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The non-volant mammals of Bega Watershed, Prosperidad, Agusan del Sur, Philippines.

INTRODUCTION

The Philippines, because of its notable biodiversity both in animal and plant species [1] has been regarded as one of the 18 mega-biodiversity countries [2] as well as a "hot spot" in the world for conservation [3]. The Philippines is the world's second largest archipelago with more than 7,100 distinct islands [4] located in Southeast Asia which has the highest mean proportion comprising 11% of endemic mammalian species and threatened species [5].

In the latest account, the Philippine mammalian fauna consists of 206 native terrestrial species of which 117 are endemic [6]. For small non-volant species, 93 (90%) of 103 species are found to be endemic [7] including 17 genera of murid rodents endemic in the Philippine archipelago [6] and about 80% of the non-volant mammals in Greater Mindanao, the second largest island in the country, are found nowhere else in the world [8]. Several studies on the mammalian fauna in the country were conducted by Heaney et al. [9] in Mount Kitanglad, Philippines who documented 58 species of mammals while a study conducted by Nuneza et al. [10] in Mt. Malindang revealed a notably high endemism of mammals at 66.67%. A survey of small mammals in eastern Mindanao by Balete et al. [11] recorded the presence of Batomys on Mt. Hamiguitan, the only other documented occurrence of this genus on Mindanao Island outside of Mt. Kitanglad. Balete et al. [12] reported 18 species of non-volant mammals from the same mountain range while Reginaldo and de Guia [13] recorded nine species with 137 individuals of small non-flying mammals in Luzon. Thus, the richness in diversity and high endemism of terrestrial mammals in the Philippines are allied to the geological history of the archipelago [14] in which many islands and many individual mountains or mountain ranges support unique assemblages of terrestrial mammals [15].

New species of mammals in the Philippines were also discovered by Balete et al. [16], Heaney et al. [17] and Heaney et al. [18] in Luzon Island. However, the remarkable diversity and endemism of flora and fauna in the Philippines [19] are greatly susceptible to anthropogenic activities like logging and illegal timber trade [1] which directly affect the mammalian species that are dependent on forest habitats [20] and shall likely lead to their extinction [19]. Consequently, species that rely on tree cavities like the tree shrews are greatly affected by human-caused forest changes such as logging that may further reduce the availability of tree cavities and woody debris [21]. However, burrow rodents which are said to be the most common inhabitant of terrestrial habitats especially in tropical countries [22] have not yet been described [23]. This implies that habitat destruction especially in lowland areas is a threat to mammals as well as to the economic and social stability of human population in Northern Mindanao [9]. Moreover, hunting of mammals is also considered to be one of the factors that has impacted the biodiversity loss in tropical Asian forests [24] as well as in the Philippines. Thus, conservation efforts are important in small fragmented and human-modified landscapes affecting the mammals [25] and the limitations of available data had limited the understanding of the Southeast Asian fauna, and the Philippine fauna in particular, from both biogeographic and ecological perspectives and hence limited conservation planning in a nation that is often cited as one of the most in need of effective conservation action [26]. The information on the diversity and distribution of small non-volant mammals in the Philippines has been growing for the past decades; however, the work is still far from completion and there is still need to conduct more surveys in many areas in the country [13]. In addition, pattern of distribution of mammals is not solely a function of elevation but also affected by the habitat type and topography of the area and other factors such as temperature, precipitation, competition, and predation [27]. Furthermore, small non-volant mammals are not given attention because they usually occur in complex communities with high species richness [28].

Mammalian composition of many places in the country has been studied but there is still lack of information on some parts of the country especially in Mindanao, the second largest island in the country where largest forest block occurs [29]. This study on the non-volant mammals of Bega Watershed in Prosperidad, Agusan del Sur would provide data on non-volant mammalian composition since no mammalian assessment has been conducted in the area. The only published work was done by Monteclaro and Nuneza [30] on the diversity of fruit bats and Calimpong and Nuneza [31] on avifauna in Bega Watershed. In addition this study would also contribute to existing records on the mammalian fauna of the country. Thus, the objective of this study is to determine the species composition, conservation and distribution status of the non-volant mammals in Bega Watershed. Species composition across sampling sites was also compared.

