International Conference on Environmental and Biological Sciences (ICEBS'2012) December 21-22, 2012 Bangkok (Thailand)

Feeding biology and diet composition of the freshwater , tawilis from () in southern ,

Richard M. Magsino

grounds in the country, it will always be important in Taal Abstract—The study investigated the feeding biology and diet Lake to study the feeding relationships of organisms inhabiting composition of the only freshwater sardine, Sardinella tawilis its freshwaters. sampled from Taal Lake in Batangas, Philippines. A total of 540 Fish feeding biology studies are important for many several samples, composed of two size-classes, were collected monthly from reasons. They provide better understanding of trophic January – June 2010, from three sampling points in Taal Lake in the relationship among different species in a specific aquatic morning, noon and afternoon periods. These were analyzed for gut ecosystem, thus they prove useful in the preliminary estimation content and zooplankton analyses in the laboratory. Results revealed that the major diet of S. tawilis in Taal Lake contained different types of trophic levels [3],[4]. These trophic models will then be of zooplankton including cladocerans, calanoid , cyclopoid used as tools to understand complex coastal ecosystems. These copepods, nauplii, , ostracods, and various species of studies are also useful in defining predator-prey relationships, protozoans and small fishes. The current study showed that copepods where they may also result in the establishment and were the most abundant at ~45–57%, followed by the cladocerans identification of stable food preferences specific for a species ranging from 28–31% also in both size classes. Various [4]. However, there is paucity of information on the dietary species (e.g., cyclopoida and ) and protozoans were variably requirement of this species of Sardinella among Philippine chosen both fish size classes. Smaller frequencies (ranging from freshwaters, except for the one worked in Taal Lake [5]. 2.1% – 18.4%) of rotifers, ostracods and small fishes were also found The present study dealt with investigating the food habits of in the gut of S. tawilis. There were significant differences in terms of the seasonal consumption of prey items in both size classes of S. Sardinella tawilis in Taal Lake. It is considered one effective tawilis. Small-sized fish consumed most of its prey in May and June approach to be able to investigate the aquatic ecology of this and this was significantly different with their prey consumption freshwater ecosystem. S. tawilis sampled approximately less pattern from January to April. In terms of feeding activity and main than a decade ago, exhibited intense feeding on various food index (MFI), most S. tawilis fishes have empty stomachs during zooplankton species including calanoid and cyclopoid the morning (Er=21.2%) and afternoon (Er=30.1%), while at night, copepods, Bosmina, Moina, Ceriodaphnia cladocerans, and most of the fish have food in their stomachs and the mean empty ratio many others [5]. However, they failed to identify size- is lowest at Er = 16.7%. This is the first study to report differences in dependent patterns in the feeding biology of this freshwater the food diet of two size classes, the MFI and frequency of food species. Moreover, they did not estimate the vacuity and the occurrence, and feeding activity of S. tawilis in relation to vacuity index or % of empty stomachs. Main Food Item indices which will indicate the food habits of this species. S. tawilis is important in the food chain of aquatic Keywords—feeding biology, fish diet, Sardinella tawilis, Taal areas such as the Taal Lake, thus [6]-[7] noted that prospects Lake of possible culture development of various fish species necessitates a detailed study on their nutrition and feeding I. INTRODUCTION behavior. In addition, results are aimed at better understanding of the biology of predator and prey species, as ARDINELLA tawilis [1] is the only freshwater sardine well as being useful for stock and ecosystem-based analyses species in the Philippines and probably in the world. It is S [4]. endemically found in the country exclusively inhabiting The general objective of the study is to determine the Taal Lake in the province of Batangas in southern Luzon [2]. feeding biology and diet composition of the freshwater Sardinella fisheries in Taal Lake form one of the most sardine, Sardinella tawilis in Taal Lake in Batangas Province. important freshwater resources in the country. They are caught in commercial quantities and available all year round, Specifically, it aims to determine the differences in the food hence it is always affordable as common source of diet of two size classes of S. tawilis, to determine the main protein. Being one of the most important freshwater fishing food item and frequency of food occurrence, and to determine the feeding activity of the species in relation to vacuity index Richard M. Magsino is with the Biology Department, College of or % of empty stomachs. Education, Arts and Sciences of De La Salle Lipa, Lipa City, Batangas, Philippines (Phone: +06343-7565555; fax: 437565555; e-mail: [email protected]).

