Philippine Journal of Science 150 (S1): 563-575, Special Issue on Biodiversity ISSN 0031 - 7683 Date Received: 30 Sep 2020

Collembola (Arthropoda: Hexapoda) Assemblages in the Canopy and Forest Floor along an Elevational Gradient at Mt. Makiling, Philippines

Marnelli S. Alviola1*, Felipe N. Soto-Adames2, Cristian C. Lucañas3,4, Virginia C. Cuevas1, Juancho B. Balatibat3,5, and Ireneo L. Lit Jr.1,3

1Environmental Biology Division, Institute of Biological Sciences College of Arts and Sciences, University of the Philippines Los Baños, Philippines 2Florida State Collection of , Division of Plant Industry Florida Department of Agriculture and Consumer Services, Gainesville, Florida, USA 3Entomology Section, University of the Philippines Los Baños Museum of Natural History, Philippines 4Graduate School, University of the Philippines Los Baños, Philippines 5Department of Forest Biological Sciences, College of Forestry and Natural Resources University of the Philippines Los Baños, Philippines

Patterns of distribution and diversity of along an elevational gradient in the canopy and forest floor of Mt. Makiling, Philippines were determined, this being the first study conducted on diversity along an elevational gradient and also the first published report of canopy arthropods in the Philippines. Springtails were extracted from soil samples from the floor and those suspended in the canopy of three natural forests at different elevations (tropical lowland evergreen rainforest, lower montane rainforest, and tropical upper montane forest). We predict that elevation and forest strata will have significant effects on the springtail assemblages. A total of 2,287 springtails representing 31 morpho-species and eight families were collected from the study. Across the elevation gradient, mean species richness and mean abundance consistently decrease as elevation increases, but only the mean abundance of the lowland forest is significantly different from that of the lower and upper montane forests. Diversity t-test (p-values less than 0.05) revealed significant differences between different sites and strata. Clustering analysis using the Bray-Curtis similarity index revealed separate groupings of the lowland forests to those of the montane forests. Lastly, the results of PERMANOVA showed that both elevation and strata were found to have significant effects on the overall assemblage of springtails. This study suggests that forest floor species assemblages are closely related to each other unlike those of the canopy, where only the upper montane and lower montane are similar. The results of this study affirm our main hypothesis that springtails (as a group) respond significantly to both elevation and strata in a tropical forest in the Philippines.

Keywords: forest strata, springtails, tropical rainforest, vegetation types

*Corresponding Author: [email protected]

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INTRODUCTION decaying plant matter (Hopkin 1997), which are abundant in the canopy of “closed” tropical rainforests (Basset et Explorations of the forest canopy have increased the global al. 2003). Addressing these hypotheses will increase our estimates of biodiversity by several folds (Greenslade et understanding as to how these organisms are structured al. 2016; Nakamura et al. 2017). The canopy has been along elevational and vertical gradients in a tropical considered as “the last biotic frontier” (Erwin 1983) due to ecosystem. Results of the study would also be of great the favorable habitat it provides for numerous organisms importance in studying the sensitivity of springtails, along that are rarely or never found on the forest floor. It also with other soil-inhabiting organisms, to climate change. serves as a “dynamic interface between organic nature This is the first study conducted on springtail diversity and the atmosphere,” which is a great avenue (in addition along an elevational gradient in the Philippines and also to the most-studied elevational gradients) for studying the first published report of canopy arthropods, especially how changes in the environment may affect biodiversity springtails, in the Philippine forests. (Nakamura et al. 2017). The arthropods make up most of the soil biodiversity, with the Collembola (springtails) and oribatid mites being the most dominant (Cassagne et al. 2006). The Collembola MATERIALS AND METHODS make up some of the most abundant and widespread soil This study was conducted in the northeastern side of Mt microarthropods in the world. They can be found in almost Makiling, a dormant volcano located on the border of the all types of terrestrial habitats where they often dominate provinces of Laguna and Batangas, Luzon, Philippines the soil community (Deharveng and Bedos 2004). Gapud [Makiling Center for Mountain Ecosystems (MCME) (1968) considered the Collembola to be one of the most Collection Permit S.N. 27 January 2018]. The reserve has neglected insect orders in the Philippines. Handschin a total land area of 4,224 ha and is located at 14°8′ north (1926, 1930) pioneered in Collembola and and 121°12′ east spanning parts of Los Baños, Bay, and recorded 18 species, including seven that are endemic to Calamba in Laguna province, and Sto. Tomas in Batangas the Philippines. Gapud (1968, 1969, 1971) expanded the province. The average rainfall, temperature, and humidity in knowledge on the Philippine Collembola as he reviewed Los Banos, Laguna during the date of collection (August– the two suborders Arthropleona and Neoarthropleona by September 2018) were 195.895 mm, 27 °C, and 84.5%, examining museum specimens and new collections. Most respectively (source: World Weather Online). of the species collected were either new to science or new Philippine records. Three natural forests (Fernando et al. 2008) at different elevations (tropical lowland evergreen, lower montane, Canopy science in the Philippines is a relatively new and tropical upper montane rainforests) were selected field. At present, there have been no published scientific (Figure 1). The first site, lowland evergreen rainforest articles on the canopy fauna of the country. The present (LL), is composed of early to late secondary growth forest study was conducted to determine patterns of distribution at an elevation between 442–655 masl. The second site, the and diversity of springtails along an elevational gradient lower montane rainforest (LM), spans from 760–899 masl, in the canopy and forest floor of Mt. Makiling, a well- with vegetation consisting of natural stands of old-growth documented biodiversity area in the Philippines (Pancho forests with prominent vines and lianas; human activities, 1973; Abraham et al. 2010). aside from hiking of mountaineers, are limited in the We hypothesized that springtails would respond strongly area. The last site is the upper montane rainforest (UM) to both elevation and strata as these parameters possess a located at the peak of Mt. Makiling starting from 900m distinct set of environmental conditions that could have asl and where trees are significantly shorter and covered discernable effects on springtail assemblages (Paoletti with thick layers of mosses. The mean temperature et al. 1991; Maunsell et al. 2013; Basset et al. 2015; during the time of collection was 26.23, 23.09, and 22.30 Bokhorst et al. 2018). Specifically, we hypothesized °C in the lowland, lower montane, and upper montane that species diversity increases with increasing altitude, forests, respectively. Soil pH decreases with increasing following the same pattern of springtail studies in elevation (LL: 7.23; LM: 6.43; UM: 5.76). On the other Mexico (Cutz-Pool et al. 2010), Sweden (Bokhorst et hand, relative humidity was highest in the lowland forest al. 2018), and China (Sun et al. 2020). We also expect (75.83%), followed by upper montane forests (72.67%) that a clear distinction between forest floor and canopy and lower montane forests (69.75%). species exists (Rodgers and Kitching 1998, 2011). Lastly, At each of the three study sites, a 20-m transect line was we hypothesized that species abundance and richness established based on rapid assessment of suspended soil are higher in the canopy than in the forest floor since presence and accessibility from the trail. Four collection the majority of springtails feed on fungal hyphae and trips were done due to an inadequate number of available