MATERIALS AND METHODS

Study Area:

The municipality of Prosperidad lies within 08[degrees]36' and 125[degrees]55' on the northern part of Agusan del Sur. It comprises 32 barangays with a total area of 505.15 square kilometers. The sampling area, Bega Watershed in Barangay Mabuhay, Prosperidad, Agusan del Sur is located at 8[degrees]43.81" North and 125[degrees]59.74" East. Fig. 1 shows the map of the Philippines and Prosperidad, Agusan del Sur. Sampling was done on May 8-17, 2014 in five established sampling sites for a total of 500 trap nights.

Sampling Sites:

Site 1 has an elevation of 250 meters above sea level (masl) with coordinates of 125[degrees]97'39.1" E 08[degrees] 69'76.2" N. The site is actually a riparian area of Bega Watershed. The site is sloping at 20-30[degrees]with a secondary vegetation type. Fallen trees were rarely observed in the site. The site is dominated by Musa sp., Ficus sp., Pandanus sp., Colocasia sp., Calamus sp., ground orchids, and grasses. Epiphytes particularly ferns were moderate. Leaf litter mixed with small twigs were 1-2 inches in depth. Exposed small, medium-sized, and large rocks were abundant. Light intensity observed in the area was low to moderate because of the trees that form continuous canopy. About 1.5 km from the site is a landslide-prone area and a passageway for vehicles.

Sampling site 2 is a lowland area located at an elevation of 230 masl with coordinates of 125[degrees]58'45.2" E 08[degrees]42'0L8" N. It has a secondary vegetation about 50 meters away from the passageway for vehicles leading to sampling site 1. This site has a flat slope and partially closed canopy where a variety of species of trees and plants thrive. It is dominated by Musa sp. and grass like Imperata cylindrica. Trees like Shorea spp. were also present. A clear pathway in the area indicates that it is disturbed. Moreover, rotten logs were found lying around and leaf litter measured 1-2 inches thick. Compared to site 1, this area has no exposed rocks. Adjacent to the area where sampling was done was an anthropogenic clearing which connotes disturbance.

Sampling site 3 was an area near the Enchanted falls at 267 masl with the coordinates 08[degrees]42'09.4" N 125[degrees]58'49.4" E. The area has 50-60[degrees]slope mostly covered with species of ferns and emergent trees like Shorea spp., Musa sp., and vines were found. Pandan density was moderately observed. Leaf litter was 1.5 inches thick. The very obvious disturbance noted was deforestation.

Sampling site 4 is another lowland area along Tiger falls, so named because the rock formation from which the water gushes looks like a tiger. The area where sampling was done is situated at an elevation of 321 masl with the coordinates 125[degrees]98'2L1" E 08[degrees]70'43.5"N.

Sampling site 5 is another lowland area at 457 masl with coordinates 08[degrees]42'09.4" N 125[degrees]72'19.2" E. Around 100 meters from the site is an agricultural area mainly planted with corn, Zea mays and a variety of banana that is used by the locals as bait for traps. The "lawaan", Shorea spp. dominates the place. Ferns were abundant. The area is pierced with sunlight because of the sporadic arrangement of canopy. The soil is dry and leaf litter was 2 inches in thickness.

Sampling, Processing, and Identification of Non-Volant Mammals:

Live traps and indigenous/native traps were used to capture small, non-volant mammals. A slice of banana (Musa paradisiaca) was used as bait and not the standard bait which is coconut because rodents in the area according to the locals are not used to eating coconuts since coconuts are rarely observed in the area. The traps were placed at 5-15 meters interval and were set on the ground near holes, probable runways, under fallen trees or opening of the root systems. Some were placed on the low-lying branches and on fallen tree trunks. The traps were checked at 2100 hours and rebaited every morning. The sampling effort constituted 500 trap nights. The non-volant mammals observed and captured by the local people through their indigenous traps were documented. The indigenous people were interviewed regarding the non-volant mammals present in the area to supplement capture and direct observation results.

