Food Habits and Distribution of the Lake Taal Sea Snake (Hydrophis semperi Garman 1881) and the Sympatric Little File Snake (Acrochordus granulatus Schneider 1799) in Lake Taal, Philippines

1The Graduate School, University of Santo Tomas, Manila, Philippines

2Research Center for the Natural and Applied Sciences, University of Santo Tomas, Manila, Philippines

3Department of Biological Sciences, University of Santo Tomas, Manila, Philippines

4Department of Science and Technology, Philippine Nuclear Research Institute, Philippines

5Center for Ecological Research, Kyoto University, Japan

6Herpetology Section, Zoology Division, National Museum of the Philippines, Philippines

Food Habits and Distribution of the Lake Taal Sea Snake (Hydrophis semperi Garman 1881) and the Sympatric Little File Snake (Acrochordus granulatus Schneider 1799) in Lake Taal, Philippines

Vhon Oliver S. GARCIA1*, Rey Donne S. PAPA1,2,3, Jonathan Carlo A. BRIONES1,3, Norman MENDOZA4, Noboru OKUDA5and Arvin C. DIESMOS6

1The Graduate School, University of Santo Tomas, Manila, Philippines

2Research Center for the Natural and Applied Sciences, University of Santo Tomas, Manila, Philippines

3Department of Biological Sciences, University of Santo Tomas, Manila, Philippines

4Department of Science and Technology, Philippine Nuclear Research Institute, Philippines

5Center for Ecological Research, Kyoto University, Japan

6Herpetology Section, Zoology Division, National Museum of the Philippines, Philippines

Our knowledge about the food habits of sea snakes and how it is associated with their distribution has seen much development through its description across a number of species available through published literature except for the key threatened species such as Hydrophis semperi. This paper aims to describe the food habits of H. semperi through gut content and stable isotope analyses. We also compared data with the Little File Snake, Acrochordus granulatus, sympatric with H. semperi. Recorded captures of H. semperi suggest that the sea snake tends to occur in the littoral zones and the shallower portions of the limnetic zone. Gut content analysis of H. semperi have shown that gobies and eels are primary prey items. Halfbeaks (Family Hemiramphidae) were recorded as one of the Lake Taal Sea Snake’s prey items which is considered as a new prey record for sea snakes. These extracted gut contents are confi rmed to be the temporal food preference of H. semperi given our detected stable isotope signatures. It appears that A. granulatus and H. semperi share common prey items suggesting possible diet overlap and resource competition. This study reports the fi rst account of the endemic Lake Taal Sea Snake’s distribution and food habits which poses implications towards its conservation as it occurs in a restricted ecosystem that has undergone considerable habitat alteration.

freshwater, diet, feeding, Hydrophis semperi, Hydrophiidae

1. Introduction

The study of an animal’s food habits has allowed expansion of knowledge on various aspects of its biology and ecology (Voris and Voris, 1983). For sea snakes in general, food habits have been reported to some extent inscientifi c literature (Glodek and Voris, 1982; Lobo et al., 2005; Rezaie-Atagholipour et al., 2013; Su et al., 2005; Voris and Voris, 1983; Voris et al., 1978). Fish was found to be the preferred food item of sea snakes with one genus (Emydocephalus) being an exception as it only consumes fi sh eggs (Glodek and Voris, 1982; McCosker, 1975; Voris, 1966; Voris and Moffett, 1981; Voris and Voris, 1983). Despite the number of studies on the food habits of sea snakes, none have documented this in the Lake Taal Sea Snake, Hydrophis semperi. From its formal description as a novel species by Garman (1881), the Lake

Taal endemic sea snake was only mentioned in a limited number of studies which only conveyed information about its locality (e.g. Dunson and Minton, 1978; Dunson, 1975; Minton, 1975) and taxonomic description (e.g. Alcala, 1986; Herre, 1942; Smith, 1926). Despite being rare and endemic in its habitat and being classifi ed as a Threatened (“Vulnerable”) species by the International Union for Conservation of Nature (IUCN), many aspects on the biology of H. semperi remain unstudied (Gatus, 2010). Thus, we investigated its food habits through the analysis of its gut contents and stable isotope ratios. These analyses provided information about spatial and temporal patterns on the food habits of the poorly studied sea snake that occurs in freshwater. Moreover, we also identified its occurrence and distribution within the lake. The Lake Taal Sea Snake’s rarity in its ecosystem, endemicity to its habitat, and high vulnerability to both natural and anthropogenic processes call for the description of its food habits and spatial distribution as these basic aspects pose implications for the sea snake’s conservation. We compared the Little File Snake Acrochordus granulatus, a species with a wider geographic distribution occurring from West India through South Asia reaching up to the Solomon Islands, with H. semperi. Acrochordus granulatus is commonly found in mangroves and shallow coastal waters as well as rivers and freshwater lakes. In the Philippines, it co-exists with H. semperi in Lake Taal (Lillywhite and Ellis, 1994).

