5-masangcay-feeding habits.pmd Feeding Habits of Mobula japanica 24 SCIENCE DILIMAN (JANUARY-JUNE 2018) 30:1, 24-44 Feed ing Habits of Mobula japanica (Chondrichthyes, Mobul idae) in Butuan Bay, Mindanao Island, Phil ippines Shirlamaine Irina G. Masangcay Caraga State University Ephrime B. Metillo* Mindanao State University-Iligan Institute of Technology Ken-Ichi Hayashizaki Kitasato University Satoru Tamada Kitasato University Shuhei Nishida University of Tokyo ABSTRACT The diet of the Spinetail Devil Ray Mobula japanica Müller and Henle 1841 from Butuan Bay, Philippines was investigated from January to May 2016 using data on its stomach contents, and C and N stable isotope analyses, in order to contribute to the scarce information on the feeding biology of the threatened tropical populations of the Mobula species. E x a m i n a t i o n o f 1 6 M . j a p a n i c a s t o m a c h s r e v e a l e d i n g e s t i o n o f t h e euphausiid Pseudeuphausia latifrons, sergestid shrimps Acetes intermedius and Lucifer spp. , copepods, and other rare prey items. The tropical krill P. l a t i f r o n s w a s t h e m o s t co m m o n , ofte n t h e s o l e fo o d , t h a t i n c r e a s e s body length of individuals towards the warmer months of April and May, w h i c h co i n c i d e w i t h t h e p e a k s e a s o n of M . j a p a n i ca f i s h e r i e s . Re s u l t s f r o m δ 1 3C a n d δ 1 5N s t a b l e i s o t o p e a n a l y s i s a r e c o n s i s t e n t w i t h t h e assimilation of large zooplankton and micronektonic crustaceans. This study is the f irst repor t on the feeding of M. japanica in tropical waters and the identif ication of euphausiid P. latifrons as its dominant prey. Keywords: Stomach content, Mobula, Pseudeuphausia latifrons, population structure, tropical _______________ *Corresponding Author ISSN 0115-7809 Print / ISSN 2012-0818 Online S.I.G. Masangcay et al. 25 INTRODUCTION The Spinetail Devil Ray Mobula japanica from the family Mobulidae is a large marine f ish with cartilaginous skeleton (Couturier et al. 2012). Locally known as Pantihan, mobulids or devil rays are pelagic f ishes found in shallow and deep waters in the tropical and temperate regions (Cortes and Blum 2008; Bizzarro et al. 2009; Scacco et al. 2009; Canese et al. 2011; Metillo and Masangcay 2015; Croll et al. 2016; Francis and Jones 2016). In New Zealand, the species is a common bycatch in skipjack tuna purse seine f isheries (Francis and Jones 2016). Most Mobula, particularly M. japanica, vary in size with disk width ranging 1–3 meters (Paulin et al. 1982; Notarbartolo di Sciara 1987; White et al. 2006b), and are commonly known to be very fast swimmers that feed on zooplankton (Couturier et al. 2012). They have low natural rate of mortality, slow-growth with long life span, late sexual maturation, and have few but large offspring (Dulvy et al. 2003; Musick and Ellis 2005; Garcia et al. 2008; Croll et al. 2016). Mobula japanica is currently listed as near-threatened by the International Union for Conservation of Nature (IUCN) Red List of Threatened Species (White et al. 2006a), yet they are still being actively f ished in Bohol Sea, central Philippines via the traditional harpoon and purse seine methods for sale and local consumption in the coastal area (Alava et al. 2002; Rayos et al. 2012; Acebes 2013; Freeman 2014; Croll et al. 2016). Fishermen (Galdo and Sanchez, personal communication) conf irmed that M. japanica are seasonally observed in Butuan Bay, Mindanao Island during the Northeast monsoon when coastal enrichment is highest in eastern Bohol Sea (Cabrera et al. 2011). Mobula species are pelagic megafauna yet they subsist on a primary diet of zooplankton and ichthyoplankton (Couturier et al. 2012). They grow very large due to the direct feeding on abundant zooplankton and ichthyoplankton in the second trophic level much closer to abundant primary producers (Shwenk 2000). Zooplanktivorous devil rays are indispensable in the marine ecosystem since they tap the lower trophic levels (Couturier et al. 2012; Jaine et al. 2012), and become important indicator species of climate change, as their planktonic food source is highly susceptible to environmental changes (e.g. , ocean acidif ication and warming waters) (Hays et al. 2005; Richardson 2008; Weeks et al. 2015). Studies on the biology and ecology of Mobulidae started since the 17th century, but information on its feeding habits is limited (Willoughby 1686; Stewart et al. 2016). Aggregations of devil rays are generally linked with local productivity and food