External measurements of the captured animals such as the total length (TL), the head and the body length (HBL), tail-vent length (TV), length of the ear (LE), length of hind foot (HF), and the body weight (WT) were taken in the field. All external measurements were taken using a vernier caliper while body weights were taken using pesola spring balance with precision scale. Field identification, classification, and distribution status of the non-volant mammals encountered in the area were based on the Non-Flying Mammals of Mindanao Island, Philippines by Heaney et al. [34] and Heaney et al. [6]. The conservation status of the non-volant mammals in Bega Watershed was based on IUCN Red List of Threatened Species [35] but local conservation status was noted based on actual observation, capture results, and key informant interview.

The number of species captured was recorded carefully on a daily basis. All the necessary information was recorded on a standard field catalogue sheet. Animals were released after a positive indication. One to two voucher specimens were fixed in buffered formalin and preserved in 70% ethanol and deposited at MSU-IIT Natural Science Museum.

Paleontological Statistics Software Package (PAST) version 2.17 [36] was used to analyze the similarity in the five sampling sites in Bega Watershed.

RESULTS AND DISCUSSION

Species Composition:

Nine non-volant mammalian species belonging to five orders, seven families, and nine genera were recorded in Bega Watershed, Prosperidad, Agusan del Sur (Table 1). Of the nine species recorded, two species, Bullimus bagobus and Rattus everetti were captured and the rest were documented through key informant interviews. This result is higher than the recorded number of species by de Guia et al. [37] and de Guia and Quibod [38] in Mount Makiling, Philippines while the same number of species was also recorded by Reginaldo and de Guia [13] in Sto. Tomas Luzon Island, Philippines. The presence of mammals in the watershed was observed to be due to the vegetation type of the area which is a secondary lowland forest having a variety of tree species and understory plants. Elevation could also be a factor for the presence of mammalian species. According to Niedzialkowska et al. [39] the presence and abundance of mammals is influenced mainly by forest productivity at the capture site and the productivity of the whole woodland. In addition, mammalian abundance and species richness is influenced by elevation wherein species richness decreases gradually with increasing elevation [40] and peaks at intermediate levels between 750 to 1000 masl [41].

There were five individuals of R. everetti and four B. bagobus that were recorded in this study. This low number of capture can be attributed to the sampling nights interrupted with outpour of rain. This result coincides with the findings of Start et al. [42] that mammalian species richness decreases with rainfall. Perry and Goodall [43] also mentioned that mammalian species richness decreases as precipitation increases. Botero et al. [44] found that decrease in rainfall is positively correlated with greater subspecies richness in terrestrial mammals. This implies that climate is one of the most important predictor variables explaining mammalian species richness and abundance patterns [45]. Moreover, McCain [46] reported that diversity of bats is affected by varying temperature and water variables and is likely the reason for the low number of captures. Conversely, R. everetti is the most abundant mammal observed in Mts. Hamiguitan and Malindang [47]. Balete et al. [48] reported the occurrence of this widespread species in Mingan Mountain, Luzon in montane/mossy forest at an elevation of 1,540 m. Nuneza et al. [10] in a study in Mt. Malindang also encountered this species. In addition, Reginaldo and de Guia [13] recorded several individuals of this species in pine forest of Mt. Sto. Tomas in Luzon that is regularly burned (1 to 2 times a year) due to agricultural activity adjacent to the forest. Moreover, this species can be found in low and middle elevations especially in disturbed forest [49] which coincides with the findings of this study. However, Salibay and Luyon [50] claimed that the main habitat of this species is undisturbed forest. This indicates that R. everetti can tolerate habitat modification where it can be found in disturbed and disturbed forests. This observation concurs with the findings of Heaney et al. [51] that this species can tolerate a range of habitats.

The two endemic species, B. bagobus and R. everetti were captured in sampling sites 3, 4, and 5. The presence of B. bagobus and R. everetti in these sampling sites can be attributed to the dense vegetation [52, 53]. These sites were at a lower elevation that are adjacent to fields of Zea mays (corn) and Oryza sativa (rice) which are known to aid in the foraging activities of the rodents [54]. This result coincides with the findings of Stuart et al. [55] that R. everetti is found in agro-forest ecosystem and prefers microhabitat with a dense canopy while Heaney et al. [53] found that B. bagobus is widespread in lower elevation forest which coincides with the habitat of this species in the present study. Moreover, the availability of food affects the diversity of mammals in tropical habitats [56].