2. Materials and Methods

Figure 1 Sampling locations for H. semperi and A. granulatus. Sampling methods were in accordance with fi shing practices in open water areas of the lake (i.e. gill-net fi shing). Sampling areas were situated at approximately 300–500 m from shore and were spread across various portions of the lake bounded by dashed lines. Sampling at sites 1 and 2 was reduced due to the presence of aquaculture structures. Immediate area at the outfl ow of Pansipit River (▲) was also surveyed.

2.1 SamplingLake Taal is a caldera lake found in the island of Luzon (Figure 1). It is the third largest lake in the Philippines with an area of approximately 268 km2. Lake water drains through its sole outlet, Pansipit River to Balayan Bay in the southwest. The Taal Volcano Island sits in the middle of the lake which partially separates its north and south basins (Perez, 2008; Ramos, 2002). Six major areas (1–6, Figure 1) around Lake Taal were sampled for H. semperi and A. granulatus from June to November 2013. Sampling was done bi-weekly at sites with few to no aquaculture structures present (sites 3–6). Sampling was reduced to once a month at sites with heavy aquaculture use (sites 1 and 2). Gill-nets were

deployed for 12 hours overnight and were checked the next day for captures. Sampling size was controlled for H. semperi to avoid possible casualties of individuals from gill-net sampling given its rare, endemic, threatened“Vulnerable” species status (Gatus, 2010). We measured (in mm) the snout-vent length (SVL), tail length (TL), neck width, and body weight (in g) of the snakes. Snake sex was determined through hemipenal eversion. All snakes were recorded to summarize encounter rates. Captured live snakes were released back to the lake while dead individuals were dissected for gut content analysis.

2.2 Gut Content AnalysisA mid-ventral incision was made to run from the anterior to the posterior portion of the snake to extract as much of the alimentary canal as possible. Regurgitation was employed (when possible) by sliding the stomach and esophageal regions between the thumb and index fi nger (Carpenter, 1958; Su et al., 2005). Gut contents were preserved in 70% ethanol. All snake specimens were preserved using 10%–15% formalin and were deposited in the National Museum of the Philippines (Accession No. ACD7829–ACD7881). Gut contents, mainly fi sh, were measured of its length, width, and depth (in mm). Its orientation in the stomach of the snake was noted as well. Food items were identified to the lowest taxonomic level possible and were described of its habits and habitats.

2.3 Food Web AnalysisSnake fl esh samples (rectangular pieces of 5 cm × 1 cm× 1 cm in size) were extracted from the dorsal side of H. semperi (n = 2) and A. granulatus (n = 3). Snakes with varying snout-vent lengths (SVL) were used to best represent the size range of each species [SVL measurements (in mm) for H. semperi: 448 and 862; for A. granulatus: 340, 630, and 641]. General guidelines for stable isotope (SI) analysis were adapted (Jardine et al., 2003). We isolated fish and snake flesh and dried each for at least 24 h in 60oC. After which, each sample was ground to a fine powder, immersed in chloroform: methanol (2:1) solution for 24 h to remove lipids, and dried again in 60oC for another 24 h. After processing, each sample was pre-weighed (～0.5 mg) and wrapped in tin capsules. These were then combusted using a High Temperature Conversion Elemental Analyzer (ThermoScientific FLASH EA) and analyzed under high vacuum using an Isotope-Ratio Mass Spectrometer (IRMS) (ThermoScientific Delta V Plus) together with known amino acid standards. IRMS data was reported as isotopic notations of carbon (δ13C) and nitrogen (δ15N) and expressed as permil (‰) deviation from standards (Vienna Pee Dee belemnite limestone carbonate and atmospheric nitrogen were used for nitrogen and carbon respectively) using the following equation:

where R =13C/12C or15N/14N. These values where used to produce an isotope biplot to elucidate the potential trophic interactions between aquatic snake species and their potential prey items in Lake Taal. For the biplot, we assumed that the trophic enrichment factor would be 3.4‰ for δ15N and 0.8‰ for δ13C (France and Peters, 1997; Fukumori et al., 2008; Shibata et al., 2011; Zanden and Rasmussen, 1999). The analytical precision based on working standards was 0.20 and 0.10 ‰ for δ13C and δ15N respectively (Tayasu et al., 2011).

