Abstract
Aquatic macrophytes may have a significant effect on associated communities such as epiphytes and macroinvertebrates, which through the structural complexity of habitat, provide shelter, resources, and interspecific interactions. We tested the hypothesis that the structural complexity of macrophytes positively modifies epiphytes and macroinvertebrates and that the interspecific interactions of epiphytes and macrophytes positively influence macroinvertebrates by synergism of epiphyte availability and increased habitat complexity. The macrophytes presented different structural complexities, ranging from low (Cyperus articulatus), medium (Nymphaea pulchella) to high complexity (Eichhornia crassipes and Ludwigia helminthorrhiza). The richness, diversity, and biomass of epiphytes presented a significant difference and positive relationship with the increase of the structural complexity of the macrophytes. The synergism between the structural complexity of the macrophytes and the epiphytic biomass (r2 = 0.37; p = 0.0002), increased the biomass of macroinvertebrates (r2 = 0.47; p = 0.003). The functional traits of the epiphytes were directly related to the morphology of the macrophytes with the unicellular, pedunculated, and firmly adhered dominating. The dominance of these traits indicates the absence or low disturbance (e.g., rain) in the studied site. The responses of the functional characteristics of the epiphytes are important to understand ecosystem functioning and dynamics. Therefore, we conclude that epiphytes showed a positive relationship with the structural complexity of the macrophytes. Moreover, macroinvertebrates showed a positive relationship with the increased macrophyte morphological complexity and increased biomass of epiphytes. The management of macrophytes with different structural complexities can be a strategy to recover the biodiversity in tropical aquatic ecosystems.
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Data, associated metadata, and calculation tools will be made available on request to the corresponding author (ariadne_moura@hotmail.com).
References
Abràmoff MD, Magalhães PJ, Ram SJ (2004) Image Processing with ImageJ. Biophotonics Int 11:36–42
Alahuhta J (2015) Geographic patterns of lake macrophyte communities and species richness at regional scale. J Veg Sci 26:564–575
Alvares CA, Stape JL, Sentelhas PC, de Moraes G, Leonardo J, Sparovek G (2013) Köppen’s climate classification map for Brazil. Meteorol Z 22:711–728
APAC (2019) Agência Pernambucana de Águas e Climas. 2019
Bartram J, Chorus I (1999) Toxic cyanobacteria in water: a guide to their public health consequences, monitoring and management. CRC Press
Bell N, Riis T, Suren AM, Baattrup-Pedersen A (2013) Distribution of invertebrates within beds of two morphologically contrasting stream macrophyte species. Fundamental and Applied Limnology/Archiv für. Hydrobiologie 183:309–321
Biggs BJ, Stevenson RJ, Lowe RL (1998) A habitat matrix conceptual model for stream periphyton. Arch Hydrobiol 143:21–56
Carr JM, Hergenrader GL, Troelstrup NH Jr (1986) A simple, inexpensive method for cleaning diatoms. Trans Am Microsc Soc 105:152–157
Casartelli MR, Ferragut C (2015) Influence of seasonality and rooted aquatic macrophyte on periphytic algal community on artificial substratum in a shallow tropical reservoir. Int Rev Hydrobiol 100:158–168
Casartelli MR, Ferragut C (2018) The effects of habitat complexity on periphyton biomass accumulation and taxonomic structure during colonization. Hydrobiologia 807:233–246. https://doi.org/10.1007/s10750-017-3396-8
