Manila bay is one of the most important bodies of water in the Philippines because of its socio-economic importance.[1] The natural resources available have been the primary source of livelihood for people in the areas within the bay. Rapid increase in population and industrialization in the watershed cause the bay to suffer from serious water quality deterioration.

Zooplankton plays a major role in the functioning and the productivity of aquatic ecosystems through its impact on the nutrient dynamics and its key position in the food webs. [2] Zooplankton community is highly sensitive to environmental change [3] they respond to disturbances in the environment like nutrient loading [4] and fish densities [5]. A change in the physico-chemical conditions in aquatic systems brings a corresponding change in the relative composition and abundance of organisms thriving in the water, therefore they can be used as a tool in monitoring water systems, [6] hence are considered of ecological importance.

Several studies have examined and reported about zooplankton, internationally in different parts of the world [3], some studies were zooplankton as indicators of water quality done by Webber et al. in 2005 [7] in Discovery Bay in Jamaica and the identification of water quality and zooplankton characteristics in Daya Bay in China done by Wang et. al., 2011 [8] but in Manila Bay, despite the studies done concentrating on the pollution of the bay especially regarding its water quality and harmful algal bloom issues, only very few studies are presently available on the structure of zooplankton community and its interaction with environmental pollution.

The study aimed to describe the species composition of zooplankton community in the bay and the spatio-temporal variations in the abundance of zooplankton in Manila Bay and to describe the environmental condition of the bay and to know the relationship of zooplankton abundance and species composition with environmental factors.

Study site

Sixteen stations in Manila bay were established for investigation. (Figure 1) Manila bay has an area of 1,994 km² (769.9 sq mi) with an average depth of 17 m (55.8 ft). It is bounded by the province of Cavite and Metro Manila in the east, Bulacan and Pampanga on the north and the province of Bataan on the west [1].

Figure 1: Study site.

Collection of samples

Zooplankton samples were collected in the months of January, March, May, July, September and November in 2013. Samples were collected using plankton net about two feet in length with 64 μM mesh size. The net is slowly lowered down the water up to 5 meters sieving 706 L of water. This is then reduced to 100 ml and then preserved in 4% formalin an aliquot of 1 ml was subjected to counting and identification.

Physico-chemical analysis of water

Physico-chemical parameters like temperature, salinity, dissolved oxygen and chlorophyll-a concentration were measured using YSI MDS 6600. Particulate and dissolved matter was separated by filtration, the water samples were filtered through a 0.45 μMmembrane filters. Nutrients such as phosphate, nitrate, nitrite and silicate were analyzed using spectrophotometry.

Analysis of zooplankton

The zooplanktons were observed and counted using sedgewick rafter cell under a microscope with 400 × magnification. It was identified to lowest possible taxa. Multivariate analysis of species composition and ecological data was done using CANOCO software. Multivariate analyses are more sensitive than univariate analyses at detecting changes in complicated biological and environmental factors. They are also exceedingly useful for analyzing differences between communities at spatial and temporal scales, and for illustrating how these communities vary along gradients of environmental conditions [9-16]. RDA was used to determine the relationships between the zooplankton and physico-chemical parameters. Redundancy analysis was done because the species exhibited a linear response to the environmental variables.

Mean temperature values in the bay in 2013 ranged from 25.29- 30.91°C, temperatures were highest in the months of May and July (Figure 2). The mean salinity values in the bay ranged from 14.83- 28.73 ppt. Salinity in the months of January, May, July and November showed almost the same spatio-temporal patterns, the concentrations were observed in the northwestern and eastern part of the bay while in March, concentration was observed in the eastern part of the bay (Figure 3).

Figure 2: Spatio-temporal variations in temperature.

Figure 3: temporal-salinity variations in salinity.

The highest DO concentration recorded was in recorded in Station 3 the month of March with a value of 9.54 mg/L and the lowest was recorded in station 10 in November with a value of 1.47 mg/L, mean concentrations in the bay ranged from 2.79-6.25 mg/L (Figure 4). The spatio-temporal patterns were shown to be uniform in in the months of January to May. The mean chl-a concentration ranged from 0.3619- 2.8546 μg/L (Figure 5). No data were obtained in the month of July.

