Abstract
Top-chain predators play a fundamental role in the functioning of shallow reservoirs. Studies to elucidate the cascade effects produced by fish on macroinvertebrates and periphytic algae are fundamental for understanding the functioning of aquatic ecosystems. We conducted an enclosure experiment to test the isolated and combined effects of macroinvertebrates and Prochilodus brevis (omnivorous fish) on periphytic algae and the floating macrophyte Eichhornia crassipes for 30 days in the Jazigo reservoir, Brazil. The predation of P. brevis on macroinvertebrates increased the biomass of periphytic algae during the experiment, while the effects of isolated macroinvertebrates decreased the biomass of periphytic algae and increased the biomass of E. crassipes. Macroinvertebrates (which freely colonized the enclosures) were reduced by fish; however, the biomass of the periphytic algae was not reduced. Our results showed that P. brevis has strong effects on the structure of macroinvertebrate and periphytic algae communities, with a visible cascade effect on the abundance of macroinvertebrates. This study contributes to our understanding of the ecology of tropical lakes and the regulation of periphytic algae and macrophyte growth.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Availability of data and material
Data, associated metadata and calculation tools will be made available on request to the corresponding author (ariadne_moura@hotmail.com).
References
Agência Pernambucana de Águas e Climas – APAC (2019). http://www.apac.pe.gov.br. Accessed 20 Mar 2019
Aguilera MA, Valdivia N, Broitman BR (2015) Herbivore-alga interaction strength influences spatial heterogeneity in a kelp-dominated intertidal community. PloS one 10:e0137287-e0137287. https://doi.org/10.1371/journal.pone.0137287
Akinbile CO, Yusoff MS (2012) Assessing water hyacinth (Eichhornia crassipes) and lettuce (Pistia stratiotes) effectiveness in aquaculture wastewater treatment. Int. J. Phytoremediation 14:201–211. https://doi.org/10.1080/15226514.2011.587482
Almeida V, Dantas Ê, Melo-Júnior M, Bittencourt-Oliveira M, Moura A (2009) Zooplanktonic community of six reservoirs in northeast Brazil. Braz J Biol 69:57–65. https://doi.org/10.1590/S1519-69842009000100007
Alvares CA, Stape JL, Sentelhas PC, de Moraes Gonçalves JL, Sparovek G (2013) Köppen's climate classification map for Brazil. Meteorol Z 22:711–728. https://doi.org/10.1127/0941-2948/2013/0507
Barker JE, HutchensJr. JJ, Luken JO (2014) Macroinvertebrates associated with water hyacinth roots and a root analog. Freshw Sci 33:159–167. https://doi.org/10.1086/674173
Basen T, Martin-Creuzburg D, Rothhaupt K-O (2011) Role of essential lipids in determining food quality for the invasive freshwater clam Corbicula fluminea. J N AM BENTHOL SOC 30:653–664. https://doi.org/10.1899/10-087.1
Bezerra LAV, Angelini R, Vitule JRS, Coll M, Sánchez-Botero JI (2018) Food web changes associated with drought and invasive species in a tropical semiarid reservoir. Hydrobiologia 817:475–489. https://doi.org/10.1007/s10750-017-3432-8
Cao Y, Li W, Jeppesen E (2014) The response of two submerged macrophytes and periphyton to elevated temperatures in the presence and absence of snails: a microcosm approach. Hydrobiologia 738:49–59. https://doi.org/10.1007/s10750-014-1914-5
Carey MP, Wahl DH (2010) Native fish diversity alters the effects of an invasive species on food webs. Ecology 91:2965–2974. https://doi.org/10.1890/09-1213.1
