Tropical forests exhibit heterogeneity and high vertical complexity brought about by varied tree heights which help maintain and increase species diversity (Vieira and Monteiro-Filho 2003). They can be vertically divided into distinct layers or strata, characterised by differing levels of water, sunlight and air circulation, but are interdependent (National Geographic Society 2020). Vertical stratification in tropical forests can be separated into three to four forest heights from ground level (<1.5 m), namely the understorey (1.5-2 m), sub-canopy (2-6 m), canopy (6-15 m) and emergent layers (Vieira and Monteiro-Filho 2003, Adams et al. 2009, Anonymous 2019). This vertical stratification of habitat layers of plant and animal communities represent a basic concept in forest ecology, which has not been well examined for patterns and often defined differently (Smith 1973, Parker and Brown 2000). Drivers of canopy stratification were found to be significant for forests with varied leaf and top heights, clustered leaf heights and those harbouring different life forms at different heights (Parker and Brown 2000). The degree of canopy stratification and woody species diversity are influenced by latitudinal thermal gradients from subtropics to tropics and this multi-layering structure helps maintain high species diversity (Feroz et al. 2015). Thus, a stratified structure is more evident in tropical than in temperate forests and this layering of vegetation affects the distribution of food resources, microclimate and faunal composition (Smith 1973).

The forest canopy refers to the upper layer or habitat zone, formed by interspersed crowns of mature trees and includes other biological organisms, such as epiphytes, bryophytes, lianas and mistletoes forming a community of associated flora and fauna (Parker 1995). For a single tree, the term “canopy” is used to refer to the extent of the outer layer of leaves of an individual tree forming its crown cover. Together, these crowns form the canopy, wherein the lower branches of the tallest trees are often in contact with the leaves and branches of adjacent trees, allowing horizontal access. Towering above the contiguous main canopy are tall crowns of scattered emergent trees, also called overstorey. Within the dense ceiling of the canopy, there is an abundance of leaves and fruits that provide food for herbivores which, in turn, are predated upon by carnivores. The middle sub-canopy normally lies 2-5 m above the ground, just below the first branches of the canopy and consists mainly of small juvenile trees, palms and woody species adapted to low light filtered by dense foliage. The understorey includes shrub and herb layers of undergrowth, consisting mostly of young saplings, shade-tolerant herbaceous shrubs and ferns slowly reaching for light from the forest floor.

Mt. Makiling is considered a low mountain with its highest peak of only 1090 m a.s.l. Despite this, the mountain uniquely consists of various habitat types, such as lowland evergreen, montane and mossy rainforests. The Mt. Makiling Forest Reserve (MMFR), due to its accessibility and historical association with the University of the Philippines Los Baños (UPLB) as a field laboratory, is one of the most studied of the ASEAN Heritage Parks (AHP) in the Philippines. Assessment of its vertebrate fauna has been noted since the early part of the 20th century (Taylor 1922), but only fully documented in the later part, especially for birds (Alviola 1977, Miranda 1987, Mendoza 1987), bats (Ingle 1992) and herpetofauna (Custodio 1986, Alcala et al. 1997, Gonzalez and Dans 1994). A more comprehensive wildlife assessment across elevational and habitat gradients was undertaken by Gonzalez and Dans in 1998 (Sajise et al. 2005), which was followed by successive studies on habitat gradients and forest stratification, such as on understorey birds and small mammals (Gonzalez 2005, Gonzalez 2008, de Guia et al. 2011), bats (Alviola 2008, Sedlock 2001, Sedlock 2002) and montane wildlife (Abraham et al. 2010). Despite the long history of biodiversity assessment, none of the studies effectively assessed the wildlife found in the upper forest strata, from sub-canopy to emergent layer. To some extent, sampling for insectivorous bats in the forest canopy has been included (Sedlock 2001, Sedlock 2002),thus showcasing the strong potential for conducting “forest canopy studies” at MMFR. Despite these comprehensive studies on the faunal diversity of MMFR, some areas of the Park remain to be fully explored – for example, the ecology and natural history of vertebrate fauna found in different forest strata, especially through the upper forest canopy and emergent layer.