3. Results

3.1 Sea Snake DistributionTwenty-four individuals of H. semperi and 88 individuals of A. granulatus were captured throughout the sampling duration. Most of the samples were obtained as by-catch from gill-net fi shing. Figure 2 shows the encounter rates for the sympatric water snakes at each sampling site of Lake Taal. Most of the samples belonging to H. semperi and A. granulatus were acquired from the littoral to shallow limnetic areas of the lake being almost absent of aquaculture structures. This area of the lake is characterized to have a heavy macrophyte assemblage especially in the littoral zone. The Lake Taal Sea Snake has been also encountered in the shallow limnetic zone and was observed to have lifted its head above water; perhaps to breathe. On other parts of the lake, as in the northern and western sampling areas, only snakes belonging to A. granulatus were captured. Throughout most of Lake Taal, our data suggest that H. semperi and A. granulatus are more of syntopic species than just sympatric. The snakes occur side-by-side and at the same habitat zones of the lake rather than just the same geographical range. Although much of the lake is yet to be explored, this may explain the observable diet overlap and resource competition between the two snakes upon the examination of its spatial and temporal food habits.

3.2 Food itemsOf the 10 individuals of H. semperi examined for gut contents, three had food in their stomachs. The contents were identifi ed as Psammogobius biocellatus (Valenciennes, 1837) (Family Gobiidae), Zenarchopterus buffonis (Valenciennes, 1847) (Family Hemiramphidae), and Anguilla marmorata Quoy & Gaimard, 1824 (Family Anguillidae). Forty-three individuals of the sympatric A. granulatus were also examined and were found to contain gut contents

identifi ed as fi sh belonging to the Family Gobiidae. These items were classified as P. biocellatus (Valenciennes, 1837), Acentrogobius suluensis (Herre, 1927), and Glossogobius giuris (Hamilton, 1822) (Table 1). For both species, all prey items were ingested head-fi rst.

Figure 2 Comparison of species encounters between H. semperi (black) and A. granulatus (gray) (▲=Pansipit River, X = localities with no captures). Most samples were retrieved from the eastern and south-eastern portions of the lake where little to no aquaculture structures are present. Note the absence of H. semperi at lake regions with habitat alteration (aquaculture structures); although there is restriction in sampling opportunities on this part of the lake. Information from Balayan Bay was acquired from a visit done during the latter part of the sampling period. Immediate bay area near the outfl ow of Pansipit River was also surveyed. The lack of record of H. semperi in the bay supports the endemicity of H. semperi to Lake Taal and its inability to inhabit a marine habitat unlike other members of the Family Hydrophiinae.

3.3 Stable Isotope AnalysisOur stable isotope analysis has detected the trophic niche of the Lake Taal Sea Snake (i.e. piscivorous) and further strengthened our findings from the extraction of food items from the snake’s gut. Stable isotope analysis for H. semperi and A. granulatus fl esh samples generated mean δ13C and δ15N values. Table 2 shows the differences between the snake’s carbon and nitrogen isotope values from their identified prey items

further confirming predator-prey association. Moreover, relative trophic positions of both snakes show close proximity with each other suggesting that both play similar roles as top predators in Lake Taal (Figure 3).

