Acta Manilana 63 (2015), pp. 51–60Printed in the PhilippinesISSN: 0065–1370

© 2015 UST Research Center for the Natural and Applied Sciences, Manila, Philippines

Phytoplankton community structure of Lake Paoayand Lake Mohicap with notes on the first record

of Ceratium (Dinophyta) in Lake Paoay

Kelsey Anne P. Sambitan2,3,4, Rey Donne S. Papa1,2,3, & Susana F. Baldia1,2,3*1Department of Biological Sciences, College of Science, 2Research Center for the Natural andApplied Sciences, & 3Graduate School, University of Santo Tomas, 1015 Manila, Philippines;

4Biological Sciences Department, College of Science and Computer StudiesDe La Salle University-Dasmariñas, Manila, Philippines

Phytoplankton are known to be biological indicators of changes in freshwater ecosystems.Hence, a study on the phytoplankton community structure revolving in their abundance andspecies composition which were then correlated with the abiotic factors was conducted inLake Paoay and Lake Mohicap — two Philippine lakes that are of contrasting limnologicalcharacteristics and geological origins. An updated phytoplankton taxonomy of the two lakesresulted to a total of 42 genera of phytoplankton for Lake Paoay and 49 genera for LakeMohicap wherein 17 genera are new records. Twelve genera were new records for LakePaoay including the dinoflagellate Ceratium which were in bloom during the cold dry seasonJanuary 2014 and had the highest density of 4.78105 cells mL–1. This occurrence was thenfollowed by a cyanobacterial bloom of Anabaena during the month of February with a densityof 1.46106 cells mL–1. Unusual blooms of Dinophyta and Cyanophyta might be attributed tothe increase in the nutrient content which indicates that Lake Paoay is already undergoingeutrophication. On the other hand, the blue green algae Chroococcus dominated Lake Mohicapwith the highest density in December and occurrences of dinoflagellates Glenodinium andPeridinium were noted. Based on the results of the study, it is evident that Lake Paoay andLake Mohicap, in spite of obvious differences in location, lake origin and physical characteristicsare undergoing similar conditions that result to phytoplankton blooms indicating increased nutrientlevels that may be attributed to human-mediated increases in nutrient inputs, such as aquacultureand increased inputs of domestic wastes.

Keywords: phytoplankton community, Lake Paoay, Lake Mohicap, Ceratium,eutrophication, dinoflagellates

*To whom correspondence should be addressedsfbaldia@yahoo.com

INTRODUCTION

Phytoplankton play a key role in supporting thefood chain of the entire aquatic ecosystem,contributing to primary productivity and servesas a link to biogeochemical changes. The

Phytoplankton community structure of Lake Paoay and Lake Mohicap

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area. Lake Paoay was also divided into foursampling sites. The sampling sites were basedon the previous researches done by the Bureauof Fisheries and Aquatic Resources in 1974followed by Papa et al. [8].

Collection of water samples. Sampling wasconducted from October 2013 to September2014. Phytoplankton were collected from theassigned sites between 1000 h and 1300 h usinga 3 L Plexi-glass water sampler that wasdeployed in three different depth layers – 0,15, and 30 m (Lake Mohicap) and 0, 3 and 6 m(Lake Paoay). Samples collected from thedifferent depth layers were fixed with Lugol’ssolution and stored in a 1-L tightly sealedbottles.

Phytoplankton analysis. For qualitative andquantitative analysis, aliquots of 1 mL weretaken from 10 mL sample after centrifugation,and were done in replicate samples. These werethen identified and counted using ahaemocytometer counting chamber [9] with theaid of a compound microscope. Data onphytoplankton density were presented in termsof cells/mL.).

Nutrient analysis and Chlorophyll adetermination. Water samples collected in thesame site with the phytoplankton water sampleswere transported in an ice cooler andimmediately stored at 0°C and were tested exsitu. NitraVer 5 nitrate reagent powder pillowsfor nitrate (mg/L) and PhospoVer amino acidreagent powder pillows for phosphate (mg/L),respectively, were analyzed through the HachDR/2010 portable data loggingspectrophotometer. Measurement ofChlorophyll a (mg/L) was analysed using themethods of Strickland and Parsons [10].