Vertical stratification is the most significant factor in the diversification of forest habitats in Mt. Makiling, as it provides potential niches by driving species to adapt for aerial and arboreal habits (Gonzalez and Dans 1997). The tropical lowland evergreen rainforest contains most of the layers amongst those forest types categorised by Fernando et al. (2008) and amongst the four types of vegetation recognised in Mt. Makiling (Lapitan et al. 2013). This multi-tiered structure of lowland forests at established monitoring plots within MMFR was the focus of the Forest Canopy Observation, Positioning and Investigation (Forest CANOPI) Program, an inter-disciplinary research which covered various aspects of canopy science, from mapping crown structure to assessing biodiversity (fauna, flora and microbial diversity). Our study was part of the programme centred on understanding tetrapod diversity across vertical layers and horizontal zones within a lowland evergreen rainforest. In particular, this paper aimed to determine species richness amongst terrestrial vertebrate fauna (amphibians, reptiles, birds and mammals) distributed across three lowland forest strata on Mt. Makiling (understorey, sub-canopy and canopy) and to be able to compare composition of tetrapod fauna, based on diet and guilds to evaluate their equivalent contributions in providing ecosystem services.

Site Description

Methods

A total of 68 wildlife species consisting of 11 species of frogs, 15 species of reptiles (3 gekkos, 6 skinks, 2 agamids and 4 snakes), 25 species of birds and 17 species of mammals (13 bats, 3 rodents and 1 carnivore) were recorded. The majority (~69%) of the recorded species were Philippine endemics associated with forested areas (Fig. 2 and Table 1). The highest percentage of Philippine endemics was observed in birds and lowest was in mammals. Species effort curves (Fig. 3) show that sampling efforts were sufficient to record the species within the area despite the differences in the duration of sampling per forest stratum.

Herpetofauna

A total of 26 species was recorded, represented by 11 species of amphibians and 15 species of reptiles. Amphibians were encountered within all of the forest strata (Table 2). Of the 11 species of frogs, two species (Platymantis luzonensis and Kaloula kalingensis) were recorded in all forest strata. The most abundant in the understorey was the Common forest frog (Platymantis dorsalis), while in the sub-canopy and canopy, the Luzon forest frog (Platymantis luzonensis) was the most abundant. The majority (63%) of the recorded frog species are Philippine endemics.

Based on known reproductive modes of the four recorded Platymantis species, they undergo direct development which skips the tadpole stage and change into froglets immediately. They inhabit the wet forest floor and arboreal sites in closed canopy forests (Alcala and Brown 1998). Woodworth’s frog (Limnonectes woodworthi) and the Puddle frog (Occidozyga laevis) inhabit pools and banks of mountain streams, although the Puddle frog may also be found in disturbed areas with polluted waters. The two species of Chorus frogs are also forest species that burrow under the soil or climb vegetation. Both Rhacophorid frogs are foam nest builders, however, Rhacophorus pardalis is commonly found in the canopies of primary and secondary rainforests, while Polypedates luecomystax is very common and can be found in almost every habitat from forest to agricultural lands (Kuraishi et al. 2013, Manthey and Grossmann 1997). Fig. 4 shows the recorded anuran species from the understorey to the canopy.

Two new records for Mt. Makiling are the Truncate-toed chorus frog (Kaloula conjuncta) and Frilled tree frog (Kurixalus appendiculatus). K. conjuncta was recorded only in the understorey, while K. appendiculatus was only recorded in the canopy. The addition of these two new records with the previous 23 recorded frog species (Alcala et al. 1997, Sajise et al. 2005, Abraham et al. 2010, Gonzalez and Dans 1997) now brings the total species number of amphibians in MMFR to 25. The results of the sampling represent approximately 49% of the previously-recorded frog species.

A total of 15 species of reptiles was recorded in all the forest levels. Of this, 60% are Philippine endemics. Seven species were recorded in the understorey, nine species were recorded in the sub-canopy and nine species were recorded in the canopy. Three species (Pinoyscincus jagori, Ahaetulla prasina and Cyrtodactylus philippinicus) were recorded in all levels (Table 3). The most abundant in all levels was Cyrtodactylus philippinicus.

