Abstract
We compare invertebrate herbivory upon 13 macrophyte species in freshwater wetland systems located in two global ecozones, the Afrotropics and Neotropics, in the context of biotic and environmental factors influencing these wetlands. The two ecozones are climatically similar regions, with similar water chemistry, but experience contrasting grazing and disturbance pressures from large mammalian herbivores. Our results for macrophytes show that small invertebrates removed significantly more lamina biomass per leaf in Neotropical macrophytes (6.55%) than Afrotropical ones (4.99%). Overall, the results indicate that underestimation of up to 15.6% of leaf biomass may occur if plant tissue removal by invertebrate herbivores is not included in estimates of plant biomass. Regarding the contrasting grazing and disturbance pressures from large herbivores influencing these wetlands, seven mammal species (especially the Black Lechwe antelope, Kobus leche) were observed impacting macrophytes in the Afrotropical wetlands, while in the Neotropics, only much smaller rodents, capybara, (Hydrochoerus hydrochaeris) were sporadically observed. We discuss the relevance of results for invertebrate herbivory in the context of both the methodological approach and the importance of large mammalian herbivores as biotic factors additionally impacting macrophyte populations in these subtropical to tropical wetlands.
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Albertoni, E. F., L. J. Prellvitz & C. Palma-Silva, 2007. Macroinvertebrate fauna associated with Pistia stratiotes and Nymphoides indica in subtropical lakes (south Brazil). Brazilian Journal of Biology 67: 499–507.
Arbo, M. M. & S. G. Tressens, 2002. Flora del Iberá. Eudene, Corrientes.
Asner, G. P., S. R. Levick, T. Kennedy-Bowdoin, D. E. Knapp, R. Emerson, J. Jacobson, M. S. Colgan & R. E. Martin, 2009. Large-scale impacts of herbivores on the structural diversity of African savannas. PNAS 106: 4947–4952.
Bakker, E. S. & B. A. Nolet, 2014. Experimental evidence for enhanced top-down control of freshwater macrophytes with nutrient enrichment. Oecologia 176: 825–836.
Bakker, E. S., K. A. Wood, J. F. Pagès, G. F. Veen Marjolijn, J. A. Christianen, L. Santamaría, B. A. Nolet & S. Hilt, 2016a. Herbivory on freshwater and marine macrophytes: a review and perspective. Aquatic Botany 135: 18–36.
Bakker, E. S., J. F. Pagès, R. Arthur & T. Alcoverro, 2016b. Assessing the role of large herbivores in the structuring and functioning of freshwater and marine angiosperm ecosystems. Ecography 39: 162–179.
Barone, J. A., 1998. Host-specificity of folivorous insects in a moist tropical forest. Journal of Animal Ecology 67: 400–409.
Boar, R. R., D. M. Harper & C. S. Adams, 1999. Biomass allocation in Cyperus papyrus in a tropical wetland, Lake Naivasha, Kenya. Biotropica 31: 411–421.
Borges, L. V. & I. Gonçalves Colares, 2007. Feeding habits of capybaras (Hydrochoerus hydrochaeris, Linnaeus 1766), in the Ecological Reserve of Taim (ESEC-Taim)-south of Brazil. Brazilian Archives of Biology and Technology 50: 409–416.
Bottino, F., M. Calijuri & K. J. Murphy, 2014. Temporal and spatial variation of limnological variables and biomass of different macrophyte species in a Neotropical reservoir (São Paulo—Brazil). Acta Limnologica Brasiliensia 25: 387–397.
Bownes, A., 2018. Suppression of the aquatic weed Hydrilla verticillata (L.f.) Royle (Hydrocharitaceae) by a leaf-cutting moth Parapoynx diminutalis Snellen (Lepidoptera: Crambidae) in Jozini Dam, South Africa. African Journal of Aquatic Science 43: 153–162.
Cabrera Walsh, G., M. C. Hernández, F. McKay, M. Oleiro, M. Guala & A. Sosa, 2017. Lessons from three cases of biological control of native freshwater macrophytes isolated from their natural enemies. Aquatic Ecosystem Health & Management 20: 353–360.
Chabwela, H. N. & G. A. Ellenbrook, 1990. The impact of hydroelectric developments on the lechwe and its feeding grounds at Kafue Flats, Zambia. In Whigham, D. F., R. C. Good & J. Kvet (eds), Wetland Ecology and Management: Case Studies. Kluwer Academic Publisher, Boston: 95–101.