Figure 4: Spatio-temporal variations in dissolved oxygen concentrations.

Phosphate concentrations with mean values ranged from 0.0135 to 0.2573 μM, of which the highest value was recorded in station 14 in September (0.7762 μM) (Figure 6), showed positive relationship with zooplankton abundance (Table 1). The average nitrate concentration in the bay ranged from 0.0265-8.3902 μM, the highest concentration was recorded in the month of November where it reached 22.6677 μM (Figure 7). Zooplankton was also abundant in the month of November, showing positive relationship with nitrate (Table 1).

Figure 5: Spatio-temporal variations in chlorophyll-a concentrations.

Figure 6: Spatio-temporal variations in phosphate concentrations.

Figure 7: Spatio-temporal variations in nitrate concentrations.

Table 1: (Summary of Monte Carlo test of significance).

The mean nitrite concentration of the bay ranged from 0.1385- 0.8396 μM. Maximum value was recorded in station 11 in November (Figure 8). Mean silicate concentration in the bay ranged from 5.4887- 53.2027 μM of which the maximum value was observed in station 10 (Figure 9). Both nitrite and silicate showed no significant relationship with the zooplankton abundance (Table 1).

Figure 8: Spatio-temporal variations in nitrite concentrations.

Figure 9: Spatio-temporal variations in silicate concentrations.

The summary of the species composition of zooplankton in Manila bay in 2013 is presented in Table 2. 29 genera excluding copepodites and copepod naupli which comprise the bulk of the zooplankton community, distributed to 7 phyla Arthropoda (14), Chordata (3), Ciliophora (3), Annelida (2), Mollusc (2), Echinoderm (2), Chaetognatha (1), Foraminifera (1), Sipunculida (1). Arthropods dominated the community making up 87% of the total population. Those that belong to the Ciliophora comprise the 6% of the population, Chaetognatha 3%and the other 4% was made up by the remaining phyla.

Table 2: Zooplankton composition and variation in the zooplankton abundance in Manila Bay from January-November 2013 (ind/m³).

The average abundance of arthropods consists mainly of copepods was 11497 ind/m³with copepod nauplii comprising the bulk of the population followed by calanids, Oithona sp. and Euterpina sp. The maximum abundance of arthropods mostly copepods was observed in the month of May, July and November (Figure 10) where the highest temperatures were also recorded.

Figure 10: Spatio-temporal variations in zooplankton abundance (ind/m³).

The mean abundance of the three genera, Codonellopsis sp., Favella sp., Tintinnopsis sp. recorded belonging to Phylum Ciliophora, was 397 ind/m³. Ciliates are most abundant in the month of July reaching 763 ind/m³. There are also three genera of chordates recorded during the survey with the mean abundance of 812 ind/m³ having Oikopleura sp. as the most abundant. A species of chaetognath also constitute to the zooplankton community making up the 3% of the total population (Table 1) with a mean abundance of 417 ind/m³.Polychaete and oligochaetelarvaes were also recorded and was found to be abundant in the months of July and September. Under the phylum Mollusca, gastropod and bivalve veliger were recorded and two genera were recorded under Echinodermata namely, Euchinopluteus sp.and Ophiopluteus sp. Globigerina sp. was observed under the phylum Foraminifera and was most abundant in the month of September and November.

Zooplanktonmean abundance in 2013 was 381 ind/m³ of which the highest density was recorded in the month of November (Figure 2) with a mean abundance of 483 ind/m³ followed by July (460 ind/m³) and May (447 ind/m³).

RDA ordination plot (Figure 11) revealed that most of the dominant zooplankton species tend to favor nutrient rich waters. Microsetella sp., Podon sp., and Oikopleura sp. favored warmer temperatures, as warmer waters were also recorded in July. Acartia sp., polychaete larvae, and copepod nauplii favored phosphate-rich waters as they dominated in the month of September. As much as the species prefer highly saline waters, they have managed to survive in an environment with low levels of salinity. The species Euterpina sp., calanids, and Oithona sp favored a nitrate rich environment as they clustered during November wherein the northern half of the bay exhibited high nitrate concentrations (Figure 7).

