The Philippines is one of the megabiodiverse countries and is considered a priority conservation area (Turner et al. 2003). A recent flora inventory conducted across the Philippines by (Barcelona et al. 2013) reported a total of 10,107 species, which is approximately five percent of the world's known plant species. Primarily due to the economic importance of forests in Southeast Asia, many studies on the flora vegetation have been conducted throughout the Philippines (Whitmore et al. 1984); (Kartawinata 1989); (Soepadmo 1995). However, only a small number of studies have been conducted in the Philippine submontane and montane Lowland regions (Ashton 1993). These regions are one of the the last remaining Lowland fragments in the Philippines and, thus, have become the focus of conservation efforts (Heaney 1993; Penafiel 1995; Hamann et al. 1999). Negros-Panay Region, where this study was conducted, is considered one of the regions most threatened and in need of conservation efforts due to the presences of endemic, critically endangered, and functionally-extinct species (Heaney et al. 1998). Some of these are Prionailurus bengalensis (Heaney et al. 1998), Shorea negrosensis (Fernando et al. 2009), Sus philippinensis and Carlito syrichta (Mallari et al. 2001) to name but a few. One of the primary threats to this area is deforestation which has been shown to be a driver of species extinction in tropical Southeast Asia (Hughes 2017). Prime areas for deforestation within Asian tropics are the lowland forests (Turner and Corlett 1996). However, protected areas are costly and often underfunded which leads to many biologically-important areas being underprotected (Corlett and Primack 2008).

Species diversity can be influenced by many types of environmental changes (Sagar et al. 2008). Different elevations and slopes have shown to influence the species richness and dispersal of tree species (Eilu and Obua 2005). According to Sharma et al. (2009), elevation may cause a difference in the insolation period, thereby forming a range of micro-climates in multifaceted landscapes. However, this pattern of biodiversity along the elevational gradient remains relatively poorly understood, partly hindered by the perceived heterogeneous conditions. Understanding biogeographical patterns and variation in species richness and endemic trends is critical to conservation strategies in elevationally-diverse areas. Additionally, biodiversity assessments are recognised globally as a fundamental activity to sustainable biodiversity conservation (Humphries et al. 1995, Margules and Pressey 2000, Williams et al. 1995). These combined concepts lead to the present study, an investigation to extend the botanical knowledge of flora composition along elevational range Lowland communities in the context of Southeast Asia. Thus, this study was carried out to answer the following questions: (i) does plant composition changes along elevation gradient and (ii) does species diversity increase with increasing elevation?

Study site

The Balinsasayao Twin Lakes Natural Park (BTLNP) is located in Negros Oriental and is surrounded by Lakes Balinsasayao and Danao (Fig. 1). It is situated 14.5 km from Dumaguete City with a total land area of 8,016.65 hectares (80.16 km²) with elevation ranging from 750 to 1,700 m above sea level. The topography of BTLNP is generally steep, with fresh and abandoned fields occupying the flatter areas, both within and around the protected area. The lower areas, mainly around the Twin Lakes, still have extensive stands of dipterocarp lowland rainforest, as well as patches of Agathis philippinensis, the largest tree in the Philippines (which can grow up to 60 m) (Brooks et al. 1992; Heideman and Erickson 1987; Hicks 2001).

Figure 1.  

Location of the established plots (red rectangles) along the elevational gradient of Balinsasayao Twin Lakes Natural Park.

Field data collection

Analyses

Threatened species

Floristic composition and community structure

A total of 351 plant species which represents 230 genera belonging to 103 families were recorded. These species were further classified as 183 species of trees, 54 herbs, 51 shrubs, 41 ferns and 22 vines. Angiosperms dominated the area, comprising 308 different plant species, while only two species were recorded for gymnosperms (Agathis philippinensis and Dacrydium beccarii). At the family level, the top 10 most abundant taxa included Rubiaceae (20 species; 6%), Lauraceae (19 species; 5%), Moraceae (18 species, 5%), Fabaceae (14; 4%), Myrtaceae (14 species; 4%), Urticaeae (11 species; 3%), Araceae (10 species; 3%), Euphorbiaceae (10 species; 3%), Melastomataceae (10 species; 3%) and Arecaceae (8 species; 2%). Moreover, amongst the elevational gradients surveyed, sub-montane ecosystems had the highest species richness (n = 287), followed by lowland (n = 96) and, lastly, montane (n = 53).