Chessel D, Dufour AB, Thioulouse J (2004) The ade4 package-I-One-table methods. R News 4:5–10
Choi J-Y, Jeong K-S, La G-H, Kim S-K, Joo G-J (2014) Sustainment of epiphytic microinvertebrate assemblage in relation with different aquatic plant microhabitats in freshwater wetlands (South Korea). J Limnol 73:197–202
Choudhury MI, McKie BG, Hallin S, Ecke F (2018) Mixtures of macrophyte growth forms promote nitrogen cycling in wetlands. Sci Total Environ 635:1436–1443. https://doi.org/10.1016/j.scitotenv.2018.04.193
Colwell RK, Chao A, Gotelli NJ, Lin SY, Mao CX, Chazdon RL, Longino JT (2012) Models and estimators linking individual-based and sample-based rarefaction, extrapolation and comparison of assemblages. J Plant Ecol 5:3–21
Cottingham KL, Carpenter SR (1998) Population, community, and ecosystem variates as ecological indicators: phytoplankton responses to whole-lake enrichment. Ecol Appl 8:508–530
Cunha DGF, do Carmo Calijuri M, Lamparelli MC (2013) A trophic state index for tropical/subtropical reservoirs (TSItsr). Ecol Eng 60:126–134
da Silva CV, Henry R (2020) Aquatic macroinvertebrate assemblages associated with two floating macrophyte species of contrasting root systems in a tropical wetland. Limnology 21:107–118
da Costa MRA, Attayde JL, Becker V (2016) Effects of water level reduction on the dynamics of phytoplankton functional groups in tropical semi-arid shallow lakes. Hydrobiologia 778:75–89
Diarra B, Konan KJ, Yapo LM, Kouassi KP (2018) Aquatic macroinvertebrates associated with free-floating macrophytes in a marginal lentic ecosystem (Ono Lagoon, Côte d’Ivoire). J Entomol Zool Stud 6:1432–1441
Dolédec S, Chessel D, Ter Braak C, Champely S (1996) Matching species traits to environmental variables: a new three-table ordination method. Environ Ecol Stat 3:143–166
dos Santos TR, Ferragut C, de Mattos Bicudo CE (2013) Does macrophyte architecture influence periphyton? Relationships among Utricularia foliosa, periphyton assemblage structure and its nutrient (C, N, P) status. Hydrobiologia 714:71–83. https://doi.org/10.1007/s10750-013-1531-8
Dray S, Legendre P (2008) Testing the species traits–environment relationships: the fourth-corner problem revisited. Ecology 89:3400–3412
Dunck B, Algarte VM, Cianciaruso MV, Rodrigues L (2016) Functional diversity and trait–environment relationships of periphytic algae in subtropical floodplain lakes. Ecol Indic 67:257–266
Ettl H (1978) Xanthophyceae. 1. Süßwasserflora von Mitteleuropa, 3 Stuttgart & New York
Fernandes UL, Oliveira ECC, Lacerda SR (2016) Role of macrophyte life forms in driving periphytic microalgal assemblages in a Brazilian reservoir. J Limnol 75:44–51
Ferreiro N, Feijoó C, Giorgi A, Leggieri L (2011) Effects of macrophyte heterogeneity and food availability on structural parameters of the macroinvertebrate community in a Pampean stream. Hydrobiologia 664:199–211
Ferreiro N, Giorgi A, Feijoó C (2013) Effects of macrophyte architecture and leaf shape complexity on structural parameters of the epiphytic algal community in a Pampean stream. Aquat Ecol 47:389–401
Fontanarrosa MS, Chaparro GN, O’Farrell I (2013) Temporal and spatial patterns of macroinvertebrates associated with small and medium-sized free-floating plants. Wetlands 33:47–63
Gianuca AT, Declerck SAJ, Lemmens P, De Meester L (2017) Effects of dispersal and environmental heterogeneity on the replacement and nestedness components of β-diversity. Ecology 98:525–533
Gosselain V, Hudon C, Cattaneo A, Gagnon P, Planas D, Rochefort D (2005) Physical variables driving epiphytic algal biomass in a dense macrophyte bed of the St. Lawrence River (Quebec, Canada). Hydrobiologia 534:11–22