564 Philippine Journal of Science Alviola et al. Collembola Across Vol. 150 No. S1, Special Issue on Biodiversity Elevation and Forest Strata

Figure 1. Location of three study sites at three elevations in the northeastern side of Mount Makiling, Philippines.

Berlese-Tullgren funnels. The dates of the collection were slides and identification of springtails were done at the 16 and 30 Aug, 11 Sep, and 26 Sep 2018. Florida State Collection of Arthropods, Department of Plant Industry, Gainesville, Florida, USA. Lastly, the springtails Twelve suspended soil samples and 12 forest floor samples were identified to the species or morpho-species with the were collected in each vegetation/elevational type. Each use of dichotomous keys and/or illustrations provided sample ideally consisted of around 1 kg. For the whole by Christiansen and Bellinger (1980), Fjellberg (2007), study, 36 canopy (suspended soils) and 36 forest floor Gapud (1968, 1969, 1971), Zhang and Deharveng (2014), samples were collected representing three vegetation types. and Soto-Adames and Bellini (2015) and other published Arthropods were extracted for a period of one week from taxonomic keys and literature available at the Checklist of the soil samples using a Berlese-Tullgren funnel, which the Collembola of the World website. For the purpose of is a closed funnel system with a light source at the top, a this study, morpho-species was resorted to when specimens screen to hold the sample at the middle, and a jar receptacle could not be identified yet due to a lack of updated at the end of the funnel with 70–90% ethyl alcohol. All taxonomic information. Morpho-species is based on the springtails were separated for slide mounting while the assumption that each morphologically different individual other arthropods were set aside and placed in microtubes belongs to a different species, which has been quite useful with 90% ethanol for future studies. Direct mounting in for rapid biodiversity assessments and sampling studies (e.g. Encinares and Lit 2014).

