Philippine Journal of Science 137 (2): 169-177, December 2008 ISSN 0031 - 7683

Zooplankton Composition and Diversity in , Is.,

Ma. Riyel Y. Aquino1, Carmela D. Cho1, May Ann S. Cruz1 Ma. Angelica G. Saguiguit1, and Rey Donne S. Papa1, 2 *

1Department of Biological Sciences, College of Science and 2Research Center for the Natural Sciences, University of Santo Tomas España, Blvd., Manila, Philippines

A study on zooplankton species composition and diversity of in Luzon Is., Philippines was conducted to update the previous zooplankton species lists in the area and provide new insights into its ecology. Samples were collected monthly from April to September 2006. Twenty-seven species were found in Paoay Lake. Of these, 45% belong to Rotifera, 29% to Cladocera, and 26% to Copepoda. Five (2 Copepoda and 3 Rotifera) species that have been reported to be rare in previous studies were frequently encountered in all sampling sites such as Paracyclops fimbriatus, Tropocyclops prasinus, Conochiloides dossuarius, Keratella cochlearis and Trichocerca capucina. Nineteen species are new records for Paoay Lake. The rotifer Keratella tropica was noted to be the most abundant among all zooplankton species observed. Species diversity and richness was lowest during April and May, the same time when high densities of K. tropica was observed, and was higher during the succeeding months due to the absence of any dominant species.

Key Words: Zooplankton, Paoay Lake, Composition, Diversity

INTRODUCTION the national government, thus enabling it to monitor and control the amount of human activity in the lake. Paoay Lake (Latitude: 18° 7' 16 N, Longitude: 120° 32' 18 E) is located in the town of Paoay in the province of There are a limited number of studies on Philippine in the northern Philippine island of Luzon. It freshwater zooplankton. Most studies focus on systematics is bounded by the towns of Suba in the north, Nanguyudan and the discovery of new species. The most recent studies in the northeast, Pasil in the east, Sungadan in the south were done by Petersen and Carlos (1984); Mamaril and Nagbacalan in the north (Figure 1). It is the only lake (1986); Tuyor & Segers (1999), and Tuyor and Baay in the Ilocos Norte province (Guerrero 2001). The lake (2001). Paoay Lake zooplankton was only mentioned in is devoid of ; its source of water comes from the works of Mamaril (1986); Petersen & Carlos (1984; ground water flow and surface run-off during rainy seasons citing Mamaril and Fernando 1978), and Petersen [2007, from the surrounding hills. Paoay Lake is one of the most citing Mamaril (1986) and Mamaril and Fernando (1978)]. scenic and historical places in the region. Aside from this, No new publications can be found based on more recent small-scale is being developed in some parts samplings conducted in Paoay Lake. of the lake as livelihood of the local townsfolk residing in the area. To avoid potential misuse of the resources Likewise, no published studies exist for physico- of the lake, it has been declared as a protected area by chemical parameters, vegetation analyses, primary productivity, and fish fauna in Paoay Lake except for *Corresponding author: [email protected] reports of the Protected Areas Management Bureau [email protected] 169 Philippine Journal of Science Papa et al.: Zooplankton Composition and Vol. 137 No. 2, December 2008 Diversity in Paoay Lake, Luzon

Paoay Lake, IN 0 2000 meters

Figure 1. Sampling Stations of Zooplankton Monitoring in Paoay Lake, Luzon Is., Philippines