Three species of lizards recorded (C. philippinicus, Gekko mindorensis and Psuedogekko compressicorpus) are arboreal species. Skinks recorded are mostly ground dwellers, except for Dasia grisea, Lamprolepis smaragdina and P. jagori which were recorded in the sub-canopy. However, the arboreality of P. jagori in the sub-canopy to canopy level needs to be verified. Based on known literature, the species is frequently found in leaf litter, rotting logs and along streambeds. Its presence in the sub-canopy might be due to other factors, such as the presence of a threat or prey. The two agamids and three snakes recorded are arboreal, but hunt prey on the ground which explains their presence in the understorey. Fig. 5 shows representative species found within the permanent plot.

New records for Mt. Makiling are the Mindoro narrow-disked gekko (Gekko mindorensis), Northern keeled-scaled tree skink (Dasia grisea), Many-keeled Mabuya (Eutropis borealis), Negros forest dragon (Gonocephalus sophiae) and Smooth-scaled rat snake (Ptyas luzonensis). G. mindorensis, E. multicarinata and P. luzonensis were only recorded in the canopy, while D. grisea was only recorded in the sub-canopy. G. sophiae was recorded from the understorey to sub-canopy.

A total of 30 reptile species have been previously recorded in Mt. Makiling (Abraham et al. 2010, Gonzalez and Dans 1994, Sajise et al. 2005). The five new records thus bring the total number of recorded reptile species in MMFR to 35. The results of the survey represent 50% of the previously-recorded species in Mt. Makiling.

Avifauna

Twenty-five species of birds represented by 89 individuals (Table 4) were captured through netting. We are aware that this is an underestimate since sampling was limited only to mist-netting to record birds in a particular forest stratum. However, this is a more accurate assessment of vertical habitat use as birds have the ability to fly between layers. Thus, in order to make the results for birds comparable with amphibians, reptiles and mammals, we only used the data sampled through netting in this analysis. Nonetheless, other methods (ex. point counts) were used to record birds across the strata during the Forest CANOPI Program, but results were not included in this paper. Most (> 80%) were endemic and forest obligates, ranging from frugivores to insectivores and carnivores. Six species were recorded in the understorey. However, a number of species possibly present within the area are ground-dwelling birds such as junglefowl, quails, rails and others which were not recorded. This may be due to the disturbances within the permanent plot at the time of sampling as a result of various on-going research projects, visitors to the reserve and proximity to human settlements (with their free-roaming dogs, cats and chickens). There were 16 species within the sub-canopy, while 13 species were recorded within the canopy.

Amongst the 25 bird species, none was common to all forest strata. Overlaps were observed between the understorey and the sub-canopy and between the sub-canopy and the canopy. Between the understorey and the sub-canopy, four species (Dicrurus balicassius, Pycnonotus urostictus, Actenoides lindsayi and Otus megalotis) were observed. Meanwhile, between the sub-canopy and the canopy, five species (Ninox philippensis, Loriculus philippensis, Bolbopsittacus lunulatus, Sarcops calvus and Phylloscopus cebuensis) were recorded. Fig. 6 shows representative bird species amongst the forest strata.

A total of 215 bird species (Abraham et al. 2010, de Guia et al. 2011, Gonzalez and Dans 1997, Sajise et al. 2005) had been previously recorded in Mt. Makiling. Our results represent only 11% of the species numbers recorded in previous studies. Again, this is expected to be an underestimate resulting from the focused methodology which relied only on netting.

Mammals

A total of 17 species consisting of 13 species of bats (Table 5) and four species of non-volant mammals were recorded. There was approximately 59% endemicity with all species associated with forested areas, albeit with varying degrees of tolerance to disturbances.

For the understorey survey, only six species of bats were recorded. Two were frugivorous and the rest were insectivorous. For the sub-canopy sampling, six species of pteropodid bats and two species of insectivorous bats plus two rodents were recorded. For the canopy sampling, seven species of fruit bats, three rodents and a civet were recorded. Only two species were common to all levels (Cynopterus brachyotis and Ptenochirus jagori). Fig. 7 shows some of the recorded mammal species in the permanent plot.

