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Effect of temperature, food quality and quantity on the feeding behavior of Simocephalus mixtus and Hyalella azteca: implications for biomanipulation

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Abstract

Increasing temperatures in aquatic ecosystems have resulted in changes in the proliferation patterns and persistence of cyanobacteria, particularly Microcystis sp.. In temperate lakes, large-sized herbivores such as Daphnia magna are used to control cyanobacterial blooms. The cladoceran, Simocephalus mixtus and the amphipod, Hyalella azteca are common in tropical and sub-tropical aquatic systems. Since both species are generalist feeders, we tested their ability to consume uni-cellular Microcystis sp. and Chlorella at different temperatures. Feeding rates and filtration rates at different temperatures (20, 25 and 30 °C) were quantified on diets of Chlorella vulgaris and Microcystis sp.; each diet separately at different concentrations (0.2, 0.5, 1.0 and 2.0 × 106 cell mL−1). Both the crustaceans were able to consume C. vulgaris and Microcystis sp. although at different rates depending on the food concentration and temperature. At 25 °C and a Microcystis sp. concentration of 2.0 × 106 cells mL−1, H. azteca fed up to 60 × 104 cells ind−1 h−1 of Microcystis sp. which was even greater than its feeding rate on C. vulgaris. Simocephalus was able to consume Microcystis sp. although at significantly lower rates as compared to C. vulgaris. Our experiments show that H. azteca can feed well on Microcystis sp.. Combined with control in fish predation pressure, both crustacean species could be used in top-down control, but further investigation on a large scale with these organisms is necessary to propose new alternatives.

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References

  • Alcocer J, Escobar-Briones E, Peralta L, Alvarez F (2002) Population structure of the macrobenthic amphipod Hyalella azteca Saussure (Crustacea: Peracarida) on the littoral zone of six crater lakes. In: Escobar-Briones E, Alvarez F (eds) Modern approaches to the study of crustacea. Springer, Boston, pp 111–115

    Chapter  Google Scholar 

  • Borowitzka MA, Borowitzka LJ (eds) (1988) Micro-algal biotechnology. Cambridge University, Cambrige

    Google Scholar 

  • Brito D, Milani N, Pereira G (2006) Tasa de filtración e ingestión de Simocephalus vetulus (Müller, 1776) (Crustacea: Cladocera) alimentado con Selenastrum capricornutum Printz, 1914 y Chlorella vulgaris Beijerinck, 1890. Interciencia 31:753–757

    Google Scholar 

  • Burns CW (1968) The relationship between body size of filter feeding cladocera and the maximum size of particle ingested. Limnol Oceanogr 13:675–678

    Article  Google Scholar 

  • Burns CW (1969) Relation between filtering rate, temperature, and body size in four species of Daphnia. Limnol Oceanogr 14:693–700

    Article  Google Scholar 

  • Camacho FA, Thacker RW (2006) Amphipod herbivory on the freshwater cyanobacterium Lyngbya wollei: chemical stimulants and morphological defenses. Limnol Oceanogr 51:1870–1875

    Article  CAS  Google Scholar 

  • Camacho FA, Thacker RW (2013) Predator cues alter habitat use by amphipod Hyalella azteca (Saussure). Freshw Sci 32:1148–1154

    Article  Google Scholar 

  • Cardinale BJ, Brady VJ, Burton TM (1998) Changes in the abundance and diversity of coastal wetland fauna from the open water/macrophyte edge towards shore. Wetlands Ecol Manag 6:59–68

    Article  Google Scholar 

  • Carpenter SR, Kitchell KL (1993) The trophic cascade in lakes. Cambridge University, Cambridge

    Book  Google Scholar 

  • Chaparro-Herrera DJ, Nandini S, Sarma SSS (2013) Effect of water quality on the feeding ecology of the axolotl Ambystoma mexicanum. J Limnol 72:555–563

    Article  Google Scholar 

  • Chorus I, Bartram J (eds) (1999) Toxic cyanobacteria in water: a guide to their public health consequences, monitoring and management. E & FN Spon, New York

    Google Scholar 

  • Corline NJ, Sommer T, Jeffres CA, Katz J (2017) Zooplankton ecology and trophic resources for rearing native fish on an agricultural floodplain in the Yolo Bypass California. USA Wetlands Ecol Manag 25(5):533–545

