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Differential ecological impacts of invader and native predatory freshwater amphipods under environmental change are revealed by comparative functional responses

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Abstract

Predicting the ecological impacts of damaging invasive species under relevant environmental contexts is a major challenge, for which comparative functional responses (the relationship between resource availability and consumer uptake rate) have great potential. Here, the functional responses of Gammarus pulex, an ecologically damaging invader in freshwaters in Ireland and other islands, were compared with those of a native trophic equivalent Gammarus duebeni celticus. Experiments were conducted at two dissolved oxygen concentrations (80 and 50 % saturation), representative of anthropogenic water quality changes, using two larval prey, blackfly (Simuliidae spp.) and mayfly (Baetis rhodani). Overall, G. pulex had higher Type II functional responses and hence predatory impacts than G. d. celticus and the functional responses of both predators were reduced by lowered oxygen concentration. However, this reduction was of lower magnitude for the invader as compared to the native. Further, the invader functional response at low oxygen was comparable to that of the native at high oxygen. Attack rates of the two predators were similar, with low oxygen reducing these attack rates, but this effect occurred more strongly for blackfly than mayfly prey. Handling times were significantly lower for the invader compared with the native, and significantly higher at low oxygen, however, the effect of lowered oxygen on handling times was minimal for the invader and pronounced for the native. Maximum feeding rates were significantly greater for the invader compared with the native, and significantly reduced at low oxygen, with this effect again lesser for the invader as compared to the native. The greater functional responses of the invader corroborate with its impacts on recipient macroinvertebrate communities when it replaces the native. Further, our experiments predict that the impact of the invader will be less affected than the native under altered oxygen regimes driven by anthropogenic influences.

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References

  • Abrams PA (2000) The evolution of predator–prey interactions: theory and evidence. Annu Rev Ecol Syst 31:79–105

    Article  Google Scholar 

  • Alexander ME, Dick JTA, O’Connor NE, Haddaway NR, Farnsworth KD (2012) Functional responses of the intertidal amphipod Echinogammarus marinus: effects of prey supply, model selection and habitat complexity. Mar Ecol Prog Ser 468:191–202

    Article  Google Scholar 

  • Alexander ME, Dick JTA, Weyl OLF, Robinson TB, David M, Robinson B, Richardson DM (2014) Existing and emerging high impact invasive species are characterized by higher functional responses than natives. Biol Lett 10:2–6

    Article  Google Scholar 

  • Allan JD (2004) Landscapes and riverscapes: the influence of land use on stream ecosystems. Annu Rev Ecol Syst 35:257–284

    Article  Google Scholar 

  • Ansa-Asare OD, Marr IL, Cresser MS (2000) Evaluation of modelled and measured patterns of dissolved oxygen in a freshwater lake as an indicator of the presence of biodegradable organic pollution. Water Res 34(4):1079–1088

    Article  CAS  Google Scholar 

  • Barrios-O’Neill D, Dick JTA, Emmerson M, Ricciardi A, MacIsaac HJ, Alexander ME (2014) Fortune favours the bold: a higher predator reduces the impact of a native but not an invasive intermediate predator. J Anim Ecol 83:693–701

    Article  Google Scholar 

  • Bergelson JM (1985) A mechanistic interpretation of prey selection by Anax junius larvae (Odonata: Aeschnidae). Ecol Soc Am 66(6):1699–1705

    Google Scholar 

  • Biological Monitoring Working Party (1978) Final report: assessment and presentation of the biological quality of rivers in Great Britain, December 1978. Water Data Unit, Department of the Environment, London

  • Bolker BM (2008) Ecological models and data in R. Princeton University Press, Princeton

  • Bollache L, Dick JTA, Farnsworth KD, Montgomery WI (2008) Comparison of the functional responses of invasive and native amphipods. Biol Lett 4:166–169

    Article  PubMed Central  PubMed  Google Scholar 

  • Carlton JT (1979) History, biogeography, and ecology of the introduced marine and estuarine invertebrates of the Pacific coast of North America Ph.D. dissertation. University of California, Davis, p 904

  • Colton TF (1987) Extending functional response models to include a second prey type: an experimental test. Ecology 68:900–912

    Article  Google Scholar 

  • Davies L, Smith CD (1958) The distribution and growth of Prosimulium larvae (Diptera: Simuliidae) in hill streams in Northern England. J Anim Ecol 27:335–348

    Article  Google Scholar 

  • Dennert HG (1974) Tolerance differences and interspecific competition in three members of the amphipod genus Gammarus. Bijd Dierk 44(1):83–99

    Google Scholar 

  • Development Core Team R (2013) R: A language and environment for statistical computing. R foundation for statistical computing, Vienna

    Google Scholar 

  • Dick JTA, Irvine DE, Elwood RW (1990) Differential predation by males on moulted females may explain the competitive displacement of Gammarus duebeni by G. pulex (Amphipoda). Behav Ecol Sociobiol 26:41–45

    Article  Google Scholar 

  • Dick JTA, Gallagher K, Avlijas S, Clarke HC, Lewis SE, Leung S, Minchin D, Caffrey J, Alexander ME, Maguire C, Harrod C, Reid N, Haddaway NR, Farnsworth KD, Penk M, Ricciardi A (2013) Ecological impacts of an invasive predator explained and predicted by comparative functional responses. Biol Invaions 15:837–846

    Article  Google Scholar 

  • Dick JTA, Alexander ME, Jeschke JM, Ricciardi A, MacIsaac HJ, Robinson TB, Kumschick S, Weyl OLF, Dunn AM, Hatcher MJ, Paterson RA, Farnsworth KD, Richardson DM (2014) Advancing impact prediction and hypothesis testing in invasion ecology using a comparative functional response approach. Biol Invasions 16(4):735–753