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Data Analysis RESULTS Data gathered were subjected to several statistical analyses using Paleontological Statistics v.3.16 Abundance and Richness (Hammer et al. 2001) and EstimateS (Colwell 2013). A total of 2,287 springtails representing 31 morpho- Rarefaction curves were used to check if the sampling species and eight families were collected during the study. effort was enough to properly assess the diversity of The canopy contributed 1,458 springtails from 27 morpho- the assemblage in the site. Rarefaction curves species and eight families, whereas the 829 springtails were also extrapolated up to 2n = 24 replicates to check collected on the forest floor included 20 morpho-species the efficiency of the sampling effort and to obtain an from seven families. Table 1 summarizes the number of estimate of the true species richness of the arthropod species and total abundance observed at each site per assemblage. True species richness values were strata. The lower montane canopy has the highest number estimated using Chao-1 (Chao 1984). The completeness of species, while the upper montane floor has the lowest. ratio was calculated by dividing the observed species The lowland canopy has the highest number of individuals richness by the estimated. while the upper montane floor has the lowest. However, The total abundance and species richness of springtails the completeness ratio for all sites was less than 85%, were summarized in preparation for univariate analysis. indicating that not all Collembola species from each Shannon diversity and dominance and Pielou’s assemblage are represented in the sample. evenness index were computed. Indices of each forest Mean species richness (Figure 2A) was consistently type and strata were compared using Hutcheson’s higher on the forest floor at all elevations, although (1970) diversity t-test. standard deviations of all sites indicate no significant Unique and shared species were noted, and similarities differences in the number of species. On the other hand, between samples were analyzed using a 1000-iteration, mean abundance (Figure 2B) did not show a consistent classical clustering analysis based on Bray-Curtis pattern, and a significant difference was only observed and Jaccard similarity indices. On the other hand, in the forest floor and suspended soil of lowland forest. the effects of elevation and forest strata on species Across the elevation gradient, mean species richness richness and assemblage were assessed using a two-way and mean abundance decrease as elevation increases, permutational multivariate ANOVA (PERMANOVA). but only the mean abundance (Figure 2B) of lowland Post hoc pairwise comparisons between forest type and forest was found significantly different from that of the strata using 1000 permutations were also conducted. montane forest. Pairs with significant differences in PERMANOVA were subjected to similarity/dissimilarity analysis using SIMPER to determine which taxa contributed to Diversity Indices the differences. Simpson’s diversity indices (Table 2) indicate moderate diversity (1/D = 3.2010–7.2674 and/or 1-D = 0.6876– 0.8624) and moderate dominance (D) index, with values less than 0.4. The diversity index is higher in the forest floor than in suspended soils in the lowland and lower

Table 1. Observed and estimated species richness, and total abundance of springtails in two forest strata from three forest types at Mt. Makiling, Philippines. Estimated species richness is based on the extrapolation of the rarefaction curves to 24 (2n) samples. Lowland Lower montane Upper montane Floor Canopy Floor Canopy Floor Canopy Species richness (observed) 17 17 15 19 14 16 Total abundance (observed) 403 984 229 277 196 198 Chao-1 (mean) 23 27 23 22 17 19 S(est) 95% CI lower bound 17 17 17 18 12 14 Species richness (estimated) 21 25 26 25 18 21 S(est) 95% CI upper bound 25 33 36 33 25 27 S(est) SD 2 4 5 4 3 3 Completeness ratio 72.37 62.99 64.79 84.48 81.21 84.25

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Figure 2. Mean species richness ± standard deviation (A) and mean overall abundance ± standard error (B) of springtails collected in the canopy and forest floor of three elevational sites in Mt. Makiling, Philippines.

Table 2. Calculated diversity indices of springtail assemblage in the canopy and forest floor of three elevational sites (lowland, lower montane, and upper montane forests) in Mt. Makiling, Philippines. Lowland Lower montane Upper montane Floor Canopy Floor Canopy Floor Canopy Simpson_1-D 0.8624 0.6876 0.7266 0.7051 0.7147 0.8309 Simpson_1/D 3.2010 7.2674 3.3909 3.6576 5.9136 3.5050 Dominance 0.1376 0.3124 0.2734 0.2949 0.2853 0.1691 Evenness 0.5456 0.2733 0.3752 0.3144 0.3746 0.4795

montane forests. There is an increasing trend of diversity Diversity t-test also reveals significant differences in the canopy in response to increasing elevation while between the following: lowland floor vs. lowland canopy the forest floor has a decreasing diversity with increasing (p = 4.09 x 10–46); lowland floor vs. lower montane floor elevation. Consequently, the evenness indices followed (p = 4.26 x 10–8); lowland floor vs. upper montane floor the same trend as that of the diversity indices while the (p = 1.10 x 10–8); lowland canopy vs. upper montane dominance indices had an opposite trend. canopy (p = 2.4 x 10–20); lower montane canopy vs. upper montane canopy (p = 1.72 x 10–5); upper montane canopy and upper montane floor (p = 1.63 x 10–5).

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Species Composition and Assemblage for each sample site. Clustering analysis using the Bray-Curtis similarity index (Figure 3A) revealed three groups for the samples: A total of 31 morpho-species from eight families were one containing all forest floor samples from all forest collected. Five species were present on all samples, while types, another containing the canopy samples from the 13 species were present in all elevations and 16 in both lower montane and upper montane forest, and finally strata. Three species were unique in the lowland forest, the separated canopy samples from the lowland canopy. four in the lower montane forest, but none in the upper Similar clustering is observed with the Jaccard similarity montane forest. Meanwhile, 11 species were unique in the index (Figure 3B), except that the lowland canopy samples canopy and four from the forest floor. Each stratum (in were grouped closer with the forest floor samples. This general) and per elevation type also harbor unique species, is supported by the number of shared and unique species as shown in Figure 4.

