Abstract
This research addressed the question of whether invertebrate food web structure varied between a native and an invasive macrophyte leaf species in the littoral zone of a tropical reservoir. We compared macroinvertebrate herbivore functional trait diversity composition with food web structure on the two macrophyte leaves, the invasive white ginger lily (Hedichium coronarium—Zingiberaceae) and the native pickerelweed (Pontederia cordata—Pontederiaceae). We predicted that the herbivore macroinvertebrate trait indices would decrease with macrophyte leaf species due to a lower resource quality with the flow-on effects in the food web structure. We calculated the number of functionally singular species (sing.sp) and herbivore functional trait richness (FRic) indices. For the macroinvertebrate food webs, we calculated the total number of trophic links (L), link density (L/S), connectance (C) and predator–prey ratios using a predator–prey matrix. We analysed the relationship between chemical traits of the macrophyte species’ leaves herbivore traits and food web indices using multivariate regression and Pearson’s correlation. Hedichium coronarium leaves had higher biomass and higher nitrogen content than the native P. cordata, which had higher phosphorus and carbohydrate content. Pontederia cordata leaves were associated with specialist macroinvertebrate species which primarily feed on biofilms (e.g. Ulmeritrus and Scirtidae) and plant leaves (e.g. Beardius). Food webs on P. cordata had lower numbers of trophic links (L), links per species (L/S) and predator–prey ratios. Connectance, which represents food web complexity, was similar between macroinvertebrate assemblages on the two leaf types. Our study suggests that chemical compounds of macrophyte leaves quality may have potential flow-on effects on food web structure.
Similar content being viewed by others
Change history
12 June 2018
In the original publication of an article, third author’s name was misspelt and some values were missed in Table 2. The correct name and the Table 2 are given in this correction.
References
Association of Official Agricultural Chemists (1995) Official methods of analysis of the AOAC, vol 1. AOAC International, Arlington, pp 1–30
Bakker ES, Wood KA, Pagès JD, Ciska Veen GF, Christianen MJA, Santamaría L, Nolet BA, Hilt S (2016) Herbivory on freshwater and marine macrophytes: a review and perspective. Aquat Bot 135:18–36
Baptista DF, Buss DF, Dias LG, Nessimian JL, Da Silva ER, Neto ADM, Andrade LR (2006) Functional feeding groups of Brazilian Ephemeroptera nymphs: ultrastructure of mouthparts. Int J Limnol 42:87–96
Boiché A, Lemoine DG, Barrat-Segretain MH, Thiébaut G (2011) Resistance to herbivory of two populations of Elodea canadensis Michaux and Elodea nuttallii Planchon St. John. Plant Ecol 212:1723–1731
Borkent A (1984) The systematic and phylogeny of the Stenochironomus complex (Diptera: Chironomidae). Mem Entomol Soc Can 128:1–269
Brasil LS, Juen L, Batista JD, Pavan MG, Cabette HSR (2014) Longitudinal distribution of the functional feeding groups of aquatic insects in streams of the Brazilian Cerrado Savanna. Neotrop Entomol 43:421–428
Bukovinszky T, van Veen FJF, Jongema Y, Dicke M (2008) Direct and indirect effects of the resource quality on food web structure. Science 319:804–807
Burlakova LE, Karatayev AY (2007) The effect of invasive macrophytes and water level fluctuations on unionids in Texas impoundments. Hydrobiologia 586:291–302
Buttakka CMM, Grybkowska M, Pinha GD, Takeda AM (2014) Habitat and trophic relationships of Chironomidae insect larvae from the Sepotuba River Basin, Pantanal of Mato Grosso, Brazil. Braz J Biol 74:395–407