availability (Celona 2004; Sleeman et al. 2007; Dewar et al. 2008; Marshall et al. 2009; Anderson et al. 2011; Couturier et al. 2011; Marshall et al. 2011) . Zooplanktivory is their generic feeding habit (Weeks et al. 2015), but species- Feeding Habits of Mobula japanica 26 specif ic differences occur. For instance, M. thurstoni is known to feed on mysid shrimps and euphausiids, and dwells in non-overlapping microhabitats with other species (Notarbartolo di Sciara 1988). Examination of the stomach contents, and C and N stable isotope techniques have shown varying feeding habits among subtropical and temperate sub-populations u n d e r t h e g e n u s M o b u l a, s u c h a s M . m o b u l a r, M . h y p o s t o m a , M . r o c h e b r u n e i , M. tarapacana, M. birostris, M. alfredi, M. japanica, and M. munkiana, which generally feed on small f ishes and crustaceans like krill (Meganyctiphanes norvegica, Nyctiphanes simplex), the mysid Mysidium sp., and other planktonic organisms (Notarbartolo di Sciara 1988; Sampson et al. 2010; Couturier et al. 2012). The diets of the near threatened species M. kuhlii and M. eregoodootenkee are unknown thus far (Pierce and Bennett 2003; Bizzarro et al. 2009). Current knowledge of the prey preference of the tropical Mobula japanica based on its stomach contents is limited to the studies of Notarbatolo di Sciara (1988) and Sampson et al. (2010) conducted off the coast of California, USA. Analyzing feeding habits of tropical populations will determine diet preference and allow inference on habitat use and feeding behavior, which are both very impor tant to the conservation and management of the ray (Stewart et al. 2016). Hence, this work investigated the feeding habits of M. japanica in Butuan Bay, northeastern part of Mindanao Island, Philippines with specif ic aims of analyzing the composition of its stomach contents, and indirectly inferring its feeding habits using C and N stable isotope analysis. MATERIALS AND METHODS Study area Butuan Bay is located in the northeastern area of Mindanao (Figure 1). Its coastline is connected to the north with Bohol Sea or Mindanao Sea, which is known to have extreme southwest movement of surface currents coming from the Pacif ic Ocean (Cabrera et al. 2011). The entire bay has an average depth of 100 meters and a maximum depth of 800 meters (NGA Nautical Chart 1996). Numerous river tributaries flow directly into the bay, including the Agusan River, the third longest river in the Philippines, carrying water discharges from interconnecting rivers, channels, and lakes (Primavera and Tumanda 2008). A biologically enriched estuarine frontal plume usually occurs near the mouth of the large Agusan River in the bay (Cabrera et al. 2011). Climatic condition in Butuan Bay includes signif icant amount of rainfall throughout the year even in the driest month. The bay is exposed to strong trade winds and storms during the northeast monsoon (December-April). S.I.G. Masangcay et al. 27 Buenavista is a f ishing coastal municipality located at the Southern portion of the bay (Figure 1) (Indab and Suarez-Aspilla 2004). The area is considered as a major f ishing ground with rich f ishery resources (BFAR 2015). Personal interviews in the locality validated the regular landing of Mobula in Buenavista, but f isherfolks report catching of rays at other locations in the bay, particularly off the coast of Carmen, Nasipit, Cabadbaran, and Tubay (Figure 1) (Metillo and Masangcay 2015). Field sampl ing of ray stomach, muscle tissue, and prey items Field collection of ray stomach samples, potential prey, and tissues for C and N stable isotopes was conducted from 18 January to 13 May 2016 to coincide with the f ishing season in Butuan Bay. Sixteen specimens of M. japanica (Table 1) were purchased from local f ishermen who caught the f ish as bycatch from sardine and skipjack tuna gill net fishing during the day in f ive locations in Butuan Bay (Figure 1). Fishermen from Buenavista and other locations in Butuan Bay consistently stressed that their devil ray collection sites are just within the Bay (Metillo and Masangcay 2015). During specimen collections of this study, a standard procedure of asking f ishermen where they captured the rays revealed that they can be found in the deep portions of Butuan Bay. The digestive tract of the 16 individuals was removed by cutting the most anterior end of the esophagus and the most posterior end of the intestine. The length and outer diameter of the stomach were measured to estimate the stomach volume that will be used