Figure 11: Redundancy Analysis Triplot of the top ten zooplankton species in Manila Bay with its environmental variables.

Coastal ecosystem is widely exposed to anthropogenic pollution sinceit receives inputs from terrestrial, littoral, marine and atmospheric sources. Urban development around coastal areas and consequent increase in the levels of anthropogenic contaminants from the catchment area cause serious water quality deterioration problems worldwide, particularly in Asian regions havinglarger populations and higher precipitation compared with other regions of the world [17].

In aquatic ecosystem, zooplankton play an important role as they themselves serve as a source of food for higher organisms. The composition and abundance of zooplankton are affected by the properties of water masses [18] like temperature and salinity.Twenty nine (29) genera of zooplankton were observed and recorded in Manila bay and was dominated by copepods during the survey from January to December 2013. Caethognath species was also recorded during the sampling period, despite the limited diversity of species, the number of individuals is large, larger than most of the zooplankton, their diet is consist mainly of copepods as it is shown in the study done by Canino and Grant (1984) in the lower Chesapeake Bay. The highest densities of zooplankton were recorded in the months of March, May, July and November (Figure 4) the highest concentrations of nitrate were also recorded in the months of July and November. The results was showed to be similar with Etilé et al. (2009) [2] who studied the spatiotemporal variations of zooplankton abundance in a tropical coastal lagoon that the copepods constituted the bulk of zooplankton during the dry season.This could be accounted to temperature and nutrients, because according to a study done by Wang et al in 2011[8] these two parameters play an important role in determining the biomass of zooplankton. Increase in nutrient in the bay would bring about an increase in the abundance of zooplankton in the bay. Temperature is one of the most important environmental factors which greatly affect biota of an ecosystem.[19] Water temperature ranging between 13.5 to 32°C is reported to be conducive for the growth of the planktonic organisms.[20] Results showed that the temperature in the bay is favourable for the survival of zooplankton.

Dissolved oxygen plays an important role in life processes in aquatic environment. [21] Dissolved oxygen concentrations in the bay ranged from 2.79-6.25 mg/Lmg/L (Figure 4) during the survey from January to December 2013. The lowest concentration of dissolved oxygen was recorded in November that reached 1.47 mg/L. Result showed that dissolved oxygen concentration in the bay is one of the deciding factors of the variation in the abundance of zooplankton (Table 1). Low dissolved oxygen concentration would bring about a decrease in the number of species thriving in the environment. Low dissolved oxygen can be attributed to eutrophication [22].

The significant positive correlation between zooplankton abundance and salinity in Manila Bay suggests that higher salinity in the bay would result to greater abundance of zooplankton in the bay. High values of salinity were recorded in the month of May where in station 2 it reached 30.37 ppt. At the same stations zooplankton abundance was also recorded higher as compared to the other stations of the same month. Salinity appeared as the major deciding factor for the composition and abundance of zooplankton in the bay. Ciliates was found in the stations with high salinity. Ciliates are heterotrophic and feed primarily on photosynthetic algae and bacteria [23] which are most commonly found in salt water [24-28].

There were 34 genera belonging to 7 phyla identified during the sampling from January-November 2013 in Manila Bay. The average zooplankton density ranged from³68-664 ind/m³. The zooplankton abundance was much higher in the months of July and November compared to the other sampling months this is due to the high temperature, salinity and nutrient concentrations which were also recorded the highest in the said months. The results indicated that zooplankton abundance has positive correlation with salinity, temperature, dissolved oxygen, phosphate, and nitrate. This would mean that changes in the environment would bring about a change in the zooplankton community.

The authors express their gratitude to National Fisheries Research And Development Institute for the facilities provided to carry out this research work. The authors would like to thank Dr. EphrimeMetillo, for his helpful discussions, Mr. James Dominic Vergara, Mr. Louie Adrianne Cedino, Ms Clarissa Gomez and Mr. Marvin Tobias for the at most help in the collection of samples and meaningful discussions.