Philippine Journal of Science 150 (S1): 525-537, Special Issue on Biodiversity ISSN 0031 - 7683 Date Received: 04 Oct 2020

Diversity of Land Snails in the Karst Areas of Sta. Teresita, Cagayan Province, Island with Notes on New Distribution Records

Julius A. Parcon1*, Ireneo L. Lit Jr.1,2, Ma. Vivian C. Camacho1,2, and Emmanuel Ryan C. de Chavez1,2

1Museum of Natural History 2Institute of Biological Sciences, College of Arts and Sciences University of the Los Baños, College 4031 , Philippines

Malacofaunal research in a karst ecosystem is very limited not only in the northern region of Luzon Island but in the entire Philippines amidst extensive habitat disturbance and destruction. To address this, the diversity and abundance of land snails in the karst areas of Santa Teresita, Cagayan Province were determined. A total of 25 5 x 5 m2 quadrats were randomly set in five stations in the karst landscape. A total of 1206 land snails comprising 45 under 36 genera representing 17 families were sampled. was the most represented family with 10 species. Luzonocoptis antennae constituted 25.1% of the total number of samples (303 individuals) and was the most abundant species in all stations. Of the 36 genera, five are new records in the Philippines. Several karst endemics and introduced species were recorded. Diversity indices showed diverse fauna with Shannon-Weiner diversity index (H’) of 2.80, with evenness (J’) of 0.36 and dominance index of (D’) of 0.11. Species accumulation curve (SAC) showed late asymptote with a completeness ratio of 0.92. The study demonstrated that land snails in Sta. Teresita, Cagayan Province are rich and diverse. It is very important to recognize Sta. Teresita as priority sites for malacofaunal conservation, and consider the further evaluation of these sites to be designated as a protected area.

Keywords: biodiversity, Cagayan, karst, land snails, limestone

INTRODUCTION 2004), hunting of bats for food (Scheffers et al. 2012), and uncontrolled tourism (Alcala et al. 2007). Furthermore, The Philippines has tropical karsts that cover about 10% biodiversity documentation in these habitats is among 2 (approximately 35,000 km ) of the country’s land area the most neglected, where only 10% of the total karsts (Piccini and Rossi 1994). The 29% (approximately 10,150 have been surveyed (NRCP 2016). Most available 2 km ) of these karst landscapes have been declared as studies were conducted on the diversity and ecology of either a national park, national monument, or a protected cave-dwelling bats from different islands (Quibod et al. landscape (Restificar et al. 2006). However, many karsts 2019). The scarcity of biological information on karsts in remote areas still lack institutionalized protection. could eventually weaken the justification in the long run These ecosystems are adversely affected by anthropogenic for the conservation of various karst-associated species activities such as limestone mining, phosphate and guano despite the increasing number of threats, which could lead extraction, harvesting of edible swiftlet nests (Hobbs to localized extinctions. *Corresponding Author: [email protected]

525 Philippine Journal of Science Parcon et al.: Diversity and Distribution of Land Vol. 150 No. S1, Special Issue on Biodiversity Snails in Sta. Teresita, Cagayan, Philippines