9 International Conference on Environmental and Biological Sciences (ICEBS'2012) December 21-22, 2012 Bangkok (Thailand)

II. MATERIALS AND METHODS number of stomachs sampled [6]. Three primary indices (N, W and F) were calculated to determine the diet of S. tawilis: N is A. Sample Collection the number of individuals of an item, W is the weight of one Samples of the freshwater fish, Sardinella tawilis were item, and F is the number of stomachs containing each item. collected using a 0.3 mm fish net for the young, and 0.8 mm These indices were calculated for each prey item and for each haul net for the adults from three sites in Taal Lake: offshore fish size class. N1 = 100 x number of individuals of item 1 / Talisay, Balete and Laurel (Fig. 1). Collected fish samples total number of prey; W1 = 100 x weight of item 1 / total (~30 individuals) were grouped into two: small fishes from weight of prey; F1 = 100 x number of stomachs containing 70-140 mm and large fishes from 150-250 mm. Samples were item 1 / number of non-empty stomachs examined. randomly collected monthly from January to June 2010, with The Main Food Item (MFI) index was then computed morning, afternoon and evening samplings. These were then combining these three indices [8]. This index was improved by placed in ice-filled container to slow down any bacterial [9] where MFI was summed and for each prey item was digestion process in the fresh stomachs and for easier prey expressed as the ratio of the total. Prey items were classified identification. Fish samples were brought in the laboratory for by decreasing relative values and cumulated ratios are gut content analyses. calculated, following the classification: Main prey: first rank cumulated MFI > 50%; Secondary prey: MFI cumulated ratio between 10% and 50% and Accessory prey: cumulated ratio MFI < 10%.

III. RESULTS AND DISCUSSIONS

A. Diet Composition of S. tawilis A total of approximately 540 individuals of S. tawilis were sampled from the three sites in Taal Lake from the period spanning January to June 2010. Morphological measurements of the fish samples revealed that ~ 65% were small-sized (i.e., 70-140 mm) while the rest of 35% were large (i.e., 150-250 mm). No effort to determine the sex of the fish samples was Fig. 1 shows the sample collection sites for Sardinella tawilis in conducted. However, visual inspection of the samples revealed Taal Lake dominance of females based on the presence of gravid individuals especially in May and June collections. B. Laboratory Analyses Results of the present study revealed that the major diet of The procedures followed in [5] were conducted in the S. tawilis in Taal Lake contained predominantly of different laboratory analyses. Samples were measured by total length types of zooplankton (Fig. 2). These zooplankton include and body weight before dissection inside the laboratory. several species of cladocerans, calanoid, harpacticoid and Internal organs were removed and stomach contents flushed cyclopoid copepods, rotifers, ostracods, and various types of with distilled water before examination under a compound protozoans and small/larval fishes. A study found that the microscope. Gut contents were examined and all food items copepod species were the most common feeding items in their were identified up to order level of classification following S. tawilis samples collected in 2003-2004 [5]. The current standard protocols. Zooplankton samples were then separated study showed that indeed, copepods were the most abundant at and preserved in 5% formalin solution. Only entire organisms approximately 45 – 57% in both size classes, followed by the were counted, those that were partially digested but could still cladocerans ranging from 28 – 31% also in both size classes. be identified were considered for counting. This was significantly different with results reporting that around 90% of the zooplankton diet of S. tawilis in their C. Statistical Treatment of Data samples is composed primarily of copepods [5]. However, in Two methods were used to describe the diet composition of the present study, the various copepod species (e.g., S. tawilis: the numerical method and the frequency of cyclopoida, harpacticoida and calanoida) when combined, occurrence (FOC) method (adapted from [6]). All components were still the most preferred food items of S. tawilis. of each feeding item were recorded for the two length classes Protozoans were variably chosen by the two fish size classes. and results were expressed in percentages (numerical). On the Smaller frequencies (ranging from 1% – 8%) of rotifers, other hand, the number of specimens where feeding ostracods and small fishes were also found in the gut of the components will be found were recorded independently of size two size classes of S. tawilis. This significant temporal of quality of organisms present (FOC) using the formula: FOC difference in the diet of S. tawilis may be attributed to recent = (100)n/N where n = number of specific feeding item found temperature increase of the freshwater ecosystem of Taal and N = total number of feeding items. brought primarily by global warming [10] although this aspect The % of empty stomachs (Er) were also determined to is still worth investigating. analyze the feeding activity of S. tawilis using the equation: Er = (100) ns/N where ns = number of empty stomachs and N =