Carniatto N, Thomaz SM, Cunha ER, Fugi R, Ota RR (2013) Effects of an invasive alien Poaceae on aquatic macrophytes and fish communities in a neotropical reservoir. Biotropica 45:747–754
Carpenter SR, Lodge DM (1986) Effects of submersed macrophytes on ecosystem processes. Aquat Bot 26:341–370
Chaij J, Devoto M, Oleiro M, Chaneton EJ, Mazía N (2016) Complexity of leaf miner-parasitoid food webs declines with canopy heights in a Patagonian beech forest. Ecol Entomol 41:599–610
Choi C, Bareiss C, Walenciak O, Gross EM (2002) Impact of polyphenols on the growth of the aquatic herbivore Acentria ephemerella. J Chem Ecol 28:2245–2256
Claeson SM, LeRoy CJ, Barry JR, Kuehn KA (2014) Impacts of invasive riparian knotweed on litter decomposition, aquatic fungi, and macroinvertebrates. Biol Invasions 16:1531–1544
Coelho-Silva JF (1967) Noções Sobre Análise de Alimentos. Impresa Universitária da Universidade Rural do Estado de Minas Gerais, Viçosa
Cornut J, Ferreira V, Gonçalves AL, Chauvet E, Canhoto E (2015) Fungal alteration of the elemental composition of leaf litter affects shredder feeding activity. Freshw Biol 60:1751–1755
Cornwell WK, Cornelissen JHC, Amatangelo K, Dorrepaal E, Eviner VT, Godoy O, Hobbie SE, Hoorens B, Kurokawa H, Pérez-Harguindeguy N, Quested HM, Santiago LS, Wardle DA, Wright IJ, Aerts R, Allison SD, Van Bodegom P, Brovkin V, Chatain A, Callaghan TV, Díaz S, Garnier E, Gurvich DE, Kazakou E, Klein JA, Read J, Reich PB, Soudzilovskaia NA, Vaieretti MV, Westoby M (2008) Plant species traits are the predominant control on litter decomposition rates within biomes worldwide. Ecol Lett 11:1065–1107
Correa-Araneda F, Boyero L, Figueroa R, Sánchez C, Abdala R, Ruiz-García A, Graça MA (2015) Joint effects of climate warming and exotic litter (Eucalyptus globulus Labill.) on stream detritivore fitness and litter breakdown. Aquat Sci 77:197–205
Creitz GI, Richards FA (1955) The estimation and characterization of plankton populations by pigment analysis: III a note on the use of “Millipore” membrane filters in the estimation of plankton pigments. J Mar Res 14:211–216
De Castro WAC, Almeida RV, Leite MB, Marrs RH, Matos DMS (2016) Invasion strategies of white ginger lily (Hedychium coronarium) J. König (Zingiberaceae) under different competitive and environmental conditions. Environ Exp Bot 127:55–62
De Oliveira CSN, Da Silva MA, Fonseca-Gessner AA (2013) Neotropical Ablabesmyia Johannsen (Diptera: Chironomidae, Tanypodinae)-part I. Zootaxa 3733:1–123
Dodds WK (2003) The role of periphyton in phosphorus retention in shallow freshwater aquatic systems. J Phycol 39:840–849
Domínguez E, Fernández HR (2009) Macroinvertebrados bentónicos sudamericanos: sistemática y biología. Tucuman, Argentina
Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356
Elger A, Barrat-Segretain MH, Willby NJ (2006) Seasonal variability in the palatability of freshwater macrophytes: a case study. In: Caffrey JM, Dutartre A, Haury J, Murphy KJ, Wade PM (eds) Macrophytes in aquatic ecosystems: from biology to management. Developments in hydrobiology. Springer, Dordrecht, pp 89–93
Graça MA, Cressa C (2010) Leaf quality of some tropical and temperate tree species as a food resource for stream shredders. Int Rev Hydrobiol 95:27–41
Hilt S, Gross EM (2008) Can allelopathically active submerged macrophytes stabilise clear-water states in shallow lakes? Basic Appl Ecol 9:422–432
Hinojosa-Garro D, Mason CF, Underwood GJC (2010) Influence of macrophyte spatial architecture on periphyton and macroinvertebrate community structure in shallow water bodies under contrasting land management. Fundam Appl Limnol 177:19–37