Figure 3. Clustering analysis of all sample sites using A) Bray-Curtis and B) Jaccard similarity indices. Abbreviations: LLF – lowland forest floor; LLC – lowland canopy; LMF – lower montane floor; LMC – lower montane canopy; UMF – upper montane floor; UMC – upper montane canopy. Bootstrap support for nodes is shown.

Figure 4. Venn diagrams showing shared and unique springtails in the canopy and forest floor (total) and in different vegetation types in Mt. Makiling, Philippines.

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The results of PERMANOVA (Table 3) also indicated = 30.2%). This species was collected in both the canopy significant effects of elevation on species richness and of and forest floor but was more abundant in the forest strata on both species richness and total abundance. Both floor (lower montane = 103; upper montane = 87) than elevation and strata were also found to have significant in suspended soils (lower montane = 21; upper montane effects on the overall assemblage of springtails. The = 8). Next to the two species of mentioned, interaction of the elevation and strata was found insignificant the significant dissimilarity between the strata (canopy in this analysis. Post hoc analysis indicated significant vs. forest floor) of the three sites was also attributed differences in springtail assemblage between strata in all to Cryptopygus (s.l.) sp. and Lepidocyrtus sp. 2. These forest types (lowland: p = 0.0001; lower montane: p = species were collected in both the canopy and forest floor 0.0006; upper montane: p = 0.0001). Similarly, significant of all sites. No consistent trend was observed with the differences were noted between lowland floor and upper distribution of Cryptopygus (s.l.) sp, while Lepidocyrtus montane floor (p = 0.0069), lowland canopy and lower sp. 2 was found to be consistently more abundant in the montane canopy (p = 0.0007), and lowland canopy and canopy than the forest floor. upper montane canopy (p = 0.0004). Significant differences between the lowland canopy and SIMPER analysis (Table 4) indicated that three lower montane canopy were attributed to Lepidocyrtus sp. Lepidocyrtus spp. () and one Cryptopygus 4 (31.59%), Lepidocyrtus sp. 2 (19.61%), and Cryptopygus (s. l.) sp. (Isotomidae) contributed the most to the (s.l.) sp. (10.69%). On the other hand, the significant dissimilarity between the species assemblage in the difference between the lowland and upper montane canopy canopy and forest floor of the three study sites. In the was due to three Lepidocyrtus species. In terms of the lowland forest, Lepidocyrtus sp. 4 contributed to the forest floor, significant differences between lowland forest most dissimilarity (26.43%), with 408 individuals from and upper montane were attributed to Cryptopygus (s.l.) the canopy and 35 individuals from the forest floor. sp. (22.3%), Lepidocyrtus coeruleocinctus Handschin Meanwhile, for lower montane and upper montane forests, 1930 (22.29%), and Alloscopus sp. (15.7%). All of these Lepidocyrtus coeruleocinctus contributed the most for morpho-species were found in all strata and study sites. the dissimilarity between the forest floor and canopy assemblage (lower montane = 29.41%; upper montane

Table 3. Summary results of PERMANOVA testing the effects of elevation (lowland, lower montane, upper montane), strata (canopy, forest floor), and interaction (elevation vs. strata) on total abundance, species richness, and assemblage composition based on families and species of springtails collected. Elevation Strata Interaction

F-value P-value F-value P-value F-value P-value Total abundance 1.2584 0.2533 7.3676 0.0042 –2.2030 0.9995 Species richness 2.8903 0.0180 5.4415 0.0038 –2.0532 1.0000 Assemblage 2.2357 0.0018 11.2890 0.0001 –0.7219 0.2035

Table 4. Summary results of SIMPER showing the top three springtail taxa contributing to differences in species assemblage composition between strata (canopy vs. floor) and elevation/study sites (lowland, lower montane, and upper montane forests). Lowland Lower montane Upper montane Lepidocyrtus sp.4 (26.43%) Lepidocyrtus coeruleocinctus(29.41%) Lepidocyrtus coeruleocinctus (30.2%) Canopy vs. Cryptopygus sp. (13.9%) Cryptopygus sp. (24.8%) Cryptopygus sp. (20.69%) Floor Lepidocyrtus sp.2 (13.22%) Lepidocyrtus sp. 2 (9.39%) Lepidocyrtus sp. 2 (11.85%) Lowland vs. Lower montane Lower montane vs. Upper montane Lowland vs. Upper montane Lepidocyrtus sp. 4 (31. 59%) – Lepidocyrtus sp. 4 (32.19%) Canopy Lepidocyrtus sp. 2 (19.61%) – Lepidocyrtus sp. 2 (20.02%) Cryptopygus sp. (10.69%) – Lepidocyrtus sp. 1 (9.862% – – Cryptopygus sp. (22.3%) Floor – – Lepidocyrtus coeruleocinctus (22.29%) – – Alloscopus sp. (15.7%)