Chambers, P. A., P. Lacoul, K. J. Murphy & S. M. Thomaz, 2008. Global diversity of aquatic macrophytes in freshwater. Hydrobiologia 595: 9–26.
Coetzee, J. A., M. P. Hill, M. J. Byrne & A. Bownes, 2011. A review of the biological control programmes on Eichhornia crassipes (Mart.) Solms (Pontederiaceae), Salvinia molesta D.S. Mitch. (Salviniaceae), Pistia stratiotes L. (Araceae), Myriophyllum aquaticum (Vell.) Verdc. (Haloragaceae) and Azolla filiculoides Lam. (Azollaceae) in South Africa. African Entomology 19: 451–468.
Corriale, M. J. & E. A. Herrera, 2014. Patterns of habitat use and selection by the capybara (Hydrochoerus hydrochaeris): a landscape-scale analysis. Ecological Research 29: 191–201.
Cristoffer, C. & C. A. Peres, 2003. Elephants versus butterflies: the ecological role of large herbivores in the evolutionary history of two tropical worlds. Journal of Biogeography 30: 1357–1380.
Cronin, G., K. D. Wissing & D. M. Lodge, 1998. Comparative feeding selectivity of herbivorous insects on water lilies: aquatic vs. semi-terrestrial insects and submersed vs. floating leaves. Freshwater Biology 39: 243–257.
Cyr, H. & M. L. Pace, 1993. Magnitude and patterns of herbivory in aquatic and terrestrial ecosystems. Nature 361: 148–150.
Di Rienzo, J. A., F. Casanoves, M. G. Balzarini, L. Gonzalez, M. Tablada & C. W. Robledo, 2017. InfoStat Software versión 2017. Grupo InfoStat, F.C.A. Universidad Nacional de Córdoba, Córdoba.
Dorn, N. J., G. Cronin & D. M. Lodge, 2001. Feeding preferences and performance of an aquatic lepidopteran on macrophytes: plant hosts as food and habitat. Oecologia 128: 406–415.
Esteves, F., 2011. Fundamentos de Limnología, 3rd ed. Editora Interciência, Rio de Janeiro.
Ferreira, M., V. Wepener & J. H. J. van Vuren, 2012. Aquatic invertebrate communities of perennial pans in Mpumalanga, South Africa: a diversity and functional approach. African Invertebrates 53: 751–768.
Franceschini, M. C., A. Poi de Neiff & M. E. Galassi, 2010. Is the biomass of water hyacinth lost through herbivory in native areas important? Aquatic Botany 92: 250–256.
Franceschini, M. C., K. J. Murphy, M. P. Kennedy, F. S. Martínez, F. Willems & H. Sichingabula, 2020. Are invertebrate herbivores of freshwater macrophytes scarce in tropical wetlands? Aquatic Botany.
Gonçalves, C. V., A. Schwarzbold, A. Jasper & M. Castro Vasconcelos, 2010. Application of a non-destructive method to determine biomass in Pontederiaceae. Acta Limnologica Brasiliensia 22: 361–366.
Grime, J. P., 1979. Plant Strategies and Vegetation Processes. Wiley, Chichester.
Grutters, B. M. C., E. M. Gross & E. S. Bakker, 2016. Insect herbivory on native and exotic aquatic plants: phosphorus and nitrogen drive insect growth and nutrient release. Hydrobiologia 77: 209–220.
Hamandawana, H., 2012. The impacts of herbivory on vegetation in Moremi Game Reserve, Botswana: 1967–2001. Regional Environmental Change 12: 1–15.
Hrabar, H. & J. T. Du Toit, 2014. Interactions between megaherbivores and microherbivores: elephant browsing reduces host plant quality for caterpillars. Ecosphere 5: 1–6.
Hurlbert, S., 1984. Pseudoreplication and the design of ecological field experiments. Ecological Monographs 54: 187–211.
Jacobsen, D. & K. Sand-Jensen, 1994. Herbivory of invertebrates on submerged macrophytes from Danish freshwaters. Freshwater Biology 28: 301–308.
Kennedy, M. P. & K. J. Murphy, 2012. A picture guide to aquatic plants of Zambian rivers. SAFRASS Deliverable Report to the African, Caribbean and Pacific Group of States (ACP Group) Science and Technology Programme, Contract No. AFS/2009/219013. University of Aberdeen, Aberdeen.