10 International Conference on Environmental and Biological Sciences (ICEBS'2012) December 21-22, 2012 Bangkok (Thailand)

and June and this was significantly different with their prey consumption pattern from January to April. The same was observed among the large-sized fish where they consumed most prey items during the periods of April to June. Seasonal differences in diet composition may be due to the capability of the species in adjusting its diet on the seasonally oscillating prey abundance [15]. Data on monthly composition of food consumption across the two size classes of S. tawilis also showed significant variation (Fig. 4). The diet differences among size classes are probably due to the energy requirements, which vary according to the developmental stage. This may reflect that smaller fishes tend to consume more copepods (i.e., calanoid, harpacticoid and cyclopoid) to provide them more sources of animal protein for to sustain

continuous growth. Indeed during ontogeny, fish often change their diet mediated by allometric, morphological changes [16], thus being able to exploit sequentially a series of prey sizes ranging from phytoplankton and small zooplankton to much larger prey.

Fig.2 Feeding composition of small – (top) and large – (bottom) sized Sardinella tawilis in Taal Lake.

Results are similar with studies on food composition of other Sardinella species sampled from other bodies of water. All of these studies indicate that copepods were the most preferred food items of different Sardinella species. Copepods were the most abundant prey item in their winter and spring samples of S. aurita, feeding alongside with other zooplankton and crustaceans [11]. A study on the feeding ecology of Brazilian sardine (S.braziliensis) found that copepod nauplii dominated the diet of the preflexion and flexion larvae feeding on a diurnal pattern of food intake [12]. A study on trophic ecology of S. gibbosa in two Kenyan locations found that this species fed mostly on copepods during the two sampling seasons, further noting that because of the flexible feeding cycles of the species [13], Sardinella are opportunistic feeders Fig. 3 shows seasonal differences in gut content of small-(top) and or foragers that feed on suitable food as encountered. A large- (bottom) sized Sardinella tawilis in Taal Lake. similar preference for nauplii and post-nauplii copepods for the round sardinella, S. aurita in the NW Mediterranean [14]. Further, copepods and cladocerans were preferred by S. tawilis for copepods because of the species’ ability to select larger prey [4]. It may be possible that S. tawilis is a particulate- feeding planktivore and a selective predator that can visually detect, locate and attack a single zooplankton individual.

B. Size-dependent variation in food consumption Fig. 3 shows there were significant differences in terms of the seasonal consumption of prey items in both size classes of S. tawilis. Small-sized fish consumed most of its prey in May

11 International Conference on Environmental and Biological Sciences (ICEBS'2012) December 21-22, 2012 Bangkok (Thailand)

protozoans and the small fish larvae) were all considered accessory preys (cumulative MFI < 10%).

Fig. 4 shows monthly composition of food consumption for small- (top) and large- (bottom) sized Sardinella tawilis in Taal Lake.