Measurement of physico-chemicalparameters. pH, and conductivity (S/m) weremeasured in situ using the Xplorer GLX(PASCO) water quality sensor. The probes were

submerged into the water, at least 5 cm from thesurface. Water transparency (m) was measuredusing a Secchi disc.

Statistical analysis. Multivariate statisticalmethods, such as non-metric multidimensionalscaling and cluster analysis, are standardanalytical tools which provide mechanisms tosummarize large amounts of community andenvironmental data [11].

RESULTS AND DISCUSSION

Phytoplankton densities and speciescomposition. A total of 42 genera wereidentified for Lake Paoay, with a total of 12new records of genera from the four phylaobserved (Table 1).

Four major algal phyla were found in LakePaoay: Cyanophyta, Chlorophyta,Bacillariophyta, and Dinophyta. Chlorophytahad the greatest number of genera of (16)followed by Bacillariophyta (15) andCyanophyta (11) (Table 1).

New genera of phytoplankton were observedfrom October 2013 to September 2014 in LakePaoay. A total of seven new genera forBacillariophyta, four Chlorophyta, twoCyanophyta and one Dinophyta were absent inthe studies done by Villaroman et al. [12] andStevenson et al. [13] in Lake Paoay.

No species from Euglenophyta were observedduring the sampling period as opposed to theprevious studies (water and sediments)conducted in Lake Paoay. This was becauseEuglenophyta prefer organic sources asnutrients rather than nitrate-nitrogen [12]. Inaddition, five genera of Bacillariophyta wereagain observed from the study of Stevenson etal. [13] although this was only observed fromthe sediments.

On the other hand, a total of 49 genera wereidentified in Lake Mohicap by which 17 are new

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records coming from five major algal phyla:Bacillariophyta, Chlorophyta, Cyanophyta,Dinophyta, and Euglenophyta (Table 2). Thesephyla were also observed by the Laguna LakeDevelopment Authority from their report in theyear 2005 with the exception of Euglenophyta.

Bacillariophyta had the greatest number ofgenera (19) followed by Chlorophyta (16),Cyanophyta (10) and both Dinophyta andEuglenophyta had two genera (Table 2). A totalof nine genera for Bacillariophyta, five forChlorophyta, one for Cyanophya, two for

Table 1. Updated listing of different phytoplankton genera in Lake Paoay

Bacillariophyta Cholorophyta Cynanophyta Dinophyta Achnanthes**** Coconeis****

Coscinodiscus**** Cyclotella* Cymbella*

Fragilaria** Gomphonema*** Gyrosigma****

Melosira** Navicula* Nitzschia*

Pinnularia**** Raphalodia****

Surirella**** Synedra**

Ankistrodesmus** Botryococcus**

Chlamydomonas**** Chlorella**

Closterium** Coelastrum**** Cosmarium** Eudorina**** Golenkinia*

Kirchneriella** Oedegonium****

Oocystis** Pediastrum**

Scenedesmus** Staurastrum** Tetraedron**

Anabaena** Chroococcus** Gloeocapsa** Lyngbya****

Merismopedia** Microcystis**

Marsonniella** Oscillatoria**

Synechococcus**** Synechocystis**

Ceratium****

****New record; ***Present in the study of Stevenson et al., 2010; **Present in the study of Villaroman et al., 2010; *Present in the previous two studies of Villaroman et al., 2010 and Stevenson et al., 2010

Table 2. Updated listing of different phytoplankton genera in Lake Mohicap

Bacillariophyta Chlorophyta Cyanophyta Dinophyta Euglenophyta Achnanthes**** Amphora**** Aulacoseira*