in the stomach content analysis. Figure 1. Geographical location of Butuan Bay in Northeastern Mindanao, and collection sites of landed Mobula japanica and plankton samples off the municipality of Carmen (triangle), Nasipit (square), Buenavista (dot), Cabadbaran (diamond), and Tubay (star) in the Province of Agusan del Norte. Inset is the map of the Philippines with the study site enclosed in a square. Feeding Habits of Mobula japanica 28 Afterwards, the stomach and intestine (Figure 2) were longitudinally dissected, spread apart, and the stomach contents were thoroughly flushed into clean plastic containers and preserved in 10% buffered formalin in f iltered seawater. Muscle tissue samples from f ive Mobula japanica individuals were obtained near the ventro- posterior area of the pectoral f ins using a sharp scalpel, and were immediately placed in a clean vial and labeled properly. T issue samples were brought to the laboratory in an ice chest, and immediately dried in an oven at a temperature of 60 oC for 48 hours. a Female 148 72 19 166 18-Jan-16 - b Male 130 68 23 160 25-Jan-16 - c Male 120 55 5 148 12-Feb-16 - d Male 137 67 16.4 146 27-Feb-16 Buenavista Area e - - - - - 11-Mar-16 Buenavista Area f Male 134 60 8 143 18-Mar-16 Buenavista Area g Male - - - - 18-Mar-16 Cabadbaran Area h - - - - - 30-Mar-16 Cabadbaran Area i Male 129 59 17 150 31-Mar-16 Buenavista Area j Male 146 69 22 142 31-Mar-16 Tubay Area k - - - - - 02-Apr-16 Buenavista Area l Female 135 60 18 154 09-Apr-16 Carmen Area m - - - - - 10-Apr-16 Carmen Area n Male 130 66 12 140 09-May-16 Buenavista Area o Male 134 63 17 148 11-May-16 Buenavista Area p Male 157 73 22 178 13-May-16 Buenavista Area Note: “-”, undetermined # Sex Disk width (D w ) Disk length (C F ) Cephal ic fin length (C F ) Tail length (T L ) Date collected Site collected Table 1. Body measurements (cm) of the 16 Mobula japanica ind ividuals collected in Butuan Bay, Northeastern Mindanao, Phil ippines Figure 2.The digestive tract of Mobula japanica from Butuan Bay, Philippines. S.I.G. Masangcay et al. 29 P l a n k t o n s a m p l e s w e r e c o l l e c t e d o n 2 5 J a n u a r y 2 0 1 6 a t t h e l o c a t i o n w h e r e M. japanica were caught (Table 2), particularly off Buenavista. Conical nets with mesh sizes of 100 μm and 20 μm were towed horizontally at sub-surface depths to collect zooplankton and particulate organic matter (POM), respectively (Metillo et al. 2015). Night sampling involving several 3-minute tows was performed until the desired amounts of plankton and POM triplicate samples were collected. Zooplankton samples were size-fractionated using a series of sieves with nylon gauzes of different mesh sizes (<100 μm, 100–200 μm, 200–335 μm, 335–1000 μm, >1000 μm), and were viewed under a dissecting stereo microscope to remove any debris in the sample. Zooplankton taxa (e.g. crab megalopa, decapod shrimp, hydrozoa) were sorted from the bulk samples to represent extra-large zooplankton (ZXL). Samples from the 20-μm mesh plankton net were f iltered, and particles trapped in the 20-μm sieve were regarded as POM (Table 3). Large zooplankton samples (ZXL, ZL, ZM) were carefully handpicked using f ine forceps, placed in foil, and dried in an oven at a temperature of 60oC for 48 hours. Smaller size fractions (ZS) of zooplankton and POM samples were separately f iltered onto pre-combusted glass f iber f ilters (GF/F), dried in the same manner as large zooplankton, and placed inside Eppendorf tubes until stable isotope analysis. Table 2. Tabulated coord inates of each plankton tow for stable isotopes analysis collected on 2016 January 25 in Butuan Bay, Northeastern Mindanao, Phil ippines 1 100 125.401405° 8.987764° 2 100 125.399261° 8.988452° 3 100 125.397559° 8.988784° 4 100 125.396298° 8.988920° 5 20 125.394506° 8.989511° 6 20 125.393166° 8.989122° 7 20 125.391468° 8.988398° 8 20 125.389072° 8.988368° 9 20 125.386612° 8.988413° 10 20 125.384991° 8.988234° 11 20 125.383185° 8.988025° Tow No. Net mesh size μm Coord inates Longitude Latitude Feeding Habits of Mobula japanica 30 Stomach content analysis The stomach content of each individual ray was removed and placed in a beaker for subsampling. The entire sample was divided into 10 parts with each tenth regarded as a subsample. Three sub-samples were then thoroughly identif ied using a stereomicroscope for large particles and a compound microscope for smaller ones. The contents of the intestine were also inspected, but the materials were already heavily digested and unidentif iable; hence, they were not included