https://doi.org/10.4081/jlimnol.2022.2070
Identification of aquatic consumer trophic pathways in four volcanic tropical lakes using fatty acid biomarkers
Submitted: 2 February 2022
Accepted: 4 July 2022
Published: 19 July 2022
Accepted: 4 July 2022
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All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.
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Food web studies rely heavily on the use of traditional gut content analysis or the fairly popular stable isotope analysis rather than fatty acid analysis (FAA) despite its straightforward process, and ability to identify and characterize more diverse trophic pathways. In this study, we employed fatty acid (FA) biomarkers as a preliminary attempt to trace and characterize trophic pathways in food webs of four tropical lakes of volcanic origin in Luzon Island, Philippines - three clustered maar lakes (Yambo, Pandin and Calibato) and a large caldera lake (Taal). These lakes have a long history of human disturbance but limited ecological data. Knowledge of basal food sources and existing trophic dynamics of organisms are generally non-existent. Particulate organic matter (POM), zooplankton, and fish species were collected in August 2019 from the study lakes as representative of three trophic guilds. Non-metric multidimensional scaling (NMDS) and principal component analysis (PCA) were conducted to analyse FA profiles and characterize trophic relationships between representative organisms. For the POM, within lakes comparison of taxon-specific FA profiles showed a significant difference between the surface and near bottom depths, with the former dominated by photoautorophs and the latter by chemotrophs, suggesting the ability of FAA to effectively delineate between micro-organisms. Between lakes comparison also showed significant difference between the caldera and maar lakes, with the latter containing higher composition of bacterial FA, reminiscent of the considerably smaller lakes’ response to the impact of unmitigated organic loadings from anthropogenic activities. Taken together with the primary consumers’ FA profiles, analysis confirmed the ability of FAA to discriminate between FA profile sources. PCA explained >70% of the variance in the FA compositions for three trophic guilds in the two deepest lakes, which delineated both zooplankton and fish species food selectivity in each lake, alluding to FAA’s capacity to characterize dietary reliance of various species in an environment with numerous food sources. Although certain limitations were encountered, such as the specificity of the sampling depths for POM, and the small sample size of the representative species of the third trophic level, this study demonstrated the effectiveness of FAA as a powerful ecological tool for disentangling intricate lake food webs comprising various food sources. Overall, this study provided baseline information on basal food sources and trophic pathways of representative organisms from four tropical lakes. Taken together, FAA studies have wide application in understanding food webs, including anthropogenically-threatened lake ecosystems.
Abdulkadir S, Tsuchiya M, 2008. One-step method for quantitative and qualitative analysis of fatty acids in marine animal samples. J Exp Mar Biol Ecol 354:1–8.
DOI: https://doi.org/10.1016/j.jembe.2007.08.024
Alfaro AC, Thomas F, Sergent L, Duxbury M, 2006. Identification of trophic interactions within an estuarine food web (northern New Zealand) using fatty acid biomarkers and stable isotopes. Estuar Coast Shelf Sci 70:271–286.
DOI: https://doi.org/10.1016/j.ecss.2006.06.017
Ander BP, Dupasquier CM, Prociuk MA, Pierce GN, 2003. Polyunsaturated fatty acids and their effects on cardiovascular disease. Exp Clin Cardiol 8:164.
Ariyaratne TMG, Amarasinghe PB, Lopez NC, Kakkaeo M, Vijverberg J, 2008. Selective feeding of small zooplanktivorous pelagic fish species in tropical Asian reservoirs (Sri Lanka, Thailand) and Lake Taal (Philippines), p. 235-248. In: F. Schiemer and B. Tokarska-Guzik (eds.), Aquatic ecosystems and development: comparative Asian perspectives. Leiden, Backhuys Publ.
Bastviken D, Cole J, Pace M, Tranvik L, 2004. Methane emissions from lakes: Dependence of lake characteristics, two regional assessments, and a global estimate. Global Biogeochem Cycles 18:GB4009.
