Abstract
The previously neglected herbivore–aquatic macrophyte interaction has received more attention among scientists in the recent decades, especially in the context of biological invasions. However, there is still a great deal of work needed to improve scientific knowledge about this relationship and to improve biological management and control techniques. This systematic review provides an overview of temporal and spatial trends and the methodological approaches, habitats, and species most studied concerning this interaction. We evaluated scientific articles published in journals indexed to Web of Science that measured the consumption or other direct effects of herbivores on freshwater macrophytes, including non-native species. From 1992 to 2017, there was a growth rate of approximately three times in the publication of such articles, although they are concentrated in the temperate and subtropical zones, neglecting tropical and subpolar environments. We have also noticed a simple general pattern in most of the topics evaluated here, such as the low preference for using tests of multiple hypotheses and for applying both experimental and fieldwork methods together. Deep lakes and rivers were the most studied ecosystems, while shallow lakes, ponds, streams and wetlands had less attention. Non-native macrophytes were more studied than non-native herbivores. The macrophyte life forms most studies were rooted submerged, free-floating and emergent species, while the herbivore taxa most often examined in these studies were fish, molluscs and crustacea. We suggest performing studies that are more complex, using multi-species biological communities, with a focus on the unexplored pointed areas to advance scientific knowledge regarding herbivory on macrophytes, especially in tropical areas.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Bakker ES, Nolet BA (2014) Experimental evidence for enhanced top-down control of freshwater macrophytes with nutrient enrichment. Oecologia 176:825–836. https://doi.org/10.1007/s00442-014-3047-y
Bakker ES, Wood KA, Pagès JF et al (2016) Herbivory on freshwater and marine macrophytes: a review and perspective. Aquat Bot 135:18–36. https://doi.org/10.1016/j.aquabot.2016.04.008
Balian EV, Segers H, Lévèque C, Martens K (2008) The freshwater animal diversity assessment: an overview of the results. Hydrobiologia 595:627–637. https://doi.org/10.1007/s10750-007-9246-3
Belovsky GE, Botkin DB, Crowl TA et al (2004) Ten suggestions to strengthen the science of ecology. Bioscience 54:345–351. https://doi.org/10.1641/0006-3568(2004)054[0345:TSTSTS]2.0.CO;2
Bianchini I Jr, Cunha-Santino MB, Milan JAM et al (2010) Growth of Hydrilla verticillata (L.f.) Royle under controled conditions. Hydrobiologia 644:301–312. https://doi.org/10.1007/s10750-010-0191-1
Bozzetti M, Schulz UH (2004) An index of biotic integrity based on fish assemblages for subtropical streams in southern Brazil. Hydrobiologia 529:133–144. https://doi.org/10.1007/s10750-004-5738-6
Brönmark C (1990) How do herbivorous freshwater snails affect macrophytes?—A comment. Ecology 71:1212–1215. https://doi.org/10.2307/1937391
Carmel Y, Kent R, Bar-Massada A et al (2013) Trends in ecological research during the last three decades—a systematic review. PLoS ONE 8:1–8. https://doi.org/10.1371/journal.pone.0059813
Casal CMV (2006) Global documentation of fish introductions: the growing crisis and recommendations for action. Biol Invasions 8:3–11. https://doi.org/10.1007/s10530-005-0231-3
Cebrián J, Duarte CM (1998) Patterns in leaf herbivory on seagrasses. Aquat Bot 60:67–82. https://doi.org/10.1016/S0304-3770(97)00070-3
Chambers PA, Lacoul P, Murphy KJ, Thomaz SM (2008) Global diversity of aquatic macrophytes in freshwater. Hydrobiologia 595:9–26. https://doi.org/10.1007/s10750-007-9154-6
Charudattan R (2001) Are we on top of aquatic weeds? Weed problems, control options, and challenges. In: Riches CR (ed) International symposium on the world’s worst weeds: british crop protection council symposium proceedings. Brighton, England, pp 43–68
Clarke DA, York PH, Rasheed MA, Northfield TD (2017) Does biodiversity–ecosystem function literature neglect tropical ecosystems? Trends Ecol Evol 32:320–323. https://doi.org/10.1016/j.tree.2017.02.012
