Advertisement

Fish-mediated zooplankton community structure in shallow turbid waters: a mesocosm study

  • Manuel A. Gayosso-Morales
  • S. NandiniEmail author
  • Fernando F. Martínez-Jeronimo
  • S. S. S. Sarma
Original Paper

Abstract

Turbidity influences the success of fish feeding, but little is known about the difference in the effects of turbidity as a result of organic and inorganic matter. To assess the feeding behaviour of a native fish, Goodea atripinnis, under turbid conditions (up to 120 NTU) generated by Microcystis aeruginosa or silt, we conducted mesocosm experiments for 25 days using 40-L plastic mesocosms. Each tank received two G. atripinnis individuals (predators) with a mean total length 61 mm and cladoceran zooplankton (prey) (Alona glabra, Chydorus sphaericus, Moina macrocopa, Simocephalus vetulus, Ceriodaphnia dubia, and Daphnia pulex) of 100 ind. L−1. Filtered water from Xochimilco Lake was used to fill the mesocosms. Goodea atripinnis had a selective effect on the zooplankton community in the form of a decrease in the number of pelagic cladocerans. The zooplankton composition, which was least affected by the fish, included small-sized (400–480 µm) benthic cladocerans (e.g. Chydorus sphaericus) and copepods (both calanoids and cyclopoids). Prey consumption by the fish was highest under conditions with inorganic turbidity, while in the fishless treatments, small cladocerans (along with calanoids) had a high density. Organic turbidity offered refuge against fish predation to A. glabra, C. sphaericus, Daphnia pulex, M. alburquerquensis and A. americanus, whereas inorganic turbidity allowed only both test copepods to coexist in the presence of fish. The results suggest that fish predation is a powerful factor regulating zooplankton communities, even in highly turbid waters.

Keywords

Fish feeding Copepods Cladocerans Silt Microcystis 

Notes

Acknowledgements

Manuel A. Gayosso-Morales thanks the Mexican Council for Science and Technology (CONACyT-211276) for a doctoral scholarship and Instituto Politécnico Nacional, ENCB  for additional help and support. SN and SSSS thank PAPIIT (UNAM) (IN216315, IN219218, and IN214618) for financial assistance. FMJ is grateful to EDI-IPN and COFAA-IPN for the partial support to this project.

Funding

PAPIIT (UNAM) (IN216315, IN219218 and IN214618). EDI-IPN and COFAA-IPN for the partial support to this project.