Kennedy, M. P., P. Lang, J. Tapia Grimaldo, S. Varandas Martins, A. Bruce, A. Hastie, S. Lowe, M. M. Ali, J. Briggs, H. Sichingabula & K. J. Murphy, 2015. Environmental drivers of aquatic macrophyte communities in southern tropical African river systems: Zambia as a case study. Aquatic Botany 124: 19–28.
Kennedy, M. P., P. Lang, J. Tapia Grimaldo, S. Varandas Martins, A. Bruce, I. Moore, R. Taubert, C. Macleod-Nolan, S. McWaters, J. Briggs, S. Lowe, K. Saili, H. Sichingabula, F. Willems, H. Dallas, S. Morrison, C. Franceschini, F. Bottino & K. J. Murphy, 2017. Niche-breadth of freshwater macrophytes occurring in tropical southern African rivers predicts species global latitudinal range. Aquatic Botany 136: 121–130.
Labandeira, C. C., 1998. Early history of arthropods and vascular plants associations. Annual Review of Earth and Planetary Sciences 26: 329–377.
Lang, P. & K. J. Murphy, 2011. Environmental drivers, life strategies and bioindicator capacity of aquatic bryophyte communities in high-latitude upland streams. Hydrobiologia 679: 1–17.
Lodge, D. M., G. Cronin, E. Van Donk & A. J. Froelich, 1998. Impact of herbivory on plant standing crop: comparisons among biomes, between vascular and nonvascular plants, and among freshwater herbivore taxa. In Jeppesen, E., M. Søndergaard & K. Christoffersen (eds), The Structuring Role of Submersed Macrophytes in Lakes. Springer, New York: 149–174.
Madnes, N., R. D. Quintana, M. Biodini & D. Loponte, 2010. Relationships between photosynthetic plant types in the diet of herbivore mammals and in the environment in the lower Paraná River basin, Argentina. Revista Chilena de Historia Natural 83: 309–319.
Marques, V. R., 1988. O gênero Holochilus (Mammalia: Cricetedidae) no Rio Grande do Sul: Taxonomia e distribução. Revista Brasilera de Zoologia 4: 347–360.
Medeiros dos Santos, A. & F. A. Esteves, 2002. Primary production and mortality of Eleocharis interstincta in response to water level fluctuations. Aquatic Botany 74: 189–199.
Milne, J. M., K. J. Murphy & S. M. Thomaz, 2008. Estudos experimentais dos impactos causados da atividade de pastagem em áreas de pasto na várzea do Alto Rio Paraná. Cadernos de Biodiversidade 5: 4–9.
Moore, I. E. & K. J. Murphy, 2015. An evaluation of alternative macroinvertebrate sampling techniques for use in tropical freshwater biomonitoring schemes. Acta Limnologica Brasiliensia 27: 213–222.
Morison, J. I. L., M. T. F. Piedade, E. Müller, S. P. Long, W. J. Junk & M. B. Jones, 2000. Very high productivity of the C4 aquatic grass Echinochloa polystachya in the Amazon floodplain confirmed by net ecosystem CO2 flux measurements. Oecologia 125: 400–411.
Murphy, K. J. & J. W. Eaton, 1983. Effects of pleasure-boat traffic on macrophyte growth in canals. Journal of Applied Ecology 20: 713–729.
Murphy, K. J., G. Dickinson, S. M. Thomaz, L. M. Bini, K. Dick, K. Greaves, M. Kennedy, S. Livingstone, H. McFerran, J. Milne, J. Oldroyd & R. Wingfield, 2003. Aquatic plant communities and predictors of diversity in a sub-tropical river floodplain: the Upper Rio Paraná, Brazil. Aquatic Botany 77: 257–276.
Murphy, K., A. Efremov, T. Davidson, E. Molina-Navarro, K. Fidanza, T. C. C. Betiol, P. Chambers, J. Tapia Grimaldo, S. Varandas Martins, I. Springuel, M. Kennedy, R. P. Mormul, E. Dibble, D. Hofstra, B. Lukács, D. Gebler, L. Baastrup-Spohr & J. Urrutia-Estrada, 2019. World distribution, diversity and endemism of aquatic macrophytes. Aquatic Botany. https://doi.org/10.1016/j.aquabot.2019.06.006.