DOI: https://doi.org/10.1029/2004GB002238
Beveridge MCM, Baird DJ, Rahmatullah SM, Lawton LA, Beattie KA, Codd GA, 1993. Grazing rates on toxic and non‐toxic strains of cyanobacteria by Hypophthalmichthys molitrix and Oreochromis niloticus. J Fish Biol 43:901–907.
DOI: https://doi.org/10.1111/j.1095-8649.1993.tb01164.x
Bowman JP, Sly LI, Nichols PD, Hayward AC, 1994. Revised taxonomy of the methanotrophs: Description of Methylobacter gen. nov., emendation of Methylococcus, validation of Methylosinus and Methylocystis species, and a proposal that the family Methylococcaceae includes only the group I methanotrophs. Int J Syst Evol 44:375.
DOI: https://doi.org/10.1099/00207713-44-2-375
Burns CW, Brett MT, Schallenberg M, 2011. A comparison of the trophic transfer of fatty acids in freshwater plankton by cladocerans and calanoid copepods. Freshwater Biol 56:889-903.
DOI: https://doi.org/10.1111/j.1365-2427.2010.02534.x
Brett MT, Müller-Navarra DC, Persson J, 2009. Crustacean zooplankton fatty acid composition, p. 115-146. In: M. Kainz, M.T. Brett, M.T. Arts (eds.), Lipids in aquatic ecosystems. New York, Springer.
DOI: https://doi.org/10.1007/978-0-387-89366-2_6
Brillo BBC, 2016a. An assessment of development of a transboundary small lake: Calibato lake, San Pablo City and Rizal, Laguna, the Philippines. Asian J Water, Environ Pollut. 13:55–67.
DOI: https://doi.org/10.3233/AJW-160017
Brillo BBC, 2016b. Development of a small lake: Ecotourism enterprise for Pandin lake, San Pablo City, Philippines. Lake Reserv Manag 21:284–292.
DOI: https://doi.org/10.1111/lre.12150
Briones JCA, Papa RDS, Cauyan GA, Mendoza N, Okuda N, 2016. Fish diversity and trophic interactions in Lake Sampaloc (Luzon Is., Philippines). Trop Ecol 57:567–581.
Carpenter SR, Cole JJ, Pace ML, Van de Bogert M, Bade DL, Bastviken D, Gille CM, Hodgson JR, Kitchell JF, Kritzberg ES, 2005. Ecosystem subsidies: terrestrial support of aquatic food webs from 13C addition to contrasting lakes. Ecology 86:2737–2750.
DOI: https://doi.org/10.1890/04-1282
Cisneros R, Hooker E, Velasquez LE, 1991. Natural diet of herbivorous zooplankton in Lake Xolotlán (Managua). Hydrobio Bull 25:163–167.
DOI: https://doi.org/10.1007/BF02291249
Corpuz MNC, Paller VG, Ocampo P, 2016. Diversity and distribution of freshwater fish assemblages in Lake Taal river systems in Batangas, Philippines. J Environ Manage 19:85–95.
DOI: https://doi.org/10.47125/jesam/2016_1/09
Coveney MF, Wetzel RG, 1992. Effects of nutrients on specific growth rate of bacterioplankton in oligotrophic lake water cultures. Appl Environ Microbiol 58:150–156.
DOI: https://doi.org/10.1128/aem.58.1.150-156.1992
Dalsgaard J, John MS, Kattner G, Müller-Navarra D, Hagen W, 2003. Fatty acid trophic markers in the pelagic marine environment. Adv Mar Biol 46:225–340.
DOI: https://doi.org/10.1016/S0065-2881(03)46005-7
De Leon KJA, Manliclic ADC, Corpuz MNC, 2017. Spatial and sexual variation on morphometrics, length and weight, and condition factor dynamics of endemic silver therapon (Leiopotherapon plumbeus, Kner). J Agric Sci Technol 13:1567–1577.
De Leon JR, Guinto SK, Tordesillas DT, Papa RDS, 2020. Depth and productivity as predictive parameters for the widespread invasion of Arctodiaptomus dorsalis (Marsh, 1907) (Copepoda: Calanoida) in tropical lakes in the Philippines. J Crust Biol 40:512–519.
