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Quantifying the top-down and bottom-up effects of a non-native grazer in freshwaters

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Abstract

Quantifying the effects of grazing and nutrient remineralization by grazers on algal biomass and productivity is important to estimate the net effects of grazing species on ecosystem structure and function. These effects may be especially important in ecosystems threatened by the invasion of non-native grazing species, as grazers can regulate the quantity of algae through both top-down (grazing) and bottom-up (remineralization) processes. In this study, we coupled mesocosm and in situ experimental manipulations to quantify the impacts of a non-native, grazing fish (Loricariidae: Pterygoplichthys) on algal biomass and primary productivity in stream ecosystems. While loricariid grazing depressed algal biomass and rates of primary production in mesocosm and in situ experiments, loricariid-mediated nutrient remineralization enhanced algal biomass and primary production in mesocosms relative to control treatments without loricariids. In sum, even when nutrient limitation was alleviated, intensive grazing by high-densities of loricariids had a negative net-effect on algal biomass and primary productivity. Examined together, our results demonstrate the need to quantify both consumptive and remineralization effects of invasive grazers in order to develop a comprehensive understanding of how non-native organisms influence ecosystem structure and function.

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References

  • Atkinson C, Vaughn CC, Forshay KJ et al (2013) Aggregated filter-feeding consumers alter nutrient limitation-consequences for ecosystem and community dynamics. Ecology 94:1359–1369

    Article  PubMed  Google Scholar 

  • Benstead JP, Cross WF, March JG et al (2010) Biotic and abiotic controls on the ecosystem significance of consumer excretion in two contrasting tropical streams. Freshw Biol 55:2047–2061

    Article  Google Scholar 

  • Blumenthal DM (2006) Interactions between resource availability and enemy release in plant invasion. Ecol Lett 9:887–895

    Article  PubMed  Google Scholar 

  • Bott TL, Brock JT, Cushing CE et al (1978) Comparison of methods for measuring primary productivity and community respiration in streams. Hydrobiologia 60:3–12

    Article  CAS  Google Scholar 

  • Capps KA, Flecker AS (2013a) Invasive aquarium fish transform ecosystem nutrient dynamics. Proc R Soc B Biol Sci 280. 10.1098/rspb.2013.1520

  • Capps KA, Flecker AS (2013b) Invasive fishes generate biogeochemical hotspots in a nutrient-limited system. PLoS One 8:e54093

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Capps KA, Booth MT, Collins SM et al (2011a) Nutrient diffusing substrata: a field comparison of commonly used methods to assess nutrient limitation. J N Am Benthol Soc 30:522–532

    Article  Google Scholar 

  • Capps KA, Nico LG, Mendoza-Carranza M et al (2011b) Salinity tolerance of non-native suckermouth armoured catfish (Loricariidae: Pterygoplichthys) in south-eastern Mexico: implications for invasion and dispersal. Aquat Conserv Mar Freshw Ecosyst 21:528–540

    Article  Google Scholar 

  • Carlsson NL, Lacoursière J (2005) Herbivory on aquatic vascular plants by the introduced golden apple snail (Pomacea canaliculata) in Lao PDR. Biol Invasions 7:233–241

    Article  Google Scholar 

  • Cucherousset J, Olden JD (2011) Ecological impacts of nonnative freshwater fishes. Fisheries 36:215–230

    Article  Google Scholar 

  • Cucherousset J, Blanchet S, Olden JD (2012) Non-native species promote trophic dispersion of food webs. Front Ecol Environ 10:406–408

    Article  Google Scholar 

  • Davis MA, Grime JP, Thompson K (2000) Fluctuating resources in plant communities: a general theory of invasibility. J Ecol 88:528–534

    Article  Google Scholar 

  • Davis MA, Chew MK, Hobbs RJ et al (2011) Don’t judge species on their origins. Nature 474:153–154

    Article  CAS  PubMed  Google Scholar 

  • Elser JJ, Urabe J (1999) The stoichiometry of consumer-driven nutrient recycling: theory, observations, and consequences. Ecology 80:735–751

    Article  Google Scholar 

  • Elser JJ, Sterner RW, Gorokhova E et al (2000) Biological stoichiometry from genes to ecosystems. Ecol Lett 3:540–550

    Article  Google Scholar 

  • Evans-White MA, Lamberti GA (2006) Stoichiometry of consumer-driven nutrient recycling across nutrient regimes in streams. Ecol Lett 9:1186–1197

    Article  PubMed  Google Scholar 

  • Feiner ZS, Rice JA, Aday DD (2013) Trophic niche of invasive white perch and potential interactions with representative reservoir species. Trans Am Fish Soc 142:628–641

    Article  Google Scholar 

  • Gido KB, Franssen NR (2007) Invasion of stream fishes into low trophic positions. Ecol Freshw Fish 16:457–464

    Article  Google Scholar 

  • Gido KB, Matthews WJ (2001) Ecosystem effects of water column minnows in experimental streams. Oecologia 126:247–253