To understand the similarity of species in response to Lowland types along the elevation gradient, a cluster analysis was performed (Fig. 2). Plots were grouped into three major clusters as a function of abundance and composition. The first cluster was plots located in the lowland Lowland and was dominated by Axonopus compressus, Nephrolepis hirsutula, Chromolaena odorata, Christella parasitica and Melastoma malabathricum. Meanwhile, plots located in the sub-montane Lowland were grouped together in cluster two. This was dominated by Pinanga insignis, Nephrolepis biserrata, Selaginella eschscholzii, Aporosa sphaeridiophora and Pleioluma firma. Lastly, cluster three, plots from montane Lowland, was dominated by Cyathea negrosiana, Freycinetia lagenicarpa, Blechnum vestitum, Tasmannia piperita and Dacrydium beccarii.

Figure 2.  

Dendogram of 18 sampling plots generated through UPGMA using Jaccard Similarity Index. Bootstraping was done at n = 1000; cophenetic correlation is 0.94. SMQ1-SMQ3 and SMQ12 are plots located in submontane (the upper part of the lake); SMQ4-SMQ11 - plots located in submontane (along the lake); LLQ1-LLQ3 are plots located in the lowland; MOQ1-MOQ3 – plots in the montane Lowland.

Species diversity and importance value

Lowland forest

The diversity estimates along the elevation gradient tend to follow this trend, high > very high > low (Fig. 3). In lowland elevations, the Shannon Diversity Index was H’ = 3.29 which can be atttributed to its fragmented vegetation under disturbed conditions. The presence of land preparation activities and agricultural farms has contributed to the removal of the Lowland cover (Pampilona et al. 2005). Consequently, pioneer and sun-loving species were accounted at this range in which agricultural crops like Cocos nucifera, Musa balbisana and Musa sapientum were also present (Suppl. material 1). Several pioneer species, such Ficus odorata, Leucosyke capitellata, Omolanthus populneus, Melicope latifolia, Macaranga bicolor, Macaranga tanarius, Ficus septica and Melastoma malabathricum, dominated the lowlands. The most common dominating species for ground cover in lowland includes Nephrolepis hirsutula, Chromolaena odorata, Christella parasitica, Nephrolepis biserrata, Lantana camara, Mikania cordata, Pteridium aquilinum and Panicum repens. These species were common in areas with high levels of sunlight, such as near agriculture and within Lowland gaps.

Figure 3.  

The Shannon Diversity and the Pielou's Evenness Indices along elevational gradient in all plant layers (A), canopy (B), intermediate (C) and ground cover (D).

Sub-montane Lowland

Sub-montane Lowland has an average diversity of H'= 4.20 which was categorised as very high, based on Fernando (2008). The canopy layer, consisiting of tall economically-important trees like Shorea polysperma, Agathis philippinensis, dominated in this Lowland (Suppl. material 2). Other frequent species that also tended to dominate were Streblus glaber, Platea excelsa, Syzygium affine, Aporosa sphaeridiophora and Phoebe sterculioides. Shorea negrosensis was found common in all types of terrain; however, it decreased in abundance at higher elevations. This trend was also observed for the other species listed. Huge mother trees of Agathis philippinensis were found only in a protected portion of the study area. It was noted that this species was very common many decades ago. The most abundant shrubs and small trees were Pleioluma firma, Euonymus javanicus, Schefflera elliptica and Pinanga insignis. Tree ferns like Cyathea contaminans and Cyathea negrosiana were also observed to be dominating in this Lowland. Ground cover was frequently dominated by several fern species, such as Nephrolepis biserrata, Christella parasitica and Selaginella eschscholzii. Dominant herb species were Aglaonema commutatum, Geophila repens and Scleria scrobiculata. The presence of Freycinetia lagenicarpa, which is a "ground-creeping" plant, was also encountered along branchlets of trees. The diversity and richness of this gradient were higher compared to lowland and montane.

Montane Lowland

This Lowland is characterised by the presence of numerous species of mosses, lichens and epiphytes. The dominant tree species was Dacrydium beccarii, while common shrubs dominating were Tasmannia piperita, Elaeocarpus argenteus, Melastoma crinitum, Vaccinium microphyllum, Freycinetia lagenicarpa, Astronia cumingiana, Dimorphanthera apoana and Eurya buxifolia and species of tree ferns were Cyathea negrosiana and Cyathea contaminans (Suppl. material 3). A low Shannon Diversity Index, 2.48, was observed at this elevation. Computed Evenness on the other hand, was 0.79 which indicates even distribution of plant species commonly shared within the plots.

