Influence of Eichhornia crassipes (Mart) Solms on a Tropical Microcrustacean Community Based on Taxonomic and Functional Trait Diversity
Abstract
:1. Introduction
2. Materials and Methods
2.1. Experimental Design
2.2. Sampling
2.3. Functional Traits
2.3.1. Feeding Type
2.3.2. Body Size
2.3.3. Habitat Preference
2.3.4. Trophic Group
2.4. Diversity Indices
2.5. Statistical Analyses
2.5.1. Niche Complementarity
2.5.2. Potential Drivers of Functional and Species Diversity
2.5.3. Density Comparison for Species and Functional Groups
3. Results
3.1. Community Structure and Environment Variables
3.2. Density of Species and Functional Groups
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Meerhoff, M.; Mazzeo, N.; Moss, B.; Rodríguez-Gallego, L. The structuring role of free-floating versus submerged plants in a subtropical shallow lake. Aquat. Ecol. 2003, 37, 377–391. [Google Scholar] [CrossRef]
- Meerhoff, M.; Iglesias, C.; Teixeira De Mello, F.; Clemente, J.M.; Jensen, E.; Lauridsen, T.L.; Jeppesen, E. Effects of habitat complexity on community structure and predator avoidance behavior of littoral zooplankton in temperate versus subtropical shallow lakes. Freshw. Biol. 2007, 52, 1009–1021. [Google Scholar] [CrossRef]
- Debastiani-Júnior, J.R.; Elmoor-Loureiro, L.M.A.; Nogueira, M.G. Habitat architecture influencing microcrustaceans composition: A case study on freshwater Cladocera (Crustacea Branchiopoda). Braz. J. Biol. 2016, 76, 93–100. [Google Scholar] [CrossRef]
- Thomaz, S.M.; Cunha, E.R. 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. 2010, 22, 218–236. [Google Scholar] [CrossRef]
- Grzybkowska, M.; Dukowska, M.; Leszczynska, J.; Lik, J.; Szczerkowska-Majchrzak, E.; Przybylski, M. The food resources exploitation by small-sized fish in a riverine macrophyte habitat. Ecol. Indic. 2018, 90, 206–214. [Google Scholar] [CrossRef]
- Castilho-Noll, M.S.M.; Câmara, C.F.; Chicone, M.F.; Shibata, E.H. Pelagic and littoral cladocerans (Crustacea, Anomopoda and Ctenopoda) from reservoirs of the northwest of São Paulo State, Brazil. Biota Neotropica 2010, 10, 1–10. [Google Scholar] [CrossRef]
- Meerhoff, M.; Fosalba, C.; Bruzzone, C.; Mazzeo, N.; Noordoven, W.; Jeppesen, E. An experimental study of habitat choice by Daphnia: Plants signal danger more than refuge in subtropical lakes. Freshw. Biol. 2006, 51, 1320–1330. [Google Scholar] [CrossRef]
- Timms, R.M.; Moss, B. Prevention of growth of potentially dense phytoplankton populations by zooplankton grazing, in the presence of zooplanktivorous fish, in a shallow wetland ecosystem. Limnol. Oceanogr. 1984, 29, 472–486. [Google Scholar] [CrossRef]
- Burks, R.L.; Lodge, D.M.; Jeppesen, E.; Lauridsen, T.L. Diel horizontal migration of zooplankton: Costs and benefits of inhabiting the littoral. Freshw. Biol. 2002, 47, 343–365. [Google Scholar] [CrossRef]
- Patel, S. Threats, management and envisaged utilizations of aquatic weed Eichhornia crassipes: An overview. Rev. Environ. Sci. Biotechnol. 2012, 11, 249–259. [Google Scholar] [CrossRef]
- Villamagna, A.M.; Murphy, B.R. Ecological and socio-economic impacts of invasive water hyacinth (Eichhornia crassipes): A review. Frashw. Biol. 2010, 55, 282–298. [Google Scholar] [CrossRef]
- Tilman, D.; Knops, J.; Wedin, D.; Reich, P.; Ritchie, M.; Siemann, E. The Influence of Functional Diversity and Composition on Ecosystem Processes. Science 1997, 7277, 1300–1302. [Google Scholar] [CrossRef]
- Villéger, S.; Mason, N.W.H.; Mouillot, D. New Multidimensional Functional Diversity Indices for a Multifaceted Framework in Functional Ecology. Ecology 2008, 89, 2290–2301. [Google Scholar] [CrossRef] [PubMed]
- Laliberté, E.; Legendre, P. A distance-based framework for measuring functional diversity from multiple traits. Ecology 2010, 91, 299–305. [Google Scholar] [CrossRef]
- Manson, N.W.H.; Bello, F.; Mouillot, D.; Pavoine, S.; Dray, S. A guide for using functional diversity indices to reveal changes in assembly processes along ecological gradients. J. Veg. Sci. 2013, 24, 794–806. [Google Scholar] [CrossRef]
