, Volume 188, Issue 3, pp 889–900 | Cite as

Do grazers respond to or control food quality? Cross-scale analysis of algivorous fish in littoral Lake Tanganyika

  • Renalda N. MunubiEmail author
  • Peter B. McIntyre
  • Yvonne Vadeboncoeur
Ecosystem ecology – original research


Food quality determines the growth rate of primary consumers and ecosystem trophic efficiencies, but it is not clear whether variation in primary consumer densities control, or is controlled by, variation in food quality. We quantified variation in the density and condition of an abundant algae-eating cichlid, Tropheus brichardi, with respect to the quality and productivity of algal biofilms within and across rocky coastal sites in Lake Tanganyika, East Africa. Adjacent land use and sediment deposition in the littoral zone varied widely among sites. Tropheus brichardi maximized both caloric and phosphorus intake at the local scale by aggregating in shallow habitats: algivore density decreased with depth, tracking attached algae productivity (rETRMAX) remarkably well (r2 = 0.84, P = 0.00033). In contrast, algivore density was unrelated to among-site variation in algal productivity. Rather, there was significant increase in algal quality (r2 = 0.44, P = 0.011) and decrease in algal biomass (r2 = 0.53, P = 0.0068) with T. brichardi density across sites, consistent with strong top-down control of primary producers. The amount of inorganic sediment on rock surfaces was the strongest predictor of among-site variation in algivore density (r2 = 0.69, P = 0.00096), and algivore gut length increased with sedimentation (r2 = 0.36, P = 0.034). These patterns indicate extrinsic and top-down forcing of algal food quality and quantity across coastal landscapes, combined with adaptive habitat selection by fish at the local scale. Factors that degrade food quality by decreasing algal nutrient content or diluting the resource with indigestible material are likely to depress grazer densities, potentially dampening top-down control in high-light, low-nutrient aquatic ecosystems.


Algivore Microphytobenthos Periphyton Food quality Productivity Tropheus Littoral Sediment C:N:P 



We thank Dr. Rashid Tamatamah, Dr. Ismael Kimirei, and the Tanzanian Fisheries Research Institute for facilitating this research. We gratefully acknowledge the field help of George Kazumbe, Len Kenyon, Ryan Satchell, Erica Hile, Sam Drerup, Ellen Hamann and Leslie Kim. Funds were provided by the US National Science Foundation (DEB 0842253 to YV and DEB 1030242 to PBM) and Wright State University’s Environmental Sciences Ph.D. Program.

Author contribution statement

RM conceived of and designed the study, collected and analyzed data, and wrote the manuscript. YV advised on study design, collected and analyzed productivity data and wrote the manuscript. PBM advised on study design, collected community fish data, and provided editorial contributions to the manuscript

Compliance with ethical standards

Statement of human and animal rights

All applicable institutional and/or national guidelines for the care and use of animals were followed.