Tropical karsts are known as biodiversity arks due to of which 171,362 ha are classified as secondary and their high species diversity arising from a multitude old-growth forests, while 3,081 ha are mossy forests. of ecological niches afforded by variable climatic The biodiversity in NECKBA is not well studied; conditions, fissured cliffs, and extensive caves (Clements however, it is considered as among important sites et al. 2006). These are unique ecosystems characterized harboring various threatened endemic species of flora by high calcium carbonate deposits considered as and fauna such as the Rafflesia leonardii, Philippine eagle evolutionary hotspots for speciation and function as (Pithecophaga jefferyi), and the Northern Luzon Giant habitat islands for many calcium-dependent , Cloud Rat (Phloeomys pallidus). The baseline data on including land snails (Schilthuizen et al. 2003; Clements the malacofauna of its karst areas is still lacking. If there et al. 2006). On the other hand, non-karst habitats such are existing records, these are probably unpublished as tropical rainforest make unfavorable habitats for land or remain as gray literature. Thus, in this preliminary snails due to lack of available nutrients, negligible litter, study, we determined and analyzed the land snail diversity and abundance of predators (Solem 1984; Schilthuizen patterns on the limestone hills of Sta. Teresita. and Rutjes 2001). The Philippines harbors 31% (22,000 out of 70,000 species) of all mollusks described worldwide (Ong et MATERIALS AND METHODS al. 2002) with approximately 90–95% endemism, but most of the recorded are marine species. There are very few terrestrial malacological studies (Bartsch 1909; Study Site Clench and Archer 1931; Faustino 1930; Valdez et al. Sta. Teresita (18°15'0" N, 121°53'0" E) in Cagayan 2021) that particularly focus on karsts. However, many Province is a fourth-class municipality that is 588 km researchers in the country are less interested to study land away from (Figure 1). Its altitude ranges from snails. Some of the reasons could be the inaccessibility 26–72 m above sea level. The area has a Type III climate of literature on Philippines mollusks, particularly on where rainfall is evenly distributed throughout the year . According to Springsteen and Leobrera mainly due to the northeast trade winds. From November– (1986), the taxonomy of these animals is likewise in a January, the northwest monsoon from East Asia brings dry state of flux due to many species are morphologically and cool winds to this valley floor. Because of the open very similar and it is difficult to identify the specimen coastline, it experiences cold mornings and evenings, even at a family level. Moreover, juveniles are sometimes with average temperatures ranging from 18–21 °C. hardly distinguishable from their adult forms. It also The soil pH is neutral ranging from 7.6–7.8, relative requires skill to find land snails in their natural habitat, and humidity from 86.77–99%, soil moisture from 4.84–8.12 3 –3 perhaps being a non-charismatic few students and m ∙ m , calcium content from 22.86–30 (me/100 g). researcher are not attracted to study them. Interestingly, Karst ecosystem of Sta. Teresita is composed of conical many new species are still being discovered; for instance, hills fragmented by non-calcareous agricultural land in there were new genera, eight new species, and two new several hundreds of meters. It has an altitude ranging subspecies described between 2017–2020 alone (Páll- from 12–72 masl with secondary and old-growth forest. Gergely et al. 2017; Batomalaque and Rosenberg 2018; Five sampling stations were randomly chosen – namely, Páll-Gergely and Schilthuizen 2019; Páll-Gergely and Ari Zero, Ari Zero-1, Bangalao, Maquera, and Tabaco Auffenberg 2019; Lipae et al. 2020). with an approximate total area of 7,878 ha. These sites are forms of conical limestone hills with caves. Likewise, Among the remote karst landscapes in the northern most sites have fragmented secondary forests surrounded region of Luzon is Santa Teresita in Cagayan Province. by agroecosystems (mostly corn and vegetable plantation) This municipality is located in the northeastern region of except for Maquera, which is located in the middle of the the Cagayan Valley Basin (CVB), a north-south trending mature second-growth forest with the presence of large sedimentary basin bounded by the Cordillera mountain trees and thick vegetation adjacent to cornfields and range in the west and Sierra Madre mountain range in vegetable farms. the east. The CVB began to form during the Oligocene as the South China Sea Plate under the Philippine Mobile Belt headed east as the western subduction was Land Snail Sampling ceased along the Luzon Trough (UPLB-MNH 2018). Samples were collected from December 2017–February Sta. Teresita is also within the coverage of the Northeast 2018 using the protocol adapted from Clements et al. Cagayan Key Biodiversity Area (NECKBA), which lies (2006), de Chavez and de Lara (2011), and Uy et al. in the northeastern tip of the Sierra Madre Mountain (2018). Within a station, five 5 x 5 m quadrats were Range. NECKBA covers an area of about 183,430 ha, set randomly located within the outcrops near or at the mouth of the caves and on limestone rocks at least 10 m

526 Philippine Journal of Science Parcon et al.: Diversity and Distribution of Land Vol. 150 No. S1, Special Issue on Biodiversity Snails in Sta. Teresita, Cagayan, Philippines

Figure 1. Location of sampling sites in Sta. Teresita Cagayan, Philippines (map source: Google Earth satellite image using QGIS ver 3.4 Madier; photo by J.A. Parcon).