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DISCUSSION The prevailing environmental conditions might also have immense effects on the decreasing total abundance Springtails, despite being minute and wingless, are among and richness from the lowland to the montane forests. the major arthropod groups present in the suspended soils With respect to elevation, temperature and soil pH also in the canopy layer of the forest (Basset 1998). In this decrease from the lowland forest to the upper montane study, the composition of species assemblages in the two forest. The species of Collembola differ in their preferred forest strata (floor and canopy) from three elevational habitat temperature range, but the majority of species live forest types (lowland, lower montane, and upper montane in regions without extreme cold temperatures (Hopkin forest) in Mt. Makiling was found to be significantly 1997). Though the temperature in the lower and upper different. montane forests is not yet physiologically damaging Unlike what we hypothesized, only the mean abundance for most springtail species, our results suggest that the was found to be higher in the suspended soil than the temperature in the lowland forest is favored by most forest floor. The mean species richness was higher springtails. The decreasing abundance and richness with in the forest floor than in suspended soil. The higher increasing soil acidity suggest that springtails, just like surface areas in the forest floor compared to the canopy most organisms, prefer basic than acidic soil. The negative layers may have contributed to the higher mean species effects of soil acidity on plants (limiting the availability richness observed in the forest floor. A study by Paoletti of nutrients, productivity, and biomass production) et al. (1991) also showed that the forest floor harbors and other soil-dwelling (nematodes and other more abundant and diverse soil fauna than the canopy. burrowing organisms) may account for this (Lavelle et al. However, it was observed that the suspended soils 1995; Fujii 2014; Ponge 2014). Collembola species have were more densely populated compared to the forest also been documented to show sensitivity to changes in floor. The same study also reported that suspended soil soil pH, thus being used as bioindicators on changes in contains a higher concentration of minerals and nutrients, land-use (Vilkamaa and Huhta 1986; Fiera 2009). Lastly, highlighting the ability to cater to more species. Similar the relative humidity is also known to highly affect the patterns of higher species richness in the canopy vs. floor survival of springtails since most of them have cutaneous were already recorded in previous studies in beetles of respiration, meaning gas exchange occurs through the skin Sulawesi (Hammond 1990) and mites of Australia (Walter or cuticle (Davies 1928). Except for some species of a few et al. 1998). Also, Basset et al. (1992) and Lowman and genera such as Sminthurus, Sminthurides, Sphyrotheca, Rinker (2004) noted that arthropod diversity is higher in etc., with special respiratory organs, low relative humidity the canopy compared to the understory strata. has been known to be detrimental to most springtail species (Hopkin 1997). This may have caused the high The present study shows that the diversity of canopy mean species richness recorded in the lowland forest, and forest floor springtails follow a contrasting pattern which recorded the highest relative humidity (75.83%). along an elevational gradient. The diversity in the canopy This may also denote that most of the species collected increases with elevation, while that of the forest floor in the study have cutaneous respiration. decreases. The pattern of diversity observed in the canopy springtails follows the same pattern of edaphic arthropods A clear distinction in the faunal composition of springtail (in general) reported by Sadaka and Ponge (2003) and assemblage in both strata (canopy vs. forest floor) Cutz-Pool et al. (2010). On the other hand, the forest floor and elevation was observed in a tropical forest in the springtails concur with the pattern of diversity observed Philippines. The distinct assemblages along elevation in mammals (Heaney 2001), as well as birds and vascular gradients concur with other studies on temperate forest plants (O’Donnell and Kumar 2006), which decreases with springtails (Maunsell et al. 2013) and with other tropical increasing elevation. This may also suggest that springtails forest arthropods (Nunes et al. 2016; Brehm et al. 2018; follow the “arboreality hypothesis” in frogs proposed by Longino et al. 2019). The distinct springtail communities Scheffers et al. (2013), in which arboreality increases along an elevation gradient may be linked to the known with increasing elevation. This pattern has been important effects of elevation on the properties, temperature, and in predicting the possible effect of climate change on moisture of soil (Jiang et al. 2015). In addition to the rainforest species, which has the ability to shift in habitat effects of the elevational gradient in soil, the changes to compensate for changes in temperature. However, this in vegetation composition may have also contributed to pattern of diversity is not universal, with other arthropod distinct communities per elevation (Bokhorst et al. 2018). groups such as ants and mites following the opposite trend Results of this study also highlight the distinctness of the (Jing et al. 2005; Ghosh-Harihar 2013), while another canopy layer with respect to the forest floor, which has study on springtails showed no pattern along an elevation also been observed for beetles (Stork and Grimbacher gradient (Jiang et al. 2015). 2006), moths (Ashton et al. 2016), and arthropods in general (Basset et al. 2015). Faunal boundaries have been