    Article  Google Scholar 

  • Dias JD, Miracle MR, Bonecker CC (2017) Do water levels control zooplankton secondary production in Neotropical floodplain lakes? Fundam Appl Limnol 190:49–62

    Article  Google Scholar 

  • Environmental Protection Agency (EPA) (2017) Cases and prevention. http://www.tandfonline.com/action/authorSubmission?show=instructions&journalCode=ulrm20. Accessed 13 Aug 2017

  • Fernandez R, Nandini S, Sarma SSS (2012) A comparative study on the ability of tropical micro-crustaceans to feed and grow on cyanobacterial diets. J Plankton Res 34:719–731

    Article  Google Scholar 

  • Figueroa-Sánchez MA, Nandini S, Sarma SSS (2014) Zooplankton community structure in the presence of low levels of cyanotoxins: a case study in a high altitude tropical reservoir (Valle de Bravo, Mexico). J Limnol 73:157–166

    Article  Google Scholar 

  • Gayosso-Morales MA, Nandini S, Mártinez-Jeronimo FF, Sarma SSS (2017) Effect of organic and inorganic turbidity on the zooplankton community structure of a shallow waterbody in Central Mexico (Lake Xochimilco, Mexico). J Environ Biol 38:1183–1196

    Article  Google Scholar 

  • Ger KA, Hansson LA, Lürling M (2014) Understanding cyanobacteria–zooplankton interactions in a more eutrophic world. Freshw Biol 59:1783–1798

    Article  Google Scholar 

  • Ghadouani A, Pinel-Alloul B, Prepas EE (2003) Effects of experimentally induced cyanobacterial blooms on crustacean zooplankton communities. Freshw Biol 48:363–381

    Article  Google Scholar 

  • Gillooly FJ, Charnow LE, Wests BG, Savage MV, Brown JH (2002) Effects of size and temperature on developmental time. Nature 417:70–73

    Article  CAS  PubMed  Google Scholar 

  • Gliwicz ZM (1990) Why do the cladocerans fail to control algal bloom? Hydrobiologia 200(201):83–97

    Article  Google Scholar 

  • Gulati RD (1990) Structural and grazing responses of zooplankton community to biomanipulation of some Dutch water bodies. Hydrobiologia 200:99–118

    Article  Google Scholar 

  • Hall DJ, Threlkeld ST, Burns CW, Crowley PH (1976) The size-efficiency hypothesis and the size structure of zooplankton communities. Ann Rev Ecol Syst 7:177–208

    Article  Google Scholar 

  • Heugens EHW, Tokkie LTB, Kraak MHS, Hendriks AJ, Van Straalen NM, Admiraal W (2006) Population growth of Daphnia magna under multiple stress conditions: join effects of temperature, food and cadmium. Environ Toxicol Chem 25:1399–1407

    Article  CAS  PubMed  Google Scholar 

  • Iglesias C, Mazzeo N, Meerhoff M, Lacerot G, Clemente JM, Scasso F, Kruk C, Goyenola G, García-Alonso J, Amsinck SL et al (2011) High predation is of key importance for dominance of small-bodied zooplankton in warm shallow lakes: evidence from lakes, fish enclosures and surface sediments. Hydrobiologia 667:133–147

    Article  Google Scholar 

  • Jeppesen E, Meerhoff M, Jacobsen BA, Hansen RS, Søndegaard M, Jensen JP, Lauridsen TL, Mazzeo N, Branco CWC (2007) Restoration of shallow lakes by nutrient control and biomanipulation-the successful strategy varies with lake size and climate. Hydrobiologia 581:269–285

    Article  CAS  Google Scholar 

  • Jeppesen E, Meerhoff M, Holmgren K, González-Bergonzoni I, Teixeira-De Mello F, Decleck SAJ, De Meester L, Søndergaard M, Lauridsen TL, Bjerring R et al (2010) Impacts of climate warming on lake fish community structure and potential effects on ecosystem function. Hydrobiologia 646:73–90

    Article  CAS  Google Scholar 

  • Kasprzak P, Benndorf J, Gonsiorczyk T, Koschel R, Krienitz L, Mehner T, Hulsmann S, Schultz H, Wagner A (2007) Reduction of nutrient loading and biomanipulation as tools in water quality management: long-term observations on Bauzen reservoir and Feldberger Haussee (Germany). Lake Reserv Manag 23:410–427