Carpenter SR, Cole JJ, Hodgson JR, Kitchell JF, Pace ML, Bade D, Cottingham KL, Essington TE, Houser JN, Schindler DE (2001) Trophic cascades, nutrients, and lake productivity: whole-lake experiments. Ecol Monogr 71:163–186. https://doi.org/10.1890/0012-9615(2001)071[0163:TCNALP]2.0.CO;2
Chellappa S, Bueno RM, Chellappa T, Chellappa NT, Val VMF (2009) Reproductive seasonality of the fish fauna and limnoecology of semi-arid Brazilian reservoirs. Limnologica 39:325–329. https://doi.org/10.1016/j.limno.2009.06.003
Chen J et al (2020) Effects of benthivorous fish disturbance and snail herbivory on water quality and two submersed macrophytes. Sci Total Environ 713:136734. https://doi.org/10.1016/j.scitotenv.2020.136734
Chirwa ER, Mtethiwa A, Jere WL, Kassam D (2019) Effects of common carp and African catfish on plankton, periphyton, benthic macroinvertebrates in pond ecosystem. Aquat Biol 28:91–100. https://doi.org/10.3354/ab00713
Cochran-Biederman JL, Wyman KE, French WE, Loppnow GL (2015) Identifying correlates of success and failure of native freshwater fish reintroductions. Conserv Biol 29:175–186. https://doi.org/10.1111/cobi.12374
Coetzee JA, Jones RW, Hill MP (2014) Water hyacinth, Eichhornia crassipes (Pontederiaceae), reduces benthic macroinvertebrate diversity in a protected subtropical lake in South Africa. Biodivers Conserv 23:1319–1330. https://doi.org/10.1007/s10531-014-0667-9
Dantas DDF, Rubim PL, de Oliveira FA, da Costa MRA, de Moura CGB, Teixeira LH, Attayde JL (2019) Effects of benthivorous and planktivorous fish on phosphorus cycling, phytoplankton biomass and water transparency of a tropical shallow lake. Hydrobiologia 829:31–41. https://doi.org/10.1007/s10750-018-3613-0
Demi LM, Simon KS, Stephen M. Coghlan J, Saunders R, Anderson D (2012) Anadromous alewives in linked lake–stream ecosystems: do trophic interactions in lakes influence stream invertebrate communities? Freshw Sci 31:973–985. https://doi.org/10.1899/11-124.1
DeMott WR, Gulati RD, Van Donk E (2001) Daphnia food limitation in three hypereutrophic Dutch lakes: Evidence for exclusion of large-bodied species by interfering filaments of cyanobacteria. Limnol Oceanog 46:2054–2060. https://doi.org/10.4319/lo.2001.46.8.2054
Detmer TM, Wahl DH (2019) Trophic cascade strength is influenced by size frequency distribution of primary consumers and size-selective predation: examined with mesocosms and modeling. Aquat Sci 81:52. https://doi.org/10.1007/s00027-019-0648-x
Dunck B, Amaral DC, Fernandes UL, Santana NF, Lopes TM, Rodrigues L (2018) Herbivory effects on the periphytic algal functional diversity in lake ecosystems: an experimental approach. Hydrobiologia 816:231–241. https://doi.org/10.1007/s10750-018-3587-y
Fang L, Wong PK, Lin L, Lan C, Qiu JW (2010) Impact of invasive apple snails in Hong Kong on wetland macrophytes, nutrients, phytoplankton and filamentous algae. Freshw Biol 55:1191–1204. https://doi.org/10.1111/j.1365-2427.2009.02343.x
Ferragut C, de Campos BD (2010) Periphytic algal community adaptive strategies in N and P enriched experiments in a tropical oligotrophic reservoir. Hydrobiologia 646:295–309. https://doi.org/10.1007/s10750-010-0168-0
Ger KA, Urrutia-Cordero P, Frost PC, Hansson L-A, Sarnelle O, Wilson AE, Lürling M (2016) The interaction between cyanobacteria and zooplankton in a more eutrophic world. Harmful Algae 54:128–144. https://doi.org/10.1016/j.hal.2015.12.005
Gordillo-Guerra JG, Guevara G, Reinoso-Flórez G (2020) A practical device for evaluating periphyton colonization dynamics in tropical shallow wetlands. Limnologica 81:125755. https://doi.org/10.1016/j.limno.2020.125755