to standardize the sampling. Macro snails (> 5 mm) with live and empty shells were searched – particularly on each microhabitat like bark and buttresses of trees, rotting logs, and undersides of epiphytes and palms. To obtain the overall diversity of the sampling sites and to increase the sample size, live snails and empty shells were pooled together (de Winter and Gittenberger 1998; Raheem et al. 2008). Some of the empty shells were collected while live specimens were then photographed and returned to their original habitat after taking their pictures. Empty shells and live snails were identified up to species level and verified using the published literature (Bartsch 1909; Faustino 1930; Springsteen and Leobrera 1986; Hemmen et al. 1987; Bouchet et al. 2017). For micro snails, samples were searched and collected by direct hand-picking on tree branches and on cave entrances Figure 2. Sample and individual-based species accumulation curve and surface of limestone formations (boulders and small of land snails in Sta. Teresita, Cagayan, Philippines. rocks). Specimens were stored in 1.5-mL microcentrifuge tubes containing absolute ethanol to preserve their DNA. In addition, 1 L of topsoil per quadrat (6 L per site) was apart. Overall, a total of 25 quadrats were established for also collected from the upper 5 cm layer using a spade and all sampling sites. We applied a combination of visual a plastic measuring cup from microhabitats such as soil searching and sorting of a standard volume of litter under rotten logs, dry leaves, in between rock, and rubbles and soil, as recommended for land snail inventories if between trees within the plot and stored in separate plastic repeated visits are not possible (Nurinsiyah et al. 2016). zipper bags. Soil samples were also collected from the A 30-min sampling effort per person/quadrat was allotted cave entrances. In the laboratory, soil samples were placed

527 Philippine Journal of Science Parcon et al.: Diversity and Distribution of Land Vol. 150 No. S1, Special Issue on Biodiversity Snails in Sta. Teresita, Cagayan, Philippines in separate basins and were sun-dried for at least a week of occurrences of individuals in the various species to remove all moisture content. Afterward, soil samples (Brower et al. 1989). Species density is the number of were subjected to cascade sieving using 1 mm steel mesh. individuals expressed per unit area. A portion of the sieved soil was stored in a container for the measurement of soil pH and exchangeable calcium. SAC. SAC was generated in order to determine the During sieving, each soil sample was systematically sampling efficiency for all the sites. Sampling efficiency sorted by hand-picking the micro land snails with the aid was evaluated using the completeness ratio (CR = of a magnifying lens. After sorting, micro snails were estimated number of species/observed number of species) photographed under a stereomicroscope with an attached (Clements et al. 2006). All species estimates were camera (Leica A-60). At least 10 frames were captured computed using Estimates ver 8.0 (Colwell 2006). The at every angle subjected to image stacking. Identification completeness ratio, which is equal to the estimated number of micro snail was conducted using published literature of species divided by the observed number of species, was by Faustino (1930), Uchida et al. (2013), Páll-Gergely et calculated to determine sampling efficiency. al. (2017), Foon et al. (2017), and Phung et al. (2018). Unidentified snails were assigned as morpho-species. All specimens were deposited and cataloged in the mollusk collection of the University of the Philippines Los Baños RESULTS Museum of Natural History (UPLB-MNH). Land Snail Fauna A total of 1,206 individuals (0.83% live snails and Data Analysis 99.17% empty shells) comprising 45 species and 36 genera Species richness, abundance, and rarity. Species richness representing 17 families were sampled in Sta. Teresita, and relative abundance per quadrat were determined. The Cagayan (Table 1). Camaenidae was the most represented total number of species per site was considered as species family with 10 species recorded from all sites, followed by richness while individual counts for a species as species Diplommatinidae with seven species, then by Chronidae abundance. Relative abundance computed as: (5), (4), (3) Subulinidae (3), Species and then Helecinidae (2) and (2). Other Relative abundance families such as , Assimineidae, , ×100 abundance = Total number Diapheridae, Dyakiidae, Gastrocoptidae, Hydrocinidae, of abundance Pupinidae, and Vertiginidae were represented by a single species. Among all species observed, Luzonocoptis Species with less than 0.5% of the total individual count antennae was the most numerous (303) and constituted are considered rare (Emberton et al. 1997). 25.1% with a mean density of 12.12/m2 from the entire samples. It was found in all sites but was most abundant Diversity indices and species density. The species in Ari Zero (96) and the fewest in Maquera (21). diversity indices of the land snails were determined using Luzonocoptis angulata was the second most abundant PAST (Paleontological Statistics) version 3.14 software species (144) and constituted 11.94%, with a mean density (Hammer et al. 2016). A good measure of diversity takes of 5.7/m2 from the entire samples (Table 1). These top into account both the number of species and the evenness