- Vejrikova, I.; Eloranta, A.P.; Vejrik, L.; Smejkal, M.; Cech, M.; Sajdlová, Z.; Frouzová, J.; Kiljunen, M.; Petarka, J. Macrophytes shape trophic niche variation among generalist fishes. PLoS ONE 2017, 12, e0177114. [Google Scholar] [CrossRef]
- Vogt, R.J.; Beisner, B.E.; Prairie, Y.T. Functional diversity is positively associated with biomass for lake diatoms. Freshw. Biol. 2010, 55, 1636–1646. [Google Scholar] [CrossRef]
- Ismael, D.; Valenti, W.C.; Matsumura-Tundisi, T.; Rocha, O. Biodiversidade do Estado de São Paulo, Brasil: Síntese do Conhecimento ao Final do Século XX. 4: Invertebrados de Água Doce, 1st ed.; Fapesp São Paulo: São Paulo, Brasil, 1999; p. 176. [Google Scholar]
- Rocha, C.M.C.; Lima, D.; Cunha, M.C.C.; Almeida, J.S. Aquatic macrophytes and trophic interactions: A scientometric analyses and research perspectives. Braz. J. Biol. 2019, 79, 617–624. [Google Scholar] [CrossRef]
- Alvares, C.A.; Stape, J.L.; Sentelhas, P.C.; de Moraes, G.; Leonardo, J.; Sparovek, G. Köppen’s climate classification map for Brazil. Meteorol. Z. 2013, 22, 711–728. [Google Scholar] [CrossRef]
- Lauridsen, T.L.; Pedersen, L.J.; Jeppesen, E.; Sondergaard, M. The importance of macrophyte bed size for cladoceran composition and horizontal migration in a shallow lake. J. Plankton Res. 1996, 18, 2283–2294. [Google Scholar] [CrossRef]
- Arcifa, M.S.; Rodrigues, R.A.; Perticarrari, A. Diel vertical migration of cladocerans in a tropical lake. Nauplius 2003, 11, 15–25. [Google Scholar]
- Maia-Barbosa, P.M.; Eskinazi-Santana, E.M.; Barbosa, F.A.R. Zooplankton composition and vertical distribution in a tropical lake (Dom Helvécio lake, Southeastern Brasil). Acta Limnol. Bras. 2003, 15, 65–74. [Google Scholar]
- Sendacz, S.; Kubo, E. Copepoda (Calanoida e Cyclopoida) de reservatórios do Estado de São Paulo. Bol. Inst. Pesca 1982, 9, 51–89. [Google Scholar]
- Reid, J.W. Chave de identificação e lista de referências bibliográficas para as espécies continentais sul-americanas de vida livre da ordem Cyclopoida (Crustacea, Copepoda). Bol. Zool. Univ. São Paulo 1985, 9, 17–143. [Google Scholar]
- Elmoor-Loureiro, L.M.A. Manual de Identificação de Cladóceros Límnicos do Brasil, 1st ed.; Editora Universa: São Paulo, Brasil, 1997; p. 155. [Google Scholar]
- McCauley, E. The estimation of the abundance and biomass of zooplankton in samples. In A Manual on Methods for the Assessment of Secundary Productivity in FreshWaters, 2nd.; Downing, J.A., Rigler, F.H., Eds.; Blackwell Scientific Publications: Oxford, UK, 1984; Volume 17, pp. 228–265. [Google Scholar]
- Barnett, A.J.; Finlay, K.B.; Beisner, E. Functional diversity of crustacean zooplankton communities: Towards a trait-based classification. Freshw. Biol. 2007, 52, 796–813. [Google Scholar] [CrossRef]
- DeMott, W.; Kerfoot, W.C. Competition among cladocerans: Nature of the interaction between Bosmina and Dapnhia. Ecology 1982, 63, 1949–1966. [Google Scholar] [CrossRef]
- Fryer, G. Evolution and the Adaptive Radiation in the Chydoridae (Crustacea, Cladocera): A Study in Comparative Functional Morphology and Ecology. Philos. Trans. R. Soc. Lond. B Biol. Sci. 1968, 254, 221–382. [Google Scholar] [CrossRef]
- Dole-Olivier, M.J.; Galassi, D.M.P.; Marmonier, P.; Creuzé Des ChâTelliers, M. The biology and ecology of lotic microcrustaceans. Freshw. Biol. 2000, 44, 63–91. [Google Scholar] [CrossRef]
- Orlova-Bienkowskaja, M.Y. Cladocera: Anomopoda, Daphiniidae: Genus Simocephalus. In Guides To identification of the Microinvertebrates of the Continental Waters of the World; Drumont, H.J.F., Ed.; Backhuys Publishers: Terneuzen, The Netherlands, 2001; pp. 1–127. [Google Scholar]
- Oksanen, J.; Blanchet, F.G.; Kindt, R.; Legendre, P.; Minchin, P.R.; O’hara, R.B.; Oksanen, M.J. Vegan: Community Ecology Package. R Package Version 2.0-9. 2013. Available online: https://www.researchgate.net/publication/304765105_vegan_Community_ecology_package_R_package_version_20-9_Computer_program_and_documentation_distributed_by_the_author (accessed on 6 November 2019).