570 Philippine Journal of Science Alviola et al. Collembola Across Vol. 150 No. S1, Special Issue on Biodiversity Elevation and Forest Strata found between the soil/litter layers, between the canopy described worldwide (Bellinger et al. 2019). Members of layers, and sometimes between the upper and lower the genus are also known to be habitat generalists, being canopy levels (Rodgers and Kitching 1998; Basset et al. widely distributed and occurring in almost all terrestrial 2015). This has been pronounced in tropical rainforests habitats (Zhang et al. 2018). Some species have also with well-delineated canopy layers, which may influence developed specialized adaptations such as egg diapause arthropod species to forage on their preferred strata and demographic strategies to ensure the survival of within the forest (Basset et al. 2003). The preference more individuals, probably contributing to their high of arthropods varies greatly with their food preferences abundances and presence in all study sites (Leinaas and in which fungivores and herbivores are most likely to Bleken 1983). Since Lepidocyrtus species collected were prefer the canopy layers, while the food generalists – identified only up to morpho-species, further taxonomic including scavengers and detritivores – usually forage studies are being recommended to determine the specific on the forest floor (Basset et al. 2015). Springtails, being niche of each species. On the other hand, Cryptopygus mostly detritivores and fungivores, may be expected in (s.l.) (Potapov et al. 2020; Family Isotomidae) is a both forest strata. Maunsell et al. (2013) highlighted the taxonomically complicated genus with several species effect of species or taxonomic level of identification in described worldwide (Bellinger et al. 2019). Lastly, studies concerning springtail ecology. Alloscopus sp. was found to be widely distributed in the study (collected in all strata and study sites) but was Species assemblages from the forest floors are closely not as abundant as the other representative species from related to one another unlike that of the canopy, where Lepidocyrtus and Cryptopygus. Only 40 individuals of only the upper montane and lower montane are similar. Alloscopus sp. were collected in the study. The shared species between elevation and strata suggests that several species of springtails are able to move between Looking separately at the springtail assemblage in the forest strata and forest types. Despite being wingless, the canopy and in the forest floor, it can be noted that springtails are able to disperse over long distances. Due the higher elevation sites (lower montane and upper to their minute size, several species of springtails are montane forests) did not differ significantly in springtail dispersed by wind, especially in colder regions (Hawes assemblage. The adjacent location of these study sites, et al. 2007; Flo and Hagvart 2013). Meanwhile, fossil in addition to almost the same prevailing environmental evidence suggests that some species disperse over long conditions (that goes along with changes in elevation), distances by attaching themselves to larger alates of social may have accounted for this result. In the canopy springtail insects (Robin et al. 2019), an event rarely observed in assemblage, significant differences at higher elevation present species. Basset (1998) noted that the occurrence of sites were observed when compared to the lowland canopy dwelling springtails, mites, and arachnids (Stork forest. The same genera (Lepidocyrtus and Alloscopus) and Brendell 1990) on the forest floor of montane forests contributed highly to this observed difference. In contrast, may be attributed to the moss and epiphytes on a tree in the forest floor assemblage, only upper montane and trunk, linking the two strata. Despite that, the springtail lowland forests were found to be significantly different. In assemblage between the canopy and forest floor of addition to Lepidocyrtus and Alloscopus, another species both montane forests in this study remains significantly from Alloscopus has highly influenced the results. different. Six morpho-species were found to highly contribute to significant differences observed in the springtail CONCLUSION assemblage in the study. Four out of these six species were from the genus Lepidocyrtus sp., while the other Data analyses used in this study generated several two species were from Cryptopygus (s.l.) and Alloscopus. significant results despite the fact that the completeness They were observed in all of the study sites in both the ratio of all sites was less than 85%. The faunal composition canopy and forest floor. of springtail assemblages showed a significant response in both elevation and strata (canopy vs. forest floor) in Mt. At the genus level, the relative abundances of Lepidocyrtus Makiling, Philippines. and Cryptopygus (s. l.) have shown to cause significant differences in the springtail assemblage of canopy vs. The forest floor species assemblages are closely related forest floor. These two taxa highly contributed to the to each other unlike those of the canopy, where only distinctness of assemblages in each stratum as they were the upper montane and lower montane are similar. The present in both the canopy and forest floor of all study distinctiveness of these springtail assemblages in the sites. This is not surprising for Lepidocyrtus, known to be canopy and higher elevation areas suggests a need to one of the most abundant springtail genera worldwide. As improve our biological data in areas or habitats often a matter of fact, it is known to have more than 400 species neglected by standard biological surveys.