Groendahl S, Fink P (2017) High dietary quality of non-toxic cyanobacteria for a benthic grazer and its implications for the control of cyanobacterial biofilms. BMC Ecology 17:1–17. https://doi.org/10.1186/s12898-017-0130-3
Gurgel LdL, Verani JR, Chellappa S (2012) Reproductive ecology of Prochilodus brevis an endemic fish from the semiarid region of Brazil. Sci World J. https://doi.org/10.1100/2012/810532
Hedges LV, Gurevitch J, Curtis PS (1999) The meta-analysis of response ratios in experimental ecology. Ecology 80:1150–1156. https://doi.org/10.1890/0012-9658(1999)080[1150:tmaorr]2.0.co;2
Hilborn ED, Beasley VR (2015) One health and cyanobacteria in freshwater systems: animal illnesses and deaths are sentinel events for human health risks. Toxins 7:1374–1395. https://doi.org/10.3390/toxins7041374
Hillebrand H (2009) Meta-analysis of grazer control of periphyton biomass across aquatic ecosystems. J Phycol 45:798–806. https://doi.org/10.1111/j.1529-8817.2009.00702.x
Hillebrand H, Dürselen CD, Kirschtel D, Pollingher U, Zohary T (1999) Biovolume calculation for pelagic and benthic microalgae. J Phycol 35:403–424. https://doi.org/10.1046/j.1529-8817.1999.3520403.x
Hillebrand H, Kahlert M, Haglund A-L, Berninger U-G, Nagel S, Wickham S (2002) Control of microbenthic communities by grazing and nutrient supply. Ecology 83:2205–2219. https://doi.org/10.1890/0012-9658(2002)083[2205:comcbg]2.0.co;2
Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biometrical Journal: Journal of Mathematical Methods in Biosciences 50:346–363. https://doi.org/10.1002/bimj.200810425
Iglesias C et al (2017) Fish but not macroinvertebrates promote trophic cascading effects in high density submersed plant experimental lake food webs in two contrasting climate regions. Water 9:1–17. https://doi.org/10.3390/w9070514
James CS, Eaton JW, Hardwick K (2006) Responses of three invasive aquatic macrophytes to nutrient enrichment do not explain their observed field displacements. Aquat Bot 84:347–353. https://doi.org/10.1016/j.aquabot.2006.01.002
Jeppesen E et al (2011) Zooplankton as indicators in lakes: a scientific-based plea for including zooplankton in the ecological quality assessment of lakes according to the European Water Framework Directive (WFD). Hydrobiologia 676:279–297. https://doi.org/10.1007/s10750-011-0831-0
Jeppesen E, Lauridsen TL, Mitchell SF, Christoffersen K, Burns CW (2000) Trophic structure in the pelagial of 25 shallow New Zealand lakes: changes along nutrient and fish gradients. J Plankton Res 22:951–968. https://doi.org/10.1093/plankt/22.5.951
Jeppesen E, Mehner T, Winfield IJ, Kangur K, Sarvala J, Gerdeaux D, Rask M, Malmquist HJ, Holmgren K, Volta P, Romo S (2012) Impacts of climate warming on the long-term dynamics of key fish species in 24 European lakes. Hydrobiologia 694:1–39. https://doi.org/10.1007/s10750-012-1182-1
Jones JI, Sayer CD (2003) Does the fish–invertebrate–periphyton cascade precipitate plant loss in shallow lakes? Ecology 84:2155–2167. https://doi.org/10.1890/02-0422
Koroleff F (1976) Determination of nutrients. In: Grasshoff K (ed) Methods of Seawater Analysis. Verlag Chemie, Weinheim, Germany, pp 117–187
Lemmens P, Declerck SA, Tuytens K, Vanderstukken M, De Meester L (2018) Bottom-up effects on biomass versus top-down effects on identity: a multiple-lake fish community manipulation experiment. Ecosystems 21:166–177. https://doi.org/10.1007/s10021-017-0144-x