Cuda JP, Charudattan R, Grodowitz MJ et al (2008) Recent advances in biological control of submersed aquatic weeds. J Aquat Plant Manag 46:15–32
Cyr H, Face ML (1993) Magnitude and patterns of herbivory in aquatic and terrestrial ecosystems. Nature 361:148–150. https://doi.org/10.1038/361148a0
Davis MA (2009) Invasion biology. Oxford University Press, Oxford
de Pinto PT, O’Farrell I (2014) Regime shifts between free-floating plants and phytoplankton: a review. Hydrobiologia 740:13–24. https://doi.org/10.1007/s10750-014-1943-0
Downing JA (2010) Emerging global role of small lakes and ponds: little things mean a lot. Limnetica 29:9–24
Dudgeon D, Arthington AH, Gessner MO et al (2006) Freshwater biodiversity: importance, threats, status and conservation challenges. Biol Rev 81:163–182. https://doi.org/10.1017/S1464793105006950
Elton CS (1958) The ecology of invasions by animals and plants. Methuen, London
Estes J, Terborgh J, Brashares J et al (2011) Trophic downgrading of planet Earth. Science 333:301–306. https://doi.org/10.1126/science.1205106
Esteves FDA (2011) Fundamentos de Limnologia, 3rd edn. Interciência, Rio de Janeiro
Farji-Brener AG (2003) Uso correcto, imparcial e incorrecto de los terminos “hipótesis” y “predicciones” en ecología. Ecol Austral 13:223–227
Feinsinger P (2013) Research methodologies in applied and basic ecology: which am I following, and why? Rev Chil Hist Nat 86:385–402
Fleming JP, Dibble ED (2015) Ecological mechanisms of invasion success in aquatic macrophytes. Hydrobiologia 746:23–37. https://doi.org/10.1007/s10750-014-2026-y
Geiger W, Alcorlo P, Baltanás A, Montes C (2005) Impact of an introduced crustacean on the trophic webs of Mediterranean wetlands. Biol Invasions 7:49–73. https://doi.org/10.1007/1-4020-3870-4_6
Gibney E (2015) Brazilian science paralysed by economic slump. Nature 526:16–17. https://doi.org/10.1038/526016a
Gozlan RE (2008) Introduction of non-naive freshwater fish: is it all bad? Fish Fish 9:106–115
Grutters BMC, Gross EM, Bakker ES (2016) Insect herbivory on native and exotic aquatic plants: phosphorus and nitrogen drive insect growth and nutrient release. Hydrobiologia 778:209–220. https://doi.org/10.1007/s10750-015-2448-1
Havel JE, Lee CE, Zanden MJV (2005) Do reservoirs facilitate invasions into landscapes? Bioscience 55:518–525. https://doi.org/10.1641/0006-3568(2005)055[0518:DRFIIL]2.0.CO;2
Hicks BJ (2003) Biology and potential impacts of rudd (Scardinius erythrophthalmus L.) in New Zealand. In: Munro R (ed) Managing invasive freshwater fish in New Zealand. Proceedings of a workshop hosted by Department of Conservation. Hamilton, New Zealand, pp 49–58
Jenkins M (2003) Prospects for biodiversity. Science 302:1175–1177. https://doi.org/10.1126/science.1088666
Jenkins M, Jakubowska J, Gaillard V, Groombridge B (2002) Living planet index. In: Loh J (ed) Living planet report 2002. WWF International, Gland, p 3
Jeppesen E, Søndergaard M, Jensen JP 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. https://doi.org/10.1111/j.1365-2427.2005.01415.x
Keddy PA (1992) Assembly and response rules: two goals for predictive community ecology. J Veg Sci 3:157–164. https://doi.org/10.2307/3235676
Lacy R (1994) Managing genetic diversity in captive populations of animals. In: Bowles M, Whelan C (eds) Restoration of endangered species: conceptual issues, planning and implementation. Cambridge University Press, Cambridge, pp 63–89
Langeland KA (1996) Hydrilla verticillata (L.F.) Royle (Hydrocharitaceae), “The Perfect Aquatic Weed”. South Appalach Bot Soc 61:293–304
Law A, Jones KC, Willby NJ (2014) Medium vs. short-term effects of herbivory by Eurasian beaver on aquatic vegetation. Aquat Bot 116:27–34. https://doi.org/10.1016/j.aquabot.2014.01.004
Levine JM (2000) Species diversity and biological invasions: relating local process to community pattern. Science 288:852–854. https://doi.org/10.1126/science.288.5467.852
Levine JM, Adler PB, Yelenik SG (2004) A meta-analysis of biotic resistance to exotic plant invasions. Ecol Lett 7:975–989. https://doi.org/10.1111/j.1461-0248.2004.00657.x