Of the seven species recorded through key informant interviews (KII), four are endemic of which two are Philippine endemic and two Mindanao Faunal Region endemic. One species is of vulnerable category. Harris et al. [57] strongly emphasized that often the status of species is based on informed opinion rather than scientific study. Being knowledgeable of the distribution and conservation status of each species is important in instituting probable conservation strategies [58, 59] when dealing with continued fragmentation of primary forest habitats, population explosion, and forfeiture of ecosystem benefits [60].

Sus philippensis, a Philippine endemic and the only vulnerable species was recorded in the study and was found uncommon at lower elevations. According to Oliver and Heaney [61], most remaining populations of this species are now widely fragmented and declining, as a result of former widespread commercial logging operations, agricultural expansion (particularly slash-and-bum cultivation or 'kaingin'), and hunting pressure. A study of Scheffers et al. [62] found that S. philippensis was hunted for direct consumption and sale. They added that it is the most sought-after ground-dwelling mammal for hunters because they can earn about 13,000 pesos for one pig weighing 76 kg. compared to the typical daily wage of 250-350 pesos per day. This indicates that conservation and protection of S. philippensis in its habitat is needed. Furthermore, the record of S. philippensis in Bega Watershed is an additional information on the wild pig population since data on this is lacking on most islands in the country, particularly the smaller islands, although the present status may be inferred from the extent of remaining forest over the wild pig's known ranges [61].

Tarsius syrichta, a Mindanao Faunal Region endemic species and a nearly- threatened species was found to be uncommon at lower elevations in this study. This could be due to the size and height of trees in the area which could not be a suitable habitat for T. syrichta because as Gursky et al. [63] reported, tarsiers are found in a forest with substantially more trees per plot with larger diameter and slightly taller. Moreover, Shekelle and Arboleda [64] found that this species is common in lower densities in edge habitats and secondary growth with many pole-sized trees and low-stature vegetation. In addition, the presence of disturbance in the watershed could also be one of the factors why T. syrichta is not common in the lowland despite being adaptable to anthropogenic habitats [64].

Cynocephalus volans, a Mindanao Faunal Region endemic species and categorized as Least Concern was also uncommon at lower elevations in this study. According to Gonzales et al. [65] this species is common in lowland primary and secondary forest which coincides with the vegetation type in the study which is a secondary forest. However, the anthropogenic disturbances in the sampling areas like destruction of habitat and deforestation which lead to habitat loss could be one of the factors of this species to be uncommon. Deforestation especially at lower elevation, commercial logging of second growth forest, and the widespread destruction of lowland forest that make them somewhat vulnerable are threats to this species [65]. Moreover, previous studies revealed that C. volans does not retreat when detected by human unless it is directly disturbed [66].

The non-endemic species, Paradoxurus hermaphroditus was found to be locally threatened. This could be due to hunting for food and pet trade. The same finding was found by Duckworth et al. [67] that in some parts of its range this species is hunted for bush meat and the pet trade. Moreover, the presence of this species in the watershed could be due to the presence of fruit bearing trees which could serve as their food source.

According to the local people who were interviewed in this study, most of the species recorded have already declined in number primarily because of excessive hunting and deforestation. Oliver and Heaney [61] reported that hunting is mostly practiced by local farmers and indigenous peoples in hinterland communities and recreational hunters from larger cities. This could negatively affect the abundance of mammals [68], and with deforestation, could result to decline in the number of mammalian species which could lead to extinction [11]. Brashares et al. [69] added that hunting plays a pivotal role in the lives of many cultures and communities and in many less-developed regions. Hunting for bushmeat provides people with relatively inexpensive food and some income. On the other hand, when there is exploitation, conservation should follow [70] as in the case of hunting, slash and burn agriculture, and illegal logging. Conservation education [71] could also be effective to make the people understand the value of mammalian species.