References

  1. Abrahams MV, Kattenfeld MG (1997) The role of turbidity as a constraint on predator-prey interactions in aquatic environments. Behav Ecol Sociobiol 40:169–174.  https://doi.org/10.1007/s002650050330 CrossRefGoogle Scholar
  2. Bruton MN (1985) The effects of suspensoids on fish. Hydrobiologia 125:221–241.  https://doi.org/10.1007/978-94-009-5522-6_16 CrossRefGoogle Scholar
  3. Carpenter SR, Kitchell KL (1993) The trophic cascade in lakes. Cambridge University, CambridgeCrossRefGoogle Scholar
  4. Chacón-Torres A (1993) Lake Patzcuaro, Mexico: watershed and water quality deterioration in a tropical high-altitude Latin American lake. Lake Reserv Manage 8:37–47.  https://doi.org/10.1080/07438149309354457 CrossRefGoogle Scholar
  5. Chang KH, Nagata T, Hanazato T (2004) Direct and indirect impacts of predation by fish on the zooplankton community: an experimental analysis using mesocosms. Limnology 5:121–124.  https://doi.org/10.1007/s10201-004-0116-7 CrossRefGoogle Scholar
  6. De Robertis A, Ryer CH, Veloza A, Brodeur RD (2003) Differential effects of turbidity on prey consumption of piscivorous and planktivorous fish. Can J Fish Aquat Sci 60:1517–1526.  https://doi.org/10.1139/f03-123 CrossRefGoogle Scholar
  7. Domínguez-Domínguez O, Nandini S, Sarma SSS (2002) Larval Behaviour of the endangered golden bumblebee goodeid. Allotoca dugesi, implications for conservation of an endangered species. Fish Manag Ecol 9:285–291.  https://doi.org/10.1046/j.1365-2400.2002.00309.x CrossRefGoogle Scholar
  8. Donohue I, Garcia-Molinos J (2009) Impacts of increased sediment loads on the ecology of lakes. Biol Rev 84:517–531.  https://doi.org/10.1111/j.1469-185X.2009.00081.x CrossRefGoogle Scholar
  9. Drenner RW, McComas SR (1980) The roles of zooplankter escape ability and fish size selectivity in the selective feeding and impact of planktivorous fish. In: Kerfoot WC (ed) Evolution and ecology of zooplankton communities. University of New England Press, Hanover, pp 587–593Google Scholar
  10. Engström J, Viherluoto M, Viitasalo M (2001) Effects of toxic and non-toxic cyanobacteria on grazing, zooplanktivory and survival of the mysid shrimp Mysis mixta. J Exp Mar Biol Ecol 257:269–280.  https://doi.org/10.1016/S0022-0981(00)00339-7 CrossRefGoogle Scholar
  11. Enríquez-García C, Nandini S, Sarma SSS (2009) Seasonal dynamics of zooplankton in Lake Huetzalin, Xochimilco (Mexico City, Mexico). Limnologica 39:283291.  https://doi.org/10.1016/j.limno.2009.06.010 CrossRefGoogle Scholar
  12. Escalera-Vazquez LH, Dominguez-Dominguez O, Sarma SSS, Nandini S (2004) Selective feeding on zooplankton by larval Skiffia multipunctata (Goodeidae). J Freshw Ecol 19:433–439.  https://doi.org/10.1080/02705060.2004.9664916 CrossRefGoogle Scholar
  13. Fey SB, Cottingham KL (2012) Thermal sensitivity predicts the establishment success of nonnative species in a mesocosm warming experiment. Ecology 93:2313–2320.  https://doi.org/10.1890/12-0609.1 CrossRefGoogle Scholar
  14. Figueroa-Sanchez 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 (Valley de Bravo, Mexico). J Limnol 73:157–166.  https://doi.org/10.4081/jlimnol.2014.784 CrossRefGoogle Scholar
  15. Gayosso-Morales MA, Nandini S, Martínez-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.  https://doi.org/10.22438/jeb/38/6(SI)/03 CrossRefGoogle Scholar
  16. Gerking SD (1994) Feeding ecology of fish. Academic Press, Cambridge, p 416Google Scholar
  17. Gliwicz ZM, Pijanowska J (1989) The role of predation in zooplankton succession. In: Sommer U (ed) Plankton ecology. Springer Verlag, London, pp 253–296CrossRefGoogle Scholar
  18. Gregory RS, Northcote TG (1993) Surface, planktonic, and benthic foraging by juvenile chinook salmon (Oncorhynchus tshawytscha) in turbid laboratory conditions. Can J Fish Aquat Sci 50:233–240.  https://doi.org/10.1139/cjfas-2015-0555 CrossRefGoogle Scholar
  19. Guthrie DM, Muntz WRA (1993) Role of vision in fish behaviour. In: Pitcher TP (ed) Behaviour of teleost fishes. Chapman and Hall, London, pp 89–121CrossRefGoogle Scholar
  20. Hessen DO, Faafeng BA, Smith VH, Bakkestuen V, Walseng B (2006) Extrinsic and intrinsic controls of zooplankton diversity in lakes. Ecology 87:433–443.  https://doi.org/10.1890/05-0352 CrossRefGoogle Scholar
  21. Jeppesen E, Jensen JP, Søndergaard M, Lauridsen T, Landkildehus F (2000) Trophic structure, species richness and biodiversity in Danish lakes: changes along a phosphorus gradient. Freshw Biol 45:201–218.  https://doi.org/10.1046/j.1365-2427.2000.00675.x CrossRefGoogle Scholar