    Article  Google Scholar 

  • Kiørboe T (2011) How zooplankton feed: mechanisms, traits and trade-offs. Biol Rev 86:311–339

    Article  PubMed  Google Scholar 

  • Komarék J, Komárkova-Legnerová J (2002) Contribution to the knowledge of planktic cyanoprokaryotes from central Mexico. Preslia Praha 74:207–233

    Google Scholar 

  • Kosten S, Huszar V, Bécares E, Costa L, Van Donk E, Hansson LA, Jeppessn E, Kruk C, Lacerot G, Mazzeo N et al (2012) Warmer climate boosts cyanobacterial dominance in shallow lakes. Glob Change Biol 18:118–126

    Article  Google Scholar 

  • Li Y, Xie P, Zhang J, Tao M, Deng X (2017) Effects of filter-feeding planktivorous fish and cyanobacteria on structuring the zooplankton community in the eastern plain lakes of China. Ecol Eng 99:238–245

    Article  Google Scholar 

  • Loiterton B, Sundbom M, Vrede T (2004) Separating physical and physiological effects of temperature on zooplankton feeding rate. Aquat Sci 66:123–129

    Article  Google Scholar 

  • Lürling M, Verschoor AM (2003) F0-spectra of chlorophyll fluorescence for the determination of zooplankton grazing. Hydrobiologia 491:145–157

    Article  Google Scholar 

  • MacIsaac JH, Hebert NPN, Schwartz SS (1985) Inter- and intraspecific variation in acute thermal tolerance of Daphnia. Physiol Zool 58:350–355

    Article  Google Scholar 

  • Mara D (2003) Domestic wastewater treatment in developing countries. Earthscan, London

    Google Scholar 

  • Marmen S, Aharonovich D, Grossowicz M, Blank L, Yacobi YZ, Sher JD (2016) Distribution and habitat specificity of potentially-toxic Microcystis sp. across climate, land and water use gradients. Front Microbiol 7:1–14

    Article  Google Scholar 

  • McMahon JW (1965) Some physical factors influencing the feeding behavior of Daphnia magna Straus. Can J Zool 43:603–611

    Article  Google Scholar 

  • Monakov AV (2003) Feeding of freshwater invertebrates. Kenobi, Ghent

    Google Scholar 

  • Moreira C, Vasconcelos V, Antunes A (2013) Phylogeny and biography of cyanobacteria and their produced toxins. Mar Drugs 11:4350–4369

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moss B (2018) Ecology of freshwater: earth’s bloodstream. John Wiley & Sons Ltd, Chichester

    Google Scholar 

  • Mur LR, Olav MS, Hans U (1999) Cyanobacteria in the environment. In: Chorus I, Bartram J (eds) Toxic cyanobacteria in water: a guide to their public health consequences, monitoring and management. E & FN Spon, New York, pp 253–255

    Google Scholar 

  • Nandini S, Rao TR (1998) Somatic and population growth in selected cladoceran and rotifer species offered the cyanobacterium Microcystis aeruginosa as food. Aquat Ecol 31:283–298

    Article  Google Scholar 

  • Nandini S, Ramírez-García P, Sarma SSS (2016) Water quality indicators in Lake Xochimilco, Mexico: zooplankton and Vibrio cholera. J Limnology 75:91–100

    Google Scholar 

  • Nelson WG (1979) Experimental studies of selective predation on amphipods: consequences for amphipod distribution and abundance. J Exp Mar Biol Ecol 38:225–245

    Article  Google Scholar 

  • Panov VE, McQueen DJ (1998) Effects of temperature on individual growth rate and body size of freshwater amphipod. Can J Zool 76:1107–1116

    Article  Google Scholar 

  • Pérez-Morales A, Sarma SSS, Nandini S (2014) Feeding and filtration rates of zooplankton (rotifers and cladocerans) fed toxic cyanobacterium (Microcystis aeruginosa). J Environ Biol 35:1013–1020

    PubMed  Google Scholar 

  • Platvoet D, Dick JTA, Konijnendijk N, Van del Velde G (2006) Feeding on micro-algae in the invasive Ponto-Caspian amphipod Dikerogammarus villosus (Sowinsky, 1894). Aquat Ecol 40:237–245

    Article  Google Scholar 

  • Richardson AJ (2008) In hot water: zooplankton and climate change. ICES J Mar Sci 65:279–295