Conservation status and endemicity

Out of 351 species recorded at the study site, 30 (9%) were classified as threatened. Of the 30 threatened species, six (6) were categorised as critically endangered, four (4) endangered and 20 vulnerable. Remarkably, twenty five of these threatened species were found thriving in the Lowland of the sub-montane (Table 3). Meanwhile, both lowland and montane had six threatened species noted. Critically-endangered species included Shorea almon, Paphiopedilum acmodontum, Shorea negrosensis, Shorea polysperma, Shorea contorta and Nepenthes ramos. Endangered species included Medinilla banahaensis, Madhuca betis, Guioa acuminata and Cyathea contaminans. Vulnerable species included Agathis philippinensis, Artocarpus blanco, Macaranga bicolor, Cinnamomum mercadoi, Dillenia philippinensis, Terminalia pellucida, Canthium dicoccum, Palaquium philippense, Palaquium luzoniense, Mangifera altissima, Canarium ovatum, Canarium luzonicum, Ardisia squamulosa, Macaranga grandifolia, Asplenium vittaeforme, Alocasia zebrina, Alpinia musifolia and Cyathea negrosiana. In addition, a total of 88 species were endemic to the Philippines. The highest number (74) of endemic species was found in the sub-montane followed by 20 in the montane and 15 in the lowland.

The findings in this study showed that the composition of flora of "BTLNP" in Negros Island is structured by elevational gradient. The distribution and composition of species within the three major Lowland types in the study site are defined and restricted by the differences in elevation which have a direct influence on the species ability to survive, compete and reproduce. Several tree species from the family Lauraceae, such as Litsea, Cinnamomum, Neolitsea, Actinodaphne, Phoebe and Machilus, were found thriving in the sub-montane forests. In addition, a number of dipterocarp species belonging to genus Shorea were also observed in this Lowland type. These observations conformed with the findings of Ashton (2003) where sub-montane forests in Southeast Asia are mainly composed of dipterocarps and oak-laurel assemblages. The plant composition of the lowland Lowland, on the other hand, was predominantly agricultural crops and pioneer species such as banana (Musaceae), figs (Moraceae), legumes (Fabaceae), herbs (Araceae) and euphorbs (Euphorbiaceae), all considered indications of farm cultivation and anthropogenic influences. These species groups were also commonly observed in open forested areas of Bohol, Philippines as reported by Reyes et al. (2015) and Bullecer et al. (2015) and in native tree farms Reyes and Sarnowski (2020) and timber plantations Reyes (2019). The open Lowland canopy allows light to penetrate to reach the Lowland floor making it available to sun-loving ground herbs, legumes and grasses in order to proliferate which explains why these species are found dominant in the lowland Lowland (Durst et al. 2016). Ultimately, the montane Lowland was characterised by the presence of mosses, lichens, epiphytes and small trees with prop and aerial roots coming out from one to a few metres from the base of the tree trunks that are irregular in shape. Trees like Dacrydium, Tasmannia, Elaeocarpus, Melastoma, Omolanthus, Vaccinium and Syzygium were observed in this site to be dwarfed and their trunks gnarled. These are indications of their adaptations to strong winds and pressure, a similar observation by Aiba and Kitayama (1999). Furthermore, the dominance of tree ferns Cyathea contaminans and Cyathea negrosiana especially in sub-montane to montane elevations was observed. Cyathea is known to play a prominent role in lower montane Lowland areas (Richter 2008) and are common inhabitants of tropical montane cloud Lowland (Penafiel 1995). The wide range of tree ferns indicate a floral group more tolerant of higher seasonality and long-term climatic fluctuations (Tejedor 2018). Meanwhile, towards high elevations, the presence of conifers, known to thrive in higher Southeast Asian mountain areas, indicates the uniqueness of this elevational habitat (Enright and Jaffre 2011).