DOI: https://doi.org/10.1093/jcbiol/ruaa052
Deines P, Fink P, 2011. The potential of methanotrophic bacteria to compensate for food quantity or food quality limitations in Daphnia. Aquat Microb Ecol 65:197–206.
DOI: https://doi.org/10.3354/ame01542
Delmendo MN, 1968. Food and feeding habits of the economic species of fish in Laguna de Bay. IPFC 12th Session Technical Paper 40. Philipp J Fish 14:213–231.
Dempster PW, Beveridge MCM, Baird DJ, 1993. Herbivory in the tilapia Oreochromis niloticus: a comparison of feeding rates on phytoplankton and periphyton. J Fish Biol 43:385–392.
DOI: https://doi.org/10.1111/j.1095-8649.1993.tb00573.x
Dumestre JF, Casamayor EO, Massana R, Pedrós-Alió C, 2001. Changes in bacterial and archaeal assemblages in an equatorial river induced by the water eutrophication of Petit Saut dam reservoir (French Guiana). Aquat Microb Ecol 26:209–221.
DOI: https://doi.org/10.3354/ame026209
Dumestre JF, Guézennec J, Galy-Lacaux C, Delmas R, Richard S, Labroue L, 1999. Influence of light intensity on methanotrophic bacterial activity in Petit Saut Reservoir, French Guiana. Appl Environ Microbiol 65:534–539.
DOI: https://doi.org/10.1128/AEM.65.2.534-539.1999
Eller G, Deines P, Grey J, Richnow HH, Krüger M, 2005. Methane cycling in lake sediments and its influence on chironomid larval δ13C. FEMS Microbiol Ecol 54:339–350.
DOI: https://doi.org/10.1016/j.femsec.2005.04.006
Falkowski PG, 1994. The role of phytoplankton photosynthesis in global biogeochemical cycles. Photosynth Res 39:235–258.
DOI: https://doi.org/10.1007/BF00014586
Farjalla VF, Marinho CC, Faria BM, Amado AM, Esteves FDA, Bozelli RL, Giroldo D, 2009. Synergy of fresh and accumulated organic matter to bacterial growth. Microb Ecol 57:657–666.
DOI: https://doi.org/10.1007/s00248-008-9466-8
France RL, 1995. Differentiation between littoral and pelagic food webs in lakes using stable carbon isotopes. Limnol Oceanogr 40:1310–1313.
DOI: https://doi.org/10.4319/lo.1995.40.7.1310
Freitas R, Vieita HH, de Moraes GP, de Melo ML, Vieira AAH, Sarmento H, 2017. Productivity and rainfall drive bacterial metabolism in tropical cascading reservoirs. Hydrobiologia 809:233–246.
DOI: https://doi.org/10.1007/s10750-017-3472-0
Fujibayashi M, Miura Y, Suganuma R, Takahashi S, Sakamaki T, Miyata N, Kazama S, 2019. Origin of carbon and essential fatty acids in higher trophic level fish in headwater stream food webs. Biomolecules 9:487.
DOI: https://doi.org/10.3390/biom9090487
Fujibayashi M, Okano K, Takada Y, Mizutani H, Uchida N, Nishimura O, Miyata N, 2018. Transfer of cyanobacterial carbon to a higher trophic-level fish community in a eutrophic lake food web: Fatty acid and stable isotope analyses. Oecologia 188:901–912.
DOI: https://doi.org/10.1007/s00442-018-4257-5
Getachew T, Fernando CH, 1989. The food habits of an herbivorous fish (Oreochromis niloticus Linn.) in Lake Awasa, Ethiopia. Hydrobiologia 174:195–200.
DOI: https://doi.org/10.1007/BF00008157
Ghashghavi M, Belova SE, Bodelier PLE, Dedysh SN, Kox MAR, Speth DR, Frenzel P, Jetten MSM, Lucker S, Luke C, 2019. Methylotetracoccus oryzae strain C50C1 is a novel type Ib gammaproteobacterial methanotroph adapted to freshwater environments. Msphere 4:e00631-18.
DOI: https://doi.org/10.1128/mSphere.00631-18
Hanson RS, Hanson TE, 1996. Methanotrophic bacteria. Microbiol Rev 60:439–471.