Li KY, Liu ZW, Hu YH, Yang HW (2009) Snail herbivory on submerged macrophytes and nutrient release: Implications for macrophyte management. Ecol Eng 35:1664–1667. https://doi.org/10.1016/j.ecoleng.2008.05.009
Li W et al (2019) Effects of nutrient enrichment and Bellamya aeruginosa (Reeve) presence on three submerged macrophytes. Hydrobiologia 833:95–105. https://doi.org/10.1007/s10750-019-3884-0
Liboriussen L, Jeppesen E, Bramm ME, Lassen MF (2005) Periphyton-macroinvertebrate interactions in light and fish manipulated enclosures in a clear and a turbid shallow lake. Aquat Ecol 39:23–39. https://doi.org/10.1007/s10452-004-3039-9
Lund J, Kipling C, Le Cren E (1958) The inverted microscope method of estimating algal numbers and the statistical basis of estimations by counting. Hydrobiologia 11:143–170. https://doi.org/10.1007/BF00007865
Mackereth FJH, Heron J, Talling JF (1978) Water analysis: some revised methods for limnologists. Scientific Publications
Maunder MN, Punt AE (2004) Standardizing catch and effort data: a review of recent approaches. Fish Res 70:141–159. https://doi.org/10.1016/j.fishres.2004.08.002
Mazzeo N et al (2010) Trophic cascade effects of Hopliasmalabaricus (Characiformes, Erythrinidae) in subtropical lakes food webs: a mesocosm approach. Hydrobiologia 644:325–335. https://doi.org/10.1007/s10750-010-0197-8
McCollum EW, Crowder LB, McCollum SA (1998) Complex interactions of fish, snails, and littoral zone periphyton. Ecology 79:1980–1994. https://doi.org/10.1890/0012-9658(1998)079[1980:ciofsa]2.0.co;2
McCormick PV, Stevenson RJ (1991) Mechanisms of Benthic Algal Succession in Lotic Environments. Ecology 72:1835–1848. https://doi.org/10.2307/1940982
Menezes RF, Attayde JL, Lacerot G, Kosten S, Souza LC, Costa LS, Van Nes EH, Jeppesen E (2012) Lower biodiversity of native fish but only marginally altered plankton biomass in tropical lakes hosting introduced piscivorous Cichla cf. ocellaris. Biol Invasions 14:1353–1363. https://doi.org/10.1007/s10530-011-0159-8
Merritt RW, Cummins KW, Berg MB (2017) Trophic relationships of macroinvertebrates. In: Hauer FR, Lamberti GA (eds) Methods in Stream Ecology, 3a edn. Academic Press, Boston, pp 413–433
Mo S, Zhang X, Tang Y, Liu Z, Kettridge N (2017) Effects of snails, submerged plants and their coexistence on eutrophication in aquatic ecosystems. Knowl Manag Aquat Ecosyst 418:44–50. https://doi.org/10.1051/kmae/2017034
Monnerjahn U (2011) Atlantic Salmon (Salmo salar L.) re-introduction in Germany: a status report on national programmes and activities. J Appl Ichthyol 27:33–40. https://doi.org/10.1111/j.1439-0426.2011.01849.x
Mormul RP, Ahlgren J, Brönmark C (2018) Snails have stronger indirect positive effects on submerged macrophyte growth attributes than zooplankton. Hydrobiologia 807:165–173. https://doi.org/10.1007/s10750-017-3391-0
Morris K, Bailey PC, Boon PI, Hughes L (2003) Alternative stable states in the aquatic vegetation of shallow urban lakes. II. Catastrophic loss of aquatic plants consequent to nutrient enrichment. Mar Freshw Res 54:201–215. https://doi.org/10.1071/MF02003
Moulton TP, Souza ML, Silveira RML, Krsulovic FAM, Silveira MP, de Assis JCF, Francischetti CN (2010) Patterns of periphyton are determined by cascading trophic relationships in two neotropical streams. Mar Freshw Res 61:57–64. https://doi.org/10.1071/MF08326
Munubi RN, McIntyre PB, Vadeboncoeur Y (2018) Do grazers respond to or control food quality? Cross-scale analysis of algivorous fish in littoral Lake Tanganyika. Oecologia 188:889–900. https://doi.org/10.1007/s00442-018-4240-1