in the analysis. The index of relative importance (IRI) of each food item category was computed using the formula of Pinkas et al. (1971): IRI = (Cn + Cv) x F , where Cn is the percentage numerical count of each food item relative to the total count of all food items; C v is the percentage volume (assuming cylindrical shape of the ray cardiac stomach) of each food item (estimated from the product of the proportion 18-Jan-16 Mobula japonica (female) MJ Day 1 Fish landing 18-Jan-16 Pseudeuphausia latifrons KA N/A 30 Net towing 25-Jan-16 M. japonica (male) MJ Day 1 Fish landing 12-Feb-16 M. japonica (male) MJ Day 1 Fish landing 27-Feb-16 M. japonica (male) MJ Day 1 Fish landing 18-Mar-16 M. japonica (male) MJ Day 1 Fish landing 25-Jan-16 Lucifer spp. LU Night 6 Net towing 25-Jan-16 Acetes intermedius AC Night 15 Net towing 25-Jan-16 Clupeidae FJ Night 4 Net towing 25-Jan-16 Exocoetidae FJ Night 1 Net towing 25-Jan-16 Blennidae F L Night 4 Net towing 25-Jan-16 Carangidae F L Night 6 Net towing 25-Jan-16 Gobidae F L Night 4 Net towing 25-Jan-16 Crab megalopa ZXL Night 2 Net towing 25-Jan-16 Decapod shrimp ZXL Night 2 Net towing 25-Jan-16 Hydrozoa ZXL Night 1 Net towing 25-Jan-16 Macrosetella sp. ZXL Night 2 Net towing 25-Jan-16 Acartia sp. ZL Night 18 Net towing 25-Jan-16 Labidocera sp. ZL Night 7 Net towing 25-Jan-16 Calanid copepods ZL Night 22 Net towing 25-Jan-16 Parthenope sp. (zoea) ZL Night 3 Net towing 25-Jan-16 Paracalanus sp. ZM Night 18 Net towing 25-Jan-16 Copepods (200-335 μm) ZM Night 1 g Net towing 25-Jan-16 mesozooplankton ZS Night 1 g Net towing (100-200 μm) 25-Jan-16 particulate matter POM Night 1 g Net towing (20-100 μm) Legend: *specimen means individual organism, except the bottom three rows where specimen is expressed in gram (g) Sampl ing dates Taxa/size group Code Period of collection No. of specimen* Source Table 3. List of specimens used for C and N stable isotope analysis. S.I.G. Masangcay et al. 31 of space occupied by each food item and the volume of the cylindrical cardiac stomach) relative to the volume of all food item combined; and F is the percentage occurrence of each food item in the stomachs of all f ish individuals analyzed. The use of the IRI (Pinkas et al. 1971) reduces biased description of animal dietary data. This method has been widely used in studying diet composition of large marine animals and proved eff icient in determining a snapshot view of prey items in the stomach (Notarbatolo di Sciara 1988; Alonso et al. 2001; Moura et al. 2008; Schluessel et al. 2010). Analysis of C and N stable isotopes Dried samples were pulverized using acid-washed mortar and pestle. Powdered samples were aseptically placed in Eppendorf tubes and properly labelled. All samples were analyzed through dual C and N stable isotopes technique using the Thermo Stable Isotopes Analyzer coupled with the Thermo Finnigan DELTA plus XP isotope ratio mass spectrometer via a ConFlo-III continuous flow interface (Metillo et al. 2015). Samples with elemental C and N ratio > 4 were corrected for effects of lipids (Post 2002). Data treatment Isotopic values between the two M. japanica individuals were compared using Student homoscedastic t-test (SPSS 2002). Results of the stable isotope analysis (SIA) were plotted and interpreted using OmniGraphSketcher version 1.1.4. Relationships between prey and predator were calculated using the trophic enrichment factor values 3.2±0.43‰ for δ15N and 1.8±0.29‰ for δ13C (McCutchan et al 2003). Trophic levels (TL) of all samples were determined based on nitrogen isotopic values using the equation (Vander Zanden and Rasmussen 2001): TL consumer = [(δ 15N consumer —δ 15N baseline )/3.4 + 2], where δ 15N consumer is the mean value of the predator, δ15N baseline is the isotopic δ15N values from the microplankton (Z1,100– 200 μm) samples, and a trophic eff iciency factor value of 3.4. RESULTS Stomach content The state of the 16 M. japanica individuals only allowed sexing 12 which comprised ten males and two females (Table I). Body size as disk width (D w ) ranged from 120– 157 cm, while disk length (D L ) ranged from 55–73 cm. The stomach of all 16 Feeding Habits of Mobula japanica 32 individuals examined contained ingested food composed of intact identif iable prey items mixed with few digested food items. Prey organisms identif ied were mostly planktonic euphausiids, sergestid shrimps, copepods, and other categories as minor food items (Table 4). Stomach contents from all rays consisted almost exclusively of adult and eggs of the krill Pseudeuphausia latifrons