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Top-down effects of an invasive omnivore: detection in long-term monitoring of large-river reservoir chlorophyll-a

  • Ecosystem ecology – original research
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Abstract

Invasive species are capable of altering ecosystems through the consumption of basal resources. However, quantifying the effects of invasive species in large ecosystems is challenging. Measuring changes in basal resources (i.e., phytoplankton) at an ecosystem scale is an important and potentially translatable response vital to the understanding of how introduced species influence ecosystems. In this study, we analyzed patterns of early summer chlorophyll-a in a large-river reservoir in response to invasion of silver carp (Hypophthalmichthys molitrix). We used 25 years of ecological data from a 30-km reach of Kentucky Lake collected before and after silver carp establishment. We found significant decreases in chlorophyll-a within certain reservoir habitats since establishment of silver carp. Additionally, environmental and biological drivers of phytoplankton production showed no significant differences before and after invasion. These results suggest seasonal, and habitat-specific consumptive effects of invasive silver carp on an important basal food web resource. Further, our results convey the utility of long-term quantitative biological and physiochemical data in understanding ecosystem responses to elements of global change (i.e., species invasions). Importantly, the observed changes in the basal food web resource of Kentucky Lake may apply to other ecosystems facing invasion by silver carp (e.g., Laurentian Great Lakes). Our study offers insight into the mechanisms by which silver carp may influence ecosystems and furthers our understanding of invasive omnivores.

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References

  • Bates D, Mächler M, Bolker B, Walker S (2014) Fitting linear mixed-effects models using lme4. arXiv preprint arXiv:1406.5823. Accessed 6 Nov 2016

  • Baxter CV, Fausch KD, Murakami M, Chapman PL (2004) Fish invasion restructures stream and forest food webs by interrupting reciprocal prey subsidies. Ecology 85:2656–2663

    Article  Google Scholar 

  • Bellard C, Cassey P, Blackburn TM (2016) Alien species as a driver of recent extinctions. Biol Lett 12:20150623

    Article  PubMed  PubMed Central  Google Scholar 

  • Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, Stevens MHH, White JSS (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 24:127–135

    Article  PubMed  Google Scholar 

  • Brett MT, Muller-Navarra DC (1997) The role of highly unsaturated fatty acids in aquatic food web processes. Freshw Biol 38:483–499

    Article  CAS  Google Scholar 

  • Bukaveckas PA, Williams JJ, Hendricks SP (2002) Factors regulating autotrophy and heterotrophy in the main channel and an embayment of a large river impoundment. Aquat Ecol 36:355–369

    Article  CAS  Google Scholar 

  • Calkins HA, Tripp SJ, Garvey JE (2012) Linking silver carp habitat selection to flow and phytoplankton in the Mississippi River. Biol Invasions 14:949–958

    Article  Google Scholar 

  • Capps KA, Ulseth A, Flecker AS (2014) Quantifying the top-down and bottom-up effects of a non-native grazer in freshwaters. Biol Invasions 17:1253–1266

    Article  Google Scholar 

  • Carpenter SR, Chisholm SW, Krebs CJ, Schindler DW, Wright RF (1995) Ecosystem experiments. Science 269:324

    Article  CAS  PubMed  Google Scholar 

  • Carpenter SR, Kitchell JF, Hodgson JR (1985) Cascading trophic interactions and lake productivity. Bioscience 35:634–639

    Article  Google Scholar 

  • Chick JH, Pegg MA (2001) Invasive carp in the Mississippi River Basin. Science 292:2250–2251

    Article  CAS  PubMed  Google Scholar 

  • Clesceri S, Greenberg A, Trussell R (1989) Standard methods for the examination of water and wastewater; 17. American Public Health Association, American Water Works Association, Washington

    Google Scholar 

  • Cross WF, Baxter CV, Rosi-Marshall EJ, Hall RO Jr, Kennedy TA, Donner KC, Wellward Kelly HA, Seegert SE, Behn KE, Yard MD (2013) Food-web dynamics in a large river discontinuum. Ecol Monogr 83:311–337

    Article  Google Scholar 

  • Demott W, Müller-Navarra DC (1997) The importance of highly unsaturated fatty acids in zooplankton nutrition: evidence from experiments with Daphnia, a cyanobacterium and lipid emulsions. Freshw Biol 38:649–664

    Article  CAS  Google Scholar 

  • Dodds WK, Robinson CT, Gaiser EE, Hansen GJ, Powell H, Smith JM, Morse NB, Johnson SL, Gregory SV, Bell T, Kratz TK, McDowell WH (2012) Surprises and insights from long-term aquatic data sets and experiments. Bioscience 62:709–721