(PAMB) on the presence of aquatic plants like Ipomoea the lake. Site I is located in the southwestern portion of aquatica (water spinach) and Eichhornia crassipes the lake parallel to the national road. It is characterized (water hyacinth), and fish Clarias batrachus (catfish), by abundance of macrophytes found in near-shore areas. Oreochromis sp. (tilapia), and Neochanna sp. (mudfish) Site II is located in the northern portion of the lake. The when they conducted an assessment of Paoay Lake for 9-hole Paoay Golf Course may be found in its northern aquaculture utilization (PAMB pers. comm.). border. Site III occupies the northeast while Site IV is in the southeast area of the lake. There are a few fish pens This current study aims to update the previous list of located near the shoreline of the said sampling sites. zooplankton species found in Paoay Lake and to provide much needed information on species composition and diversity. It also aims to provide more recent data on some Sample Collection physico-chemical parameters like depth, temperature, Vertical plankton sampling was done to collect the samples Secchi Disc Transparency (SDT), dissolved oxygen using a conical plankton net (Diameter: 0.254m; Mesh (DO), and pH and to correlate these with the data on the size: 80um) (modified from Petersen and Carlos 1984). zooplankton of Paoay Lake. Two samples with 3 replicates were collected from different areas in each sampling site which was taken during the day (approximately between 0800–1000 hours) from all 4 sampling sites of the lake from the months MATERIALS AND METHODS of April to September, 2006. These were preserved in 10% formalin and stored in properly labeled capped bottles. The samples were brought to the laboratory for Study Area identification and analysis. Identification was done with Samples were taken in Paoay Lake from four stations, the aid of taxonomic keys and illustrations on Philippine designated as Site I (Nagbacalan), Site II (Suba), Site zooplankton by Mamaril & Fernando (1978), Mamaril III (Nanguyudan), and Site IV (Sungadan) (Figure 1). (1986), and Petersen (2007). Sites were chosen to represent the four major areas of

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Physico-Chemical Parameters Table 1. List of zooplankton species in Paoay Lake Water temperature, pH, Secchi Disc Transparency, Depth, Percent Percent Taxa and Dissolved Oxygen were noted for each of the sites. Abundance Frequency Surface temperature was obtained by using a laboratory Copepoda thermometer, Secchi Disc transparency (SDT) readings Ectocyclops pharelatus ^ 3.58 54.16 were obtained using a Secchi Disc; pH was obtained Eucyclops serrulatus 3.1 100 using a portable pH meter; and Dissolved Oxygen (DO) Filipinodiaptomus insulanus ^ 1.89 75 was obtained by using the Winkler Iodometric Method Mesocyclops sp. ^ 1.09 79.16 (Umaly & Cuvin 1988). Paracyclops fimbriatus* ^ 2.72 50 Thermocyclops crassus 1.22 91.67 Tropocyclops prasinus * ^ 0.86 70.83 Data Analyses Tropodiaptomus australis ^ 2.22 66.67 Zooplankton abundance expressed as density (inds. / l) Cladocera and occurrence expressed as % were computed. Species Biapertura pseudoverrucosa 0.03 20.83 diversity and species richness were computed using Bosmina longirostris ^ 0.29 54.16 Shannon-Weiner diversity index (H′), and Margalef’s Ceridodaphnia cornuta 11.69 100 Diversity (DMG), respectively. (Magurran 2004). These Chydorus barroisi 3.23 100 indices were compared across sampling periods using One Chydorus ventricosus ^ 0.01 8.3 Way ANOVA (PAST Software Version 1.81). Diaphanosoma sarsi ^ 3.94 95.83 Moina macrocopa ^ 0.02 8.3 Moina micrura^ 3.14 100 Rotifera Aplanchnopus multiceps 0.06 8.3 RESULTS Brachionus falcatus ^ 2.23 100 Brachious forficula ^ 4.89 100 Zooplankton Composition Conochiloides dossuarius* ^ 8.16 100 Twenty seven species including 11 rotifers, 8 cladocerans Filinia opoliensis ^ 2.66 83.33 and 8 copepods were recorded in Paoay Lake; 8 were Keratella cochlearis * ^ 0.12 12.5 previously recorded by Mamaril (1986) while the Keratella tropica ^ 34.7 100 remaining 19 species were new records for Paoay. Of Lecane bulla 0.11 14.81 Polyarthra vulgaris ^ 3.38 54.16 these, 5 species (Keratella cochlearis, Paracyclops Testudinella patina 0.47 62.5 fimbriatus, Tropocyclops prasinus, Conochiloides Trichocerca capucina * ^ 5.09 33.33 dossuarius, and Trichocerca capucina), noted to be rare N.B.: Those species with * were previously noted to be of rare occurrence in the in previously examined Philippine samples (Mamaril Philippines (Mamaril 1986); those with ^ are new records Paoay Lake 1986) were present in samples collected during the entire sampling period (Table 1). Rotifers were the most abundant of the 3 zooplankton groups comprising 61.90% of the total number of organisms, followed by the cladocerans at 22.39%. The least abundant species belong to the Copepoda with 15.71% (Figure 2). The rotifer K. tropica was the most abundant species with peak densities observed during the months of April and May. Among the cladocerans, the most abundant was C. cornuta while the most abundant copepod was Ectocyclops pharelatus (Figure 3). Ranking percentage abundances of the different zooplankton species present also revealed that 4 out of the 5 species with the highest percentage abundances were rotifers, the most abundant species of which was K. tropica at 34.7%. This was followed by the cladoceran C. cornuta at 11.7%. The computed percentage occurrence (%Occurrence) of the different zooplankton species found in the lake revealed that the rotifers Keratella tropica, Brachionus falcatus, Figure 2. Percentage abundance of the major zooplankton taxa present Brachionus forficula, and C. dossuarius; cladocerans in Paoay Lake