Graham LE, Wilcox LW (2000) Algae. Prentice-Hall, Upper Saddle River
Grutters BM, Pollux BJ, Verberk WC, Bakker ES (2015) Native and non-native plants provide similar refuge to invertebrate prey, but less than artificial plants. PLoS ONE 10:e0124455
Halley J, Hartley S, Kallimanis A, Kunin W, Lennon J, Sgardelis S (2004) Uses and abuses of fractal methodology in ecology. Ecol Lett 7:254–271
Hao B, Wu H, Cao Y, Xing W, Jeppesen E, Li W (2017) Comparison of periphyton communities on natural and artificial macrophytes with contrasting morphological structures. Freshw Biol 62:1783–1793
Heino J, Schmera D, Erős T (2013) A macroecological perspective of trait patterns in stream communities. Freshw Biol 58:1539–1555
Hillebrand H, Dürselen CD, Kirschtel D, Pollingher U, Zohary T (1999) Biovolume calculation for pelagic and benthic microalgae. J Phycol 35:403–424
Jeppesen E et al (2005) Lake responses to reduced nutrient loading–an analysis of contemporary long-term data from 35 case studies. Freshw Biol 50:1747–1771
Jeppesen E et al (2014) Climate change impacts on lakes: an integrated ecological perspective based on a multi-faceted approach, with special focus on shallow lakes. J Limnol 73:88–111
John DM, Whiton BA, Brook AJ (2002) The freshwater algal flora of the British Isles: an identification guide of freshwater and terrestrial algae. Cambridge University Press, Cambridge
Komarek J (2013) Cyanoprokaryota: heterocytous genera. 3rd Part vol 19. Springer Spektrum
Komárek J, Anagnostidis K (2005) Cyanoprokaryota 2. Teil/2nd part: oscillatoriales. Susswasserflora Von Mitteleuropa 19:1–759
Komárek J, Cronberg G (2001) Some chroococcalean and oscillatorialean Cyanoprokaryotes from southern African lakes, ponds and pools. Nova Hedwigia 73:129–160
Koroleff F (1976) Determination of nutrients. In: Grasshoff K (ed) Methods of seawater 297 analysis. Verlag Chemie, Weinheim
Krammer K, Lange-Bertalot H (1991a) Bacillariophyceae 3 Centrales, Fragilariaceae, Eunotiaceae. In: Ettl H, Gerloff J, Heynig H, Mollenhauer D (eds) Susswaser flora von Mitteleuropa. Gustav Fischer, Stutgart, p 576
Krammer K, Lange-Bertalot H (1991b) Bacillariophyceae. 4. Achnanthaceae; kritische Ergänzungen zu Navicula (Lineolatae) und Gomphonema; Gesamtliteraturverzeichnis Teil. In: Ettl H, Gerloff J, Heynig H, Mollenhauer D (eds) Sübwasserflora von Mitlleuropa. Gustav Fischer, Stutgart, p 437
Lange K, Liess A, Piggott JJ, Townsend CR, Matthaei CD (2011) Light, nutrients and grazing interact to determine stream diatom community composition and functional group structure. Freshw Biol 56:264–278
Li J, Yang X, Wang Z, Shan Y, Zheng Z (2015) Comparison of four aquatic plant treatment systems for nutrient removal from eutrophied water. Biores Technol 179:1–7
Louault F, Pillar V, Aufrere J, Garnier E, Soussana JF (2005) Plant traits and functional types in response to reduced disturbance in a semi-natural grassland Journal of vegetation. Science 16:151–160
Lucena-Moya P, Duggan IC (2011) Macrophyte architecture affects the abundance and diversity of littoral microfauna. Aquat Ecol 45:279–287
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
Lv T, He Q, Hong Y, Liu C, Yu D (2019) Effects of water quality adjusted by submerged macrophytes on the richness of the epiphytic algal community. Front Plant Sci 9:1–8
MacArthur RH, MacArthur JW (1961) On bird species diversity. Ecology 42:594–598
Mackereth FJH, Heron J, Talling JF (1978) Water analysis: some revised methods for limnologists. Freshw Biol Assoc Sci Pub 36:117
Magurran A (2004) Measuring biological diversity. Blackwell Pub, Oxford, p 260