    Article  Google Scholar 

  • Ehrenfeld JG (2010) Ecosystem consequences of biological invasions. Annu Rev Ecol Evol Syst 41:59–80

    Article  Google Scholar 

  • Ellis BK, Stanford JA, Goodman D, Stafford CP, Gustafson DL, Beauchamp DA, Chess DW, Craft JA, Hansen BS (2011) Long-term effects of a trophic cascade in a large lake ecosystem. Proc Natl Acad Sci 108:1070–1075

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Finke DL, Denno RF (2004) Predator diversity dampens trophic cascades. Nature 429:407–410

    Article  CAS  PubMed  Google Scholar 

  • Fukushima M, Takamura N, Sun L, Nakagawa M, Matsushige K, Xie P (1999) Changes in the plankton community following introduction of filter-feeding planktivorous fish. Freshw Biol 42:719–735

    Article  Google Scholar 

  • Gallardo B, Clavero M, Sánchez MI, Vilà M (2016) Global ecological impacts of invasive species in aquatic ecosystems. Glob Change Biol 22:151–163

    Article  Google Scholar 

  • Holz JC, Hoagland KD, Spawn RL, Popp A, Andersen JL (1997) Phytoplankton community response to reservoir aging, 1968–92. Hydrobiologia 346:183–192

    Article  CAS  Google Scholar 

  • Irons KS, Sass GG, McClelland MA, Stafford JD (2007) Reduced condition factor of two native fish species coincident with invasion of non-native Asian carps in the Illinois River, USA Is this evidence for competition and reduced fitness? J Fish Biol 71:258–273

    Article  Google Scholar 

  • Johnson KS (1992) Chemical structure of Ledbetter Embayment, Kentucky Lake, and comparisons with the tributary creek and the mainstem. Master’s thesis, Department of Biololgy, Murray State University, Murray, Kentucky, USA

  • Kautza A, Sullivan SMP (2016) The energetic contributions of aquatic primary producers to terrestrial food webs in a mid-size river system. Ecology 97:694–705

    PubMed  Google Scholar 

  • Kenward MG, Roger JH (1997) Small sample inference for fixed effects from restricted maximum likelihood. Biometrics 53:983–997

    Article  CAS  PubMed  Google Scholar 

  • Kimmel BL, Lind OT, Paulson LJ (1990) Reservoir primary production. In: Thornton KW, Kimmel BL, Payne FE (eds) Reservoir limnology: ecological perspectives. Wiley, New York, pp 133–193

    Google Scholar 

  • Kreps TA, Baldridge AK, Lodge DM (2012) The impact of an invasive predator (Orconectes rusticus) on freshwater snail communities: insights on habitat-specific effects from a multilake long-term study. Can J Fish Aquat Sci 69:1164–1173

    Article  Google Scholar 

  • Lehner E, Liermann CR, Revenga C, Vörösmarty C, Fekete B, Crouzet P, Döll P, Endejan M, Frenken K, Magome J, Nilsson C, Robertson JC, Rödel R, Sindorf N, Wisser D (2011) High-resolution mapping of the world’s reservoirs and dams for sustainable river-flow management. Front Ecol Environ 9:494–502

    Article  Google Scholar 

  • Lenth RV, Hervé M (2014) lsmeans: Least-Squares Means. R package version 2.11. http://CRAN.R-project.org/package=lsmeans. Accessed 6 Nov 2016

  • Levine T, White D, Francisco Rice G (2014) Comparison of Schindler-Patalas traps and Wisconsin nets for monitoring zooplankton in a large, shallow reservoir. J Ky Acad Sci 74:30–36

    Google Scholar 

  • Lin Q, Jiang X, Han BP, Jeppesen E (2014) Does stocking of filter-feeding fish for production have a cascading effect on zooplankton and ecological state? A study of fourteen (sub) tropical Chinese reservoirs with contrasting nutrient concentrations. Hydrobiologia 736:115–125

    Article  CAS  Google Scholar 

  • Lodge DM, Kershner MW, Aloi JE, Covich AP (1994) Effects of an omnivorous crayfish (Orconectes rusticus) on a freshwater littoral food web. Ecology 75:1265–1281

    Article  Google Scholar 

  • Lu M, Xie P, Tang H, Shao Z, Xie L (2002) Experimental study of trophic cascade effect of silver carp (Hypophthalmichthys molitrixon) in a subtropical lake, Lake Donghu: on plankton community and underlying mechanisms of changes of crustacean community. Hydrobiologia 487:19–31

    Article  Google Scholar 

  • R Development Core Team (2014) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/. Accessed 6 Nov 2016