Huntly N (1991) Herbivores and the dynamics of communities and ecosystems. Annu Revi Ecol Syst 22:477–503
Kelly DJ, Hawes I (2005) Effects of invasive macrophytes on littoral-zone productivity and food web dynamics in a New Zealand high-country lake. J N Am Benthol Soc 24:300–320
Kovalenko KE, Dibble ED (2011) Effects of invasive macrophyte on trophic diversity and position of secondary consumers. Hydrobiologia 663:167–173
Kratina P, LeCraw RM, Ingram T, Anholt BR (2012) Stability and persistence of food webs with omnivory: Is there a general pattern? Ecosphere 3:1–18
Laliberté E, Legendre P (2010) A distance-based framework for measuring functional diversity from multiple traits. Ecology 91:299–305
Laliberté E, Legendre P, Shipley B (2014) FD: measuring functional diversity from multiple traits, and other tools for functional ecology. R package version 1-12
Leite-Rossi LA, Trivinho-Strixino S (2012) Are sugarcane leaf-detritus well colonized by aquatic macroinvertebrates? Act Limnol Bras 24:303–313
Leite-Rossi LA, Saito VS, Cunha-Santino MB, Trivinho-Strixino S (2016) How does leaf litter chemistry influence its decomposition and colonization by shredder Chironomidae (Diptera) larvae in a tropical stream? Hydrobiologia 77:119–130
Lorenzi H (1991) Plantas daninhas do Brasil: terrestres, aquáticas, parasitas, tóxicas e medicinais. Instituto Plantarum, Nova Odessa
Lorenzi H, Souza H (2001) Plantas ornamentais. Plantarum, São Paulo
Makkar HP, Blümmel M, Borowy NK, Becker K (1993) Gravimetric determination of tannins and their correlations with chemical and protein precipitation methods. J Sci Food Agric 61:161–165
Marshall JK (1968) Methods for leaf area measurement of large and small leaf samples. Photosynthetica 2:41–47
Merritt RW, Cummins KW (1996) An introduction to the aquatic insect of North America. Kendall Hunt Publishing Co., Dubuque, Iowa
Mertens DR (2002) Gravimetric determination of amylase-treated neutral detergent fiber in feeds with refluxing in beaker or crucibles: collaborative study. J AOAC Int 85:1217–1240
Montgomery HAC, Thom NS, Cockburn A (1964) Determination of dissolved oxygen by the Winkler method and the solubility of oxygen in the pure water and sea water. J Chem Technol Biotechnol 14:280–296
Morrison WE, Hay ME (2011) Induced chemical defences in a freshwater macrophyte suppress herbivore fitness and the growth of associated microbes. Oecologia 165:427–436
Motta RL, Uieda VS (2004) Diet and trophic groups of an aquatic insect community in a tropical stream. Braz J Biol 64:809–817
Newman RM, Kerfoot WC, Hanscom Z (1996) Watercress allelochemical defends high-nitrogen foliage against consumption: effects on freshwater invertebrate herbivores. Ecology 77:2312–2323
Nordström MC, Aarnio K, Törnroos A, Bonsdorff E (2015) Nestedness of trophic links and biological traits in a marine food web. Ecosphere 6:1–14
Perdomo G, Sunnucks P, Thompson RM (2012) Food web: an open-source program for the visualisation and analysis of compilations of complex food webs. Package ‘foodweb’—CRAN.R-project.org. https://cran.r-project.org/web/packages/foodweb/foodweb.pdf
Reynaga MC, Martín PAR (2014) Trophic analysis of three species of Marilia (Trichoptera: Odontoceridae) from the neotropics. Rev Biol Trop 62:543–550
Robertson JB, Van Soest PJ (1981) The detergent system of analysis and its application to human foods. In: James WPT, Theander O (eds) The analysis of dietary fiber in food. Marcel Deller, New York, pp 123–158
RStudio Team (2015) RStudio: integrated development for R. RStudio, Inc, Boston. http://www.rstudio.com/