Table 1. Relative abundance, relative density, and rare land snails recorded in the karst areas of Sta. Teresita, Cagayan Province, Philippines. Family Species Ari Ari Bangalao Maquera Taba Total Relative Relative Remarks Zero Zero-1 abundance density co (%) (25m2) Achatinidae Lisachatina fulica Ferussac, 9 12 3 1 14 39 3.23 1.56 1821* Ariophantidae Ariophanta sp.** 1 1 0 4 0 6 0.49 0.24 Rare Euplecta sp. ** 0 0 0 1 0 1 0.08 0.04 Rare Microcystina sp** 5 8 2 2 1 18 1.49 0.68 Assimineidae Acmella polita Möllendorff, 28 8 18 24 16 94 7.79 3.76 1887** Camaenidae Bradybaena fodiens (L. 9 6 9 12 0 36 2.98 1.44 Pfeiffer, 1845)*

528 Philippine Journal of Science Parcon et al.: Diversity and Distribution of Land Vol. 150 No. S1, Special Issue on Biodiversity Snails in Sta. Teresita, Cagayan, Philippines

Calocochlia festiva (Donovan, 0 0 1 13 0 14 1.16 0.56 1825)** Chloraea psittacina 4 1 7 4 0 16 1.32 0.64 (Deshayes, 1861)** Chloraea bifasciata 0 0 1 0 0 1 0.08 0.04 Rare multifasciata Möllendorff, 1898** Chloraea smaragdina 0 0 0 1 0 1 0.08 0.04 Rare (Grateloup, 1840)** Pachysphaera sphaerica (G.B 0 0 1 3 0 4 0.33 0.16 Rare Sowerby I, 1841) ** Hypselostyla carinata 6 0 1 1 2 10 0.89 0.36 (Möllendorff, 1897)** Calocochlea lignaria (L. 6 4 5 6 2 23 1.90 0.92 Pfeiffer, 1846)+ Ganesella sp** 1 0 0 0 0 1 0.08 0.04 Rare Obba moricandi Pfeiffer, 1842 0 0 0 1 0 1 0.08 0.04 Rare Charopidae Charopa sp. **** 3 1 0 7 3 14 1.16 0.56 Chronidae Hemitrichiella setiger (G.B. 3 2 1 5 0 11 0.91 0.44 Sowerby I, 1841)** Hemiglypta cuvieriana (I. 3 0 0 9 0 12 0.99 0.48 Lea, 1840)** Kaliella micropetasus 1 3 0 7 0 11 0.91 0.44 Möllendorff, 1893** Kaliella microconus 0 0 1 0 0 1 0.08 0.04 Rare (Mousson, 1865)** Kaliella sp** 0 0 0 0 1 1 0.08 0.04 Rare Cyclophoridae sp**** 1 1 2 0 0 4 0.33 0.16 Rare woodianus Lea, 30 26 19 41 18 134 11.11 5.36 1862** Leptopoma helicoides 3 0 4 2 0 9 0.74 0.36 Grateloup, 1840** Lagocheilus sp *** 0 0 0 3 0 3 0.24 Rare Diapheridae Diaphera strophostoma 2 0 7 9 1 19 1.57 0.76 (Quadras and Möllendorff, 1896)** Diplommatinidae Palaina cristata Quadras and 17 14 11 38 15 95 7.87 3.80 Möllendorff, 1893 ** 0 2 0 19 0 21 1.74 0.84 Arinia pallida Möllendorff,1896 *** Diplommatina kochiana 0 0 1 2 0 3 0.24 0.12 Rare Möllendorff,1887** Diplommatina microstoma 2 2 0 5 0 9 0.74 0.36 Möllendorff,1887 *** Diplommatina sp.*** 0 0 0 2 0 2 0.16 0.08 Rare Luzonocoptis angulata Pall- 39 22 40 18 25 144 11.94 5.76 Rare Gegely & Hunyadi, 2017 *** Luzonocoptis antennae Pall- 96 42 68 21 76 303 25.12 12.12 Gegely & Hunyadi, 2017 *** Dyakiidae Dyakia sp. (juvenile) **** 0 0 0 1 0 1 0.08 0.04 Rare Gastrocoptidae Tonkinospira sp **** 7 0 5 1 0 13 1.07 0.52

