica, Ficus ampelas, and Macaranga tanarius, may persist in these human-modified forests.

Management implications for non-native species

The heritage values of exotic tropical species in STBG and YBV could be maintained with caution. For example, yellow butterflies (Catopsilia pomona) in YBV are attracted to the exotic tree species, Senna siamea (Chen 2013). The butterfly is one of the important assets for the local people to develop tourism (Tsai et al. 2013). However, we did not find any naturally regenerated Senna siamea saplings. Hence, managers could try to plant Senna siamea. The absence of naturally regenerated saplings of Senna siamea in YBV and STBG may be attributed to water deficiency during the seedling establishment stage. Kondoh et al. (2006) suggest that Senna siamea has high water efficient vessels, resulting in a fast growth rate, but also making it more susceptible to drought. The fruiting season of Senna siamea coincides with the drought period, from October to April, in Meinong. Thus, seedlings were hardly recorded (Yang et al. 2010). Our follow up observation showed that Senna siamea seeds collected in YBV germinated and established after soaking with sufficient water (LCL personal observation). However, there has been no record of successful natural regeneration of Senna siamea since 1936 (Yang et al. 2010).

While acknowledging the heritage values of exotic tropical species in STBG and YBV, managers should also be aware of the invasive potential of some exotic tree species. Trees that have regenerated and naturalized in STBG may become invasive species to primary forests in the future. For example, Sindora cochinchinensis, Markhamia hildebrandtii, Swietenia macrophylla, Spathodea nilotica, and Litsea perrottetii had individuals in size class 1 (DBH ≥1 and <10 cm) (Additional file 1: Appendix B), indicating successful regeneration and possible naturalization of these species. Yang et al. (2010) noted an increase in population size of 38 non-native species in STBG, especially Swietenia macrophylla, Spathodea nilotica, and Litsea perrottetii. Extraordinarily, individuals of Swietenia macrophylla had increased from the initially planted 373 individuals in 1935–1257 individuals in 2008 (Yang 2001; Yang et al. 2010). Special caution is urgently required to manage these naturalized non-native species.

Our study further provides evidence of the first alert that two of the non-native species in STBG, Spathodea nilotica and Markhamia hildebrandtii, have saplings recorded in YBV (Additional file 1: Appendix B). Due to no records of adult tree plantation in YBV, the two species could have been dispersed naturally from STBG to YBV, suggesting an invasive potential. The observed pattern implied that an exotic species-rich plantation is likely to introduce some invasive species in the new locality, based on the tens-rule (Williamson et al. 1986; Richardson and Pyšek 2006). One of the two naturalized species, Spathodea nilotica, is from the same genus as Spathodea campanulata, which has already diagnosed as a highly invasive tree in the Pacific region (Pacific Island Ecosystem at Risk 2010). Moreover, Spathodea nilotica has winged seeds that are likely to be dispersed by wind. The second naturalized species, Markhamia hildebrandtii belongs to the same family as Spathodea nilotica (Bignoniaceae) and it also has winged seeds. For winged-seed > 300 mg, the travel distance can be up to 100 m (Corlett 2009). Therefore, these two wind-dispersed trees have the potential to migrate from the current location into other nearby forests. The potential of this negative ecological impact needs to be further monitored.