G.O. Sars 1883, which exhibited IRI values of 15,180.28 and 4,537.11, respectively. The other prey items in decreasing order of IRI values were the sergestoid shrimp Lucifer > sergestid shrimp Acetes intermedius > copepods > flatworm > plant fragments > polychaete larvae = mollusc veligers. Although A. intermedius was found to have a low IRI value of 10.65, it dominated the stomach content of one M. japanica. Pseudeuphausia latifrons 588,413 76.594 75.209 100.00 15,180.28 76.66 Krill egg 175,866 22.893 22.479 100.00 4,537.11 22.91 Lucifer sp. 3,348 0.436 0.638 68.75 73.85 0.37 Acetes intermedius 540 0.070 1.634 6.25 10.65 0.05 Copepods 47 0.006 0.017 31.25 0.72 0.00 Flatworm 5 0.001 0.018 6.25 0.12 0.00 Mollusc veligers 1 0.000 0.001 6.25 0.01 0.00 Polychaete larvae 1 0.000 0.001 6.25 0.01 0.00 Plant fragments 1 0.000 0.003 6.25 0.02 0.00 Prey Number % N % V % FO IRI % IRI Table 4. Diet analysis of Mobula japanica based on 9 prey types collected from the stomachs of 16 ind ividuals. N, Number; V, Volume; FO, Frequency of occurrence; IRI, Index of relative importance C and N stable isotope values We obtained muscle tissues from f ive M. japanica individuals with sizes ranging from 130–147 cm (D w ) (Table 5). Individual values of C and N stable isotopes for these individuals were not signif icantly different (t = 1.56, df = 3, p = 0.22). Mean isotopic values for the f ive M. japanica were -16.07±0.52‰ for δ13C and 10.69± 0.34‰ for δ15N. The δ15N isotopic values were accordingly used to calculate and determine the trophic positions of M. japanica and its potential prey types. The 3.27 (female) and 3.16 (male) TL for the f ive M. japanica fall within those of secondary consumers. The stable isotope biplot displays the TL and carbon source of each taxon (Figure 3). On the other hand, isotopic signals of M. japanica show an enriched 13C compared to potential preys which have mean values ranging from -19.46‰ (medium size zooplankton) to -17.15‰ (juvenile f ish), with the exception of f ish larvae (-13.83‰). Mean δ13C values for ichthyoplankton (juvenile and larvae) differed with more depleted values for juveniles than those of larvae. Sergestid S.I.G. Masangcay et al. 33 shrimps A. intermedius had more enriched mean values (-18.47‰ for δ13C and 7.89‰ for δ15N) than those of Lucifer spp (-19.03‰ for δ13C and 6.29‰ for δ15N). The mean δ13C values of both large zooplankton (ZL 335-1000 μm, and ZXL >1000μm) are more enriched at -18.65‰ to -18.40‰ in comparison to the value of smaller zooplankton (Z1 100–200 μm: -19.27‰). The krill P. latifrons exhibited a mean δ13C value (-17.96‰) which is roughly similar to those of large zooplankton. Figure 3. Isotopic values of 13C and 15N for Mobula japanica (MJ) and potential prey from Butuan Bay, Northeastern Mindanao, Philippines. ZS, zooplankton (100–200 μm); ZM, zooplankton (200–335 μm); ZL, zooplankton (335–1000 μm); ZXL, zooplankton (> 1000 μm); FJ, f ish juvenile; FL, f ish larva; POM, particulate organic matter; AC, Acetes intermedius; KA, adult Pseudeuphausia latifrons; LU, Lucifer spp. M. japanica (female) MJ1 -16.20±0.16 10.69± 0.04 1 3.27 M. japanica (male) MJ2 -15.68±0.35 10.44±0.25 4 3.16 Acetes intermedius AC -18.45±0.10 7.89±0.23 3 2.44 Lucifer spp. LU -19.03±0.27 6.29±0.30 3 2.44 P. latifrons KA -17.96±0.48 8.34±0.08 3 2.34 Fish juvenile FJ -17.15±0.55 7.37±1.00 2 2.29 Fish larvae F L -13.83±4.67 7.11±0.47 2 2.22 Macrozooplankton (>1000μm) ZXL -18.40±1.36 6.40±0.19 3 2.01 Mesozooplankton (100-200μm) ZS -19.27±0.24 6.38±0.10 3 2.00 Mesozooplankton (200-335μm) ZM -19.46±0.12 6.71±0.12 3 2.10 Mesozooplankton (335-1000μm) ZL -18.65±0.21 6.47±0.80 3 2.03 Microzooplankton (20-100μm) POM -15.96±1.32 2.78±0.80 3 1.82 Taxa Code Mean δδδδδ13C Mean δδδδδ15C n Trophic position (TP) Table 5. δδδδδ13C and δδδδδ15N isotopic values (mean±standard deviation) and trophic position of M. japanica and its potential prey. Numbers in the species codes represent the repl icate used for analysis. Feeding Habits of Mobula japanica 34 DISCUSSION Diet of M. japanica All collected M. japanica (D w = 120–157 cm) in this study were immature (Notarbatolo Sciara 1988; White et al. 2006b) and dominated by males. According to Sampson et al. (2010), M. japanica individuals that are <205 cm (D w ) are considered immature. The sizes of the M. japanica of the present study were def initely smaller compared to those of the New Zealand population with individuals showing an average of 200 cm (D w ) and 100 cm (D L ) (Francis and Jones 2016). The predominance of immature individuals may reflect the