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Helicinidae Ceratopoma cagayanica 2 3 1 3 1 10 0.82 3.76 Bartsch, 1921** Sulfurina citrina (Grateloup, 1 0 1 1 1 4 0.33 0.16 Rare 1840) ** Hydrocenidae Georissa carinulata Quadras 0 0 1 3 1 5 0.41 0.16 Rare &

Möllendorff, 1896*** Pupinidae Pupinella pupiniformis 0 0 5 0 0 5 0.41 0.20 Rare (Sowerby, 1842)** Subulinidae clavulinum (Potiez & 6 1 13 3 9 32 2.65 1.28 Michaud, 1838) * Allopeas gracile (T. Hutton, 6 3 7 6 5 27 2.23 1.08 1834) * Opeas nitidum Quadras & 0 0 6 0 0 6 0.49 0.24 Rare

Möllendorff, 1893 * Trochomorphidae Geotrochus conus (Philippi, 0 2 3 3 4 12 0.99 0.48 1841) **** Videna metcalfei Pfeiffer, 4 2 6 11 1 24 4.98 0.96 1845 ** Vertiginidae Nesopupa malayana (Issel, 0 0 1 4 1 6 0.49 0.24 Rare 1874) ** Total number of Individuals 295 166 251 297 197 1206 Number of species 27 22 31 38 20 45 Note: + endemic species, * invasive species, ** native species, ***karst-endemic, ****new country record. two abundant species from the family Diplommatinidae possibly new records in the country. These genera have were recently described by Páll-Gergely et al. (2017) in not yet been listed in the summary of land shells in the the town of Baggao, a nearby municipality from the study Philippines of Faustino (1930) and there is no other site. The 3rd in rank was Cyclophorus woodianus (134) updated Philippines checklist of land snails published. with a relative abundance of 11.11% with a mean density Thus, we included these genera as new records in the of 5.36 m2. On the other hand, twenty (20) species are country. rare in the study site with less than 0.5% relative density. Table 2 summarize the species diversity, evenness and Five introduced species were identified – namely, dominance index of land snails in the five stations of Lisachatina fulica (Achatinidae); Bradybaena fodiens Sta. Teresita, Cagayan. A total of 1206 individuals (Camaenidae); and Allopeas gracile, Allopeas clavulinum, were obtained from 45 different species with a Shannon and Opeas nitidum (Subulinidae). All introduced species Index score H’ = 2.80. It also obtained a Simpson index were collected in all sampling stations except for Opeas score of D’ = 0.108, which is near-zero, thus indicating a nitidum, which was only collected at Bangalao. All relatively high species diversity. Based on the Simpson recorded species with (**) were native in the country index of diversity (1-D), there is about an 89% probability except Calocochlea lignaria (L. Pfeiffer, 1846), which of obtaining two randomly chosen individuals belonging is endemic in Northern Luzon. Several karst-endemic to the two different species in the community, thus species were also recorded, such as Palaina cristata, suggesting a high species richness. Evenness index value Arinia pallida, Diplommatina kochiana, Diplommatina (J’ = 0.3361) that is closer to zero indicates few species microstoma, Diplommatina sp., Luzonocoptis antennae, dominating in the study site (Table 2). Luzonocoptis angulata (Diplommatinidae), and Georissa carinulata (Hydrocenidae). Interestingly, some genera of SAC land snails in this study such as Charopa sp. of the family The generated SACs compared the estimated species Charopidae (Figure 4H), Aulopoma sp. (Cylophoridae) richness to the number of individuals and quadrats of the (Figure 5F), Dyakia sp. (Dyakiidae) (Figure 7D), entire Sta. Teresita. The graph exhibited an α-dominated Tonkinospira sp. (Gastrocoptidae) (Figure 7E), and diversity characterized by late asymptote (Figure 3). Geotrochus conus (Trochomorphidae) (Figure 9A) were

530 Philippine Journal of Science Parcon et al.: Diversity and Distribution of Land Vol. 150 No. S1, Special Issue on Biodiversity Snails in Sta. Teresita, Cagayan, Philippines