  22. Jeppesen E, Søndergaard M, Mazzeo N, Meerhoff M, Branco C, Huszar V, Scasso F (2005) Lake restoration and biomanipulation in temperate lakes: relevance for subtropical and tropical lakes. In: Reddy V (ed) Tropical eutrophic lakes: their restoration and management. Science Publishers Inc, Enfield, pp 341–359Google Scholar
  23. Kamjunke N, Mehner T (2001) Coupling the microbial food web with fish: are bacteria attached to cyanobacteria an important food source for underyearling roach? Freshw Biol 46:633–639.  https://doi.org/10.1046/j.1365-2427.2001.00701.x CrossRefGoogle Scholar
  24. Kamjunke N, Schmidt K, Pflugmacher S, Mehner T (2002) Consumption of cyanobacteria by roach (Rutilus rutilus): useful or harmful to the fish? Freshw Biol 47:243–250.  https://doi.org/10.1046/j.1365-2427.2002.00800.x CrossRefGoogle Scholar
  25. Keshavanath P, Beveridge MC, Baird DJ, Lawton LA, Nimmo A, Codd GA (1994) The functional grazing response of a phytoplanktivorous fish Oreochromis niloticus to mixtures of toxic and non-toxic strains of the cyanobacterium Microcystis aeruginosa. J Fish Biol 45:123–129.  https://doi.org/10.1111/j.1095-8649.1994.tb01291.x Google Scholar
  26. Koste W (1978) Rotatoria. Borntraeger, BerlinGoogle Scholar
  27. Krebs JR, Davies NB (1993) Behavioural ecology. An evolutionary approach. Wiley, LondonGoogle Scholar
  28. Lynch M (1979) Predation, competition, and zooplankton community structure: an experimental study. Limnol Oceanogr 24:253–272.  https://doi.org/10.4319/lo.1979.24.2.0253 CrossRefGoogle Scholar
  29. Lyons J, Gutierrez-Hernandez A, Díaz-Pardo E, Soto-Galera E, Medina-Nava M, Pineda-Lopez R (2000) Development of a preliminary index of biotic integrity (IBI) based on fish assemblages to assess ecosystem condition in the lakes of central Mexico. Hydrobiologia 418:57–72.  https://doi.org/10.1023/A:1003888032756 CrossRefGoogle Scholar
  30. Maes J, Taillieu A, Van Damme K, Cottenie K, Ollevier F (1998) Seasonal patterns in the fish and crustacean community of a turbid temperate estuary. Estuar Coast Shelf Sci 47:143–151.  https://doi.org/10.1006/ecss.1998.0350 CrossRefGoogle Scholar
  31. Meager JJ, Batty RS (2007) Effects of turbidity on the spontaneous and prey-searching activity of juvenile Atlantic cod (Gadus morhua). Philos Trans R Soc Lond B Biol Sci 362:2123–2130.  https://doi.org/10.1098/rstb.2007.2104 CrossRefGoogle Scholar
  32. Mercado-Silva N, Helmus MR, Zanden M (2009) The effects of impoundment and non-native species on a river food web in Mexico’s central plateau. River Res Appl 25:1090–1108.  https://doi.org/10.1002/rra.1205 CrossRefGoogle Scholar
  33. Miller RR, Minckley WL, Norris S, StevenMark M (2009) Freshwater fishes of Mexico. University of Chicago Press, Chicago, p 490Google Scholar
  34. Miranda R, Galicia D, Monks S, Pulido-Flores G (2010) First record of Goodea atripinnis (Cyprinodontiformes: Goodeidae) in the state of Hidalgo (Mexico) and some considerations about its taxonomic position. Hidrobiológica 20:185–190Google Scholar
  35. Nandini S, Ramírez-García P, Sarma SSS (2016) Water quality indicators in Lake Xochimilco, Mexico: zooplankton and Vibrio cholera. J Limnol 75(1):91–100.  https://doi.org/10.4081/jlimnol.2015.1213 Google Scholar
  36. Niemisto J, Tallberg P, Horppila J (2005) Sedimentation and resuspension-factors behind the clay-turbidity in Lake Hiidenvesi. Adv Limnol 59:25–38Google Scholar
  37. Nurminen L, Pekcan-Hekim Z, Horppila J (2010) Feeding efficiency of planktivorous perch Perca fluviatilis and roach Rutilus rutilus in varying turbidity: an individual-based approach. J Fish Biol 76:1848–1855.  https://doi.org/10.1111/j.1095-8649.2010.02600.x CrossRefGoogle Scholar
  38. Pace ML (1986) An empirical analysis of zooplankton community size structure across lake trophic gradients. Limnol Oceanogr 31:45–55.  https://doi.org/10.4319/lo.1986.31.1.0045 CrossRefGoogle Scholar
  39. Parkos JJ, Santucci VJ, Wahl DH (2003) Effects of adult common carp (Cyprinus carpio) on multiple trophic levels in shallow mesocosms. Can J Fish Aquat Sci 60:182–192.  https://doi.org/10.1139/f03-011 CrossRefGoogle Scholar
  40. Pekcan-Hekim Z, Lappalainen J (2006) Effects of clay turbidity and density of pikeperch (Sander lucioperca) larvae on predation by perch (Perca fluviatilis). Naturwissenschaften 93:356–359.  https://doi.org/10.1007/s00114-006-0114-1 CrossRefGoogle Scholar