Murphy, K., P. Carvalho, A. Efremov, J. Tapia Grimaldo, E. Molina-Navarro, T. A. Davidson & S. M. Thomaz, 2020. Latitudinal variation in global range-size of aquatic macrophyte species shows evidence for a Rapoport effect. Freshwater Biology. https://doi.org/10.1111/fwb.13528.
Nachtrieb, J. G., M. J. Grodowitz & R. M. Smart, 2011. Impact of invertebrates on three aquatic macrophytes: American pondweed, Illinois pondweed, and Mexican water lily. Journal of Aquatic Plant Management 49: 32–36.
Newman, R. M., 1991. Herbivory and detritivory on freshwater macrophytes by invertebrates: a review. Journal of the North American Benthological Society 10: 89–114.
Newman, R. M. & R. D. Rotjan, 2013. Re-examining the fundamentals of grazing: freshwater, marine and terrestrial similarities and contrasts (commentary on Burkepile 2013). Oikos 122: 317–320.
Padial, A. A., L. M. Bini & S. M. Thomaz, 2008. The study of aquatic macrophytes in Neotropics: a scientometrical view of the main trends and gaps. Brazilian Journal of Biology 68: 1051–1059.
Poi de Neiff, A., 2003. Invertebrados de la vegetación del Iberá. In Poi de Neiff., A. (ed.), Limnología del Iberá: Aspectos fiscos, químicos y biológicos de las aguas. Eudene, Corrientes: 171–191.
Poi de Neiff, A. S. & S. L. Casco, 2003. Biological agents that accelerate winter decay of Eichhornia crassipes Mart. Solms. in northeastern Argentina. In Thomaz, S. M. & L. M. Bini (eds), Ecología e manejo de macrófitas aquáticas. Maringá, UEM: 127–144.
Poi de Neiff, A. & J. J. Neiff, 2006. Riqueza y similaridad de los invertebrados que viven en las plantas flotantes de la planicie de inundación del Río Paraná (Argentina). Interciencia 31: 220–225.
Quintana, R. D., S. L. Malzof, M. V. Villar, P. L. Saccone, E. Astrada, W. Prado, S. Rosenfeldt & F. Brancolini, 2012. Plantas, animales y hongos de las islas. Una introducción a la biodiversidad del Bajo Delta del Río Paraná, Latingrafica, Buenos Aires.
Ramos, Y. G. C., I. A. Aximoff & C. Alves da Rosa, 2018. Capybaras (Rodentia: Cavidae) in highlands: environmental variables related to distribution, and herbivory effects on a common plant species. Journal of Natural History 52: 1801–1815.
Rasband W. S. ImageJ. U.S. National Institute of Health, Bethesda https://imagej.nih.gov/ij/, 1997–2016.
Redfern, J. V., R. Grant, H. Biggs & W. M. Getz, 2003. Surface water constraints on herbivore foraging in the Kruger National Park, South Africa. Ecology 84: 2092–2107.
Reys, P., J. Sabino & M. Galetti, 2009. Frugivory by the fish Brycon hilarii (Characidae) in western Brazil. Acta Oecologica 35: 141–163.
Sacco, J., G. Cabrera Walsh, M. C. Hernández, A. J. Sosa, M. V. Cardo & G. Elsesser, 2013. Feeding impact of the planthopper Taosa longula (Hemiptera: Dictyopharidae) on waterhyacinth, Eichhornia crassipes (Pontederiaceae). Biocontrol Science and Technology 23: 160–169.
Selford, V. E., 1918. Conditions of existence. In Ward, H. B. & G. C. Whipple (eds), FreshWater Biology. Wiley, New York: 21–60.
Schivo, F., P. P. Kandus, P. Minotti & R. Quintana, 2010. Mapa de aptitud ecológica potencial para el carpincho (Hydrochoerus hydrochaeris) en la provincia de Corrientes, Argentina. Rasadep 1: 83–100.
Silva, T. S. F., M. P. F. Costa & J. M. Melack, 2009. Annual net primary production of macrophytes in the eastern Amazon Floodplain. Wetlands 29: 747–758.
Soti, P. G. & J. C. Volin, 2010. Does water hyacinth (Eichhornia crassipes) compensate for simulated defoliation? Implications for effective biocontrol. Biological Control 54: 35–40.
Strange, E., J. M. Hill & J. A. Coetzee, 2018. Evidence for a new regime shift between floating and submerged invasive plant dominance in South Africa. Hydrobiologia. https://doi.org/10.1007/s10750-018-3506-2.