New records for Mt. Makiling are the Philippine dusky roundleaf bat (Hipposideros antricola) and the Philippine dawn bat (Eonycteris robusta). H. antricola was only recorded in the understorey, while E. robusta was only recorded in the canopy. A total of 50 mammal species (Abraham et al. 2010, de Guia et al. 2011, Gonzalez and Dans 1997, Heaney et al. 1998) have been reported in Mt. Makiling. Our two new records now bring the total to 52 species. The results of our study represents ~34% of the total species recorded. This underlies the potential for more species records or even new species discovery with higher forest strata samplings.

Trends in species richness, based on forest vertical stratification

To compare the different fauna found between different vertical forest stratification, species-richness values were compared using proportions. Overall, our results showed that species richness increased from the understorey to the canopy layer (Fig. 8). The similarity between strata were computed using the Sørensen similarity index (θ) (Table 6). Highest similarity was observed between the sub-canopy and the canopy (θ_subxcan = 0.56) indicating an overlap between the species that occupy these two strata. Lowest similarity was observed between the canopy and the understorey (θ_underxcan= 0.19) suggesting exclusivity of species between the two forest strata. This is also the case between the understorey and the sub-canopy (θ_underxsub= 0.37), although not as low as between the understorey and the canopy. Due to increasing forest heterogeneity brought about by greater vertical stratification, species richness and composition was high in the upper strata, as this affords more vertical habitat use, in particular, canopy use (Vieira and Monteiro-Filho 2003).

Species richness of a vertebrate group varied amongst the forest strata. It has been generally observed that, except for amphibians, all other vertebrate taxa have increasing species richness the higher the vertical stratification. Scheffers et al. (2013) stated that the arboreality of frogs decreases at lower elevations and increases at higher elevations specifically from 900 m a.s.l. and above. Based on the data gathered during the sampling, the understorey had a species richness of 0.7 and sub-canopy and canopy with 0.36, coinciding with the low elevation of the study site at 350 m a.s.l. Furthermore, in terms of amphibian diversity, the understorey had low similarity with the sub-canopy and the canopy (θ_frogs = 0.33; 0.18)

Increasing species richness with higher vertical forest strata was observed for reptiles (understorey = 0.46; sub-canopy = 0.6; canopy = 0.6). The similarity between the understorey and the sub-canopy and canopy was also low (θ_reptiles = 0.44; 0.43) Trends in reptilian species richness may also be highly affected by the high complexity and heterogeneity of habitats (Vignoli et al. 2017). As an example in Vitt and Caldwell (2013), reptile species richness was influenced by horizontal stratification caused by habitat patchwork or fragmentation rather than vertical stratification. Our results suggest that species richness is influenced by vertical stratification and may be due to the presence of rich canopies with branches filled with epiphytes and various vines.

For birds, Jayson and Matthew (2003) determined that higher bird species richness was found in the middle strata compared to the lower and top strata. This concurs with our results as species richness was also highest in the sub-canopy (u = 0.24; s= 0.64 and u = 0.56). Higher foliage density was observed within the sub-canopy which may be utilised by birds for feeding and nesting. Similarities amongst the three strata were also quite low (θ_underxcan = 0.19; θ_{subxcan =} 0.39; θ_underxsub = 0.34) although the sub-canopy and the canopy are more similar.