Lodge DM (1991) Herbivory on freshwater macrophytes. Aquat Bot 41:195–224. https://doi.org/10.1016/0304-3770(91)90044-6
Lodge DM, Cronin G, Van Donk E, Froelich AJ (1998a) Impact of herbivory on plant standing crop: comparisons among biomes, between vascular and nonvascular plants, and among freshwater herbivore taxa. In: Jeppesen E, Søndergaard M, Søndergaard M, Christoffersen K (eds) The structuring role of submerged macrophytes in lakes. Springer, New York, pp 149–174
Lodge DM, Stein RA, Brown KM et al (1998b) Predicting impact of freshwater exotic species on native biodiversity: challenges in spatial scaling. Aust J Ecol 23:53–67. https://doi.org/10.1111/j.1442-9993.1998.tb00705.x
Lowry E, Rollinson EJ, Laybourn AJ et al (2013) Biological invasions: a field synopsis, systematic review, and database of the literature. Ecol Evol 3:182–196. https://doi.org/10.1002/ece3.431
Lu X, Ding J (2012) History of exposure to herbivores increases the compensatory ability of an invasive plant. Biol Invasions 14:649–658. https://doi.org/10.1007/s10530-011-0106-8
McKinney ML, Lockwood JL (1999) Biotic homogenization: a few winners replacing many losers in the next mass extinction. Trends Ecol Evol 14:450–453. https://doi.org/10.1016/S0169-5347(99)01679-1
McRae L, Freeman R, Marconi V (2016) State of the natural planet. In: Oerlemans N (ed) Livng planet report 2016: risk and resilience in a new area. WWF International, Gland, pp 19–42
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
Moyle PB, Light T (1996) Biological invasions of fresh water: empirical rules and assembly theory. Biol Conserv 78:149–161. https://doi.org/10.1016/0006-3207(96)00024-9
Naylor R (1996) Invasions in agriculture: assessing the cost of the golden apple snail in Asia. Ambio 25:443–448
O’Hare MT, Aguiar FC, Asaeda T et al (2018) Plants in aquatic ecosystems: current trends and future directions. Hydrobiologia 812:1–11. https://doi.org/10.1007/s10750-017-3190-7
Palmer M, Bernhardt E, Chornesky E et al (2004) Ecological science and sustainability for a crowded planet: 21st century. Front Ecol Environ 3(1):4–11. https://doi.org/10.1126/science.1095780
Parker IM, Simberloff D, Lonsdale WM et al (1999) Impact: toward a framework for understanding the ecological effects of invaders. Biol Invasions 1:3–19. https://doi.org/10.1023/A:1010034312781
Pelicice FM, Vitule JRS, Lima Junior DP et al (2014) A serious new threat to Brazilian freshwater ecosystems: the naturalization of nonnative fish by decree. Conserv Lett 7:55–60. https://doi.org/10.1111/conl.12029
Pimentel D, Zuniga R, Morrison D (2005) Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecol Econ 52:273–288. https://doi.org/10.1016/j.ecolecon.2004.10.002
Platt JR (1964) Strong inference. Science 146:347–353
Poore AGB, Campbell AH, Coleman RA et al (2012) Global patterns in the impact of marine herbivores on benthic primary producers. Ecol Lett 15:912–922. https://doi.org/10.1111/j.1461-0248.2012.01804.x
Prior KM, Powell THQ, Joseph AL, Hellmann JJ (2015) Insights from community ecology into the role of enemy release in causing invasion success: the importance of native enemy effects. Biol Invasions 17:1283–1297. https://doi.org/10.1007/s10530-014-0800-4
Qian H, Ricklefs RE (2007) A latitudinal gradient in large-scale beta diversity for vascular plants in North America. Ecol Lett 10:737–744. https://doi.org/10.1111/j.1461-0248.2007.01066.x
Qiu JW, Kwong KL (2009) Effects of macrophytes on feeding and life-history traits of the invasive apple snail Pomacea canaliculata. Freshw Biol 54:1720–1730. https://doi.org/10.1111/j.1365-2427.2009.02225.x
Rahel FJ (2002) Homogenization of freshwater faunas. Annu Rev Ecol Syst 33:291–315. https://doi.org/10.1146/annurev.ecolysis.33.010802.150429
Sala OE, Chapin FS III, Armesto JJ et al (2000) Global biodiversity scenarios for the year 2100. Science 287:1770–1775. https://doi.org/10.1126/science.287.5459.1770
Santamaría L (2002) Why are most aquatic plants widely distributed? Dispersal, clonal growth and small-scale heterogeneity in a stressful environment. Acta Oecol 23:137–154. https://doi.org/10.1016/S1146-609X(02)01146-3