DOI: https://doi.org/10.1128/mr.60.2.439-471.1996
Hartwich M, Martin-Creuzburg D, Wacker A, 2013. Seasonal changes in the accumulation of polyunsaturated fatty acids in zooplankton. J Plankton Res 35:121–134.
DOI: https://doi.org/10.1093/plankt/fbs078
Ho PC, Okuda N, Miki T, Itoh M, Shiah FK, Chang CW, Hsiao SS, Kao SJ, Fujibayashi M, Hsieh CH, 2016. Summer profundal hypoxia determines the coupling of methanotrophic production and the pelagic food web in a subtropical reservoir. Freshwater Biol 61:1694–1706.
DOI: https://doi.org/10.1111/fwb.12809
Itoh M, Kojima H, Ho PC, Chang CW, Chen TY, Hsiao SSY, Kobayashi Y, Fujibayashi M, Kao SJ, Hsieh CH, Fukui M, Okuda N, Miki T, Shiah FK, 2017. Integrating isotopic, microbial, and modeling approaches to understand methane dynamics in a frequently disturbed deep reservoir in Taiwan. Ecol Res 32:861–871.
DOI: https://doi.org/10.1007/s11284-017-1502-z
Jansson M, Bergström AK, Lymer D, Vrede K, Karlsson J, 2006. Bacterioplankton growth and nutrient use efficiencies under variable organic carbon and inorganic phosphorus ratios. Microb Ecol 52:358–364.
DOI: https://doi.org/10.1007/s00248-006-9013-4
Jones RI, Carter CE, Kelly A, Ward S, Kelly DJ, Grey J, 2008. Widespread contribution of methane‐cycle bacteria to the diets of lake profundal chironomid larvae. Ecology 89:857–864.
DOI: https://doi.org/10.1890/06-2010.1
Jones RI, Grey J, 2011. Biogenic methane in freshwater food webs. Freshwater Biol 56:213–229.
DOI: https://doi.org/10.1111/j.1365-2427.2010.02494.x
Kankaala P, Taipale S, Li L, Jones RI, 2010. Diets of crustacean zooplankton, inferred from stable carbon and nitrogen isotope analyses, in lakes with varying allochthonous dissolved organic carbon content. Aquatic Ecol 44:781–795.
DOI: https://doi.org/10.1007/s10452-010-9316-x
Kenyon CN, 1972. Fatty acid composition of unicellular strains of blue-green algae. J Bacteriol 109:827–834.
DOI: https://doi.org/10.1128/jb.109.2.827-834.1972
Kobayashi Y, Kojima H, Itoh M, Okuda N, Fukui M, Shiah FK. 2016. Abundance of planktonic methane-oxidizing bacteria in a subtropical reservoir. Plankton Benthos Res 11:144–146.
DOI: https://doi.org/10.3800/pbr.11.144
Kock M, Focken U, Richter H, Becker K, Santiago CB, 2000. Feeding ecology of silverperch, Terapon plumbeus Kner, and the impact of fish‐pens in Laguna de Bay, Philippines. J Appl Ichthyol 16:240–246.
DOI: https://doi.org/10.1046/j.1439-0426.2000.00240.x
Kurt H, 2019. Depth distribution of microbial diversity in lakes, p. 225-262. In: S. Bandh (ed.), Freshwater microbiology: Perspectives of bacterial dynamics in lake ecosystems. Cambridge, Academic Press.
DOI: https://doi.org/10.1016/B978-0-12-817495-1.00006-2
Lau DC, Vrede T, Pickova J, Goedkoop W, 2012. Fatty acid composition of consumers in boreal lakes–variation across species, space and time. Freshwater Biol 57:24–38.
DOI: https://doi.org/10.1111/j.1365-2427.2011.02690.x
Lew S, Glińska-Lewczuk K, 2018. Environmental controls on the abundance of methanotrophs and methanogens in peat bog lakes. Sci Total Environ 645:1201–1211.
DOI: https://doi.org/10.1016/j.scitotenv.2018.07.141
Laguna Lake Development Authority. 2008. Water Quality Report of the Seven Crater Lakes (2006-2008).