Coscinodiscus**** Cyclotella** Cymbella*** Fragilaria***

Gomphonema*** Gyrosigma**** Hantzschia****

Melosira*** Navicula** Nitzschia*

Pinnularia**** Placoneis****

Rhopalodia**** Stauroneis****

Surirella*** Synedra*

Ankistrodesmus* Asterococcus**** Botrycoccus***

Chlamydomonas**** Chlorella*

Chlorococcom**** Coelastrum*** Crucigenia**** Golenkenia**** Kirchneriella**

Oocystis*** Pediastrum*

Scenedesmus*** Schroederia*** Staurastrum*

Tetraedron***

Anabaena* Chroococcus*** Gleocapsa***

Gomphosphaeria*** Hapalosiphon****

Merismopedia* Microcystis***

Nostoc*** Oscillatoria*

Synechococcus***

Glenodinium**** Peridinium****

Cryptomonas**** Trachelomonas***

****New record; ***Present in the study Zafaralla 2014; **Present in the study of Cordero and Baldia, 2015; *Present both in the previous studies of Zafaralla, and Cordero and Baldia, 2015

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Dinophyta, and one Euglenophyta were absentin the studies of Cordero and Baldia, [14] andZafaralla [15].

Different phytoplankton phyla dominated thetwo lakes. In Lake Paoay, Chlorophytadominated while in Lake Mohicap, it wasBacillariophyta, specifically Nitzschia thatdominated the lake suggesting that LakeMohicap is now undergoing eutrophication.Species like Nitzschia palea, are found to betolerant of organic pollution to sewage effluenteffect at Lake Inlet [16]. In addition, Acnantheswas found in both lakes and for the first time, abloom of Ceratium sp. (Dinophyta) wasobserved in Lake Paoay.

The highest density of Bacillariophyta in LakeMohicap was observed during the wet monthof October and declined towards August of thefollowing year. A different scenario wasobserved in Lake Paoay, the low densities wereobserved from the months of October untilDecember and started increasing towards thesummer. The presence of Bacillariophyta isinversely proportional to the amount ofdissolved oxygen in both lakes. When there isan increase in Bacillariophyta, there is adecrease in dissolved oxygen and vice versa.

The highest phytoplankton density for LakePaoay (1.46106 cells mL–1) and Lake Mohicap(3.51106 cells mL–1) was from the membersof the Cyanophyta group. The highest densityof Cyanophyta in Lake Paoay peaked during themonth of February having a density of1.46106 cells mL–1, while the highest densityof Cyanophyta in Lake Mohicap was during themonths of October and December. Theincrease and decrease in the density can berelated to the water quality parameters. Also,the densities of Cyanophyta based on the data,would indicate that nitrates is inverselyproportional with the densities of this group.When there is an increase in the amount ofnitrates, there is a decrease in the species of

Cyanophyta and the other way around. Thismay be due to the specific genera ofCyanobacteria in the area that does notmetabolize nitrogen such as Chroococcus andMerismopedia.

A separate bloom of both Ceratium(4.78106 cells mL–1) and the cyanobacteriumAnabaena (1.46106 cells mL–1) was observedin the months of January and February,respectively. According to Mowe et al. [17]less than 7% of total blooms that occurred inthe tropical Asia were dominated byAnabaena.

The organisms’ tendency to cluster indicate thatthey “choose” places offering the bestconditions to live. For instance in LakeMohicap, cyanobacteria dominated the monthsof October and December with a density of3.5106 cells mL–1. In addition, somefreshwater dinoflagellates appeared in LakeMohicap but in low abundance such asPeridinium and Glenodinium but were onlyobserved during the wet to cold dry season andwere no longer seen during the summer season.

Seasonal cycles of temperature, solarirradiance and precipitation as well as otherdisturbances will lead to changes in agriculturalrunoff, mixing in lakes, nutrient supply andplankton growth. According to Villaroman etal. [12] Manifestation of complex organismssuch as Cyanophyta and Dinophyta occurs afterthe presence of Bacillariophyta whichhappened in Lake Paoay. The existence ofcertain phytoplankton genera like Cosmariumand Ceratium can be attributed to thecharacteristic feature of marine environmentwhich took place during the formation of LakePaoay, not to mention, that there are also othergenera which are evident in the marineecosystem. However, those genera found inLake Mohicap are naturally occurring in afreshwater environment with the exception ofsome genera from Bacillariophyta.