4. Discussion

4.1 Water snake distributionin Lake TaalThe distribution of H. semperi in Lake Taal shows association with the sea snake’s prey habits and habitats. As in previous studies, habits and habitats of the prey items of sea snakes have been valuable source of indirect data which helped in the formulation of inferences about its locations and distribution (Voris and Voris, 1983). Sites with high encounters of H. semperi are described to have heavy macrophyte assemblage. These macrophytes make good “sitting” grounds and refuges for sedentary or burrowing fishes which are the common prey items of H. semperi. This may account for the relatively high H. semperi encounters at these sites since the sea snake is able to employ its hunting strategy of investigating nooks and holes for any prey item. In comparison, sites that yielded low H. semperi captures and encounters were aquaculture sites in the lake. The effect of aquaculture on H. semperi distribution at these areas relate well to the fi ndings of Papa et al. in 2011 where they reported a decline in water quality at locations near the vicinity of aquaculture structures. Moreover, increased microbial activity especially at the benthic portion of the lake was observed and was attributed to uneaten fish feed as well as feces from reared fish (Hallare et al., 2009). This consequence of mismanaged aquaculture practices reduced the quality of the habitats of sedentary fishes and of the sea snake as well. Such disturbance resulting to habitat degradation has been noted as a potent cause of dispersal, population decline, and even species loss in aquatic snakes (Dodd Jr., 1987; Lukoschek et al., 2013).

4.2 Food items and observed prey patternsThe Lake Taal Sea Snake is an exception to its family (Hydrophiinae) whose members are classifi ed as true sea snakes in that it inhabits Lake Taal which is a freshwater lake (Papa et al., 2011; Rezaie-Atagholipour et al., 2013). Despite the sea snake occurring in a freshwater habitat, its prey items are consistent with the general food habits of sea snakes found in seawater. Here, food items came from a limited sample size but represented previous food item observations (Glodek and Voris, 1982; Heatwole et al., 1978; Voris and Voris, 1983) and interestingly added a new record in the food habit of sea snakes in general.

Figure 3 Stable isotope plot for H. semperi and A. granulatus with other Lake Taal biota (● = Fish; □ = Snake). Arrows indicate fi sh species that were extracted from the guts of the snakes. Although some of the fi sh species were not found in the guts of these water snakes (e.g. Atherinomorus spp., Hippichthys heptagonus, Oligolepis acutipenis), stable isotope signatures refl ect that these prey appear to be potential food habits of the snakes. It is worthy to note that these fi sh species share a common morphology. Moreover, the positions of the two water snakes suggest that they are the top predators in the lake ecosystem.

Table 1 Prey items of H. semperi and A. granulatus. Take note of the similarity in the diet in terms of fi sh family as well as prey item habit. This suggests that both snakes could have similar hunting modes (investigation of nooks and crannies) which further support previous fi ndings. The sympatric water snakes also share Gobiid species as a preferred food item. With the natural restriction due to their habitat (i.e. lake), a possible diet overlap and resource competition could be present.

Table 2 Mean stable isotope values of H. semperi and A. granulatus together with other Lake Taal biota. Take note of the values between the snakes and the fi sh items. An assumption for a stepwise enrichment of trophic level can be made for an increase of 3.4 and 0.8 for δ13C and δ15N respectively. This trend can also be approximated for prey items that were not extracted from the gut of the snakes.

Eels and gobies being common prey items of sea snakes due to their morphology, scale type, and habitat is a result consistent with our study (Voris and Voris, 1983). The elongated morphology of these fishes facilitates ingestion upon capture. Also eels and gobies have naked scales, a characteristic of fi shes that occur in the benthic zone, which allow easy penetration of fangs for energyeffi cient prey capture. Their habitat as well matches the microcephalic characteristic of H. semperi, as in other species of the genus Hydrophis. Sea snakes of this genus have exceptionally small head regions relative to the size of their posterior girths which allows them to investigate nooks and crevices for “sitting” gobies or find eels that occur as burrowers when taking refuge (McCosker, 1975). Should a prey be captured, their strategy of prey ingestion is also advantageous to their characteristic small heads. Sea snakes, as in H. semperi, ingest its food headfi rst to avoid injury from fi ns and spines that might pierce the small Hyrophiid head.

In this study, aside from commonly known sea snake prey of eels and gobies, we report a species from the Family Hemiramphidae (Halfbeaks) as a prey item of H. semperi. This family is not included in the study of Voris and Voris (1983) which summarized published data on sea snake diets. Halfbeaks are characterized to have similar morphology as gobies and eels as they possess elongated body forms. Despite being an unusual record, this further supports previous studies that reported sea snakes, even though generally known to be specialist predators, prey on fi shes with similar morphologies across different fi sh families (Rezaie-Atagholipour et al., 2013; Su et al., 2005).