Mancuso CA, Franzmann PD, Burton HR, Nichols PD, 1990. Microbial community structure and biomass estimates of a methanogenic Antarctic Lake ecosystem as determined by phospholipid analyses. Microb Ecol 19:73–95.
DOI: https://doi.org/10.1007/BF02015055
Martin TJ, Blaber SJM, 1984. Morphology and histology of the alimentary tracts of Ambassidae (Cuvier) (Teleostei) in relation to feeding. J Morphol 182:295–305.
DOI: https://doi.org/10.1002/jmor.1051820305
Mendoza MU, Briones JCA, Itoh M, Padilla KSAR, Aguilar JI, Okuda N, Papa RDS, 2019a. Small maar lakes of Luzon Island, Philippines: their limnological status and implications on the management of tropical lakes–a review. Philipp J Sci 148:565–578.
Mendoza MU, Dur G, Rosana MR, Santos M, Mutia T, Kawit NS, Ite MO, Villanueva LS, Souissi S, Papa RDS, 2019b. Water quality and weather trends preceding fish kill occurrences in Lake Taal (Luzon Is., Philippines) and recommendations on its long-term monitoring. Philipp Sci Lett 12:147–156.
Mendoza MU, Legaspi K, Acojido M, Cabais A, de Guzman JL, Favila A, Lazo S, Rivera J, Briones JCA, Papa RDS, 2015. Dietary habits and distribution of some fish species in the Pansipit River-Lake Taal Connection, Luzon Island, Philippines. J Environ Sci Manage 18:1–9.
DOI: https://doi.org/10.47125/jesam/2015_2/01
Mendoza‐Pascual MU, Itoh M, Aguilar JI, Padilla KSAR, Papa RDS, Okuda N, 2021. Controlling factors of methane in tropical lakes of different depths. J Geophys Res 126:e2020JG005828.
DOI: https://doi.org/10.1029/2020JG005828
Mercurio AL, Querijero BL, Ching JA, 2016. Phytoplankton community in aquaculture and non-aquaculture sites of Taal Lake, Batangas, Philippines. J Exp Biol Agric Sci 4 66–73.
DOI: https://doi.org/10.18006/2016.4(1).66.73
Murase J, Sugimoto A, 2005. Inhibitory effect of light on methane oxidation in the pelagic water column of a mesotrophic lake (Lake Biwa, Japan). Limnol Oceanogr 50:1339–1343.
DOI: https://doi.org/10.4319/lo.2005.50.4.1339
Nakano SI, Ishii N, Manage PM, Kawabata Z, 1998. Trophic roles of heterotrophic nanoflagellates and ciliates among planktonic organisms in a hypereutrophic pond. Aquat Microb Ecol 16:153–161.
DOI: https://doi.org/10.3354/ame016153
Nakano SI, Manage PM, Nishibe Y, Kawabata Z, 2001. Trophic linkage among heterotrophic nanoflagellates, ciliates and metazoan zooplankton in a hypereutrophic pond. Aquat Microb Ecol 25:259–270.
DOI: https://doi.org/10.3354/ame025259
Napolitano GE. 1999. Fatty acids as trophic and chemical markers in freshwater ecosystems, p. 21–44. In: M.T. Arts, B.C. Wainman (eds.), Lipids in freshwater ecosystems. New York, Springer.
DOI: https://doi.org/10.1007/978-1-4612-0547-0_3
Newton RJ, Jones SE, Eiler A, McMahon KD, Bertilsson S, 2011. A guide to the natural history of freshwater lake bacteria. Microbiol Mol Biol Rev 75:14-49.
DOI: https://doi.org/10.1128/MMBR.00028-10
Njiru M, Okeyo‐Owuor JB, Muchiri M, Cowx IG, 2004. Shifts in the food of Nile tilapia, Oreochromis niloticus (L.) in Lake Victoria, Kenya. African J Ecol 42:163-170.