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First record of occurrence of Ceratium sp.(Dinophyta) in Lake Paoay. The presence ofCeratium in Lake Paoay was observed duringthe cool dry months of December 2013 untilFebruary 2014 and was no longer seen duringthe wet season. In the Atlantic and Pacificoceans, some species of Ceratium areprimarily found in colder water although it issometimes found in the tropics [18].

Ceratium consists of a large number ofspecies, many of which are very common andwidespread; they constitute a characteristic andoften dominant part of the plankton [18]. Thegenus Ceratium Schrank 1793 is the oldestgenus name of dinoflagellates in use. Thisgenus contained numerous (77) marine speciesand a few (7) freshwater species [19].Morphological and molecular data supportedthe split of the marine and freshwater speciesat the genus level [19].

On the basis of their distribution, Graham [20]classified Ceratium species as either tropical,subpolar or cosmopolitan. Most Ceratium aretropical in distribution [21]. Also, Ceratium arenormally found in water which is rich innutrients like phosphates and nitrates, and is

usually found in close association withCyanophyta [22]. Tunisi et al. [23] suggestedthat this occurrence is related to the intenseprocess of mixing which might have caused asharp increase in the phosphorus content in thewater column, hence, favoring the rapid bloomof this algae and exchange with cyanobacteria.Its unusual bloom had been recorded andconsidered an invasive species in severalstanding freshwater bodies of the world, suchas in Hartbeespoort Dam in South Africa [24],and in a large enclosure located in Lake Biwa,Japan [25]. Although they thrive in nutrient richenvironment, the studies of Graham andBronikovsky [18] indicated that phosphorusconcentration has no direct effect on thehorizontal distribution of Ceratium. They didfind that the relative phosphorus values in agiven region bear some relation to theCeratium flora but suggested that some factorassociated with an increase in phosphorus wassignificant rather than the phosphorus itself.Besides from nutrient availability, Ceratiumcan also be observed in a great range ofenvironmental condition such as temperature(6.1–28.2°C), and pH (7.80–8.37). Theseenvironmental conditions were observed inLake Paoay during its occurrence.

Figure 2. Venn diagram of phytoplankton genera of LakePaoay and Lake Mohicap

Figure 3. Total density of the different phytoplanktonphyla in Lake Paoay and Lake Mohicap (Legend: BA– Bacillariophyta; CL – Chlorophyta; CY –Cyanophyta; DI – Dinophyta; EU – Euglenophyta)

Kirchnierella Melosira Merismopedia

Paoay Phytoplankton

Shared Phytoplankton

Mohicap Phytoplankton

Ceratium

Costerium

Coconeis

Cosmarium

Eudorina

Lyngbya

Oedegonium

Synechocystis

Marsonniella

AmphoraAsteroccus

AulacoseiraChlorococcom

CrucigeniaCryptomonas

GlenodiumGomphosphaeria

HantzchiaHepalosiphon

NostocPeridium

PlaconeizSchroederia

StauroneisTrachelomonas

AchnanthesAnabaena

AnkistrodesmusBotryococcus

Chlamydomonas ChlorellaChroococcus CoelastrumCoscinodiscus Cyclotella

Cymbella Fragilaria GloeocapsaGolenkinia Gomphonema Gyrosigma

Microcystis Navicula NitzschiaOocystis Oscillatoria Pediastrum

Pinnularia RaphalodiaScenedesmus Staurastrum

Surirella SynechococcusSynedra

Tetraedron

2013 2014

500 –

400 –

300 –

200 –

100 –

0 –

Tota

l Den

sity

Oct Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep

A. Lake MohicapB. Lake Paoay

BACLCYDIEU

A

B

Phytoplankton community structure of Lake Paoay and Lake Mohicap

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Variations in physico-chemical parametersand its effect to the different phytoplanktoncommunities in Lake Paoay and LakeMohicap. Fluctuations in the differentenvironmental parameters affect thephytoplankton community structuresignificantly (Fig. 4). The pattern ofphytoplankton community and water quality areinterdependent [26].