    Article  Google Scholar 

  • Rigler FH (1971) Feeding rates. Zooplankton. In: Downing JD, Rigler FH (eds) A manual on methods for the assessment of secondary productivity in fresh waters. Blackwell, Oxford

    Google Scholar 

  • Sinha R, Peason LA, Davis TW, Burford MA, Orr PT, Neilan BA (2012) Increased incidence of Cylindrospermopsis raciborskii in temperate zones—is climate change responsible? Water Res 46:1408–1419

    Article  CAS  PubMed  Google Scholar 

  • Sushchenya LM (1975) Kolichestvennye zakonomernosti pitaniya rakoobraznykh (Quiantitative regularities of crustacean feeding). In: Monakov AV (ed) Feeding of freshwater invertebrates. Kenobi, Ghent, pp 133–174

    Google Scholar 

  • Venthuis M, De Senerpont Domis LN, Frenken T, Stephan S, Kazanjian G, Aben R, Hilt S, Kosten S, Van Donk E, Van de Waal DB (2017) Warming advances top-down control and reduces producer biomass in a freshwater plankton community. Ecosphere 8:1–e01651

    Google Scholar 

  • Von Elert E, Wolffrom T (2001) Supplementation of cyanobacterial food with polyunsaturated fatty acids does not improve growth of Daphnia. Limnol Oceanogr 46:1552–1558

    Article  Google Scholar 

  • Weber CI (ed) (1993) Methods for measuring the acute toxicity of effluents and receiving waters to freshwater and marine organisms. EPA, Cincinnati

    Google Scholar 

  • Whitton BA, Potts M (2000) The ecology of cyanobacteria: their diversity in time and space. In: Whitton BA, Potts M (eds) Introduction to the cyanobacteria. Springer, Netherlands, pp 1–11

    Google Scholar 

  • Yin XW, Liu PF, Zhu SS, Chen XX (2010) Food selectivity of the herbivore Daphnia magna (Cladocera) and its impact on competition outcome between two freshwater green algae. Hydrobiologia 655:15–23

    Article  Google Scholar 

  • Zhang J, Xie P, Tao M, Guo L, Chen J, Li L, Zhang XZ, Zhang L (2013) The impact of fish predation and cyanobacteria on zooplankton size structure in 96 Subtropical lakes. PLoS ONE 4:e76378

    Article  CAS  Google Scholar 

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Acknowledgements

M.A.F.S. thanks Programa de doctorado en Ciencias Biológicas y de la Salud, Universidad Autónoma Metropolitana, Xochimilco (UAM-X), Consejo Nacional de Ciencia y Tecnología (CONACyT) for a doctoral scholarship (491214), Administración de Pista de Remo y Canotaje, Xochimilco, Mexico City. S.N. and S.S.S.S. thank DIP, FESI-UNAM and CONACyT (20520 and 18723) and PAPIIT (Grant No. IN219218 and IN214618 UNAM) for support.

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Authors and Affiliations

  1. Doctorado en Ciencias Biológicas y de la Salud, Universidad Autónoma Metropolitana, Unidad Xochimilco, Calzada del Hueso 1100, Villa Quietud, Coyoacán, P.C. 04960, Ciudad de México, Mexico

    Michael Anai Figueroa-Sánchez

  2. Lab. de Zoología Acuática, Universidad Nacional Autónoma de México, Campus Iztacala, Av. de los Barrios No.1, AP 314, P.C. 54090, Tlalnepantla, Mexico

    S. Nandini & S. S. S. Sarma

  3. Departamento el Hombre y su Ambiente, Lab. de Rotiferología y Biología Molecular de Plancton, Universidad Autónoma Metropolitana, Unidad Xochimilco, Calzada del Hueso 1100, Villa Quietud, Coyoacán, P.C. 04960, Ciudad de México, Mexico

    Maria Elena Castellanos-Páez

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  1. Michael Anai Figueroa-Sánchez
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  2. S. Nandini
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  3. Maria Elena Castellanos-Páez
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Correspondence to S. Nandini.

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Figueroa-Sánchez, M.A., Nandini, S., Castellanos-Páez, M.E. et al. Effect of temperature, food quality and quantity on the feeding behavior of Simocephalus mixtus and Hyalella azteca: implications for biomanipulation. Wetlands Ecol Manage 27, 353–361 (2019). https://doi.org/10.1007/s11273-019-09664-5

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