C. Feeding biology of S. tawilis Table 1 reveals that in terms of feeding activity and main food index, most S. tawilis fishes have empty stomachs during the morning (Er=21.2%) and afternoon (Er=30.1%), confidence interval at α 0.05. At night, most of the fish have food in their stomachs and the mean empty ratio is lowest at Er = 16.7%, confidence interval at α = 0.05. No computations for mean repletion index were performed, nevertheless results on % of empty stomach show that most individuals of S. tawilis are feeding actively at night. This observation agrees with results of [6] for the bigeye scad, Selar crumenopthalmus in La Reunion Islands which also feeds mainly during the night. Fish populations observed in Hawaii [17] and in the Virgin Islands [18] also revealed species feeding at dusk to midnight. Fig. 5 shows prey classification obtained with the Main Food Item Night feeding is not common for epipelagic fish, although (MFI) index of small – (top) and large – (bottom) sized Sardinella tawilis in Taal Lake. small plankton feeders, like sprats and anchovies can feed actively at night [19]. The comparatively large eye size of bigeye scad, and maybe of sardine, S. tawilis, probably IV. SUMMARY AND CONCLUSION explains their ability to prey at night in the dark and particularly on small floating from the macroplankton. The diet composition and feeding activity of the freshwater The feeding items obtained for the two size classes of S. sardine, Sardinella tawilis in Taal Lake in Southern Luzon tawilis were classified using the main food item (MFI) index have been determined. The most predominant prey item (MFI (Fig. 5). Results on food composition of S. tawilis showed that > 50%) of S. tawilis are different species of zooplankton such this species is zooplanktivorous both as juveniles and adults. as and copepods (e.g., calanoid, cyclopoid and Results also showed no prey size selectivity for both size harpacticoids) secondary prey item includes rotifers and classes based on the similar food diet composition data. It ostracods (MFI between 10 – 49%), others such as protozoans appears that both small- and large-sized freshwater and fish larvae were classified as accessory preys (MFI < feed mainly on cladocerans and different species of 10%). Significant seasonal differences on diet of small-sized (P=0.0018***) and large-sized (P=0.0032***) S. tawilis. The species was also found to primarily feed at night based on lowest % of empty stomachs (vacuity index), compared with fishes caught in the morning and in mid-day.

ACKNOWLEDGMENT The study is indebted to the De La Salle Lipa – Office for Research and Publications for the provision of research funds. Local fishermen from the various lake barangays of Talisay, Balete and Laurel also helped in the collection of S. tawilis calanoid, cyclopoid, and harpacticoid copepods with samples monthly for six months. The Biology Department cumulated MFI of > 50%). Rotifers and ostracods were the Laboratory of DLSL also provided the space, use of equipment secondary categories with cumulated MFI between 10-50%, of and various materials used in the stomach content analysis. prey in both size classes. The other food items (e.g., the Thanks is also due to the DLSL Presidential Research Fund for

12 International Conference on Environmental and Biological Sciences (ICEBS'2012) December 21-22, 2012 Bangkok (Thailand) the provision of travel support for the paper presentation of the physical sciences to both major and non-major students of Science for four author in the 14th Zonal R & D Review of the Southern Luzon years in 2004-2008. He is a BS Biology graduate of De La Salle University-Dasmarinas in Zonal Center for Aquatic and Marine Research and Cavite and finished MS Marine Biology at the University of the Philippines Development held at the Western Philippines University in Diliman (UPD) as the Chancellor’s Award for Most Outstanding Student in Puerto Princesa City, Palawan, 3 – 5 November 2010. 2004. In UPD, he worked as a University Research Associate in the Marine Science Institute where he was able to work with some of the country’s finest and seasoned marine biologists. Together, they were able to publish scientific REFERENCES articles in international ISI, peer-reviewed journals in the field of population genetics in the marine environment using molecular markers. Presently, his [1] A.W. Herre, “Four new fishes from Lake Taal (Bombon).” Philipp. J. research interests are in the areas of marine and freshwater biology and Sci., 1927, 34:273-279 integrated coastal management. [2] M.T Mutia , L. Magistrado, F. Muyot, “Assessment of Lake Taal