For bats, Carvalho et al. (2013) observed that bat diversity increases with vertical stratification. Overall, this was also our observation (u = 0.35; s = 0.58; and c=0.65). However, more insectivorous bats were captured in the understorey, while more frugivorous bats were captured in the sub-canopy. Insectivorous bat activity across three vertical strata in south-eastern Australian forests were influenced by vegetation structure. Mean bat activity was > 10x higher in the sub-canopy and canopy than in the understorey, whereas bat activity was lower in the two upper strata of young regrowth forests than in old regrowth, due to more cluttered vegetation and less vertical space available. Less cluttered vegetation in forest strata offer more vertical space and this higher index of vegetation openness influences greater bat activity (Adams et al. 2009). For non-volant mammals, the species richness is greatly affected by forest structural complexity (Grelle 2003). This may explain the absence of non-volant mammals in the understorey during the sampling. The same similarity patterns were also observed with mammals. Highest similarity was observed between the sub-canopy and the canopy while the least similarity was observed between the understorey and the canopy (θ_underxcan = 0.24; θ_{subxcan =} 0.67; θ_underxsub = 0.38). Arboreal species of small mammals were observed to exclusively inhabit the upper forest strata (canopy and sub-canopy) of Atlantic rainforests in southeast Brazil and, being adapted to canopy use, they can no longer compete for habitats with other small mammals in the forest floor (Vieira and Monteiro-Filho 2003).

Research Implications

Our study showed that, for most of the vertebrate fauna, species richness increases from the understorey to the canopy levels of a lowland evergreen rainforest. It follows the hypothesis that distinct stratification and increasing vertical complexity contribute to upper vertical habitat utilisation and, therefore, more species are partitioned or segregated in each stratum. As a result, the increased forest heterogeneity afforded by vertical stratification not only maintains species richness, but also increases in the upper strata, due to more canopy use. The disparity of records of vertebrate fauna between the more accessible understorey versus the less-studied canopy level, as well as other upper strata of the complex lowland evergreen rainforest indicates that many ground-based studies under-assess the species present. This has implications with the standard methods limited to understorey sampling which underestimates the species that are present in forested areas. Thus, it is imperative to include the sub-canopy and the canopy layers during sampling to obtain a more accurate inventory of species essential in designing conservation strategies for wildlife. More passive observation methods are also recommended for further studies to reduce disturbances and possible stress to the animals.

JCTG, APOdG, JCD and NCB conceived the research project. WOG and KVP conducted the fieldwork and wrote the draft reports under the supervision of JCTG, APOdG and JCD. APOdG wrote the first draft of the manuscript. All authors read and edited the manuscript.

We would like to extend our deepest gratitude to the Emerging Interdisciplinary Research (EIDR) Program of the University of the Philippines Office of the Vice President for Academic Affairs for funding the first year of our research programme and the Department of Science and Technology (DOST) for funding the second year. To the U.P. Museum of Natural History (UPLB MNH) staff: the late James DV. Alvarez, Edison A. Cosico, Julius A. Parcon, Jeremy Carlo R. Naredo, Florante A. Cruz, Rafael D. Tandang and Roseller B. Duque for their ideas and suggestions to further improve project sampling methods and other project activities. Volunteers: Camila G. Meneses, Geneva Chavez, Glaiza S. Ibanez, Yvonne P. Riza and Bill Thaddeus A. Padasas for contributing their time, effort and knowledge during CANOPI fieldworks. Thesis and Special Problem students: Deolito M. Bicua, Jr., Darlene P. Lovina, Michael H. Galapon and Paul Alan M. Umale, for undertaking various research aspects of the project. Our field assistants Wilson B. Bulalacao, Jayson B. Bulalacao, Bengie C. Gurobat, Edwin Sungcaya, Ryan D. Llamas, Primitivo Aznar, Jr. and Jonas D. Llamas. We are deeply thankful for the support and cooperation of the Makiling Center for Mountain Ecosystems (MCME) of the College of Forestry and Natural Resources, U.P. Los Baños, the Philippine Council for Agriculture, Aquatic and Natural Resources Research and Development (PCAARRD)-DOST and to the members of the Forest CANOPI Program, for giving us the opportunity to be part of this pioneering research endeavour in the Philippines, particularly For. Leonardo D. Barua, For. Karla Jane P. Gonzalvo, Dr. Manuel A. Castillo, Prof. Juancho B. Balatibat, For. Lawrence Adolf M. Amada, For. John Ryan L. Navidad, Dr. Jocelyn T. Zarate, Johnry S. Maloles, Dr. Noel G. Sabino, Dr. Lucille C. Villegas, Dr. Jessica F. Simbahan, Robynne Olive S. Eslit and Mia Beatriz C. Amoranto.