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ACKNOWLEDGMENTS DEJEAN A, FAGAN JL, FLOREN A, KITCHING RL, MEDIANERO E, DE OLIVEIRA EG, ORIVEL This work was funded by the Department of Science J, POLLET M, RAPP M, RIBEIRO SP, ROISIN Y, and Technology (DOST)–Philippine Council for SCHMIDT JB, SORENSEN L, LEWINSOHN TM, Agriculture, Aquatic, and Natural Resources Research LEPONCE M. 2015. Arthropod distribution in a and Development; DOST–Science Education Institute tropical rainforest: tackling a four dimensional puzzle. Accelerated Science and Technology Human Resource PLoS ONE 10(12): e0144110. doi:10.1371/journal. Development Program; DOST–National Research pone.0144110 Council of the Philippines; Center for Systematic Entomology; and UPLB Institute of Biological Sciences BELLINGER PF, CHRISTIANSEN KA, JANSSENS (IBS). The authors would also like to thank the following F. 2019. Checklist of the Collembola of the World. institutions and persons: MCME, UPLB Museum of Retrieved on December 2019 from http://www.col- Natural History, Florida State Collection of Arthropods, lembola.org Florida Department of Agriculture and Consumer BOKHORST S, VEEN GFC, SUNDQVIST M, DE Services, UPLB IBS–Cave Ecology Laboratory, Mr. LONG JR, KARDOL P, WARDLE DA. 2018. Con- Jeremy Carlo B. Naredo, Mr. Orlando L. Eusebio, Mr. trasting responses of springtails and mites to elevation Joseph B. Rasalan, Mr. Maximo D. Tandang, Mr. Jose S. and vegetation type in the sub-Arctic. Pedobiologia – Duya, and Ms. Kexya O. Gustilo. Journal of Soil Ecology 67: 57–64. BREHM G, ZEUSS D, COLWELL RK. 2018. Moth body size increases with elevation along a complete tropi- REFERENCES cal elevational gradient for two hyperdiverse clades. Ecography 42(4): 632–642. ABRAHAM ERG, GONZALEZ JCT, CASTILLO ML, LIT IL JR., FERNANDO ES. 2010. Forest cover and CASSAGNE N, GAUQUELIN T, BAL-SERIN MC, biodiversity profile of the crater area of Mt. Makiling, GERS C. 2006. Endemic Collembola, privileged Luzon, Philippines. Asia Life Sciences Supplement bioindicators of forest management. Pedobiologia 4: 49–82. 50: 127–134. ASHTON LA, NAKAMURA A, BASSET Y, BURWELL CHAO A. 1984. Non-parametric estimation of the number CJ, CAO M, EASTWOOD R, ODELL E, DE OLIVEI- of classes in a population. Scandinavian Journal of RA EG, HURLEY K, KATABUCHI M, MAUNSELL Statistics 11: 265–270. S, MCBROOM J, SCHMIDT J, SUN Z, TANG Y, CHRISTIANSEN K, BELLINGER P. 1980. The Col- WHITAKER T, LAIDLAW MJ, MCDONALD WJF, lembola of North America moth of the Rio Grande. KITCHING RL. 2016. Vertical stratification of moths A taxonomic analysis. Grinnell College, Grinnell, across elevation and latitude. Journal of Biogeography Iowa. 1322p. 43: 59–69. COLWELL RK. 2013. EstimateS: statistical estimation BASSET Y, ABERLENC HP, DELVARE G. 1992. of species richness and shared species from samples. Abundance and stratification of foliage arthropods in a Version 9 – User’s Guide and Application. http://purl. lowland rainforest of Cameroon. Ecological Entomol- Oclc.Org/estimates ogy 17: 310–318. CUTZ-POOL L, PALACIOS-VARGAS J, CANO-SAN- BASSET Y. 1998. Invertebrates in the canopy of tropi- TANA Z, CASTAÑO-MENESES G. 2010. Diversity cal rain forests: how much do we really know? Plant patterns of Collembola in an elevational gradient in the Ecology 153: 87–107. NW slope of Iztaccihuatl Volcano, State of Mexico, BASSET Y, NOVUTNY V, MILLER SE, KITCHING Mexico. Entomological News 121(3): 249–261. RL eds. 2003. Arthropods of Tropical Forests. Spatio- DAVIES WM. 1928. The effect of variation in relative temporal Dynamics and Resource Use in the Canopy. humidity on certain species of Collembola. Journal of USA: Cambridge University Press. 474p. Experimental Biology 6: 79–86. BASSET Y, CIZEK L, CUENOUD P, DIDHAM RK, NO- DEHARVENG L, BEDOS A. 2004. Insecta: Collembola. VOTNY V, ODEGAARD F, ROSLIN T, TISHECH- In: Freshwater Invertebrates of the Malaysian Region. KIN AK, SCHMIDL J, WINCHESTER NN, ROUBIK Yule CM, Yong HS eds. Malaysia: Academy of Sci- DW, ABERLENC HP, BAIL J, BARRIOS H, BRIDLE ences, Malaysia. p. 384–393. JR, MENESES GC, CORBARA B, CURLETTI G, DE LA ROCHA W, DE BAKKER D, DELABIE JHC,