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(K. tropica) Density (Ind./L)

(C. cornuta) Density (Ind./L)

(E. pharelatus) Density (Ind./L)

April May June July August September Figure 3. Density (Ind. / L.) of the dominant species (for each of the three zooplankton groups studied in Paoay Lake

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C. cornuta, Moina micrura and Chydorus barroisi; and Species diversity and richness varied in all sites from copepod Eucyclops serrulatus were found in all 4 sampling April to September (Figure 4). Species diversity was stations from April to September. Asplanchnopus lowest during the month of May in 1 of the 4 sampling multiceps and Chydorus ventricosus both had the lowest stations. An increase in diversity was observed from % Occurrence at 8.33% each. April to July. Highest diversity was noted in Site 1 for 4 of the 6 sampling months, except for the month of May. The succeeding months saw no drastic change in species Species Diversity and Richness diversity for the 4 sampling sites. There are significant differences among values obtained for both species diversity and richness across months Species richness was noted to be lowest during the based on the results obtained using One Way ANOVA first 3 sampling months with DMG values ranging from (p < 0.05). 2–2.5. An increase was observed in July, and which is

Figure 4. Shannon-Weiner Diversity (A) and Margalef’s Diversity (B) of the zooplankton species present in the 4 sampling sites of Paoay Lake from April-September 2006