- R Core Team. R: A Language and Environment for Statistical Computing; R Foundation for Statistical Computing: Vienna, Austria, 2014; Available online: http://www.R-project.org/ (accessed on 6 November 2019).
- Laliberté, E.; Legendre, P.; Shipley, B.; Laliberté, M.E. Package ‘FD’. Measuring Functional Diversity from Multiple Traits, and Other Tools for Functional Ecology. 2014. Available online: https://mran.microsoft.com/snapshot/2014-11-17/web/packages/FD/FD.pdf (accessed on 6 November 2019).
- Gotelli, N.J.; Entsminger, G.L. Swap and fill algorithms in null model analysis: Rethinking the knight’s tour. Oecologia 2001, 129, 281–291. [Google Scholar] [CrossRef]
- Kembel, S.W.; Cowan, P.D.; Helmus, M.R.; Cornwell, W.K.; Morlon, H.; Ackerly, D.D.; Blomberg, S.P.; Webb, C.O. Picante: R tools for integrating phylogenies and ecology. Bioinformatics 2010, 26, 1463–1464. [Google Scholar] [CrossRef]
- Wood, S.; Wood, M.S. Package ‘mgcv’. R Package Version. 2015, pp. 1–7. Available online: http://cran.uib.no/web/packages/mgcv/mgcv.pdf (accessed on 6 November 2019).
- Bolduc, P.; Bertolo, A.; Pinel-Alloul, B. Does submerged aquatic vegetation shape zooplankton community structure and functional diversity? A test with a shallow fluvial lake system. Hydrobiologia 2016, 778, 151–165. [Google Scholar] [CrossRef]
- Williamson, C.E. The swimming and feeding behavior of Mesocyclops. Hydrobiologia 1986, 134, 11–19. [Google Scholar] [CrossRef]
- Lansac-Thôa, F.V.; Velho, L.F.M.; Higuti, J.; Takahashi, E.M. Cyclopidae (Crustacea, Copepoda) from the upper Paraná river floodplain, Brazil. Braz. J. Biol. 2002, 62, 125–133. [Google Scholar] [CrossRef] [PubMed]
- Fryer, G. Functional Morphology and the Adaptive Radiation of the Daphniidae (Branchopoda: Anomopoda). Philos. Trans. R. Soc. Lond. B Biol. Sci. 1991, 331, 1–99. [Google Scholar] [CrossRef]
- Iglesias, C.; Goyenola, G.; Mazzeo, N.; Meerhoff, M.; Rodó, E.; Jeppesen, E. Horizontal dynamics of zooplankton in subtropical Lake Blanca (Uruguay) hosting multiple zooplankton predators and aquatic plant refuges. Hydrobiologia 2007, 584, 179–189. [Google Scholar] [CrossRef]
- Kuczynska-Kippen, N. The use of bdelloids in reference to rotifer biocoenotic indices as an indicator of the ecological state of small field water bodies: The effect of macrophytes, shading and trophic state of water. Ecol. Indicat. 2018, 89, 576–583. [Google Scholar] [CrossRef]
- González-Sagrario, M.L.A.; Balseiro, E.; Ituarte, R.; Spivak, E. Macrophytes as reguge or risky area for zooplankton: A balance set by littoral predacious macroinvertebrates. Freshw. Biol. 2009, 54, 1042–1053. [Google Scholar] [CrossRef]
- González-Sagrario, M.L.A.; Balseiro, E. The role of macroinvertebrates and fish in regulating the provision by macrophytes of refugia for zooplankton in a warm temperate shallow lake. Freshw. Biol. 2010, 55, 2153–2166. [Google Scholar] [CrossRef]