movement of larger rays to other areas (White et al. 2006b). These rays were caught by f ishermen during the day, which validates the f indings of Croll et al. (2012) that M. japanica is commonly observed at the surface waters (<5 m) during daytime and goes to deeper waters (>50 m) at night in search for food. Devil rays in general are surface water dwellers that spend long periods in the surface during the day (Gadig et al. 2003). It is suggested that surface aggregation of this species may be attributed to the daytime swarming of the krill prey P. latifrons (Wilson et al. 2001) and Nyctiphanes simplex (Gendron 1992). Generally, stomach content analysis (SCA) provides information on prey items in l i m i t ed t i m e s c a l e s ( e . g . h o u r s to d a y s ) . I n t h i s s t u d y, S CA r e s u l t s co n f i r m e d M. japanica to have a strong feeding aff inity with planktonic organisms, which may be associated with its gill morphology (Paig-Tran et al. 2011). Rays are eff icient in capturing zooplanktonic prey by funnelling microscopic plankton into their mouth and trapping them onto the gills which are made up of f ilter-like mesh of small bones (Paig-Tran et al. 2013). All 16 M. japanica actively fed since their stomachs contained quantif iable prey. By contrast, Notarbatolo di Sciara (1988) reported only 19 (24%) out of 78 M. japanica individuals had food in their stomach. In this study, the predominance of the tropical krill P. latifrons in almost all of the stomach contents of M. japanica was observed (Masangcay et al. 2018). By comparison, the subtropical populations of M. japanica and M. thurstoni exclusively feed on the subtropical krill N. simplex, while M. munkiana feed on the mysid Mysidium sp. (Notarbatolo di Sciara 1988; Sampson et al. 2010). Mobula thurstoni primarily feeds on euphausiids (Gadig et al. 2003), but it was also observed to intensively feed on mysid shrimps (Notarbartolo di Sciara, 1988). Manta birostris (Wilson et al. 2001) and Rhincodon typus (Wilson and Newbound 2001; Jarman and Wilson 2004) are also reported to prey on P. latifrons at daytime. These f indings are in close agreement with our study, which identif ies the krill species P. latifrons S.I.G. Masangcay et al. 35 as the most important prey of M. japanica from Butuan Bay. In addition, our local plankton net tows did yield a few P. latifrons at the locations off Buenavista where fishermen capture devil rays. The few P. latifrons collected is attributable to the inefficiency of the conical plankton net in catching micronektonic krill (Nemoto 1983; Wiebe et al. 2005). Aside from adult krill, other prey items include krill eggs, whose abundance is due to the large number of egg-carrying female P. latifrons that can bear up to 164 eggs or more per individual (Wilson et al. 2003a). Although it is possible that the eggs would have been ingested as freely suspended eggs in the water column, we believe these were most likely dislodged from the mother krill’s brood pouch as a result of the peristalsis of the ray stomach. Interestingly, the shallow water sergestid shrimp A. intermedius dominated one stomach of M. japanica, indicating ingestion of other shallow water/estuarine micronektonic crustaceans (Jarman and Wilson 2004) and a possible switch to alternative prey (Notarbatolo di Sciara 1988; Wetherbee and Cortés 2004). Past studies on ray stomach content report the importance of pelagic micronektonic crustaceans like euphausiids (true krill), sergestid shrimps like Acetes spp. , and other planktonic species (Couturier et al. 2012). Micronektonic crustaceans form dense swarms and f ilter-feeding devil rays might have evolved to track large aggregations of micronektonic crustaceans whose sizes ensure energy to support the activities of these pelagic megafauna (Sampson et al. 2010; Couturier et al. 2013). Population structure analysis of P. latifrons showed changes in the size-structure, reflecting individual growth from January to May (Masangcay et al. 2018). Breeding season of this species appears to be during the warm and dry months of March to May, which coincides with the decrease in number of juvenile individuals and the increase in abundance of large egg-carrying females during these months. Incidentally, the f ishing season of M. japanica in Bohol Sea (Alava et al. 2002; Acebes 2013; Freeman 2014) and Butuan Bay (Metillo and Masangcay 2015) is from September to May with the peak season lasting from February to April. However, sightings and f ishing of devil rays could extend up to June in Butuan Bay (Metillo