  • Radke RJ, Kahl U (2002) Effects of a filter-feeding fish [silver carp, Hypophthalmichthys molitrix (Val.)] on phyto-and zooplankton in a mesotrophic reservoir: results from an enclosure experiment. Freshw Biol 47:2337–2344

    Article  Google Scholar 

  • Ricciardi A, Hoopes MF, Marchetti MP, Lockwood JL (2013) Progress toward understanding the ecological impacts of nonnative species. Ecol Monogr 83:263–282

    Article  Google Scholar 

  • Sagouis A, Cucherousset J, Villéger S, Santoul F, Boulêtreau S (2015) Non-native species modify the isotopic structure of freshwater fish communities across the globe. Ecography 38:979–985

    Article  Google Scholar 

  • Sampson SJ, Chick JH, Pegg MA (2009) Diet overlap among two Asian carp and three native fishes in backwater lakes on the Illinois and Mississippi rivers. Biol Invasions 11:483–496

    Article  Google Scholar 

  • Sass GG, Cook TR, Irons KS, McClelland MA, Michaels NN, O’Hara TM, Stroub MR (2010) A mark-recapture population estimate for invasive silver carp (Hypophthalmichthys molitrix) in the La Grange Reach, Illinois River. Biol Invasions 12:433–436

    Article  Google Scholar 

  • Sass GG, Hinz C, Erickson AC, McClelland NN, McClelland MA, Epifanio JM (2014) Invasive bighead and silver carp effects on zooplankton communities in the Illinois River, Illinois, USA. J Gt Lakes Res 40:911–921

    Article  Google Scholar 

  • Scavia D, Allanb JD, Arendc KK, Bartelld S, Beletskye D, Boschf NS, Brandtg SB, Brilandh RD, Daloğlub I, DePintoi JV, Dolanj DM, Evansk MA, Farmerh TM, Gotol D, Hanm H, Höökn TO, Knighto R, Ludsinh SA, Masonp D, Michalakq AM, Richardsr RP, Robertss JJ, Rucinskib DK, Rutherfordp E, Schwabt DJ, Sesterhennn TM, Zhange H, Zhouq Y (2014) Assessing and addressing the re-eutrophicationof Lake Erie: central basin hypoxia. J Gt Lakes Res 40:226–246

    Article  CAS  Google Scholar 

  • Schaus MH, Vanni MJ (2000) Effects of gizzard shad on phytoplankton and nutrient dynamics: role of sediment feeding and fish size. Ecology 81:1701–1719

    Article  Google Scholar 

  • Schindler DW (1998) Whole-ecosystem experiments: replication versus realism: the need for ecosystem-scale experiments. Ecosystems 1:323–334

    Article  Google Scholar 

  • Solomon LE, Pendleton RM, Chick JH, Casper AF (2016) Long-term changes in fish community structure in relation to the establishment of Asian carps in a large floodplain river. Biol Invasions 18:1–13

    Article  CAS  Google Scholar 

  • Starling FLDRM (1993) Control of eutrophication by silver carp (Hypophthalmichthys molitrix) in the tropical Paranoa Reservoir (Brasilia, Brazil): a mesocosm experiment. Hydrobiologia 257:143–152

    Article  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, Caraco NF, Cole JJ, Findlay S, Pace ML (1999) Transformation of freshwater ecosystems by bivalves. Bioscience 49:19–27

    Article  Google Scholar 

  • Strong DR (1992) Are trophic cascades all wet? Differentiation and donor-control in speciose ecosystems. Ecology 73:747–754

    Article  Google Scholar 

  • Thompson RM, Hemberg M, Starzomski BM, Shurin JB (2007) Trophic levels and trophic tangles: the prevalence of omnivory in real food webs. Ecology 88:612–617

    Article  PubMed  Google Scholar 

  • Thorp JH, Delong MD (2002) Dominance of autochthonous autotrophic carbon in food webs of heterotrophic rivers. Oikos 96:543–550

    Article  Google Scholar 

  • Tilman D, Reich PB, Knops JM (2006) Biodiversity and ecosystem stability in a decade-long grassland experiment. Nature 441:629–632

    Article  CAS  PubMed  Google Scholar 

  • Tilzer MM (1988) Secchi disk—chlorophyll relationships in a lake with highly variable phytoplankton biomass. Hydrobiologia 162:163–171

    Article  CAS  Google Scholar 

  • Townsend CR (2003) Individual, population, community, and ecosystem consequences of a fish invader in New Zealand streams. Conserv Biol 17:38–47

    Article  Google Scholar 

  • Vander Zanden MJ, Casselman JM, Rasmussen JB (1999) Stable isotope evidence for the food web consequences of species invasions in lakes. Nature 401:464–467