Nagdali SS, Gupta PK (2002) Impact of mass mortality of a mosquito fish, Gambusia affinis on the ecology of a fresh water eutrophic lake (Lake Naini Tal, India). Hydrobiologia 468:45–51. https://doi.org/10.1023/A:1015270206187
Nieoczym M, Kloskowski J (2015) Responses of epibenthic and nektonic macroinvertebrate communities to a gradient of fish size in ponds. J Limnol 74:50–62. https://doi.org/10.4081/jlimnol.2014.981
O’Farrell I, De Tezanos PP, Rodríguez PL, Chaparro G, Pizarro HN (2009) Experimental evidence of the dynamic effect of free-floating plants on phytoplankton ecology. Freshw Biol 54:363–375. https://doi.org/10.1111/j.1365-2427.2008.02117.x
Ousterhout BH, Graham SR, Hasik AZ, Serrano M, Siepielski AM (2018) Past selection impacts the strength of an aquatic trophic cascade. Funct Ecol 32:1554–1562. https://doi.org/10.1111/1365-2435.13102
Pinheiro J, Bates D, DebRoy S, Sarkar D, Heisterkamp S, Van Willigen B, Maintainer R (2017) Package ‘nlme’ Linear and nonlinear mixed effects models, version 3
Ripple WJ, Estes JA, Schmitz OJ, Constant V, Kaylor MJ, Lenz A, Motley JL, Self KE, Taylor DS, Wolf C (2016) What is a trophic cascade? Trends Ecol Evol 31:842–849. https://doi.org/10.1016/j.tree.2016.08.010
Ros, J (1979) Práctica de Ecologia. Barcelona, Omega
Santos TRd, Ferragut C (2018) Changes in the taxonomic structure of periphytic algae on a free-floating macrophyte (Utricularia foliosa L.) in relation to macrophyte richness over seasons. Acta Bot Brasilica 32:595–601. https://doi.org/10.1590/0102-33062018abb0031
Sekar R, Nair KVK, Rao VNR, Venugopalan VP (2002) Nutrient dynamics and successional changes in a lentic freshwater biofilm. Freshw Biol 47:1893–1907. https://doi.org/10.1046/j.1365-2427.2002.00936.x
Shurin JB (2001) Interactive effects of predation and dispersal on zooplankton communities. Ecology 82:3404–3416. https://doi.org/10.1890/0012-9658(2001)082[3404:IEOPAD]2.0.CO;2
Smith SDP (2014) The roles of nitrogen and phosphorus in regulating the dominance of floating and submerged aquatic plants in a field mesocosm experiment. Aquat Bot 112:1–9. https://doi.org/10.1016/j.aquabot.2013.07.001
Stevenson RJ (1996) An introduction to algal ecology in freshwater benthic habitats. Algal ecology Freshw Benth Ecosystems 2:3–30
Stevenson CF, Demes KW, Salomon AK (2016) Accounting for size-specific predation improves our ability to predict the strength of a trophic cascade. Ecol Evol 6:1041–1053. https://doi.org/10.1002/ece3.1870
Strandberg U, Taipale SJ, Hiltunen M, Galloway AWE, Brett MT, Kankaala P (2015) Inferring phytoplankton community composition with a fatty acid mixing model. Ecosphere 6:1–18. https://doi.org/10.1890/ES14-00382.1
Strickland, JDH, Parsons, TRA (1972) A practical handbook of seawater analysis. B Fish Res Board Can
Symons CC, Shurin JB (2016) Climate constrains lake community and ecosystem responses to introduced predators. Proceedings of the Royal Society B: Biol Sci 283:20160825. https://doi.org/10.1098/rspb.2016.0825
Taylor BW, Flecker AS, Hall RO (2006) Loss of a harvested fish species disrupts carbon flow in a diverse tropical river. Science 313:833–836. https://doi.org/10.1126/science.1128223
Teixeira-de Mello F, Meerhoff M, Pekcan-Hekim Z, Jeppesen E (2009) Substantial differences in littoral fish community structure and dynamics in subtropical and temperate shallow lakes. Freshw Biol 54:1202–1215. https://doi.org/10.1111/j.1365-2427.2009.02167.x