  1. Ahlgren G, Vrede T, Goedkoop W (2009) Fatty acid ratios in freshwater fish, zooplankton and zoobenthos—are there specific optima? In: Arts MT, Brett MT, Kainz M (eds) Lipids in aquatic ecosystems. Springer Verlag, New York, pp 147–178CrossRefGoogle Scholar
  2. Alin SR, Cohen AS, Bills R, Gashagaza MM, Michel E, Tiercelin J-J, Martens K, Coveliers P, Mboko SK, West K, Soreghan M, Kimbadi S, Ntakimazi G (1999) Effects of landscape disturbance on animal communities in Lake Tanganyika, East Africa. Conserv Biol 13:1017–1033CrossRefGoogle Scholar
  3. Anderson TM, Hopcraft JGC, Eby S, Ritchie M, Grace JB, Olff H (2010) Landscape-scale analyses suggest both nutrient and antipredator advantages to Serengeti herbivore hotspots. Ecology 91:1519–1529CrossRefGoogle Scholar
  4. Andre ER, Hecky RE, Duthie HC (2003) Nitrogen and phosphorus regeneration by cichlids in the littoral zone of Lake Malawi, Africa. J Great Lakes Res 29:190–201CrossRefGoogle Scholar
  5. Bates D, Machler M, Bolker BM, Walker SC (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48CrossRefGoogle Scholar
  6. Bracken MES, Menge BA, Foley MM, Sorte CJB, Lubchenco J, Schiel DR (2012) Mussel selectivity for high-quality food drives carbon inputs into open-coast intertidal ecosystems. Mar Ecol Prog Ser 459:53–62. CrossRefGoogle Scholar
  7. Burkepile DE, Hay ME (2006) Herbivore vs. nutrient control of marine primary producers: context-dependent effects. Ecology 87:3129–3139Google Scholar
  8. Cebrian J (1999) Patterns in the fate of production in plant communities. Am Nat 154:449–468CrossRefGoogle Scholar
  9. Cebrian J, Shurin JB, Borer ET, Cardinale BJ, Ngai JT, Smith MD (2009) Producer nutritional quality controls ecosystem trophic structure. PLoS One 4:e4929CrossRefGoogle Scholar
  10. Cohen AS, Bills R, Cocquyt CZ, Caljon AG (1993) The impact of sediment pollution on biodiversity in Lake Tanganyika. Conserv Biol 7:667–677CrossRefGoogle Scholar
  11. Cohen AS, Gerguricha EL, Kraemer BM, McGluec MM, McIntyre PB, Russell JM, Simmonsa JD, Swarzenskie PW (2016) Climate warming reduces fish production and benthic habitat in Lake Tanganyika, one of the most biodiverse freshwater ecosystems. Proc Natl Acad Sci USA 113:9563–9568CrossRefGoogle Scholar
  12. Corman JR, McIntyre PB, Kuboja B, Mbemba W, Fink D, Wheeler CW, Flecker AS (2010) Upwelling couples chemical and biological dynamics across the littoral and pelagic zones of Lake Tanganyika, East Africa. Limnol Oceanogr 55:214–224CrossRefGoogle Scholar
  13. Crain CM, Kroeker K, Halpern BS (2008) Interactive and cumulative effects of multiple human stressors in marine systems. Ecol Lett 11:1304–1315CrossRefGoogle Scholar
  14. DeForest J, Vis M, Drerup SA (2016) Using fatty acids to fingerprint biofilm communities: a means to quickly and accurately assess stream quality. Environ Monit Assess 188:277. CrossRefPubMedGoogle Scholar
  15. Devlin SP, Vander Zanden MJ, Vadeboncoeur Y (2016) Littoral-benthic primary production estimates: sensitivity to simplifications with respect to periphyton productivity and basin morphometry. Limnol Oceanogr Methods 14:138–149CrossRefGoogle Scholar
  16. Donohue I, Verheyen E, Irvine K (2003) In situ experiments on the effects of increased sediment loads on littoral rocky shore communities in Lake Tanganyika, East Africa. Freshw Biol 48:1603–1616. CrossRefGoogle Scholar
  17. Elser JJ, Fagan WF, Denno RF, Dobberfuhl DR, Folarin A, Huberty A, Sterner RW (2000) Nutritional constraints in terrestrial and freshwater food webs. Nature 408:578–580CrossRefGoogle Scholar
  18. Evans-White MA, Lamberti GA (2006) Stoichiometry of consumer driven nutrient recycling across nutrient regimes in streams. Ecol Lett 9:1186–1197CrossRefGoogle Scholar
  19. Flecker AS, Taylor BW (2004) Tropical fishes as biological bulldozers: density effects on resource heterogeneity and species diversity. Ecology 85:2267–2278CrossRefGoogle Scholar
  20. Froese R (2006) Cube law, condition factor and weight–length relationships: history, meta-analysis and recommendations. J Appl Ichthyol 22:241–253CrossRefGoogle Scholar