and Masangcay 2015) and Bohol Sea (Freeman 2014). We are convinced that the preponderance of M. japanica individuals during these months could be linked with the availability of swarms of P. latifrons. High primary production in Butuan Bay drives the abundance of P. latifrons, which prefer habitats with high abundance of zooplankton depending on dense phytoplankton (Wilson et al. 2003b). However, P. latifrons are reported to also feed on detritus (Hirota and Nemoto 1989). The peak of surface chlorophyll α is often o b s e r v e d i n B u t u a n B a y a t a r o u n d 2 0 – 3 0 m d e p t h ( V i l l a n oy, p e r s o n a l Feeding Habits of Mobula japanica 36 communication). The primary production in Butuan Bay is at maximum during December to February when heavy rainfall causes highest river discharge (as indicated by highest chromophoric dissolved organic matter or CDOM) (Figure 4 in Cabrera et al. 2011) and a pronounced plume from Agusan River, the second largest river in the Philippines (Villanoy et al. 2011). Another primary production enhancement mechanism in Butuan Bay is the “double estuarine type circulation”, which is mostly driven by the large inflow of waters from the Pacif ic Ocean passing through Surigao Strait and entrains large amounts of deep, nutrient-rich waters to the surface (Cabrera et al. 2011). This mechanism is strongest during the months of December to March when the northeast monsoon winds generate the westbound surface current Bohol Jet in the Bohol Sea (Cabrera et al. 2011). This regular circulation pattern, together with the highest freshwater discharge from the large Agusan River, eventually leads to nutrient enrichment and phytoplankton bloom, which in turn fuel high zooplankton abundance that feed the P. latifrons population. C and N stable isotope values Stable isotope analysis allowed the determination of a consumer-food relationship between M. japanica and its potential prey in Butuan Bay. The isotopic signature of δ15N reflects an organism’s trophic position, while isotopic differences among δ13C values can trace the original dietary carbon source of the consumer, whether it originated from a marine, freshwater, or terrestrial environment (Shiffman et al. 2012). Furthermore, δ13C gradients may also reflect the food web relationship between coastal or benthic, and offshore or pelagic regions (Dahl et al. 2003; Hussey et al 2011). Depleted δ13C values (-22‰ to -17‰) denote pelagic feeding, whereas enriched δ13C values (> -17‰) imply coastal and/or benthic foraging (France 1 9 9 5 ) . Here, we report the C and N stable isotopes values of one female and four male M. japanica individuals from Butuan Bay. Values among M. japanica individuals did not differ, which agrees with the study of Sampson et al. (2010) who repor ted no difference in δ13C and δ15N values between stage of maturity, between sex, among monthly values, and between species (M. thurstoni and M. japanica). Similarly, Couturier et al. (2013) found similar δ13C and δ15N stable isotopes in Manta alfredi from both Lady Elliot Island and North Stradbroke Island in Queensland, Australia. Less stable isotope variation in these large organisms may be explained by the long-term (months) turnover rates of C and N stable isotopes in muscle tissues of mobulids (Sampson et al. 2010). The low variability in stable isotope values (0.16— S.I.G. Masangcay et al. 37 0.35 for δ13C and 0.04—0.25 for δ15N in this study) is also indicative of a highly specialized diet (Sweeting et al. 2005). Mean δ13C isotopic value (-16.07‰) of M. japanica falls within the enriched category which implies that its diet would most likely be composed of prey from offshore marine and planktonic habitat (France 1995). The present study reports comparable δ13C values reported in other Mobulidae studies: M. thurstoni (-16.74‰) and M. japanica (-16.78‰) (Sampson et al. 2010); M. diabolus (-16.02‰) (Borell et al. 2011); and M. alfred i (-17.4‰) (Couturier et al. 2013). 