- Meerhoff, M.; Clemente, J.M.; Mello, F.T.; Iglesias, C.; Pedersen, A.R.; Jeppesen, E. Can warm climate-related structure of littoral predator assemblies weaken the clear water state in shallow lakes? Glob. Chang. Biol. 2007, 13, 1888–1897. [Google Scholar] [CrossRef]
- Williamson, C.E.; Reid, J. Copepoda. In Ecology and Classification of North American Freshwater Invertebrates; James, T., Covich, A.P., Eds.; Academic Press: Cambridge, MA, USA, 2001; pp. 915–954. [Google Scholar]
- Kraznai, E.; Borics, G.; Várbíro, G.; Abonyi, A.; Padisák, J.; Deák, C.; Tóthmérész, B. Characteristics of pelagic phytoplankton in shallow oxbow. Hydrobiologia 2010, 637, 173–184. [Google Scholar] [CrossRef]
- Meschiatti, A.J.; Arcifa, M.S.; Fenerich-Verani, N. Ecology of fish in oxbow lakes of Mogi-Guaçu River. In Estudos Integrados em Ecossistemas: Estação Ecológica de Jataí, 1st ed.; Santos, J.E., Pires, J.S.R., Eds.; Editora Rima: São Carlos, Brasil, 2000; pp. 817–830. [Google Scholar]
- Hévert, M.P.; Beisner, B.E.; Maranger, R. Linking zooplankton communities to ecosystem functioning: Toward an effect-trait framework. J. Plankton Res. 2016, 39, 3–12. [Google Scholar] [CrossRef] [Green Version]
Feeding Types | Abbreviations |
---|---|
Daphnia filtration | d.filt |
Sida filtration | s.filt |
Bosmina filtration | b.filt |
Raptorial | raptorial |
Stationary suspension | stat.susp |
Burrowing | burrow |
Attached | attach |
Size Class | |
0.1 to 0.5 mm | class A |
0.6 to 1.0 mm | class B |
1.1 to 1.5 mm | class C |
1.6 to 2.0 mm | class D |
Habitat Preference | |
Benthic | benthic |
Open water | open.water |
Vegetation | vegetation |
Open water vegetation | open.water.vegetation |
Trophic Group | |
Herbivore | herb |
Herbivore–detritivore | herb.detr |
Omnivore | omnivore |
Omnivore–carnivore | omnivore.carnivore |
Cladocerans | Abbreviation |
---|---|
Diaphanosoma spinulosum Herbst, 1967 | disp |
Pseudosida bidentata Herrick, 1884 | psbi |
Bosmina longirostris (O. F. Muller, 1785) | bolo |
Moina minuta Hansen, 1889 | momi |
Ceriodaphnia cornuta Sars, 1886 | ceco |
Simocephalus serrulatus (Koch, 1841) | sise |
Ilyocryptus spinifer Herrick, 1882 | ilsp |
Macrothrix paulensis (Sars, 1901) | mapa |
Copepods | Abbreviation |
Thermocyclops decipiens female (Kiefer, 1929) | thdef |
Thermocyclops decipiens male | thdem |
Mesocyclops meridianus female (Kiefer, 1926) | mesmef |
Mesocyclops meridianus male | mesmem |
Argyrodiaptomus furcatus female (Sars, 1901) | arfuf |
Argyrodiaptomus furcatus male | arfum |
Notodiaptomus iheringi female (Wrigth, 1935) | noihf |
Notodiaptomus iheringi male | noihm |
Calanoid copepodid | coca |
Cyclopoid copepodid | cocy |
Copepod nauplii | naup |
Functional Trait | Treatment | Zone | Treatment × Zone | ||||||
---|---|---|---|---|---|---|---|---|---|
F | p | df | F | p | df | F | p | df | |
Feeding Types | |||||||||
attached | 5.923 | 0.019 | 1 | 7.570 | 0.009 | 1 | 10.710 | 0.002 | 1 |