  21. Gratwicke B, Speight MR (2005) The relationship between fish species richness, abundance and habitat complexity in a range of shallow tropical marine habitats. J Fish Biol 66:650–667. CrossRefGoogle Scholar
  22. Guo F, Kainz MJ, Valdez D, Sheldon F, Bunn SE (2016) The effect of light and nutrients on algal food quality and their consequent effect on grazer growth in subtropical streams. Freshw Sci 35:1202–1212CrossRefGoogle Scholar
  23. Higgins SN, Hecky RE, Taylor WD (2001) Epilithic nitrogen fixation in the rocky littoral zones of Lake Malawi, Africa. Limnol Oceanogr 46:976–982CrossRefGoogle Scholar
  24. Hill WR, Smith JG, Stewart AJ (2010) Light, nutrients and herbivore growth in oligotrophic streams. Ecology 91:518–527CrossRefGoogle Scholar
  25. Hillebrand H, Sommer U (1999) The nutrient stoichiometry of benthic microalgal growth: redfield proportions are optimal. Limnol Oceanogr 44:440–446CrossRefGoogle Scholar
  26. Izagirre O, Serra A, Guasch H, Elosegi A (2009) Effects of sediment deposition on periphytic biomass, photosynthetic activity and algal community structure. Sci Total Environ 407:5694–5700CrossRefGoogle Scholar
  27. Karino K (1998) Depth-related differences in territory size and defense in the herbivorous cichlid, Neolamprologus moorii, in Lake Tanganyika. Ichthyol Res 45:89–94CrossRefGoogle Scholar
  28. Kelly BM, Mtiti M, McIntyre PB, Vadeboncoeur Y (2017) Stable isotopes reveal nitrogen loading to Lake Tanganyika from remote shoreline villages. Environ Manag 59:264–273CrossRefGoogle Scholar
  29. Konings A (2015) Tanganyika Cichlids in their Natural Habitat, 3rd edn. Cichlid Press, El PasoGoogle Scholar
  30. Liess A, Hillebrand H (2004) Invited review: direct and indirect effects in herbivore-periphyton interactions. Arch Hydrobiol 159:433–453CrossRefGoogle Scholar
  31. Loeb SL (1981) An in situ method for measuring the primary productivity and standing crop of the epilithic periphyton community in lentic systems. Limnol Oceanogr 26:394–399CrossRefGoogle Scholar
  32. McCormick MI (1994) Comparison of field methods for measuring surface topography and their associations with a tropical reef fish assemblage. Mar Ecol Prog Ser 112:87–96CrossRefGoogle Scholar
  33. McIntyre PB, Michel E, France K, Rivers A, Hakizimana P, Cohen AS (2005) Individual- and assemblage-level effects of anthropogenic sedimentation on snails in Lake Tanganyika. Conserv Biol 19:171–181CrossRefGoogle Scholar
  34. McIntyre PB, Michel E, Olsgard M (2006) Top-down and bottom-up controls on periphyton biomass and productivity in Lake Tanganyika. Limnol Oceanogr 51:1514–1523CrossRefGoogle Scholar
  35. McIntyre PB, Jones LE, Flecker AS, Vanni MJ (2007) Fish extinctions alter nutrient recycling in tropical freshwaters. Proc Natl Acad Sci USA 104:4461–4466CrossRefGoogle Scholar
  36. McIntyre PB, Flecker AS, Vanni MJ, Hood JM, Taylor BW, Thomas SA (2008) Fish distributions and nutrient cycling in streams: can fish create biogeochemical hotspots? Ecology 89:2335–2346CrossRefGoogle Scholar
  37. Menge BA, Menge DNL (2013) Dynamics of coastal meta-ecosystems: the intermittent upwelling hypothesis and a test in rocky intertidal regions. Ecol Monogr 83:283–310CrossRefGoogle Scholar
  38. Munubi RN (2015) Algal Quality Controls the Distribution, Behavior and Growth of Algivorous Cichlids in Lake Tanganyika. Ph.D. Dissertation, Wright State University, Dayton, Ohio, USAGoogle Scholar
  39. Pagès JF, Gera A, Romero J, Alcoverro T (2014) Matrix composition and patch edges influence plant herbivore interactions in marine landscapes. Funct Ecol 28:1440–1448CrossRefGoogle Scholar
  40. Perkins RG, Kromkamp JC, Serȏdio J, Lavaud J, Jesus B, Mouget JL, Lefebvre S, Forster RM (2011) The application of variable chlorophyll fluorescence to microphytobenthic biofilms. In: Suggett DJ (ed) Chorophyll a fluorescence in aquatic sciences: methods and applications, developments in applied phycology, vol 4. Springer, Dordrecht. CrossRefGoogle Scholar