Bray-Curtis Analysis of Species Composition in Five Sampling Sites:

The five sampling sites were all found in a lowland area ranging from 230-450 masl. Figure 2 shows the similarity of captured species with respect to the sampling sites. Sampling sites 1 and 2 are closely related. Both these sites are disturbed and no species was captured in these sites. This indicates that these two sites could not be suitable habitat for mammalian species. On the other hand, sampling sites 3, 4, and 5 are closely associated because of the presence of captured R. everetti and B. bagobus in these sites. Light penetration in these areas was milder and these sites have a much thicker ground cover. Moreover, the fern locally called "agsam" present in these sites is used as runways of rodents which were clearly observed because of the swept leaf litters. Mallari and Jensen [72], Heaney et al. [73] and Tabaranza et al. [74] pointed out that rats occupy various habitats as these species differ in their ability to utilize lowland, montane or mossy forests. Thus, forest cover has different effects on mammalian species [75]. Moreover, emergent trees like Shorea spp. were observed to be more in number than in sampling sites 1 and 2.

Threats to- Non-Volant Mammalian Fauna in Bega Watershed:

Threats to the non-volant mammals in Bega Watershed include habitat loss and destruction. Habitat loss and destruction is one of the leading causes of mammalian extinction [76] brought about by slash-and-burn agriculture [77]. Timber extraction and hunting for food, mainly anthropogenic which are threats to mammalian species [78, 1] are also present in the area. The lowland areas where the study was conducted appeared to be fragmented and this can lead to limited area for movement and food-searching activities [79] and causing wildlife declines and extinctions [80, 81, 82, 83]. Moreover, habitat that appears to be fragmented is responsible for biodiversity loss and a threat in tropical forests leading to isolation [84, 85]. Thus, the species composition and abundance change as fragmentation occurs in landscapes by losing those species that require large areas and the native vegetation left after such modifications may also be reduced in size and disconnected from adjacent, continuous habitat [85]. It was also found that forest type in lowland area supports species that are somehow absent or less common at higher elevations [86].

Some areas were burned for the establishment of shanties to be places of rest for farm owners when monitoring their farm. Resource extraction is driven by demands of thriving population that leads to rampant poverty [87].

There were small houses observed from the base camp at 245 masl elevation which gave an idea that people are already invading these areas which used to be habitats for non-volant mammals. As years go by, remaining lowland forest will be denuded [60]. The occurrence of habitat destruction and unregulated hunting for food threatens the survival of the small and large non-volant mammals in the area. P. hermaphroditus, B. bagobus, and R. everetti were the most severely hunted. Local people also acknowledged that they hunt for food and protein source. Subsistence hunting is one of the major threats to the persistence of species [88]. Key informants also said that population of these mammals in the area was known to be abundant but because of the threats, they are declining. Hunting is considered to be a major threat to mammals [69].

Most of the hunters interviewed in the study grow up in a rural environment which influences participation [89] in hunting while urban area is negatively associated with it [90]. There were more males hunting than females. This outcome can be explained by the tradition of hunter-gatherer concept [91] that depends on division of labor where men usually hunt wild animals [92]. Women don't hunt because it is incompatible with child care demands [93]. Most of the male respondents that practice hunting have only attained elementary level of education. DuWors et al. [94] reported that higher level of education resulted to less participation. Ethnicity has also a significant effect on hunting practice. In this study, mostly indigenous people hunt. They are likely to practice hunting because of the rural setting of the place they live in [92]. Almost all of the hunters are middle-aged male adults. Research indicates that hunting participation is directly associated with hunting activities as a youth [95]. Respondents also claimed that they have been influenced by their fathers in pursuing hunting.

Conclusions:

Species richness is low in Bega watershed but endemism is high. The presence of six endemic and one vulnerable species indicates that Bega watershed is important for conservation. Major threats observed were mainly anthropogenic activities particularly hunting for food. Results indicate the need to conserve and protect both species and their habitats. Sampling in upper elevations of the watershed may result in more number of species.