Figure 3. Representative land snail species of Sta. Teresita, Cagayan, Figure 4. Representative land snail species of Sta. Teresita, Cagayan, Philippines: A) Lissahatina fulica (Bowdich, 1822) Philippines: A) Chloraea bifasciata multifasciata UPLMNHLS 001; B) Ariophanta sp. UPLMNHLS 003; Möllendorff, 1898 UPLBMNH 012; B) Chloraea C) Euplecta sp. UPLMNHLS 056; D) Microcystina sp. smaragdina (G.B Sowerby I, 1841) UPLBMNHLS 013 UPLBMNHLS 005; E) Acmella polita Möllendorff, 1887 (juvenile); C) Pachysphaera sphaerica (G.B Sowerby I, UPLBMNHLS 042; F) Bradybaena fodiens (L.Pfieffer, 1845) 1841), UPLBMNHLS 017; D) Hypselostyla carinata (I. UPLBMNH 008; G) Calocochlia festiva (Donovan, 1825) Lea, 1840) UPLBMNHLS 014; E) Calocochlea lignaria UPLBNH 009; H) Chloraeapsittacina UPLBMNH 012. (Pfieffer, 1846) UPLBMNHLS 015; F) Ganesella sp. UPLBMNHLS 019; G) Obba moricandi Pfeiffer, 1842 UPLBMNHLS 020; H) Charopa sp. UPLBMNHLS 021.

The sample-based and individual-based SACs showed very high completeness ratios for the karst area of Sta. Teresita (0.92). Table 2. Diversity indices obtain use to characterized malacofauna of Sta. Teresita, Cagayan Province, Philippines. Diversity index Values obtained Shannon (H’) 2.802 DISCUSSION Dominance (D’) 0.108 This study focused on the diversity and abundance of land Simpson (1-D) 0.892 snails since they are very vulnerable to human disturbance. Evenness (EH/S) 0.3661 The land snail assemblage in Sta. Teresita has a relatively higher diversity (45 species and 17 families) compared to 13 localities that were sampled by Uchida et al. (2013) in and Rutjes (2001) in Danum Valley, Sabah, Malaysia Sabah, Malaysia; these localities included three limestone with 61 species and 14 families. When compared to other outcrops, with 39 species belonging to 12 families. On the sites in the Philippines, the land snails diversity of Sta. other hand, the malacofaunal assemblage of Sta. Teresita Teresita Karst is similar to that of the Masungi Georeserve, Karst is lower than what was observed by Schilthuizen which has 43 species in 12 families (Valdez et al. 2021),

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Figure 5. Representative of land snail species of Sta. Teresita, Figure 6. Representative of land snail species of Sta. Teresita, Cagayan, Philippines: A) Hemitrichiella setigera (G.B. Cagayan, Philippines: A) Lagocheilus sp. UPLBMNHLS Sowerby, 1841) UPLBMNHLS 022; B) Hemiglypta 044; B) Diaphera strophostoma (Quadras and cuvieriana (I. Lea, 1840) UPLBMNHLS 057; C) Kaliella Möllendorff, 1896) UPLBMNHLS 052; C) Palaina micropetasus Möllendorff, 1893 UPLBMNHLS 023; D) cristata Quadras and Möllendorff 1893, UPLBMNHLS Kaliella sp. UPLBMNHLS 025; E) Kaliella microconus 048; D) Arinia pallida Möllendorff, 1896 UPLBMNHLS (Mousson, 1865) UPLBMNH 046; F) Aulopoma sp. 031; E) Diplommatina kochiana Moellendorf, 1887 UPLBMNHLS 026; G) Cyclophorus woodianus Lea, UPLBMNHLS 031; F) Diplommatina microstoma 1862 UPLBMNHLS 028; H) Leptopoma helicoides Moellendorf, 1887 UPLBMNHLS 033. Grateloup, 1840 UPLBMNHLS 029. but the former has more families. Sta. Teresita is also attributed to the acidic nature of rainforest soil due to the more diverse than Mt. Makiling having 24 species in litter composition that causes leaching of calcium necessary nine families (de Chavez de Lara 2011; Uy et al. 2018) for shells and egg production of the snails (Schilthuizen and Marinduque having 29 species in 16 families (Sosa and Rutjes 2001; Schilthuizen et al. 2003). Sta. Teresita et al. 2014). However, Mt. Makiling and Marinduque soil has an alkaline pH (7.6–7.8) with high calcium content are not comparable to this study because of the different (22.86–30 me/100 g), which is favorable to the calcium methodologies employed and different environments. requirement of the snails. Aside from this, the high species diversity in Ari Zero, Bangalao, and Maquera could also Land snails are abundant and species-rich in karst areas be attributed to the presence of large trees (such as Ficus because the calcium-rich soils favor their growth and spp.) with extensive canopy cover, which is suitable for reproduction (Graveland et al. 1994). According to both macro and micro snails. Large trees may accumulate Schilthuizen et al. (2003), calcium availability in karst a high organic layer that provides moisture to snails, thus are two to 10 times higher compared to non-limestone preventing desiccation (Kappes 2006). substrates. In fact, several calcicole micro snails were sampled in the study site, particularly Family The majority of land snails sampled in the study sites were Diplommatinidae with seven species recorded. In contrast, empty shells and only the undamaged shells were counted. the low abundance of land snails in the non-karst are These shells accumulated over the years possibly due to