Sarruge JR, Haag HP (1974) Análises químicas em plantas. Escola Superior de Agricultura Luiz de Queiroz. Universidade de São Paulo, Piracicaba
Saulino HHL, Trivinho-Strixino S (2017) Forecasting the impact of an invasive macrophyte species in the littoral zone through aquatic insect species composition. Iheringia Serie Zool 107. https://doi.org/10.1590/1678-4766e2017043
Saulino HHL, Trivinho-Strixino S (2018) Native macrophyte leaves influence more specialisation of neotropical shredder chironomids than invasive macrophyte leaves. Hydrobiologia 813:189–198
Scotti M, Bondavalli C, Bodini A, Allesina S (2009) Using trophic hierarchy to understand food web structure. Oikos 118:1695–1702
Shultz R, Dibble E (2012) Effects of invasive macrophytes on freshwater fish and macroinvertebrate communities: the role of invasive plant traits. Hydrobiologia 684:1–14
Silva FL, Fonseca-Gessner AA, Ekrem T (2014) A taxonomic revision of genus Labrundinia Fittkau, 1962 (Diptera: Chironomidae: Tanypodinae). Zootaxa 3769:1–185
Thompson RM, Townsend CR (2005) Energy availability, spatial heterogeneity and ecosystem size predict food-web structure in streams. Oikos 108:137–148
Thompson RM, Dunne J, Woodward G (2012) Freshwater food webs: towards a more fundamental understanding of biodiversity and community dynamics. Freshw Biol 57:1329–1341
Trivinho-Strixino S (2011) Larvas de Chironomidae: guia de identificação. Departamento de Hidrobiologia/Lab, De Entomologia Aquática, São Carlos
Trivinho-Strixino S (2012) A systematic review of Neotropical Caladomyia Säwedal (Diptera: Chironomidae). Zootaxa 3495:1–41
Trivinho-Strixino S, Pepinelli M (2015) A systematic study on Endotribelos Grodhaus (Diptera: Chironomidae) from Brazil including DNA barcoding to link males and females. Zootaxa 3936:1–41
Villéger S, Mason NW, Mouillot D (2008) New multidimensional functional diversity indices for a multifaceted framework in functional ecology. Ecology 89:2290–2301
Wallace JB, Webster JR (1996) The role of macroinvertebrates in stream ecosystem function. Annu Rev Entomol 41:115–139
Warfe DM, Barmuta LA (2006) Habitat structural complexity mediates food web dynamics in a freshwater macrophyte community. Oecologia 150:141–154
Wong PK, Yan L, Liu NY, Qiu JW (2010) Palatability of macrophytes to the invasive freshwater snail Pomacea canaliculata: differential effects of multiple plant traits. Freshw Biol 55:2023–2031
Wood KA, O’Hare MT, McDonald C, Searle KR, Daunt F, Stillman RA (2017) Herbivore regulation of plant abundance in aquatic ecosystems. Biol Rev 92:1128–1141
Acknowledgements
We would like to thank CNPQ (National Counsel of Technological and Scientific Development) for their financial support (process—141020/2013-0). We would also like to thank Marcela B. Cunha-Santino (Universidade Federal de São Carlos) for helping with the chemical analyses of the macrophyte leaves.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflict of interest.
Ethical approval
All applicable international, national and/or institutional guidelines for the care and use of animals were followed.
Additional information
Handling Editor: Piet Spaak.
Rights and permissions
About this article
Cite this article
Saulino, H.H.L., Thompson, R.M. & Trivinho-Strxino, S. Herbivore functional traits and macroinvertebrate food webs have different responses to leaf chemical compounds of two macrophyte species in a tropical lake’s littoral zone. Aquat Ecol 52, 165–176 (2018). https://doi.org/10.1007/s10452-018-9652-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10452-018-9652-9