There was no variation in pH for both lakes withthe highest pH notable in October and Augustin Lake Paoay (8.28) and Lake Mohicap(13.370), respectively. Such pH levels were stillwithin the common range for freshwater.

Conductivity started to increase in the monthof January until September with the highestvalue obtained in the month of March(524.045 S m–1) in Lake Mohicap. Meanwhile,the highest value in Lake Paoay was observedin the months of January and April whichcoincided with the appearance of Ceratium andAnabaena blooms in Lake Paoay. Ceratiumspecies are known to be classical inhabitantsof mineralized waters with high conductivity[27].

Since Lake Paoay is surrounded by crop fields,nutrient inputs may come from agriculturalrunoff and from the fish pens in the area. The

immediate massive inputs of these nutrientshad led to Ceratium and Anabaena blooms.These blooms were attributed to suddenchanges in vertical stability, depletion ofnutrients and alterations in the underwater lightclimate.

According to Gillbricht [28], the increase innutrients resulted in the species shift fromdiatoms to dinoflagellates. A fairly highnutrient inputs of nitrogen and phosphorus werefound during the formation of Ceratium bloomin January with 7.94 mg L–1 and 0.82 mg L–1,respectively. An inverse result was found whenthe cyanobacterium Anabaena appeared inFebruary with a decrease in phosphate whilenitrates slightly increased.

Ceratium can develop high densities andbiomasses from mesotrophic to eutrophiclakes which are rich in organic matter as organicnitrogen. This is one reason, why they cancompete for dominance with cyanobacterialbloom; they can even precede their bloom,more often follow them, and hardly ever co-dominate with them [29]. Olrik [30] stated thatthe species of Ceratium often bloom in lakeswith strong thermal stability. Chlorophyll acoincided with the occurrence of Ceratium andthe cyanobacterium Anabaena, with an increaseof Chlorophyll a of 0.085 mg L–1 and 0.147 mg

Figure 4. Non-metric multidimensional scaling of LakePaoay and Lake Mohicap (Legend: PS – Paoay Site;MS – Mohicap Site; CO – Conductivity; TRANS –Transparency; pH – pH; PO3 – Phosphates; NO3 –Nitrates; CL-a – Chlorophyll a)

Figure 5. Hierarchical cluster analysis of Lake Paoay andLake Mohicap (Legend: PS – Paoay Site; MS –Mohicap Site)

40 –80 –

120 –160 –200 –240 –280 –320 –360 –400 –

PS4

Dist

ance

PS2PS1PS3MS3MS4 MS2MS1

0.24 –

0.18 –

0.12 –

0.06 –

0.00 –

–0.06 –

–0.12 –

–0.18 –

–0.24 –

–0.30 ––0.80

PS4

PO3COTRANSMS1

MS2MS4MS3

PS3PS2

Cl-a pH

NO3PS1

–0.64 –0.48 –0.32 –0.16 0.00 0.16 0.32 0.48

Sambitan KAP, Papa RDS, & Baldia SFActa Manilana 63 (2015)

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L–1 obtained in January and February,respectively.

The highest amount of Chlorophyll a for LakesPaoay and Mohicap were observed during themonth of June which is 0.284 mg L–1 and0.099 mg L–1. The amount of nitrates andphosphates in Lake Paoay peaked during the wetseason, which can be due to the runoff offertilizers from agricultural areas during therainy months. The amount of nitrates isobserved to be inversely proportional to certainphytoplankton species such as the Cyanophyta.In Lake Mohicap, the amount of phosphates andnitrates occurred differently. During the wetmonths, nitrates were at their lowest andincreased towards summer while phosphateshad the highest peaked but decreased towardsthe summer. The parameters used were able toshow the differences between Lake Paoay andLake Mohicap, that although both of them arelocated in a tropical country, several factorscan affect the succession of organisms andtrophic status of the lakes.