Utermöhl H (1958) Zur Vervolkomnung der quantitative Phytoplankton-Methodik. Mitt Int Ver Theor Angew Limnol 9:1–38. https://doi.org/10.1080/05384680.1958.11904091
Vadeboncoeur Y, Power ME (2017) Attached algae: the cryptic base of inverted trophic pyramids in freshwaters. Annu Rev Ecol Evol Syst 48:255–279. https://doi.org/10.1146/annurev-ecolsys-121415-032340
Vander Zanden MJ, Vadeboncoeur Y (2002) Fishes as integrators of benthic and pelagic food webs in lakes. Ecology 83:2152–2161. https://doi.org/10.1890/0012-9658(2002)083[2152:faioba]2.0.co;2
Vercellino IS, Bicudo DdC (2006) Sucessão da comunidade de algas perifíticas em reservatório oligotrófico tropical (São Paulo, Brasil): comparação entre período seco e chuvoso. Braz J Bot 29:363–377. https://doi.org/10.1590/S0100-84042006000300004
Warfe DM, Barmuta LA (2006) Habitat structural complexity mediates food web dynamics in a freshwater macrophyte community. Oecologia 150:141–154. https://doi.org/10.1007/s00442-006-0505-1
Yang L et al (2020) Mesocosm experiment reveals a strong positive effect of snail presence on macrophyte growth, resulting from control of epiphyton and nuisance filamentous algae: Implications for shallow lake management. Sci Total Environ 705:135958. https://doi.org/10.1016/j.scitotenv.2019.135958
Ye J, Tang Y, Zhang X, Zhong P, Liu Z (2019) Omnivorous shrimp Neocaridina denticulata sinensis enhances the growth of submerged macrophyte Vallisneria denseserrulata. Knowl Manag Aquat Ecosyst 420:32–37. https://doi.org/10.1051/kmae/2019025
Acknowledgements
This work was supported by the Brazilian National Council of Technological and Scientific Development-CNPq, Brazil (grant ID 305829/ 2019-0), and financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior-Brasil (CAPES)-Finance Code 001, which granted a scholarship to SLNF. We also thank the anonymous reviewers for their valuable comments and suggestions on our article.
Author information
Authors and Affiliations
Contributions
SLNF: Conceptualization, Methodology, Validation, Data curation, Formal analysis, Writing-original draft, Writing-review and editing. ADNM: Conceptualization, Supervision, Methodology, Writing-review and editing.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethics approval
The use of fish was authorized by the Animal Use Ethics Committee of the Federal Rural University of Pernambuco (Process 23082.009799/2018-70).
Research Involving Human Participants and/or Animals
The use of fish was authorized by the Animal Use Ethics Committee of the Federal Rural University of Pernambuco (Process 23082.009799/2018-70).
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Handling Editor: Vinicius Farjalla
Supplementary Information
Below is the link to the electronic supplementary material.
10452_2021_9853_MOESM1_ESM.pdf
Abiotic water limnological variables during the experiment in the Jazigo reservoir. DIN: dissolved inorganic nitrogen (± standard deviation) (PDF 15 kb)
10452_2021_9853_MOESM2_ESM.pdf
Abundance of macroinvertebrates with herbivorous, detritivorous and carnivorous eating habits during the experiment in treatments C (control), F (fish only), M (macroinvertebrates only) and MF (macroinvertebrates + fish) (PDF 14 kb)
Rights and permissions
About this article
Cite this article
do Nascimento Filho, S.L., do Nascimento Moura, A. Strong top-down effects of omnivorous fish and macroinvertebrates on periphytic algae and macrophytes in a tropical reservoir. Aquat Ecol 55, 667–680 (2021). https://doi.org/10.1007/s10452-021-09853-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10452-021-09853-6