173 Philippine Journal of Science Papa et al.: Zooplankton Composition and Vol. 137 No. 2, December 2008 Diversity in Paoay Lake, Luzon the month that had the highest species richness during the DISCUSSION entire sampling period. Species richness for the months August and September decreased from the previous There were 27 species of zooplankton recorded in this high noted for July with values ranging from 2.6–3.5. study. Nineteen species were new records for Paoay Lake. Species richness was also noted to be highest in Site 1 Previously mentioned rare species were also found to be as compared to the other 3sampling sites for the months well distributed in the 6 sampling months and in all 4 of May, July, August, and September. sampling sites. An increase in sampling effort to 6 months in more sampling sites covering both littoral and limnetic areas might have caused the higher yield in the number of Physico-Chemical Parameters zooplankton species in this study. Mamaril’s collections Mean lake depth was highest for the month of September in Paoay Lake was only limited to the near-shore areas at 4.94 meters. Among all the sampling sites, Sites 2 of the lake (Mamaril 1986; Petersen 2007). and 3 were deepest having mean depths at 4.14 and 4.46 meters, respectively, while Site 1 was shallowest at This study revealed that the most frequently occurring 2.83 meters mean depth. The pH values of all sampling and abundant zooplankton belong to the Rotifera, which months obtained ranged from 6.75 to 7.88. Highest included 11 species- the most number of species belonging values were obtained in June (7.88) and July (7.58). to a single group among the three that were studied. The Highest mean water temperature (33.83° C) was noted dominance of rotifers was similar to findings from other during the month of June. The lowest water temperatures Philippine . Petersen and Carlos (1984) recorded 43 were obtained in August and September (30° C; 31.67° rotifer species mainly from (though his C). Mean Secchi disc transparency (SDT) readings analyses also included formalin preserved samples from (0.60–0.88m) were low. Site 1 and 2 of September had Paoay, the Seven Lakes of Laguna, a fishpond in Los Baños, the highest mean SDT values (1.06, 1.11m). June and Laguna, , and Manila Bay). This number was July had the lowest mean SDT values (0.62-0.60m). far greater than the results for Cladocera (15 spp.) and Dissolved oxygen (DO) values from April-July have Copepoda (22 spp.) in the same study. A paper published higher mean values (surface: 3.65-7.13, bottom: 3.25- by Tuyor and Segers (1999) on monogonont rotifers 6.31) than August and September (surface: 1.96-2.69, counted a total of 50 species from 10 samples collected bottom: 1.95-3.21) (Tables 2 and 3). from different freshwater bodies in Laguna province in Luzon Island and in province in Visayas Island. The most comprehensive study done on Philippine Table 2. Mean values for physico-chemical parameters from April to zooplankton by Mamaril revealed a total of 61 species of September rotifers recorded for the entire Philippine Archipelago Depth Temp. SDT (Mamaril & Fernando 1978). This went up to 76 in a more pH DO (ppm) (m) (° C) (m) recent paper, which included samples taken mainly from Surface Bottom Lakes Laguna, Lanao, Taal, and Mainit; as well as from April 2.63 6.9 31.67 0.72 4.41 6.31 La Mesa Dam and several ponds, ditches, and rivers in the Philippines (Mamaril 2001). Meanwhile, studies on May 2.5 7.29 33.09 0.88 7.13 5.94 the zooplankton of tropical reservoirs in Brazil likewise June 2.88 7.88 33.83 0.62 4.75 4.13 revealed 76 species of rotifers, 7 species of copepods, July 4.15 7.58 31.92 0.6 3.65 3.25 and 26 species of cladocerans (Sampaio et al. 2002). August 4.5 7.21 30 0.69 2.69 3.21 The high number of rotifer species present in a particular September 4.94 6.75 31.67 0.8 1.96 1.95 freshwater ecosystem may be attributed to rotifers reacting less to different trophic levels given that some species like Keratella cochlearis (which is present in Paoay Lake) Table 3. Mean values for physico-chemical parameters from sites 1 to 4 may be observed in both eutrophic and oligo-mesotrophic lakes (Ferrara et al. 2002). Rotifers are also considered Site 1 Site 2 Site 3 Site 4 as important zooplankton because of their high numbers Depth (m) 2.83 4.14 4.46 2.96 in aquatic ecosystems and their reliability as continuous pH 6.92 7.46 7.15 7.55 indicators for the evaluation of physical processes. Temperature (° C) 31.93 32.07 32.13 32.17 Southeast Asian zooplankton communities, including SDT (m) 0.8 0.74 0.64 0.69 that of Paoay Lake are typically tropical, with its rotifer DO (ppm) Surface 4.83 3.99 3.55 4.02 composition having the highest number of species Bottom 4.4 4.87 3.6 3.65 present and is also represented mainly by the genera Brachionus and Keratella. Members of these 2 genera