Stuart, C. & M. Stuart, 2006. Field guide to the larger mammals of Africa, 3rd ed. Struik Nature, Cape Town.
Tapia Grimaldo, J., L. M. Bini, V. Landeiro, M. T. O’Hare, J. Caffrey, A. Spink, S. Varandas Martins, M. P. Kennedy & K. J. Murphy, 2016. Spatial and environmental drivers of macrophyte diversity and community composition in temperate and tropical calcareous rivers. Aquatic Botany 132: 49–61.
Tapia, Grimaldo J., M. O’Hare, M. Kennedy, T. A. Davidson, J. Bonilla-Barbosa, B. Santamaría, L. Gettys, S. Varandas Martins, S. Thomaz & K. J. Murphy, 2017. Environmental drivers of freshwater macrophyte diversity and community composition in calcareous warm-water rivers of America and Africa. Freshwater Biology 62: 1511–1527.
Thomaz, S. M. & E. R. Da Cunha, 2010. The role of macrophytes in habitat structuring in aquatic ecosystems: methods of measurement, causes and consequences on animal assemblages’ composition and biodiversity. Acta Limnologica Brasiliensia 22: 218–236.
Trindade, C. R. T., V. L. Landeiro & F. Schneck, 2018. Macrophyte functional groups elucidate the relative role of environmental and spatial factors on species richness and assemblage structure. Hydrobiologia. https://doi.org/10.1007/s10750-018-3709-6.
Varandas Martins, S., J. Milne, S. M. Thomaz, S. McWaters, R. P. Mormul, M. Kennedy & K. J. Murphy, 2013. Human and natural drivers of changing macrophyte community dynamics over twelve years in a Neotropical riverine floodplain system. Marine and Freshwater Ecosystems 23: 678–697.
Viljoen, P., 2011. Bangweulu Wetlands Zambia. Aerial Wildlife Survey. African Parks Network Report, Lusaka.
Wantzen, K. M., M. R. Marchese, M. I. Marques & D. L. Battirola, 2016. Invertebrates in a Neotropical floodplain. In Batzer, D. & D. Boix (eds), Invertebrate in freshwater wetlands: an international Perspective of their ecology. Springer International Publishing, Switzerland: 493–524.
Wetzel, R. G., 2001. Limnology. Lake and River Ecosystems, 3rd ed. Elsevier Academic Press, California.
Wissinger, S. A., 1999. Ecology of wetlands invertebrates: Synthesis and application for conservation management. In Batzer, D., B. R. Russell & S. A. Wissinger (eds), Invertebrate in freshwater wetlands of North America: ecology and management. Wiley, New York: 1043–1086.
Wood, K. A., M. T. O’Hare, C. McDonald, K. R. Searle, F. Daunt & R. A. Stillman, 2016. Herbivore regulation of plant abundance in aquatic ecosystems. Biological Review. https://doi.org/10.1111/brv12272.
Zamora, R. & J. M. Gómez, 1993. Vertebrate herbivores as predators of insect herbivores: an asymmetrical interaction mediated by size differences. Oikos 66: 223–228.
Acknowledgements
We thank the Kasanka Trust and Zambia Wildlife Authority (ZAWA) for their support and assistance during sampling in Africa. This study was funded by PICT 2160-2011, PICT 1910-2015 of the Agencia Nacional de Promoción Científica y Tecnológica and PI 17Q003 of the Secretaría General de Ciencia Técnica de la Universidad Nacional del Nordeste (Argentina), the Carnegie Trust for the Universities of Scotland, and the Commission of the European Community/ACP Science and Technology Programme (Grant Number AFS/2009/219013). The authors declare no conflict of interest in undertaking this work. We are grateful for comments on the draft ms from Dr. Sidinei Thomaz (Universidade Estadual de Maringa, Brazil), Dr. Kim Canavan (Rhodes University, South Africa) and Dr. Martin Nuñez (Universidad Nacional del Comahue, Argentina).
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Franceschini, M.C., Murphy, K.J., Moore, I. et al. Impacts on freshwater macrophytes produced by small invertebrate herbivores: Afrotropical and Neotropical wetlands compared. Hydrobiologia 847, 3931–3950 (2020). https://doi.org/10.1007/s10750-020-04360-5
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DOI: https://doi.org/10.1007/s10750-020-04360-5