Schäfer RB, Cooke SJ, Arlinghaus R et al (2011) Perspectives from early career researchers on the publication process in ecology—a response to Statzner & Resh (2010). Freshw Biol 56:2405–2412. https://doi.org/10.1111/j.1365-2427.2011.02673.x
Schemske DW, Mittelbach GG, Cornell HV et al (2009) Is there a latitudinal gradient in the importance of biotic interactions? Annu Rev Ecol Evol Syst 40:245–269. https://doi.org/10.1146/annurev.ecolsys.39.110707.173430
Schultz R, Dibble E (2012) Effects of invasive macrophytes on freshwater fish and macroinvertebrate communities: the role of invasive plant traits. Hydrobiologia 684:1–14. https://doi.org/10.1007/s10750-011-0978-8
Simberloff D, Von Holle B (1999) Positive interactions of nonindigenous species: invasional meltdown? Biol Invasions 1:21–32. https://doi.org/10.1023/A:1010086329619
Smolders AJP, Vergeer LHT, van der Velde G, Roelofs JGM (2000) Phenolic contents of submerged, emergent and floating leaves of aquatic and semi-aquatic macrophyte species: why do they differ? Oikos 91:307–310. https://doi.org/10.1034/j.1600-0706.2000.910211.x
Sousa WTZ (2011) Hydrilla verticillata (Hydrocharitaceae), a recent invader threatening Brazil’s freshwater environments: a review of the extent of the problem. Hydrobiologia 669:1–20. https://doi.org/10.1007/s10750-011-0696-2
StatSoft I (2005) STATISTICA (data analysis software system), version 7.1
Taylor KL, Grace JB (1995) The effects of vertebrate herbivory on plant community structure in the coastal marshes of the Pearl River, Louisiana, USA. Wetlands 15:68–73. https://doi.org/10.1007/BF03160681
Thiébaut G (2007) Invasion success of non-indigenous aquatic and semi-aquatic plants in their native and introduced ranges. A comparison between their invasiveness in North America and in France. Biol Invasions 9:1–12. https://doi.org/10.1007/s10530-006-9000-1
Thomaz SM, Mormul RP, Michelan TS (2015a) Propagule pressure, invasibility of freshwater ecosystems by macrophytes and their ecological impacts: a review of tropical freshwater ecosystems. Hydrobiologia 746:39–59. https://doi.org/10.1007/s10750-014-2044-9
Thomaz SM, Kovalenko KE, Havel JE, Kats LB (2015b) Aquatic invasive species: general trends in the literature and introduction to the special issue. Hydrobiologia 746:1–12. https://doi.org/10.1007/s10750-014-2150-8
Umetsu C, Evangelista H, Thomaz S (2012) Colonization, regeneration potential and growth rates of fragments of the exotic aquatic macrophyte Hydrilla verticillata. Aquat Biol 16:197–202. https://doi.org/10.3354/ab00450
van der Veer G, Nentwig W (2015) Environmental and economic impact assessment of alien and invasive fish species in Europe using the generic impact scoring system. Ecol Freshw Fish 24:646–656. https://doi.org/10.1111/eff.12181
Wood KA, Stillman RA, Clarke RT et al (2012) Understanding plant community responses to combinations of biotic and abiotic factors in different phases of the plant growth cycle. PLoS ONE 7:1–8. https://doi.org/10.1371/journal.pone.0049824
Wood KA, O’Hare MT, Mcdonald C et al (2017) Herbivore regulation of plant abundance in aquatic ecosystems. Biol Rev 92:1128–1141. https://doi.org/10.1111/brv.12272
Xie Y, Zhang CN, Lai Q (2014) China’s rise as a major contributor to science and technology. Proc Natl Acad Sci U S A 111:9437–9442. https://doi.org/10.1073/pnas.1407709111
Acknowledgements
M. M. Pulzatto, N. Louback-Franco, and L. A. Lolis thank the Coordination for the Improvement of Higher Education Personnel (CAPES) and Brazilian Council for Scientific and Technological Development (CNPq) for their scholarships. R. P. Mormul also acknowledges CNPq for research grants. The authors thank the anonymous reviewers for careful review of this manuscript and especially the editor Kevin J. Murphy for his kind suggestions for improvement of this work.
Author information
Authors and Affiliations
Corresponding author
Additional information
Handling Editor: Kevin Murphy.
Rights and permissions
About this article
Cite this article
Pulzatto, M.M., Lolis, L.A., Louback-Franco, N. et al. Herbivory on freshwater macrophytes from the perspective of biological invasions: a systematic review. Aquat Ecol 52, 297–309 (2018). https://doi.org/10.1007/s10452-018-9664-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10452-018-9664-5