DOI: https://doi.org/10.1111/j.1365-2028.2004.00503.x
Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O'Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H, 2020. vegan: Community Ecology Package. R package version. 2.5-7. Available from: https://CRAN.R-project.org/package=vegan
Pace ML, Cole JJ, Carpenter SR, Kitchell JF, Hodgson JR, Van de Bogert MC, Bade DL, Kritzberg ES, Bastviken D, 2004. Whole-lake carbon-13 additions reveal terrestrial support of aquatic food webs. Nature 427:240–243.
DOI: https://doi.org/10.1038/nature02227
Papa RDS, Briones JCA, 2017. The history of freshwater research in the Philippines with notes on its origins in the University of Santo Tomas and present-day contributions. Philipp J Syst Biol 11:16–28.
DOI: https://doi.org/10.26757/pjsb.2017a11002
Papa RDS, Li H, Tordesillas DT, Han B, Dumont HJ, 2012. Massive invasion of Arctodiaptomus dorsalis (Copepoda, Calanoida, Diaptomidae) in Philippine lakes: a threat to Asian zooplankton biodiversity? Biol Invasions 14:2471-2478.
DOI: https://doi.org/10.1007/s10530-012-0250-9
Papa RDS, Mamaril Sr AC, 2011. History of the biodiversity and limno-ecological studies on Lake Taal with notes on the current state of Philippine limnology. Philipp Sci Lett 4:1-10.
Papa RDS, Pagulayan RC, Pagulayan AEJ, 2008. Zooplanktivory in the endemic freshwater sardine, Sardinella tawilis (Herre 1927) of Taal Lake, the Philippines. Zool Stud 47:535-543.
Persson J, Vrede T, 2006. Polyunsaturated fatty acids in zooplankton: variation due to taxonomy and trophic position. Freshwater Biol 51:887-900.
DOI: https://doi.org/10.1111/j.1365-2427.2006.01540.x
Quilang JP, Basiao ZU, Pagulayan RC, Roderos RR, Barrios EB, 2007. Meristic and morphometric variation in the silver perch, Leiopotherapon plumbeus (Kner, 1864), from three lakes in the Philippines. J Appl Ichthyol 23:561-567.
DOI: https://doi.org/10.1111/j.1439-0426.2007.00862.x
Sanseverino AM, Bastviken D, Sundh I, Pickova J, Enrich-Prast A, 2012. Methane carbon supports aquatic food webs to the fish level. PloS One 7:e42723.
DOI: https://doi.org/10.1371/journal.pone.0042723
Schubert CJ, Lucas FS, Durisch-Kaiser E, Stierli R, Diem T, Scheidegger O, Vazquez F, Müller B, 2010. Oxidation and emission of methane in a monomictic lake (Rotsee, Switzerland). Aquat Sci 72:455–466.
DOI: https://doi.org/10.1007/s00027-010-0148-5
Simopoulos AP, 2002. The importance of the ratio of omega-6/omega-3 essential fatty acids. Biomed Pharmacother 56:365–379.
DOI: https://doi.org/10.1016/S0753-3322(02)00253-6
Sundh I, Bastviken D, Tranvik LJ, 2005. Abundance, activity, and community structure of pelagic methane-oxidizing bacteria in temperate lakes. Appl Environ Microbiol 71:6746–6752.
DOI: https://doi.org/10.1128/AEM.71.11.6746-6752.2005
Taipale S, Kankaala P, Jones RI, 2007. Contributions of different organic carbon sources to Daphnia in the pelagic foodweb of a small polyhumic lake: results from mesocosm DI 13 C-additions. Ecosystems 10:757–772.
DOI: https://doi.org/10.1007/s10021-007-9056-5
Thompson PA, Harrison PJ, Whyte JN, 1990. Influence of irradiance on the fatty acid composition of phytoplankton 1. J Phycol 26:278–288.
DOI: https://doi.org/10.1111/j.0022-3646.1990.00278.x
Torres-Ruiz M, Wehr JD, Perrone AA, 2007. Trophic relations in a stream food web: importance of fatty acids for macroinvertebrate consumers. J N Am Benthol Soc 26:509–522.