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are also good indicators of eutrophication and pollution large crustacean zooplankton (Fernando 2002). The high (Saksena 1987) and eutrophic lakes have been noted to percentage occurrence of 4 of the 8 cladoceran species harbor high numbers of Brachionus and Keratella (Arora present in Paoay may be due to the low number of both 1961). Paoay Lake has 2 species each from each genus invertebrate and vertebrate predators. Mesocyclops sp. (K. tropica, K. cochlearis, B. falcatus, and B. forficula), is the only invertebrate predator present in the lake while which were all observed in Paoay Lake in all the sampling possible vertebrate predators may come from the larval sites for all 6 months. Furthermore, K. tropica and K. and juvenile tilapia, catfish, and mudfish noted to be cochlearis were both new records for Paoay Lake. They present in the lake. No true zooplanktivore is present in have been noted as limnetic species (Mamaril 2001). Their Paoay, unlike in that is home to the endemic absence in previous collections may again be attributed Sardinella tawilis: a size selective zooplanktivore (Papa to the lack of limnetic samples taken during that time. et al. in press). Added to this is the fact that species like Petersen and Carlos (1984) also previously mentioned the Moina micrura have highly transparent bodies that help occurrence of Anuraeopsis navicula in Paoay Lake. This them avoid predation. was likewise mentioned as typical for tropical habitats. Samples examined for this study revealed that there were There were also 8 species of copepods (6 no A. navicula present in Paoay Lake at this time. Tuyor Cyclopoida, 2 Calanoida) present in Paoay Lake. and Segers (1999), Mamaril and Fernando (1978) and Among the cyclopoids, Thermocyclops crassus and Mamaril (1986; 2001) also did not observe the occurrence Mesocyclops sp. were the most widely occurring of this species in the localities sampled. species while Ectocyclops pharelatus had the highest percentage abundance. The identity of Mesocyclops Eight species of cladocerans were present in Paoay collected from Paoay Lake was previously placed Lake, which is comparatively lower than the 17 species under M. leuckarti; however, recent publications recorded co-occurring in a single sample collected from on the identity of Philippine Mesocyclops spp. Bustos Dam in Bulacan province, in Luzon Island; the 25 suggest the need for revisions (Tuyor & Baay 2001; species present in Lake Lanao; the 24 species reported in Holynska pers. comm.). Even though T. crassus, La Mesa Dam, and the 20–25 species that may be observed and Mesocyclops sp. were widely distributed in all to co-occur in other tropical lakes (Mamaril 2001). the sampling sites throughout the 6-month sampling period, they do not contribute much to overall copepod Among the cladocerans, Ceriodaphnia cornuta, abundance as compared to E. pharelatus which in Chydorus barroisi, Moina micrura, and Diaphanosoma spite of having a lower percentage occurrence occurs sarsi were all found to occur heavily in the lake. in higher densities. The distribution of Mesocyclops Diaphanosoma sarsi, and M. micrura were both new sp. and T. crassus in Paoay is comparable with results records for Paoay while C. cornuta, and C. barroisi have gathered by Mamaril (2001) on these 2 organisms as previously been noted by Mamaril to be present in Paoay. the dominant cyclopoids present in the Philippines C. cornuta has also been noted to be second to K. tropica and other Southeast Asian countries. Tropical lakes in terms of over-all percentage abundance and is the most usually have at least 1 species of cyclopoid copepod abundant cladoceran found in Paoay Lake. Cladocerans (Lewis 1979); this is consistent with the results of have been noted to be second to rotifers in terms of number this study and other studies on Philippine zooplankton of species present in several localities in the Philippines (Mamaril & Fernando 1978; Mamaril 1986; Mamaril (Mamaril 2001; Petersen & Carlos 1984). Philippine 2001; and Petersen & Carlos 1984). There are also 2 cladocera are made up of approximately 49 species calanoid copepods present in this study: the endemic (Mamaril & Fernando 1978; Mamaril 1986; 2001). Filipinodiaptomus insulanus and Tropodiaptomus The genus Daphnia is absent in the tropics (Mamaril australis - both were not mentioned in previous studies 2001; Fernando 2002), however species replacements in Paoay Lake and were previously found to co-occur belong to the genera Moina and Diaphanosoma. Both only in 3 localities (Mamaril & Fernando 1978). This are known to include limnetic and pelagic species. Their study adds Paoay Lake to the list of lakes where these being new records in Paoay Lake may again be attributed 2 calanoids are known to occur. Calanoids have an to sampling being limited to lakeshore areas in previous irregular distribution among Philippine lakes and have studies. These 2 have also been noted to be the largest been notably absent in many large lakes where they (in terms of size) of the cladoceran species present in can be expected (Mamaril 2001). Filipinodiaptomus Taal Lake (Papa 2005) though overall observation of insulanus was previously noted to be restricted to the the cladoceran community of Philippine lakes would provinces of Bulacan, Rizal, and Laguna (Mamaril & suggest that they are made up of mostly small sized Fernando 1978). This is the first reported occurrence organisms. Tropical lakes and reservoirs rarely harbor of F. insulanus in northern Luzon.