    Article  CAS  Google Scholar 

  • Walsh JR, Carpenter SR, Vander Zanden M (2016) Invasive species triggers a massive loss of ecosystem services through a trophic cascade. Proc Natl Acad Sci 113:4081–4085

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang JQ, Flickinger SA, Be K, Liu YAO, Xu H (1989) Daily food consumption and feeding rhythm of silver carp (Hypophthalmichthys molitrix) during fry to fingerling period. Aquaculture 83:73–79

    Article  Google Scholar 

  • Wetzel RG (2001) Limnology: lake and river ecosystems. Gulf Professional Publishing, San Diego

    Google Scholar 

  • White DS, Johnston KL, Rice GT (2007) The Center for Reservoir Research over its first twenty years with special reference to the long-term monitoring program. J Ky Acad Sci 68:2–10

    Google Scholar 

  • Williamson CJ, Garvey JE (2005) Growth, fecundity, and diets of newly established silver carp in the middle Mississippi River. Trans Am Fish Soc 134:1423–1430

    Article  Google Scholar 

  • Xiao L, Ouyang H, Li H, Chen M, Lin Q, Han BP (2010) Enclosure study on phytoplankton response to stocking of silver carp (Hypophthalmichthys molitrix) in a eutrophic tropical reservoir in South China. Int Rev Hydrobiol 95:428–439

    Article  CAS  Google Scholar 

  • Xie P (1999) Gut contents of silver carp, Hypophthalmichthys molitrix, and the disruption of a centric diatom, Cyclotella, on passage through the esophagus and intestine. Aquaculture 180:295–305

    Article  Google Scholar 

  • Xie P, Yang Y (2000) Long-term changes of Copepoda community (1957–1996) in a subtropical Chinese lake stocked densely with planktivorous filter-feeding silver and bighead carp. J Plankton Res 22:1757–1778

    Article  Google Scholar 

  • Yurista PM, White DS, Kipphut GW, Johnston K, Rice G, Hendricks SP (2004) Nutrient patterns in a mainstem reservoir, Kentucky Lake, USA, over a 10-year period. Lake Reserv Manag 20:148–163

    Article  CAS  Google Scholar 

  • Zhang H, Rutherford ES, Mason DM, Breck JT, Wittmann ME, Cooke RM, Lodge DM, Rothlisberger JD, Zhu X, Johnson TB (2016) Forecasting the impacts of silver and bighead carp on the Lake Erie food web. Trans Am Fish Soc 145:136–152

    Article  Google Scholar 

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Acknowledgements

We would like to thank D. White for sharing his expertise on the Kentucky Lake ecosystem and helpful comments on earlier manuscript drafts. Additionally, we are very grateful to the numerous other faculty and volunteers of Hancock Biological Station including G. Harris, K. Johnston, A. Hayden, R. Trites, and C. Hendrix for their long dedication and continued contribution to the Kentucky Lake Long-Term Monitoring Program. We thank M. Moore, and C. Mecklin for their statistical advice and consult. We also thank the Whiteman lab, B. Richardson, D. Jent, S. Peterson and A. Gilmore for their helpful dialogue throughout the project. Finally, we are thankful for L. Barmuta and two anonymous reviewers whose comments led to a greatly improved manuscript. Funding for this project was provided by Watershed Studies Institute of Murray State University, U.S. Fish and Wildlife Grant Number (F13AP00999) and the Research Enhancement Award from Kentucky Water Resource Research Institute awarded to B.B. Tumolo.

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  1. Benjamin B. Tumolo

    Present address: Department of Ecology, Montana State University, P.O. Box 173460, Bozeman, MT, 59717-3460, USA

Authors and Affiliations

  1. Watershed Studies Institute, Murray State University, Murray, KY, 42071, USA

    Benjamin B. Tumolo & Michael B. Flinn

  2. Hancock Biological Station, Murray State University, Murray, KY, 42071, USA

    Benjamin B. Tumolo

  3. Department of Biological Sciences, Murray State University, 2112 Biology Building, Murray, KY, 42071, USA

    Michael B. Flinn

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  1. Benjamin B. Tumolo
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Contributions

MBF conceived the idea; BBT and MBF developed the experimental design; BBT compiled and organized long-term data into data matrices for analysis; BBT and MBF conducted analyses and discussed results. BBT wrote the original manuscript draft and MBF contributed revisions.

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Correspondence to Benjamin B. Tumolo.

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Communicated by Leon A. Barmuta.

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Tumolo, B.B., Flinn, M.B. Top-down effects of an invasive omnivore: detection in long-term monitoring of large-river reservoir chlorophyll-a . Oecologia 185, 293–303 (2017). https://doi.org/10.1007/s00442-017-3937-x

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