532 Philippine Journal of Science Parcon et al.: Diversity and Distribution of Land Vol. 150 No. S1, Special Issue on Biodiversity Snails in Sta. Teresita, Cagayan, Philippines

Figure 7. Representative of land snail species of Sta. Teresita, Figure 8. Representative of land snail species of Sta. Teresita, Cagayan, Philippines: A) Diplommatina sp. Cagayan, Philippines: A) Georissa carinulata Quadras UPLBMNHLS 036; B) Luzonocoptis angulata Pall- & Möllendorff, 1896 UPLBMNHLS 043; B) Pupinella Gegely & Hundai, 2017 UPLBMNHLS 035; C) pupiniformis (G.B. Sowerby I, 1842) UPLBMNHLS Luzonocoptis antennae Pall-Gegely & Hundai, 2017 047; C) Allopeas clavulinum (Potiez & Michaud, 1838) UPLBMNHLS 034; D) Dyakia sp. UPLBMNHLS 006; UPLBMNHLS 053; D) Allopeas gracile (T. Hutton, E) ­­ Tonkinospira sp. UPLBMNHLS 045; F) Ceratopoma 1834) UPLBMNH 054; E) Opeas nitidum Quadras cagayanica Barstch, 1921 UPLBMNHLS 004; G) & Möllendorff, 1893 UPLBMNHLS 055; F) Vedina Sulfurina citrina Grateloup, 1840 UPLBMNHLS 041. metcalfei Pfeiffer, 1845 UPLBMNHLS 058.

their natural death or caused by predation. The perceived higher abundance and diversity on limestone may be artifactually increased since most of the assessments of snail abundance were based on the number of empty shells on the forest floor (Schilthuizen et al. 2003). These could be possibly a part of the longer persistence of shells rather than higher abundance. Given that snail population densities are higher on limestones, it is not surprising that diversities are higher (Schilthuizen et al. 2003). Based on the diversity index, Sta. Teresita’s diversity was high (H’ = 2.80) but lower when compared to Masungi Georeserve’s diversity index with H’ = 2.94 (Valdez et al. Figure 9. Representative of land snail species of Sta. Teresita, 2021). According to Magurran (2004), the diversity index Cagayan, Philippines: A) Geotrochus conus (L. Pfeiffer, 1841) UPLBMNH 024; B) Nesupupa malayana (Issel, in the natural ecosystem ranges from 1.5–3.5, wherein the 1874) UPLBMNHLS 059. value above 3.0 indicates a stable habitat while under 1.0