A sharp decline of species richness and diversity as altitude increased beyond 1,450 m a.s.l. was observed. This decline is due to the extreme environmental conditions, such as very low temperature, high relative humidity and low decomposition rate in the montane Lowland. Low temperature affects the respiratory process of trees through high retention of water vapour (Aureo and Bande 2019, Bernatzky 1978). Another contributary factor to the decrease in the number of species and diversity in the montane Lowland is organic matter storage and decomposition essential for plant growth (Culmsee and Leuschner 2013, Krishna and Mohan 2017). Low decomposition rates in the montane Lowland result in the building up of organic matter and nutrient stocks in soil which are not readily available for plant growth. Fast decomposition rates in submontane and lowland forests help to meet plant intake requirements (Isaac and Nair 2005). Another notable observation was that flora richness peaks at sub-montane and decreases at both lowlands and montane elevations which follow a bell shape curve. The diversity value of lowland was 3.29, which is relatively high, but lower than sub-montane Lowland. Lowland elevation was identified primarily as agroforestry-dominated where human impacts are evident in the form of open spaces. This may prevent the establishment of shade-tolerant species (Villanueva and Buot 2018). The Evenness Index, an indication of species representation, was 0.88 or 88% for the lowland, demonstrating a high level of similarity between plots within the lowland habitat. This could be because of the presence of ecotones and the transition zone (from lowland to sub-montane) near the established plots in the lowland area. In sub-montane, the Shannon Diversity Index was very high. This can possibly be attributed to the various Lowland structures formed from transitional zones of lowland extending towards the lakes. Furthermore, submontane Lowland has a lower Evenness Index indicating that a certain species at this elevation over-dominate while other species are not well represented. As so many species were observed at the sub-montane level, it would not be expected for all species to be represented evenly. Montane Lowland, on the other hand, had low species diversity. In addition, the species Evenness Index value was 0.79 which indicates that 79% of the species amongst montane elevations are common amongst the plots. These findings correlate with previous tropical mountain research in which the number of species, genera and families decreases with increasing elevation (Aiba and Kitayama 1999, Kitayama 1992, Sharma et al. 2009). However, this finding is not consistent across other tropical mountains in the Philippines, such as in Mt. Pulag (Buot and Okitsu 1998), Mt. Mayon (Buot 2008), Mt. Makiling (Buot and Osumi 2011) and Mt. Ilong (Villanueva and Buot 2018), wherein an increase in diversity along elevation was observed. These contrasting observations could be explained by how a certain mountain ranges arebeing utilised. For instance, the lowland Lowland, which is located within 600-750 m a.s.l., is being utilised as agroforestry which accounts for both the planted and natural flora.

Thirty threatened and 88 Philippine endemic species were observed in BTLNP. Most of the threatened and endemic species were found in the sub-montane Lowland along the lake and are less in the montane and lowland. Elevation is known to be the greatest influencing factor in changes on floristic composition and diversity in tropical mountains (Hemp 2006). The threatened species found in BTNLP were mostly families belonging to Dipterocarpaceae and Sapotaceae which are mostly sensitive to extreme environmental conditions. Species belonging to the family Dipterocarpaceae, which was commonly found in this study, is known as a good source of timber and is considered economically important, thus constitutes a threat for future exploitation of these tree species (Reyes and Sarnowski 2020).

The present study highlights the floristic composition, community structure and diversity of BTLNP along its elevational gradient, from lowland, sub-montane and montane. Our findings revealed that lowland and sub-montane forests had higher number of species compared to the montane Lowland. Furthermore, we observed a change in plant species composition along elevation gradients with a trend of decreasing species diversity with increasing elevation. It is worth noting that most of the threatened species observed in this study are mostly found in the sub-montane Lowland and are more easily accessible to humans compared to the montane.

These results indicate that BTLNP should follow appropriate conservation and management strategies to protect all elevations, but have a special focus on the sub-montane level, as well as threatened species. Additional care should be taken in the development of ecotourism, as human distrubance has been shown to alter the floral composition. Lastly, this study not only provides a floral baseline for BTLNP, but can also be used as a reference for additional species composition and elevational research within the Central Visayas.

The authors wish to thank Philippine Council for Agriculture, Aquatic and Natural Resources Research and Development (PCAARRD), for the financial assistance of the project. The Department of Environment and Natural Resources (DENR) and the Protected Area Management Board (PAMB) also with the BTLFAI Peoples Organization (PO) members of Balinsasayao Twin Lakes Natural Park is also acknowledged for allowing and supporting the researchers in the conduct of their study. We would like to also convey deep gratitude and heartfelt appreciation to the Central Visayas biodiversity survey team, Rochelyn Parba, Jessie Josol, Jessica Josol, Arianne Pacarat and Oscar Ido.

Biodiversity Assessment for Sustainable Management in Key Biodiversity Areas of Central Visayas

Bohol Island State University

Specimen Collection Gratuitous Permit (GP) Number VII-2019-04 (DENR Region VII)

The authors declare that there is no conflict of interest.