  41. Peña-Aguado F, Nandini S, Sarma SSS (2009) Functional response of Ameca splendens (Family Goodeidae) fed cladocerans during the early larval stage. Aquacult Res 40:1594–1604.  https://doi.org/10.1111/j.1365-2109.2009.02259.x CrossRefGoogle Scholar
  42. Pepin P, Penney RW (1997) Patterns of prey size and taxonomic composition in larval fish: are there general size-dependent models? J Fish Biol 51:84–100.  https://doi.org/10.1111/j.1095-8649.1997.tb06094.x CrossRefGoogle Scholar
  43. Peredo-Alvarez VM, Sarma SSS, Nandini S (2004) Studies on the functional responses of the Mexican live bearer fish Allotoca meeki (Goodeidae: Cyprinodontiformes). Adv Fish Wildl Ecol Biol 3:27–40Google Scholar
  44. Picapedra PHS, Sanches PV, Lansac-Tôha FA (2018) Effects of light-dark cycle on the spatial distribution and feeding activity of fish larvae of two co-occurring species (Pisces: Hypophthalmidae and Sciaenidae) in a Neotropical floodplain lake. Braz J Biol 78:763–772.  https://doi.org/10.1590/1519-6984.179070 CrossRefGoogle Scholar
  45. Radke RJ, Gaupisch A (2005) Effects of phytoplankton-induced turbidity on predation success of piscivorous Eurasian perch (Perca fluviatilis): possible implications for fish community structure in lakes. Naturwissenschaften 92:91–94.  https://doi.org/10.1007/s00114-004-0596-7 CrossRefGoogle Scholar
  46. Reid SM, Fox MG, Whillans TH (1999) Influence of turbidity on piscivory in largemouth bass (Micropterus salmoides). Can J Fish Aquat Sci 56:1362–1369.  https://doi.org/10.1139/f99-056 CrossRefGoogle Scholar
  47. Schwartz JS, Dahle M, Robinson BR (2008) Concentration-duration frequency curves for stream turbidity: possibilities for assessing biological impairment. J Am Water Resour Assoc 44:879–886.  https://doi.org/10.1111/j.1752-1688.2008.00186.x CrossRefGoogle Scholar
  48. Shoup DE, Wahl DH (2009) The effects of turbidity on prey selection by piscivorous largemouth bass. Trans Am Fish Soc 138:1018–1027.  https://doi.org/10.1577/T09-015.1 CrossRefGoogle Scholar
  49. Smirnov NN (1974) Fauna of the U.S.S.R. Crustacea. Keter Publishing House, JerusalemGoogle Scholar
  50. Smith VH (2003) Eutrophication of freshwater and coastal marine ecosystems a global problem. Environ Sci Pollut Res 10:126–139.  https://doi.org/10.1065/espr2002.12.142 CrossRefGoogle Scholar
  51. Sohel S, Mattila J, Lindström K (2017) Effects of turbidity on prey choice of three-spined stickleback Gasterosteus aculeatus. Mar Ecol Progr Ser 566:159–167.  https://doi.org/10.3354/meps12014 CrossRefGoogle Scholar
  52. Soto D, Hurlbert SH (1991) Long-term experiments on calanoid–cyclopoid interactions. Ecol Monogr 61:245–266.  https://doi.org/10.2307/2937108 CrossRefGoogle Scholar
  53. Stowasser A, Buschbeck EK (2012) Electrophysiological evidence for polarization sensitivity in the camera-type eyes of the aquatic predacious insect larva Thermonectus marmoratus. J Exp Biol 215:3577–3586.  https://doi.org/10.1242/jeb.075028 CrossRefGoogle Scholar
  54. Sweka JA, Hartman KJ (2003) Reduction of reactive distance and foraging success in smallmouth bass, Micropterus dolomieu, exposed to elevated turbidity levels. Environ Biol Fish 67:341–347.  https://doi.org/10.1023/A:1025835031366 CrossRefGoogle Scholar
  55. Ter Braak CJ, Smilauer P (2002) CANOCO reference manual and CanoDraw for Windows user’s guide: software for canonical community ordination (version 4.5). www.canoco.com
  56. Turesson H, Brönmark C (2007) Predator–prey encounter rates in freshwater piscivores: effects of prey density and water transparency. Oecologia 153:281–290.  https://doi.org/10.1007/s00442-007-0728-9 CrossRefGoogle Scholar
  57. Utne-Palm AC (2002) Visual feeding of fish in a turbid environment: physical and behavioural aspects. Mar Freshw Behav Phyiol 35:111–128.  https://doi.org/10.1080/10236240290025644 CrossRefGoogle Scholar
  58. Vinyard GL, O’Brien WJ (1976) Effects of light and turbidity on the reactive distance of bluegill (Lepomis macrochirus). J Fish Res Board Can 33:2845–2849.  https://doi.org/10.1139/f76-342 CrossRefGoogle Scholar
  59. Yoshida T, Kagami M, Gurung TB, Urabe J (2001) Seasonal succession of zooplankton in the north basin of Lake Biwa. Aquat Ecol 35:19–29.  https://doi.org/10.1023/A:1011498202050 CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Instituto Politécnico Nacional, Escuela Nacional de Ciencias Biológicas, Posgrado en Ciencias QuimicobiológicasMexico CityMexico
  2. 2.Laboratory of Aquatic Zoology, Division of Research and Post-graduate StudiesNational Autonomous University of MexicoTlalnepantlaMexico

Personalised recommendations