13C values of potential prey are enriched. The difference in values for juvenile and larval f ishes may be related with migration, wherein larvae are spawned in deep spawning ground (more enriched 13C signature) but juveniles move to shallow nursery habitats (more depleted 13C signature) (Tanaka et al. 2008). Therefore, the 13C values of the juvenile f ish Acetes spp. , P. latifrons, and zooplankton are reflective of shallow neritic and estuarine organisms. The stomach content analysis in this study reveals that M. japanica preys on zooplankton, par ticularly micronektonic shrimps euphausiid (P. latifrons) and sergestid (A. intermedius) in Butuan Bay. The calculated trophic position based on mean values of M. japanica suggests the species is a low trophic level secondary consumer that assimilates nitrogen of primary consumers, concurring with the f indings of the stomach analysis. However, following the mean trophic enrichment factors (3.2‰ for δ15N and 1.8±0.29‰ for δ13C) of McCutchan et al. (2003), M. japanica would primarily eat not only the krill P. latifrons and the sergestid Acetes intermedius, but also juvenile f ish. This is not surprising as other mobulids are reported to ingest ichthyoplankton, proving plasticity in its feeding habits (Stewart et al. 2016). CONCLUSION Stomach contents of 16 M. japanica individuals were dominated by adults and eggs of Pseudeuphausia latifrons euphausiid, followed by a much lesser amount of sergestid shrimps (Lucifer sp. and Acetes intermedius), copepods, and planktonic remains. Larger female P. latifrons was observed to be the most dominant in the diet of M. japonica, which coincided during the peak of the reproductive cycle of the krill. Stable isotopes of C and N in muscle tissues of f ive M. japanica individuals and potential preys conf irm the strong feeding aff inity of M. japanica with micronektonic crustaceans. This study is the f irst formal report on the feeding of M. japanica in tropical Philippine waters. Although the current f indings are useful Feeding Habits of Mobula japanica 38 input to local conservation and management of M. japanica, we recommend that longer period of study should be made to include other ray species in the Philippines. ACKNOWLEDGEMENTS The authors gratefully acknowledge the Department of Research, MSU-Iligan Institute of Technology; Department of Science and Technology (DOST)-Advance Science and Technology Human Resources Development Program; Department of Science and Technology (DOST )-Science Education Institute (SEI); and the Japan Society for the Promotion of Science (JSPS) (the Asian CORE and the Core-to-Core Programs) for their financial and technical support. We also thank Dr. MTRD Sanchez- Metillo for copyediting the manuscript. REFERENCES Acebes JMV. 2013. Hunting “Big Fish”: A marine environmental history of a contested f ishery in the Bohol Sea [doctoral disser tation]. Per th, Western Australia: Murdoch University. 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Bulletin of Marine Science. 68(1):157-162. W i l s o n S G , C a r l e t o n J H , M e e k a n M G . 2 0 0 3 a . S p a t i a l a n d t e m p o r a l p a t t e r n s i n t h e distribution and abundance of macrozooplankton on the southern North West Shelf, Western Australia. Estuarine, Coastal and Shelf Science. 56:897-908. Wilson SG, Meekan M, Carleton J, Stewart T, Knott B. 2003b. Distribution, abundance and reproductive biology of Pseudeuphausia latifrons and other euphausiids on the southern Nor th West Shelf, Western Australia. Marine Biology. 142:369-379. _____________ Shirlamaine Irina G. Masangcay is a graduate of B.S. Marine Biology from Mindanao State University-Iligan Institute of Technology. She graduated M.S. Marine Biology from Mindanao State University-Iligan Institute of Technology on time as a DOST- ASTHRDP scholarship in 2016, and was hired immediately after graduation as Instructor at the Caraga State University, Butuan City, Philippines. Ephrime B. Metillo is B.S. Zoology graduate at the Mindanao State University Marawi City. He was University Research Assistant at the Marine Science Institute of the University of the Philippines Diliman before doing a straight Ph.D. Program at the University of Tasmania at Hobart, Australia under the Australian International Development Assistance Bureau (AIDAB) Equity and Merit Scholarship Scheme. He is now Professor at the Mindanao State University-Iligan Institute of Technology, Iligan City, Philippines. Ken-Ichi Hayashizaki is a marine scientist, an expert on stable isotope analysis and currently Associate Professor at Kitasato University, Sagamihara, Japan. Satoru Tamada is a recent graduate of Master of Science Marine Bioscience at Kitasato University, Japan with focus on the use of stable isotope analysis in the ecology of the Japanese flounder. Shuhei Nishida is a recently retired Professor at the Atmosphere and Ocean Research Institute of the University of Tokyo, Japan. He has published more than 110 papers in the f ield of marine biology and became Editor of the Springer journal Marine Biology. His main f ield of interest is marine zooplankton biology and ecology.