Mamani A, Koncurat M, Boveri M (2019) Combined effects of fish and macroinvertebrate predation on zooplankton in a littoral mesocosm experiment. Hydrobiologia 829:19–29
Matsuda JT, Lansac-Tôha FA, Martens K, Velho LFM, Mormul RP, Higuti J (2015) Association of body size and behavior of freshwater ostracods (Crustacea, Ostracoda) with aquatic macrophytes. Aquat Ecol 49:321–331. https://doi.org/10.1007/s10452-015-9527-2
Munguia P, Osman RW, Hamilton J, Whitlatch R, Zajac R (2011) Changes in habitat heterogeneity alter marine sessile benthic communities. Ecol Appl 21:925–935
Oksanen J (2011) Vegan : community ecology package. R package version 1.17–9 https://cranr-projectorg/package=vegan
Osgood RA (2017) Inadequacy of best management practices for restoring eutrophic Lakes in the United States: guidance for policy and practice. Inland Waters 7:401–407. https://doi.org/10.1080/20442041.2017.1368881
Osório NC, Cunha ER, Tramonte RP, Mormul RP, Rodrigues L (2019) Habitat complexity drives the turnover and nestedness patterns in a periphytic algae community. Limnology 20:297–307
Passy SI, Blanchet FG (2007) Algal communities in human-impacted stream ecosystems suffer beta-diversity decline. Divers Distrib 13:670–679. https://doi.org/10.1111/j.1472-4642.2007.00361.x
Pérez GR (1988) Guía para el Estudio de los Macroinvertebrados Acuáticos del Departamento de Antioquia. Fondo Fen Colombia/Colciencias/Universidad de Antioquia, Antioquia
Pettit NE, Ward DP, Adame MF, Valdez D, Bunn SE (2016) Influence of aquatic plant architecture on epiphyte biomass on a tropical river floodplain. Aquat Bot 129:35–43. https://doi.org/10.1016/j.aquabot.2015.12.001
Pierre JI, Kovalenko KE (2014) Effect of habitat complexity attributes on species richness. Ecosphere 5:1–10
Popovsky JL, Pfiester A (1990) Dinophyceae Dinoflagellida. In: Mollenhauer (ed) Sübwasser flora von Mitteleuropa. Gustav Fischer Verlag, Sttugart, pp 1–272
Prescott GW, Vinyard WC (1982) A Synopsis of North American Desmids. University of Nebraska Press, Nebraska
R Core Team (2014) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. URL http://www.R-project.org/
Rangel LM, Soares MCS, Paiva R, Silva LHS (2016) Morphology-based functional groups as effective indicators of phytoplankton dynamics in a tropical cyanobacteria-dominated transitional river–reservoir system. Ecol Indic 64:217–227. https://doi.org/10.1016/j.ecolind.2015.12.041
Rennie MD, Jackson LJ (2005) The influence of habitat complexity on littoral invertebrate distributions: patterns differ in shallow prairie lakes with and without fish. Can J Fish Aquat Sci 62:2088–2099
Ros J (1979) Práctica de Ecologia. Omega, Barcelona
Scheffer M, Hosper SH, Meijer ML, Moss B, Jeppesen E (1993) Alternative equilibria in shallow lakes. Trends Ecol Evol 8:275–279. https://doi.org/10.1016/0169-5347(93)90254-M
Schneck F, Schwarzbold A, Melo AS (2011) Substrate roughness affects stream benthic algal diversity, assemblage composition, and nestedness. J N Am Benthol Soc 30:1049–1056
Schuler MS, Chase JM, Knight TM (2017) Habitat size modulates the influence of heterogeneity on species richness patterns in a model zooplankton community. Ecology 98:1651–1659
Seto M, Takamura N, Iwasa Y (2013) Individual and combined suppressive effects of submerged and floating-leaved macrophytes on algal blooms. J Theor Biol 319:122–133. https://doi.org/10.1016/j.jtbi.2012.11.016
Sládecková A, Sládecek V (1977) Periphyton as indicator of the reservoir water quality II - pseudo-periphyton. Arch Hydrobiol 19:176–191