fisheries. Taal, Batangas, Philippines”: National Fisheries Biological

Center, 2001, 1-17 [3] P. Sa-a, M.L.D. Palomares, D. Pauly, “The FOOD ITEMS Table”. In FishBase 1997 CD-ROM. ICLARM, Manila, 1997 [4] R.H. Lopez-Peralta, C.A.T. Arcila, “Diet composition of fish species from the southern continental shelf of Colombia.” Naga: WorldFish Center Quarterly, 2002, 25:3-4 [5] R.S. Papa, R.C. Pagulayan, A.J. Pagulayan, “Zooplanktivory in the endemic sardine, Sardinella tawilis (Herre 1927) of Taal Lake, the Philippines.” Zool Stud 2008, 47(5):535-543 [6] O. Roux, F. Conand ”Feeding habits of the bigeye scad Selar crumenopthalmus (Carangidae), in La Reunion Island waters (Southwestern Indian Ocean).” Cybium 2008, 24(2): 173-179 [7] Pagdilao C (pers. comm.) Southern Luzon Zonal Center for Marine and Aquatic Zonal Review [8] C.D. Zander “Feeding ecology of littoral gobiid and blennioid fish of the Banyuls area (Mediterranean Sea). I. Main food and trophic dimension of niche and ecotope”. Vie Milieu 1982, 32: 1-10 [9] E. Rosecchi, Y. Nouaze “Comparison of five digestive indices and its utility for stomach content analyses” Rev Trav Inst Pêches marit 1985, 49(3-4): 111-123 [10] Papa RS (pers. comm.) Southern Luzon Zonal Center for Marine and Aquatic Zonal Review [11] A.C. Tsikliras, M. Torre, K.I. Stergiou “Feeding habits and trophic level of round sardinella (Sardinella aurita) in the northeastern Mediterranean (Aegean Sea, Greece).” J Biol Res 2005, 3:67-75 [12] F.W. Kurtz, Y. Matsuura “Food and feeding ecology of Brazilian sardine (Sardinella brasiliensis) larvae from the southeastern Brazilian bight” Rev Bras Oceanogr 2001, 49(1/2):61-74 [13] J.A. Nyunja, K.M. Mavuti, E.O. Wakwabi “Trophic ecology of Sardinella gibbosa (Pisces:) and Atherinomorous lacunosus (Pisces:Atherinidae) in Mtwapa Creek and Wasini Channel, Kenya Western Indian Ocean” J Mar Sci 2002, 1:2 181-189 [14] E. Morote, M. Polivar, F. Villate, I. Uriarte “Diet of round sardinella, Sardinella aurita larvae in relation to plankton availability in the NW Mediterranean” J Plankton Res 2008, 30(7):807-816 [15] H. Nieland “The food of Sardinella aurita (Val.) and Sardinella eba (Val.) of the coast of Senegal” Rapports et process-verbaux des reunions conseil international pour l’exploration de la mer, 1982, 180:369-373 [16] V.S. Karpouzi, KI Stergiou, “The relationships between mouth size and shape and body length for 18 species of marine fishes and their trophic implications,” J Fish Biol 2003, 62:1353-1365 [17] P.Y. Kawamoto “Management investigation of the akule or bigeye scad, Trachurops crumenophthalmus (Bloch).” Hawaii Division of Fisheries and Game, Project Report N° H-4-R, 1973, 28 p [18] W. Tobias “Resource evaluation of the bigeye scad, Selar crumenophthalmus in the insular shelf waters around St Croix, US Virgin Islands.” Proc Gulf Carib Fish Inst 1987, 40: 82-98 [19] D.A. Milton, S.J.M. Blaber, N.J.F. Rawlinson “Diet and prey selection of six species of tuna baitfish in three coral reef lagoons in the Solomon Islands.” J Fish Biol 1990, 37: 205-224

Richard M. Magsino (BS’97-MS’04) is currently an assistant professor of Biology in De La Salle Lipa (DLSL) in Batangas, Philippines. He served as the chairman of the Biology Department and Science Area for two consecutive years in 2009-2011. Prior to his affiliation with DLSL, he has been connected with the Southern Luzon State University in Quezon Province, also in the Philippines, where he taught various biological and

13