It is important to note the addition of fi shes from the Family Hemiramphidae as prey items of sea snakes and H. semperi in particular. Fishes from this family are known to be planktivorous and utilize the pelagic zones of lakes (Barletta and Blaber, 2007). With that habit, sea snakes that characteristically rise to the surface of the water in order to respire may encounter such fish and consider them as prey due to the similarity in morphology with its other food items.

Diet overlap has been observed to be minimal between sympatric sea snake species (Su et al., 2005). In Lake Taal, H. semperi is sympatric with A. granulatus and is suggested to be syntopic given previous findings. In this study, the stomach contents of A. granulatus only included Gobiid species which are also prey items for H.

semperi showing that both species share a similar fish family as prey. This is further supported by stable isotope analysis confirming that these prey items captured the long-term food habits of H. semperi and A. granulatus. Furthermore, this similarity in prey between H. semperi and A. granulatus in Lake Taal suggests that there is a possible diet overlap between the two water snakes that occurs temporally as well. This result is parallel with the findings on Lapemis hardwickii Gray 1834 (Hydrophiidae) and A. granulatus at Sungai Buloh and Parit Botak in Malaysia. Sharing four species as their prey items, maximum diet overlap was observed between the L. hardwickii and A. granulatus (Voris and Glodek, 1980; Voris and Voris, 1983). However, H. semperi could be addressing this possible overlap in diet by considering other fi sh prey with the same morphology, as in other sea snakes; a pattern not observed in A. granulatus (Glodek and Voris, 1982; Voris and Glodek, 1980). Nonetheless, the limitation in available prey brought by a lake ecosystem aggravated by habitat alteration may intensify the presence of diet overlap between the two syntopic species. However, a more detailed investigation is needed to confirm the level of diet overlap between the two species.

4.3 Baseline information onH. semperi The results highlighted in this study fills in the lack of published information on the snakes in Lake Taal particularly on the endemic H. semperi. As other more complex aspects on the biology of H. semperi remain to be explored, the baseline information presented here can provide suggestions towards efforts in conservation of the H. semperi and its habitat. This study underlines the presence of an important sea snake species in Lake Taal and may initiate management actions towards its protection. The relevance of this study can be further emphasized considering the sea snake’s habitat that experiences intensified habitat alteration; a known cause of snake population decline in nature (Dodd Jr., 1987).

This study presents the fi rst account on the food habits and distribution of H. semperi which are typical of sea snakes in having specialized feeding on fish from few families having the same morphology. Similar food items as well were shown to be shared between H. semperi and A. granulatus. Moreover, spatial and temporal food habit data are consistent and confirm predatorprey relationships between the snakes and fish species as shown by the snakes’ gut contents and stable isotope signatures respectively. A possible diet overlap could be present between the species and the nature of their habitat could play largely towards this condition, although much investigation regarding this is needed. Also, the reported limited distribution of H. semperi in the lake can be associated with habitat alteration due to aquacultureinduced eutrophication. Despite our limited sampling across the lake area, this study gives baseline information regarding the endemic Lake Taal Sea Snake which is virtually unstudied in scientifi c literature.

AcknowledgementsWe like to express our sincerest gratitude to the following institutions that provided facilities and equipment support for this project: Research Center for the Natural and Applied Sciences (RCNAS), University of Santo Tomas; Herpetology Section, National Museum of the Philippines; Philippine Nuclear Research Institute (PNRI), Department of Science and Technology; Center for Ecological Research, Kyoto, Japan; the Fisheries Biological Station Complex, Bureau of Fisheries and Aquatic Resources for the identifi cation of the gut contents of the sea snakes; and the Rufford Small Grants Foundation for the fi nancial support in this project. N. Okuda, R. Papa, J. Briones, and N. Mendoza were also fi nancially supported by the Feasibility Study Grant from the Research Institute for Humanity and Nature and the Cooperative Research Grant from the Center for Ecological Research, Kyoto University, Japan. We would also like to thank Jinzhong Fu for his comments on the manuscript.

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*Corresponding author: Vhon Garcia, from the University of Santo Tomas Graduate School, Philippines, with his work on amphibians and reptiles particularly the biology, ecology, systematics, and phylogenetics of the endemic freshwater sea snake, Lake Taal Sea Snake (Hydrophis semperi).

E-mail: garcia.vhon@gmail.com

Received: 30 July 2014 Accepted: 17 November 2014