Squires MM, Lesack LFW, Hecky RE, Guildford SJ, Ramlal P, Higgins SN (2009) Primary production and carbon dioxide metabolic balance of a Lake-Rich Arctic River floodplain: partitioning of phytoplankton, Epipelon, Macrophyte, and Epiphyton Production among Lakes on the Mackenzie Delta. Ecosystems 12:853–872. https://doi.org/10.1007/s10021-009-9263-3
Strickland JDH, Parsons TRA (1972) A pratical handbook of seawater analysis. B Fish Res Board Can 125:1–310
Sugihara G, May RM (1990) Applications of fractals in ecology. Trends Ecol Evol 5:79–86. https://doi.org/10.1016/0169-5347(90)90235-6
Sultana M, Asaeda T, Azim ME, Fujino T (2010) Morphological responses of a submerged macrophyte to epiphyton. Aquat Ecol 44:73–81
Taniguchi H, Nakano S, Tokeshi M (2003) Influences of habitat complexity on the diversity and abundance of epiphytic invertebrates on plants. Freshw Biol 48:718–728. https://doi.org/10.1046/j.1365-2427.2003.01047.x
Tarkowska-Kukuryk M, Toporowska M (2021) Long-term responses of epiphytic midges (Diptera, Chironomidae) to emergent macrophytes removal and P concentrations in a shallow hypertrophic lake ecosystem. Sci Total Environ 750:141508
Thomaz SM, Cunha ERD (2010) The role of macrophytes in habitat structuring in aquatic ecosystems: methods of measurement, causes and consequences on animal assemblages’ composition and biodiversity. Acta Limnol Bras 22:218–236
Thomaz SM, Dibble ED, Evangelista LR, Higuti J, Bini LM (2008) Influence of aquatic macrophyte habitat complexity on invertebrate abundance and richness in tropical lagoons. Freshw Biol 53:358–367. https://doi.org/10.1111/j.1365-2427.2007.01898.x
Tokeshi M, Arakaki S (2012) Habitat complexity in aquatic systems: fractals and beyond. Hydrobiologia 685:27–47
Trivinho-Strixino S (2011) Chironomidae (Insecta, Diptera, Nematocera) do Estado de São Paulo, Sudeste Do Brasil. Biota Neotrop 11:675–684
Tuji A (2000) Observation of developmental processes in loosely attached diatom (Bacillariophyceae) communities. Phycol Res 48:75–84. https://doi.org/10.1046/j.1440-1835.2000.00188.x
Utermöhl H (1958) Zur Vervollkommnung der quantitativen 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
Walker PD, Wijnhoven S, van der Velde G (2013) Macrophyte presence and growth form influence macroinvertebrate community structure. Aquat Bot 104:80–87. https://doi.org/10.1016/j.aquabot.2012.09.003
Wolters JW, Verdonschot RCM, Schoelynck J, Verdonschot PFM, Meire P (2018) The role of macrophyte structural complexity and water flow velocity in determining the epiphytic macroinvertebrate community composition in a lowland stream. Hydrobiologia 806:157–173
Zhou X, He Z, Jones KD, Li L, Stoffella PJ (2017) Dominating aquatic macrophytes for the removal of nutrients from waterways of the Indian River Lagoon basin, South Florida, USA. Ecol Eng 101:107–119
Zhu L, Li Z, Ketola T (2011) Biomass accumulations and nutrient uptake of plants cultivated on artificial floating beds in China’s rural area. Ecol Eng 37:1460–1466
Acknowledgements
We thank the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for a productivity Grant to ANM (Process 304237/2015-9), and the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brazil (CAPES)—Finance Code 001. We also thank Cihelio Alves Amorim from the Federal Rural University of Pernambuco, Brazil, for his significant contribution to the revision of the text.
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do Nascimento Filho, S.L., Gama, W.A. & do Nascimento Moura, A. Effect of the structural complexity of aquatic macrophytes on epiphytic algal, macroinvertebrates, and their interspecific relationships. Aquat Sci 83, 57 (2021). https://doi.org/10.1007/s00027-021-00812-9
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DOI: https://doi.org/10.1007/s00027-021-00812-9