    Article  Google Scholar 

  • Gruner DS, Smith JE, Seabloom EW et al (2008) A cross-system synthesis of consumer and nutrient resource control on producer biomass. Ecol Lett 11:740–755

    Article  PubMed  Google Scholar 

  • Hill BH, Lazorchak JM, McCormick FH et al (1997) The effects of elevated metals on benthic community metabolism in a Rocky Mountain stream. Environ Pollut 95:183–190

    Article  CAS  PubMed  Google Scholar 

  • Hillebrand H (2002) Top-down versus bottom-up control of autotrophic biomass: a meta-analysis on experiments with periphyton. J N Am Benthol Soc 21:349–369

    Article  Google Scholar 

  • Hillebrand H (2009) Meta-analysis of grazer control of periphyton biomass across aquatic ecosystems. J Phycol 45:798–806

    Article  Google Scholar 

  • Hood JM, Vanni MJ, Flecker AS (2005) Nutrient recycling by two phosphorus-rich grazing catfish: the potential for phosphorus-limitation of fish growth. Oecologia 146:247–257

    Article  PubMed  Google Scholar 

  • Jeschke JM, Strayer DL (2005) Invasion success of vertebrates in Europe and North America. Proc Natl Acad Sci USA 102:7198–7202

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170

    Article  Google Scholar 

  • Knoll LB, McIntyre PB, Vanni MJ et al (2009) Feedbacks of consumer nutrient recycling on producer biomass and stoichiometry: separating direct and indirect effects. Oikos 118:1732–1742

    Article  CAS  Google Scholar 

  • Kohler TJ, Murdock JN, Gido KB et al (2011) Nutrient loading and grazing by the minnow Phoxinus erythrogaster shift periphyton abundance and stoichiometry in mesocosms. Freshw Biol 56:1133–1146

    Article  Google Scholar 

  • Kulhanek SA, Leung B, Ricciardi A (2011a) Using ecological niche models to predict the abundance and impact of invasive species: application to the common carp. Ecol Appl 21:203–213

    Article  PubMed  Google Scholar 

  • Kulhanek SA, Ricciardi A, Leung B (2011b) Is invasion history a useful tool for predicting the impacts of the world’s worst aquatic invasive species? Ecol Appl 21:189–202

    Article  PubMed  Google Scholar 

  • Liess A, Hillebrand H (2006) Role of nutrient supply in grazer-periphyton interactions: reciprocal influences of periphyton and grazer nutrient stoichiometry. J N Am Benthol Soc 25:632–642

    Article  Google Scholar 

  • Marchetti MP, Moyle PB, Levine R (2004) Alien fishes in California watersheds: characteristics of successful and failed invaders. Ecol Appl 14:587–596

    Article  Google Scholar 

  • McClain M, Dent L, Gergel S et al (2001) Hot spots and hot moments in landscape biogeochemistry. Ecological Society of America Annual Meeting Abstracts, pp 26–26

  • McIntyre PB, Michel E, Olsgard M (2006) Top-down and bottom-up controls on periphyton biomass and productivity in Lake Tanganyika. Limnol Oceanogr 51:1514–1523

    Article  CAS  Google Scholar 

  • McIntyre PB, Jones LE, Flecker AS et al (2007) Fish extinctions alter nutrient recycling in tropical freshwaters. Proc Natl Acad Sci USA 104:4461–4466

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • McIntyre PB, Flecker AS, Vanni MJ et al (2008) Fish distributions and nutrient cycling in streams: can fish create biogeochemical hotspots? Ecology 89:2335–2346

    Article  PubMed  Google Scholar 

  • Mendoza RE, Cudmore B, Orr R et al (2009) Trinational risk assessment guidelines for aquatic alien invasive species. CEC Project Report. Commission for Environmental Cooperation, Montréal

  • Moore J, Herbst D, Heady W et al (2012) Stream community and ecosystem responses to the boom and bust of an invading snail. Biol Invasions 14:2435–2446

    Article  Google Scholar 

  • Moyle PB, Light T (1996) Biological invasions of fresh water: empirical rules and assembly theory. Biol Conserv 78:149–161

    Article  Google Scholar 

  • Murdock JN, Gido KB, Dodds WK et al (2010) Consumer return chronology alters recovery trajectory of stream ecosystem structure and function following drought. Ecology 91:1048–1062

    Article  PubMed  Google Scholar 

  • Nico LG, Martin RT (2001) The South American suckermouth armored catfish, Pterygoplichthys anisitsi (Pisces : Loricariidae), in Texas, with comments on foreign fish introductions in the American southwest. Southwest Nat 46:98–104

    Article  Google Scholar 

  • Nummi P, Vaananen VM, Malinen J (2006) Alien grazing: indirect effects of muskrats on invertebrates. Biol Invasions 8:993–999

    Article  Google Scholar 

  • Power ME (1990) Resource enhancement by indirect effects of grazers: armored catfish, algae, and sediment. Ecology 71:897–904