  41. Power ME (1984a) Habitat quality and the distribution of algae-grazing catfish in a Panamanian stream. J Anim Ecol 53:357–374CrossRefGoogle Scholar
  42. Power ME (1984b) The importance of sediment in the grazing ecology and size class interactions of an armored catfish, Ancistrus spinosus. Environ Biol Fish 10:173–181CrossRefGoogle Scholar
  43. Power ME (1984c) Depth-distribution of armored catfish: predator-induced resource avoidance? Ecology 65:523–528CrossRefGoogle Scholar
  44. Power ME, Stewart AJ, Matthews WJ (1988) Grazer control of algae in an Ozark mountain stream: effects of short-term exclusion. Ecology 69:1894–1898CrossRefGoogle Scholar
  45. Rosemond AD, Mulholland PJ, Elwood JW (1993) Top-down and bottom-up control of stream periphyton: effects of nutrients and herbivores. Ecology 74:1264–1280CrossRefGoogle Scholar
  46. Schlosser IJ (1987) The role of predation in age- and size-related habitat use by stream fishes. Ecology 68:651–659. CrossRefGoogle Scholar
  47. Sefc KM, Baric S, Salzburger W, Sturmbauer C (2007) Species-specific population structure in rock-specialized sympatric cichlid species in Lake Tanganyika, East Africa. J Mol Evol 64:33–49CrossRefGoogle Scholar
  48. Stainton MJ, Capel MJ, Armstrong FAJ (1977) The chemical analysis of fresh water. Environ Can Freshw Inst Misc Spec Publ 25:67–69Google Scholar
  49. Steinman AD (1996) Effects of grazers on freshwater benthic algae. In: Stevenson RJ, Bothwell ML, Lowe RL (eds) Algal ecology: freshwater benthic ecosystems. Aquatic ecology series. Academic Press, Boston, pp 341–373CrossRefGoogle Scholar
  50. Sterner RW, Elser JJ (2002) Ecological stoichiometry: the biology of elements from molecules to the biosphere. Princeton University Press, PrincetonGoogle Scholar
  51. Sterner RW, Elser JJ, Fee EJ, Guildford SJ, Chrzanowski TH (1997) The light: nutrient ratio in lakes: the balance of energy and materials affects ecosystem structure and process. Am Nat 150:663–684CrossRefGoogle Scholar
  52. Strandberg U, Taipale SJ, Hiltunen MA, Galloway WE, Brett MT, Kankaala P (2015) Inferring phytoplankton community composition with a fatty acid mixing model. Ecosphere 6:16. CrossRefGoogle Scholar
  53. Takeuchi Y, Ochi H, Kohda M, Sinyinza D, Hori M (2010) A 20-year census of a rocky littoral fish community in Lake Tanganyika. Ecol Freshw Fish 19:239–248CrossRefGoogle Scholar
  54. R Core Team (2016) R: A language and environment for statistical computing. R foundation for Statistical Computing. Vienna, Austria. Accessed Mar 2016
  55. Vadeboncoeur Y, Power ME (2017) Attached algae: the cryptic base of inverted trophic pyramids in fresh waters. Annu Rev Ecol Evol Syst 48:255–279CrossRefGoogle Scholar
  56. Vadeboncoeur Y, McIntyre PB, Vander Zanden MJ (2011) Borders of biodiversity: life at the edge of the world’s Great Lakes. Bioscience 61:526–537CrossRefGoogle Scholar
  57. Vadeboncoeur Y, Devlin SP, McIntyre PB, Vander Zanden MJ (2014) Is there light after depth? Distribution of periphyton chlorophyll and productivity in lake littoral zones. Freshw Sci 33:524–536CrossRefGoogle Scholar
  58. Vanni MJ, McIntyre PB (2016) Predicting nutrient excretion rates of aquatic animals using metabolic ecology and ecological stoichiometry: a global synthesis. Ecology 97:3460–3471CrossRefGoogle Scholar
  59. Wagenhoff A, Lange K, Townsend CR, Matthaei CD (2013) Patterns of benthic algae and cyanobacteria along twin-stressor gradients of nutrients and fine sediment: a stream mesocosm experiment. Freshw Biol 58:1849–1863CrossRefGoogle Scholar
  60. Wagner CE, McCune AR (2009) Contrasting patterns of spatial genetic structure in sympatric rock-dwelling cichlid fishes. Evolution 63:1312–1326CrossRefGoogle Scholar
  61. Wagner CE, McIntyre PB, Buels KS, Gilbert DM, Michel E (2009) Diet predicts intestine length in Lake Tanganyika’s cichlid fishes. Funct Ecol 23:1122–1131CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Biological SciencesWright State UniversityDaytonUSA
  2. 2.Center for LimnologyUniversity of WisconsinMadisonUSA
  3. 3.Sokoine University of AgricultureMorogorroTanzania

Personalised recommendations