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Species structure within a given ecosystem may be in a wide number of environmental factors including defined as the number of species present and their relative water temperature, light, chemistry (particularly pH, abundance. This may be used to determine aspects of the oxygen, salinity, toxic contaminants), food availability position of certain species in the zooplankton community (algae, bacteria), and predation by fish and invertebrates. (McGowan & Miller 1980). Tropical freshwater Though this is true of zooplankton, no drastic changes zooplankton are not as diverse as their counterparts in or shifts to extreme levels were observed in the different temperate regions and marine ecosystems (Fernando physico-chemical parameters that were measured leading 2002). This study has established the rank abundance to little or no impact on species composition and diversity of 27 zooplankton species present in Paoay Lake. The in the lake. Valuable information on nutrient availability, lake is dominated by rotifers with Keratella tropica with algal biomass, macrophyte density, and zooplankton the highest percentage abundance. The abundance of predation may give a more comprehensive account on K. tropica in Paoay Lake may be due to the absence of its effect on the zooplankton community of Paoay Lake a predator. Saunders and Lewis (1988) observed high and its trophic status. numbers of Keratella when Chaoborus larvae were not plentiful. Among the 5 highest values for percentage abundance, Ceriodaphnia cornuta was the only non- rotifer. K. tropica is 1 of 3 common rotifer species ACKNOWLEDGMENTS present in the Philippines, though no studies have noted The researchers would like to thank the DENR PAMB its abundance and distribution in any Philippine lake. Region I and Gov. Jr. for permission The magnitude of the diversity and richness indices is to conduct sampling in Paoay Lake and Prof. Augustus sensitive both to the degree of dominance and the number C. Mamaril, Sr. for assistance and guidance in species of species present. Diversity is also well correlated with identification. the number of species (McGowan & Miller 1980). In this study, lower values for diversity and richness coincided with the high number of K. tropica during the months of April and May. The increase in diversity during the REFERENCES month of July and similar diversity and richness values ARORA HC. 1961. Rotifera as Indicators of Pollution. for August and September may be attributed to the lower CPHERI Bull 3 and 4: 24. abundance of dominant species like C. cornuta and E. pharelatus. An increase in zooplankton diversity in the FERRARA O, VAGAGGINI D, MARGARITORA F. study of Osore et al. (2004) in Mida Creek, Kenya was 2002. Zooplankton abundance and diversity in Lake noted when abundances were also low and when no Bracciano, Italy. J Limnol 61 (2): 169-175. dominant taxa were observed. FERNANDO C. (ed.). 2002. A Guide to Tropical Paoay is a shallow lake with depths reaching Freshwater Zooplankton –Identification, Ecology and a maximum of 4.94 meters during the month of Impact on Fisheries. Leiden, the Netherlands: Backhuys September. This increase in depth during the months Publishers. 291p. of July–September may be due to higher rainfall during GUERRERO III RD. 2001. Sustainable development these months. The occurrence of a recent typhoon in of Philippine lake resources: An agenda for research September, which hit the area previous to the sample and development, pp. 19-23. In: Santiago CB, Cuvin- collection might have caused a further increase in mean Aralar ML, and Basiao ZU (eds.). Conservation and water depth. Water pH ranges from neutral to slightly Ecological Management of Philippine Lakes in relation alkaline (maximum pH = 7.88). This may be attributed to Fisheries and Aquaculture. SEAFDEC; PCAMRD to shallow water depth and the photosynthetic activity and BFAR, Philippines. 187p. of aquatic macrophytes and present in some areas of the lake (Papa pers. obs.) leading to the LEWIS, WM. 1979. Zooplankton Community Analysis. increase in pH. Low Secchi Disc Transparency (SDT) Springer-Verlag. and Dissolved Oxygen (DO) values may be attributed MCGOWAN JA, MILLER CB. 1980. Larval Fish and to the occurrence of blooms of the colonial green Zooplankton Community Structure. CalCOFI Report, algae Botryococcus braunii from April to September XXI: 29-36. 2006, which may have been caused by excessive nutrient input from the nearby golf course (Papa et MAGURRAN AE. 2004. Measuring Biological Diversity. al. 2008). Zooplankton are susceptible to variations Blackwell Publishing. 256p.

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