    Article  Google Scholar 

  • Power ME, Matthews WJ, Stewart AJ (1985) Grazing minnows, piscivorous bass, and stream algae: dynamics of a strong interaction. Ecology 66:1448–1456

    Article  Google Scholar 

  • Reisinger AJ, Presuma DL, Gido KB et al (2011) Direct and indirect effects of central stoneroller (Campostoma anomalum) on mesocosm recovery following a flood: can macroconsumers affect denitrification? J N Am Benthol Soc 30:840–852

    Article  Google Scholar 

  • Ricciardi A (2003) Predicting the impacts of an introduced species from its invasion history: an empirical approach applied to zebra mussel invasions. Freshw Biol 48:972–981

    Article  Google Scholar 

  • Ricciardi A, Atkinson SK (2004) Distinctiveness magnifies the impact of biological invaders in aquatic ecosystems. Ecol Lett 7:781–784

    Article  Google Scholar 

  • Romanuk TN, Zhou Y, Brose U et al (2009) Predicting invasion success in complex ecological networks. Philos Trans R Soc B Biol Sci 364:1743–1754

    Article  Google Scholar 

  • Rosemond AD, Mulholland PJ, Elwood JW (1993) Top-down and bottom-up control of stream periphyton: effects of nutrients and herbivores. Ecology 74:1264–1280

    Article  Google Scholar 

  • Scott SE, Pray CL, Nowlin WH et al (2012) Effects of native and invasive species on stream ecosystem functioning. Aquat Sci 74:793–808

    Article  Google Scholar 

  • Small GE, Helton AM, Kazanci C (2009) Can consumer stoichiometric regulation control nutrient spiraling in streams? J N Am Benthol Soc 28:747–765

    Article  Google Scholar 

  • Small GE, Pringle CM, Pyron M et al (2011) Role of the fish Astyanax aeneus (Characidae) as a keystone nutrient recycler in low-nutrient Neotropical streams. Ecology 92:386–397

    Article  PubMed  Google Scholar 

  • Steinman AD (1996) Effects of grazers on freshwater benthic algae. In: Stevenson RJ, Bothwell ML, Lowe RL (eds) Algal ecology: freshwater benthic ecosystems. Elsevier, San Diego

    Google Scholar 

  • Sterner RW, Elser JJ (2002) Ecological stoichiometry: the biology of elements from molecules to the biosphere. Princeton University Press, Princeton

    Google Scholar 

  • Strayer DL (2010) Alien species in fresh waters: ecological effects, interactions with other stressors, and prospects for the future. Freshw Biol 55:152–174

    Article  Google Scholar 

  • Strayer DL (2012) Eight questions about invasions and ecosystem functioning. Ecol Lett 15:1199–1210

    Article  PubMed  Google Scholar 

  • Vanni MJ (2010) When and where do fish have strong effects on stream ecosystem processes? In: Gido KB, Jackson DA (eds) Advances in stream fish community ecology: concepts, approaches and techniques. American Fisheries Society, Bethesda, pp 531–538

    Google Scholar 

  • Vanni MJ, Flecker AS, Hood JM et al (2002) Stoichiometry of nutrient recycling by vertebrates in a tropical stream: linking species identity and ecosystem processes. Ecol Lett 5:285–293

    Article  Google Scholar 

  • Wakida-Kusunoki AT, Ruiz-Carus R, Amador-del-Angel E (2007) Amazon sailfin catfish, Pterygoplichthys pardalis (Castelnau, 1855) (Loricariidae), another exotic species established in southeastern Mexico. Southwest Nat 52:141–144

    Article  Google Scholar 

  • Weber C (1991) New taxa in Pterygoplichthys S I (Pisces, Siluriformes, Loricariidae). Rev Suisse Zool 98:637–643

    Google Scholar 

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Acknowledgments

This work was funded by the National Science Foundation (Doctoral Dissertation Enhancement Program Grant (183-8371); Integrated Graduate Education and Research in Biogeochemistry and Environmental Biocomplexity (0221658) Small Grant Program), the Fulbright-Hays Doctoral Dissertation Research Abroad Program, Sigma Xi, the Tinker Field Research Grant, the Andrew and Margaret Paul Graduate Fellowship in the Life Sciences, and the American Cichlid Association Paul V. Loiselle Conservation Fund. Organisms were harvested in Mexico using Mexican collection permit number DGOPA.07525.25706.3233 and fishes were handled using methods outlined in the IACUC protocol 2006-0169 from Cornell University. We thank Rocío Rodiles-Hernández, Sebastian Heilpern, Jessica Strickland, and Daniel Rodríguez for help with fieldwork in Mexico. We would like to thank the personnel of the Hotel Nututun for their support in Mexico. Finally, we would like to thank the editor and the three anonymous reviewers who provided insightful comments to early versions of this manuscript.

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Correspondence to Krista A. Capps.

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Capps, K.A., Ulseth, A. & Flecker, A.S. Quantifying the top-down and bottom-up effects of a non-native grazer in freshwaters. Biol Invasions 17, 1253–1266 (2015). https://doi.org/10.1007/s10530-014-0793-z

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