b.filtr | 12.526 | 0.001 | 1 | - | - | 1 | - | - | 1 |
burrow | 12.972 | 0.001 | 1 | 4.111 | 0.049 | 1 | - | - | 1 |
d.filtr | - | - | 1 | - | - | 1 | - | - | 1 |
raptorial | - | - | 1 | - | - | 1 | - | - | 1 |
s.filtr | - | - | 1 | - | - | 1 | - | - | 1 |
stat.susp | 4.545 | 0.039 | 1 | - | - | 1 | - | - | 1 |
Habitat Preference | |||||||||
benthic | 12.972 | 0.001 | 1 | 4.111 | 0.049 | 1 | - | - | 1 |
open.water | 5.378 | 0.025 | 1 | - | - | 1 | - | - | 1 |
open.water.vegetation | - | - | 1 | - | - | 1 | - | - | 1 |
vegetation | 4.305 | 0.04 | 1 | - | - | 1 | - | - | 1 |
Trophic Group | |||||||||
herb | - | - | 1 | - | - | 1 | - | - | 1 |
herb.detr | 12.972 | 0.001 | 1 | 4.111 | 0.049 | 1 | - | - | 1 |
omnivore | 7.196 | 0.010 | 1 | - | - | 1 | - | - | 1 |
omnivore.carnivore | 14.243 | <0.001 | 1 | - | - | 1 | - | - | 1 |
Size Class | |||||||||
class.A | - | - | 1 | - | - | 1 | - | - | 1 |
class.B | - | - | 1 | - | - | 1 | - | - | 1 |
class.C | - | - | 1 | - | - | 1 | - | - | 1 |
class.D | 118.521 | <0.001 | 1 | - | - | 1 | - | - | 1 |
Species | Treatment | Zone | Treatment × Zone | ||||||
---|---|---|---|---|---|---|---|---|---|
F | p | df | F | p | df | F | p | df | |
Disp | - | - | 1 | - | - | 1 | - | - | 1 |
Bolo | 12.526 | <0.001 | 1 | - | - | 1 | - | - | 1 |
Mapa | 20.444 | <0.001 | 1 | - | - | 1 | 4.033 | 0.050 | 1 |
Ilsp | 8.256 | 0.006 | 1 | 7.345 | 0.009 | 1 | - | - | 1 |
Psbi | 11.139 | 0.001 | 1 | 4.187 | 0.046 | 1 | 4.187 | 0.046 | 1 |
Momi | - | - | 1 | - | - | 1 | - | - | 1 |
Sise | 5.923 | 0.019 | 1 | 7.57 | 0.008 | 1 | 10.71 | 0.002 | 1 |
Ceco | 9.124 | 0.004 | 1 | - | - | 1 | - | - | 1 |
Noihm | - | - | 1 | - | - | 1 | - | - | 1 |
Noihf | - | - | 1 | - | - | 1 | - | - | 1 |
Arfuf | 118.521 | <0.001 | 1 | - | - | 1 | - | - | 1 |
Arfum | 56.446 | <0.001 | 1 | - | - | 1 | - | - | 1 |
Thdef | - | - | 1 | - | - | 1 | - | - | 1 |
Naup | 7.515 | 0.008 | 1 | - | - | 1 | - | - | 1 |
Cocy | 1.223 | 0.008 | 1 | - | - | 1 | - | - | 1 |
Coca | - | - | 1 | - | - | 1 | - | - | 1 |
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Stephan, L.R.; Beisner, B.E.; Oliveira, S.G.M.; Castilho-Noll, M.S.M. Influence of Eichhornia crassipes (Mart) Solms on a Tropical Microcrustacean Community Based on Taxonomic and Functional Trait Diversity. Water 2019, 11, 2423. https://doi.org/10.3390/w11112423
Stephan LR, Beisner BE, Oliveira SGM, Castilho-Noll MSM. Influence of Eichhornia crassipes (Mart) Solms on a Tropical Microcrustacean Community Based on Taxonomic and Functional Trait Diversity. Water. 2019; 11(11):2423. https://doi.org/10.3390/w11112423
Chicago/Turabian StyleStephan, Lígia R., Beatrix E. Beisner, Samuel G. M. Oliveira, and Maria Stela M. Castilho-Noll. 2019. "Influence of Eichhornia crassipes (Mart) Solms on a Tropical Microcrustacean Community Based on Taxonomic and Functional Trait Diversity" Water 11, no. 11: 2423. https://doi.org/10.3390/w11112423