533 Philippine Journal of Science Parcon et al.: Diversity and Distribution of Land Vol. 150 No. S1, Special Issue on Biodiversity Snails in Sta. Teresita, Cagayan, Philippines indicates a highly disturbed environment. On the other dispersal of land snails, including , which have hand, Flores and Zafaralla (2012) stated that a diversity low natural mobility (Bergey et al. 2014). According index lesser than 2.5 is relatively low; thus, Sta. Teresita to Baguinon et al. (2003), the Philippines has a long has a relatively high diversity index. story of the introduction of plants; from pre-history to post-war, many exotic plants were brought here. Merrill Based on the SACs, land snail community assemblage (1912) also noted introduced plants in the Philippines in showed an α-dominated pattern in Sta. Teresita that is his flora publication. characterized by late asymptotes. An α-dominated pattern means that fewer quadrats and individuals were needed in Karst landscapes provide protection and safety to order to capture the entire species diversity. This indicates numerous species (Clements et al. 2006), in which the that many species can be found in a relatively small area surface vegetation is often distinctive and supports a wide and that these species are interactive. This also suggests range of karst-endemic species of plants, vertebrates, that the sampling sites were saturated, niche assembled, and and invertebrates – including the land snails. Limestone locally rich. According to Shackell et al. (2012), sites with hills form reservoirs for malacofauna by supporting a α-dominated diversity can recover faster from population large population and endemism. The extinction of some depletion than those with a β-dominated diversity. This is site-endemic species has been documented in Malaysia because an α-dominated diversity indicates species that (Vermeulen 1994). Sadly, the majority of the sampling are interactive. Thus, a locally depleted population can be sites in Sta. Teresita was also exposed to human activities replenished by a neighboring population. Since the study such as the conversion of a karst-forest ecosystem to site has an α-dominated pattern, it is possible that their forest agricultural areas via slash-and-burn and logging (Figure was repopulated caused by habitat destruction. Although the 10). Land snails are prone to natural and anthropogenic completeness ratio in Sta. Teresita is relatively high (0.92), disturbances. Micro land snails are more susceptible to the sampling is not enough as the asymptote graph is still disturbance due to their extremely limited mobility and going upward. This means that more species can be sampled dispersal (Baur and Baur 1998; Uy et al. 2018). Thus, in the study site. To capture the total diversity, more quadrats humans activities like this might put the land snails at risk (~ 25) and individuals (~ 1,206) were needed in order to for extinction. Thus, further research for the conservation attain a completeness ratio of 1. Furthermore, sampling for of biodiversity of the karst area is urgently needed to two periods with increased sampling effort can potentially develop and utilize sound-criteria for karst conservation increase the total diversity of land snails for this study. planning to prevent further population reductions and Nonetheless, the sample-based and individual-based SACs extinctions of karst-endemic species. in the study site showed a relatively high completeness ratio. Several introduced species were also documented in the sampling sites, such as the African giant snail CONCLUSION AND Lisachatina fulica, which was also reported by de Chavez and de Lara (2011) in Mt. Makiling. This species is more RECOMMENDATION associated with highly disturbed forest, plantation, The present study demonstrated that land snails in Sta. and former slash-and-burn patches. Also, it is an easily Teresita, Cagayan Province are very diverse and abundant recordable indicator of disturbance since it occurred in all in karsts despite exposure to various anthropogenic sampling sites in Sta. Teresita and has a high abundance disturbances. Thus, it is very important to recognize in the area of Tabaco and Arizero. The abundance of Sta. Teresita Karst is a priority site for malacofaunal introduced species increased with decreasing density of conservation and considers designating it as a protected the canopy cover and increasing anthropogenic activities area. Scattered karst forests in Sta. Teresita should be since much of the forest vegetation is secondary growth protected in order to conserve the population and diversity in all stations, with some patches planted of vegetable of land snails and other flora and fauna. Among sampling crops such as corn in Bangalao and Ari zero station. sites, Maquera has the most forested area; however, slash- Other introduced species recorded in Sta. Teresita and-burn and charcoal making in some hills are already were small snails Allopeas clavulinum, Allopeas present in this area. To prevent habitat loss and protect the graciles, Opeas nitidum, and Bradybaena fodiens, which forest, frequent patrolling and active enforcement should have been also collected in all stations except for Opeas be implemented by the local government unit (LGU) nitidum, which was only present in the Bangalao station. of Sta. Teresita. Furthermore, a proposed eradication This species might be accidentally introduced to the program of invasive land snails such as Lissachatina fulica Philippines via ornamental plant trade, in which the must be implemented by integrating a trapping system snail tends to attach to the soil of the plant. The plant into direct snail removal to protect the native species and trade provides a major mechanism for the long-distance to prevent damage to agricultural crops and native plants.

534 Philippine Journal of Science Parcon et al.: Diversity and Distribution of Land Vol. 150 No. S1, Special Issue on Biodiversity Snails in Sta. Teresita, Cagayan, Philippines

Figure 10. Some disturbances observed in Sta. Teresita, Cagayan, Philippines: A) charcoal making; B) illegal cutting of trees made into a lumber; C and D) vegetation removal in karst hills.

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