DOI: https://doi.org/10.1899/06-070.1
Traugott M, Kamenova S, Ruess L, Seeber J, Plantegenest M, 2013. Empirically characterising trophic networks: what emerging DNA-based methods, stable isotope and fatty acid analyses can offer, p. 177–224. In: G. Woodward, D.A. Bohan (eds.), Advances in ecological research. Cambridge, Academic Press.
DOI: https://doi.org/10.1016/B978-0-12-420002-9.00003-2
R Core Team, 2013. R: A language and environment for statistical computing. Vienna, R Foundation for Statistical Computing.
Rahalkar M, Deutzmann J, Schink B, Bussmann I, 2009. Abundance and activity of methanotrophic bacteria in littoral and profundal sediments of Lake Constance (Germany). Appl Environ Microbiol 75:119–126.
DOI: https://doi.org/10.1128/AEM.01350-08
Raven JA, Maberly SC, 2009. Phytoplankton nutrition and related mixotrophy, p. 192-196. In: G.E. Likens (ed.), Encyclopedia of inland waters. Amsterdam, Elsevier.
DOI: https://doi.org/10.1016/B978-012370626-3.00138-1
Ravet JL, Brett MT, Arhonditsis GB, 2010. The effects of seston lipids on zooplankton fatty acid composition in Lake Washington, Washington, USA. Ecology 91:180–190.
DOI: https://doi.org/10.1890/08-2037.1
Rissanen AJ, Saarenheimo J, Tiirola M, Peura S, Aalto SL, Karvinen A, Nykänen H, 2018. Gammaproteobacterial methanotrophs dominate methanotrophy in aerobic and anaerobic layers of boreal lake waters. Aquat Microb Ecol 81:257–276.
DOI: https://doi.org/10.3354/ame01874
Rott E, Silva EIL, Enriquez EE, Ingthamjitr S, 2008. Phytoplankton community structure with special reference to species diversity in five tropical Asian water bodies, p. 81–120. In: F. Schiemer, B. Tokarska-Guzik (eds.), Aquatic ecosystems and development: Comparative Asian perspectives. Weikersheim, Margaf & Backhuys Publishers.
Rumisha C, Nehemia A, 2013. Feeding selectivity of wild and pond-cultured Nile tilapia Oreochromis niloticus in the Lake Victoria basin in Mara, Tanzania. African J Aquat Sci 38:55–60.
DOI: https://doi.org/10.2989/16085914.2013.784698
Scofield V, Jacques S, Guimarães JR, Farjalla VF, 2015. Potential changes in bacterial metabolism associated with increased water temperature and nutrient inputs in tropical humic lagoons. Front Microbiol 6:310.
DOI: https://doi.org/10.3389/fmicb.2015.00310
Wickham H, 2016. ggplot2: Elegant Graphics for Data Analysis. New York, Springer.
DOI: https://doi.org/10.1007/978-3-319-24277-4
Xiao M, Li M, Reynolds CS, 2018. Colony formation in the cyanobacterium Microcystis. Biol Rev 93:1399–1420.
DOI: https://doi.org/10.1111/brv.12401
Zenebe T, Ahlgren G, Gustafsson IB, Boberg M, 1998. Fatty acid and lipid content of Oreochromis niloticus L. in Ethiopian lakes - dietary effects of phytoplankton. Ecol Freshw Fish 7:146–158.
DOI: https://doi.org/10.1111/j.1600-0633.1998.tb00181.x
Zigah PK, Oswald K, Brand A, Dinkel C, Wehrli B, Schubert CJ, 2015. Methane oxidation pathways and associated methanotrophic communities in the water column of a tropical lake. Limnol Oceanogr 60:553–572.
DOI: https://doi.org/10.1002/lno.10035
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Diego Copetti, CNR-IRSA Brugherio, ItalyHow to Cite
de Leon, Justine R., Megumu Fujibayashi, Frances Mikayla Petilla, Bon Ivan Yumul, Milette U. Mendoza-Pascual, Rey Donne S. Papa, and Noboru Okuda. 2022. “Identification of Aquatic Consumer Trophic Pathways in Four Volcanic Tropical Lakes Using Fatty Acid Biomarkers”. Journal of Limnology 81 (1). https://doi.org/10.4081/jlimnol.2022.2070.
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