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APPENDIX

Mean abundance (± SE) of taxa of Collembola recorded in the canopy and forest floor of three elevational sites in Mt. Makiling, Philippines. Lowland Lower montane Upper montane Canopy Floor Canopy Floor Canopy Floor Order Poduromorpha Family Neanuridae Ceratrimeria sp. 0 0.25 (± 0.13) 0 0.92 (± 0.67) 0.00 0.17 (± 0.17) Neanura hirtella 0 0.42 (± 0.42) 0.17 (± 0.11) 0.33 (± 0.22) 0.17 (± 0.11) 0.00 Neanura sp. 1.17 (± 1.17) 0.42 (± 0.34) 0 0.08 (± 0.08) 0.08 (± 0.08) 0.00 Family Hypogastruridae Xenylla sensilis 0.42 (± 0.23) 0.5 (± 0.36) 0.25 (± 0.25) 0.17 (± 0.17) 1.08 (± 0.48) 0.08 (± 0.08) Order Entomobryomorpha Family Isotomidae Cryptopygus (s.l.) sp. 2 (± 1.29) 7.08 (± 2.06) 11.75 (± 10.9) 4.42 (± 1.45) 2.92 (± 1.86) 4.5 (± 1.54) Proisotoma sp. 0 0 1.25 (± 1.25) 0 3.75 (± 2.67) 0.00 Family Entomobryidae Alloscopus sp. 3.58 (± 3.58) 6.58 (± 4.51) 0.08 (± 0.08) 0.92 (± 0.50) 0.08 (± 0.08) 1.17 (± 0.77) Lepidocyrtus sp. 1.92 (± 0.87) 2.25 (± 1.04) 1.5 (± 0.53) 0.42 (± 0.34) 2.33 (± 1.02) 0.08 (± 0.08) Lepidocyrtus coeruleocinctus 0 5.58 (± 1.67) 1.75 (± 1.06) 8.58 (± 2.60) 0.67 (± 0.36) 7.25 (± 1.51) Lepidocyrtus sp. 2 29.8 (± 20.96) 1.58 (± 1.58) 3.17 (± 2.47) 0.08 (± 0.08) 4 (± 1.83) 0.67 (± 0.40) Lepidocyrtus sp. 3 0 0.08 (± 0.08) 0 0 0.00 0.33 (± 0.19) Lepidocyrtus sp. 4 34 (± 16.92) 2.92 (± 1.98) 0 0.08 (± 0.08) 0.00 0.00 Lepidocyrtus sp .5 5.5 (± 2.19) 0 0 0 0.25 (± 0.25) 0.00 Lepidocyrtus sp. 6 0.92 (± 0.92) 0 0 0 0.00 0.00 Lepidocyrtus sp. 7 0 0.17 (± 0.11) 0 0 0.00 0.00 Lepidosira sp. 0.42 (± 0.34) 0 0.58 (± 0.50) 0 0.00 0.00 Seira schaefferi 0 0 0.08 (± 0.08) 0 0.00 0.00 Seira sp. 0 0 0.08 (± 0.08) 0 0.00 0.00 Willowsia jacobsoni 0.08 (± 0.08) 0 0 0 0.00 0.00 Family Paronellidae Bromacanthus sp. 0 0 0 0.08 (± 0.08) 0.08 (± 0.08) 0.00 Callyntrura aff.gapudi 0.17 (± 0.11) 3.42 (± 0.54) 0 2 (± 0.65) 0.00 1 (± 0.48) Callyntrura aff. zonata 0 0 0.17 (± 0.11) 0 0.00 0.00 Lepidonella sp. 0.25 (± 0.25) 0.58 (± 0.43) 0 0 0.00 0.25 (± 0.13) Salina indica 0 0 0.17 (± 0.11) 0 0.08 (± 0.08) 0.00 Salina sp. 0.17 (± 0.11) 0.42 (± 0.34) 0.5 (± 0.23) 0.33 (± 0.26) 0.25 (± 0.18) 0.00 Salina sp. 2 0.58 (± 0.50) 0 0.17 (± 0.17) 0.25 (± 0.18) 0.17 (± 0.11) 0.08 (± 0.08) Order Neelipleona Family Neelidae Neelus sp. 0 0 0.08 (± 0.08) 0 0.17 (± 0.17) 0.00 Order Symphypleona Family Dicyrtomidae Ptenothrix sp. 0.08 (± 0.08) 0.08 (± 0.08) 0 0 0.00 0.08 (± 0.08) Family Sminthurus sp. 0 0 0.08 (±0.08) 0 0.00 0.00 Sphyrotheca sp. 0 0 0 0.5 (± 0.34) 0.00 0.5 (± 0.34) Sphyrotheca cf. dawydoffi 0.92 (± 0.75) 1.25 (± 0.52) 1.17 (± 0.91) 0 0.42 (± 0.29) 0.17 (± 0.11)

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