ARTICLE INFO

Article history:

Received 5 August 2015

Accepted 28 August 2015

Available online 15 September 2015

ACKNOWLEDGEMENTS

The Local Government Unit of Prosperidad headed by Mayor Albin Magdamit and the Municipal Tourism Office under Ms. Noradel Martinez are acknowledged for the funding and logistical support. We also acknowledge Josephine Dumas for assistance in the field.

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(1) Shella Mae P. Jalique and (2) Olga M. Nuneza

(1,2) Department of Biological Sciences, College of Science and Mathematics, Mindanao State University-Iligan Institute of Technology, Iligan City, 9200, Philippines.

Corresponding Author: Olga M. Nuneza, Department of Biological Sciences, College of Science and Mathematics, Mindanao State University-Iligan Institute of Technology, Iligan City, 9200, Philippines.

E-mail: olgamnuneza@yahoo.com

Table 1: Species composition, distribution status, conservation
status, and local conservation status of non-volant mammals in Bega
Watershed.

Species                     Distribution   Conservation
                            Status         Status
                                           (IUCN, 2015)

I. Order RODENTIA

A. Family MURIDAE

Bullimus bagobus (Large     MFRE           LC
Mindanao Forest Rat)

Rattus everetti             PE             LC
(Philippine Forest Rat)

B. Family SCIURIDAE

Sundasciurus                PE             LC
philippinensis
(Philippine Tree
Squirrel)

II. Order CETARTIODACTYLA

A. Family SUIDAE

Sus philippensis            PE             VUL
(Philippine Warty Pig)

III. Order CARNIVORA

A. Family VIVERRIDAE

Paradoxurus                 NE             LC
hermaphrodites (Common
Palm Civet)

Viverra tangalunga          NE             LC
(Malayan Civet)

IV. Order DERMOPTERA

A. Family CYNOCEPHALIDAE

Cynocephalus volans         MFRE           LC
(Philippine Flying Lemur)

V. Order PRIMATES

A. Family CERCOPITHECIDAE

Macaca fascicularis         NE             LC
(Long-tailed Macaque)

B. Family TARSIIDAE

Tarsius syrichta            MFRE           NT
(Philippine Tarsier)

Total number of species     9

Total number of endemic     6
species

Total number of captured    2
species

Total number of species     7
based on key informant
interview

Species                     Local Conservation   Means of
                            Status Observed in   Observation
                            Bega Watershed

I. Order RODENTIA

A. Family MURIDAE

Bullimus bagobus (Large     Locally threatened   C
Mindanao Forest Rat)

Rattus everetti             Locally threatened   C
(Philippine Forest Rat)

B. Family SCIURIDAE

Sundasciurus                Uncommon at          KII
philippinensis              disturbed sites
(Philippine Tree
Squirrel)

II. Order CETARTIODACTYLA

A. Family SUIDAE

Sus philippensis            Uncommon at lower    KII
(Philippine Warty Pig)      elevations

III. Order CARNIVORA

A. Family VIVERRIDAE

Paradoxurus                 Locally threatened   KII
hermaphrodites (Common
Palm Civet)

Viverra tangalunga          Uncommon at lower    KII
(Malayan Civet)             elevations

IV. Order DERMOPTERA

A. Family CYNOCEPHALIDAE

Cynocephalus volans         Uncommon at lower    KII
(Philippine Flying Lemur)   elevations

V. Order PRIMATES

A. Family CERCOPITHECIDAE

Macaca fascicularis         Uncommon at lower    KII
(Long-tailed Macaque)       elevations

B. Family TARSIIDAE

Tarsius syrichta            Uncommon at lower    KII
(Philippine Tarsier)        elevations

Total number of species

Total number of endemic
species

Total number of captured
species

Total number of species
based on key informant
interview

Legend: MFRE-Mindanao Faunal Region Endemic, LC-Least Concern, PE-
Philippine Endemic, VUL-Vulnerable, C-Captured, NT-Nearly Threatened,
KII-Key Informant Interview.
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Author:Jalique, Shella Mae P.; Nuneza, Olga M.
Publication:Advances in Environmental Biology
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