Comparative analysis of the different sitesof Lake Paoay and Lake Mohicap. Therelationships between environmentalparameters and phytoplankton groups for thedifferent sites of Lake Paoay and Lake Mohicapwere analysed using the non-metricmultidimensional scaling and cluster analysisin PAST. Figure 4 and Fig. 5 imply that theamount of nitrates and environmentalparameters such as pH, Chlorophyll a, in LakePaoay sites 2 and 3 were increasing while forPaoay site 4, the conductivity and transparencywere decreasing and is not affected by thementioned parameters in sites 2 and 3. Paoaysite 1 as shown in Fig. 4, was not affected byany parameters used in the study and has otherfactors which were affecting it.

The presence of four groups of phytoplanktonwere affected individually by differentparameters and can be seen to dominate a

specific site. This is true in the case ofDinophyta, its highest density was observed inPaoay site 1 and was not much affected by theparameters used. One factor which might haveaffected it was the season as it only occurredduring the dry cold season. Cyanophyta wasobserved all throughout the lake but in a varietyof density. Its relationship is closer to thedecrease in turbidity rather than increase innitrates although Cyanophyta are known to fixnitrogen compounds. One main reason was thegenera that occurred, the lake was dominatedby colonial genera like Chroococcus rather thanfilamentous blue-green algae. Its highestdensity occurred in site 4 where the amount ofphosphates is high in contrast with the othersites. Cyanophyta are known to have highstorage capacity for phosphorus as well as highmaximum rate of phosphorus uptake [5].Bacillariophyta and Chlorophyta were observedin nearly equal densities although higherdensities were in site 3 and were affected bythe different parameters. Euglenophyta was notobserved in Lake Paoay since environmentalvariables were not favorable for its growth.

Sites in Lake Mohicap were more affected bythe decreasing conductivity and transparency.High variation in the different environmentalparameters were not observed as they occur inalmost equal amounts (Fig. 5). Thisphenomenon might be attributed to the smallersurface area (22.89 ha) of Lake Mohicap incontrast to the bigger surface area (440 ha) ofLake Paoay. Another factor that might havecaused this equal measurements of parametersis the difference of shapes of the two lakes.Lake Paoay has an irregular shape while LakeMohicap is round.

Amount of phosphates were higher in LakeMohicap in contrast with Lake Paoay sincephosphorus can enter the lake from manysources like rain runoff, agricultural nonpointsources, fertilizers applied to crops, bird andanimal waste, plant debris, and detergents [31].

Phytoplankton community structure of Lake Paoay and Lake Mohicap

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This is true for Lake Mohicap since it is beingdomesticated by people living near the area andis enclosed in one barangay unlike with the caseof Lake Paoay wherein there is a variety ofnutrient entry coming from four barangays.Cyanophyta had the highest density and this wasdue to the higher amount of phosphates in LakeMohicap which also caused the transparencyto decrease due to the abundance of colonyformations. Low nitrogen and high phosphorusconditions often favor cyanobacteria in freshand saltwater systems [32] especially forcolonial genera such as Microcystis andChroococcus.

CONCLUSION

The abundance and distribution ofphytoplankton community structure werecarried out in Lake Paoay and Lake Mohicap.The results showed that a new record ofCeratium species for the first time was co-inhabiting with the other algal groups in LakePaoay. Cyanophyta was the most dominantamong all algal groups in Lake Mohicap interms of density and was dominated byBacillariophyta in terms of diversity.Occurrence of Peridinium and Glenodiniumin low densities had also been noted. Unusualoccurrences of specific genera from differentphyla can be attributed to the different changesthat the two lakes are undergoing. Such factorsthat affect their presence are seasonality, andnutrient enrichment. There is still a need forcontinuous lake monitoring since there wereunusual occurrences of other algal species inboth lakes. There had been changes among theenvironmental variables in both lakes. Futureresearch should be focused on the abundanceand composition of these freshwaterdinoflagellates in both lakes as these can beindicators on rapid changes in lakes.

ACKNOWLEDGMENTS

The authors would like to thank Kenoses L.Legaspi, Lawrence Victor D. Vitug for their

assistance during field collection andpreliminary analyses. This research was fundedby the Commission on Higher Education-Philippine Higher Education and ResearchNetwork (CHED-PHERNet) grant to SFB andRDSP (Project A2).

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