    Article  Google Scholar 

  • Dodd JA, Dick JTA, Alexander ME, MacNeil C, Dunn AM, Aldridge DC (2014) Predicting the ecological impacts of a new freshwater invader: functional responses and prey selectivity of the “killer shrimp”, Dikerogammarus villosus, compared to the native Gammarus pulex. Freshw Biol 59(2):337–352

    Article  Google Scholar 

  • Francis-Floyd R (2003) Dissolved oxygen for fish production (FA27). University of Florida Institute of Food and Agricultural Sciences, Gainesville. http://edis.ifas.ufl.edu/DLN. Accessed 19 May 2014

  • Gallardo B, Aldridge DC (2013a) Priority setting for invasive species management: risk assessment of Ponto-Caspian invasive species into Great Britain. Ecol Appl 23(2):352–364

    Article  PubMed  Google Scholar 

  • Gallardo B, Aldridge DC (2013b) The “dirty dozen”: socio-economic factors amplify the invasion potential of 12 high-risk aquatic invasive species in Great Britain and Ireland. J Appl Ecol 50(3):757–766

    Article  Google Scholar 

  • Hassell MP (1978) The dynamics of arthropod predator–prey systems. Princeton University Press, Princeton, pp 28–49

    Google Scholar 

  • Hassell MP, May RM (1973) Stability in insect host-parasite models. J Anim Ecol 42:693–726

    Article  Google Scholar 

  • Holling CS (1959) Some characteristics of simple types of predation and parasitism. Can Entomol 91:385–398

    Article  Google Scholar 

  • Hossie TJ, Murray DL (2010) You can’t run but you can hide: refuge use in frog tadpoles elicits density-dependent predation by dragonfly larvae. Oecologia 163:395–404

  • Iacarella JC, Dick JTA, Alexander ME, Ricciardi A (in press) Ecological impacts of invasive alien species along temperature gradients: testing the role of environmental matching. Ecol Appl

  • Jazdzewski K, Konopacka A, Grabowski M (2004) Recent drastic changes in the gammarid fauna (Crustacea, Amphipoda) of the Vistula River deltaic system in Poland caused by alien invaders. Divers Distrib 10:81–87

    Article  Google Scholar 

  • Jeschke JM, Kopp M, Tollrian R (2002) Predator functional responses: discriminating between handling and digesting prey. Ecol Monogr 72(1):95–112

    Article  Google Scholar 

  • Juliano SA (2001) Non-linear curve fitting: predation and functional response curves. In: Scheiner SM, Gurevitch J (eds) Design and analysis of ecological experiments. Oxford University Press, Oxford, pp 178–196

    Google Scholar 

  • Kelly DW, Dick JTA, Montgomery WI (2002) The functional role of Gammarus (Crustacea, Amphipoda): shredders, predators or both? Hydrobiologia 485:199–203

    Article  Google Scholar 

  • Kelly DW, Dick JTA, Montgomery WI, MacNeil C (2003) Differences in composition of macroinvertebrate communities with invasive and native Gammarus spp. (Crustacea: Amphipoda). Freshw Biol 48:306–315

    Article  Google Scholar 

  • Kelly DW, Bailey RJE, MacNeil C, Dick JTA, McDonald RA (2006) Invasion by the amphipod Gammarus pulex alters community composition of native freshwater macroinvertebrates. Divers Distrib 12:525–534

    Article  Google Scholar 

  • Kurtak DC (1978) Efficiency of filter feeding of black fly larvae (Diptera: Simuliidae). Can J Zool 56(7):1608–1623

    Article  Google Scholar 

  • Long WC, Seitz RD (2008) Trophic interactions under stress: hypoxia enhances foraging in an estuarine food web. Mar Ecol Prog Ser 362:59–68

  • Long WC, Whitefleet-Smith L (2013) Cannibalism in red king crab: habitat, ontogeny, and the predator functional response. J Exp Mar Biol Ecol 449:142–148

    Article  Google Scholar 

  • Long WC, Seitz RD, Brylawski BJ, Lipcius RN (2014) Individual, population and ecosystem effects of hypoxia on a dominant benthic bivalve in Chesapeake Bay. Ecol Monogr 84:303–327

    Article  Google Scholar 

  • MacNeil C, Montgomery WI, Dick JTA, Elwood RW (2001) Factors influencing the distribution of native and introduced Gammarus spp. in Irish river systems. Arch Hydrobiol 151:353–368

    Google Scholar 

  • MacNeil C, Prenter J, Briffa M, Fielding NJ, Dick JTA, Riddell GE, Hatcher MJ, Dunn AM (2004) The replacement of a native freshwater amphipod by an invader: roles for environmental degradation and intraguild predation. Can J Fish Aquat Sci 61:1627–1635

    Article  Google Scholar 

  • MacNeil C, Dick JTA, Gell FR, Selman R, Lenartowicz P, Hynes HBN (2009) A long-term study (1949–2005) of experimental introductions to an island; freshwater amphipods (Crustacea) in the Isle of Man (British Isles). Divers Distrib 15:232–241

    Article  Google Scholar 

  • MacNeil C, Dick JTA, Alexander ME, Dodd JA, Ricciardi A (2013) Predators vs. alien: differential biotic resistance to an invasive species by two resident predators. NeoBiota 19:1–19

    Article  Google Scholar 

  • Médoc V, Spataro T, Arditi R (2013) Prey: predator ratio dependence in the functional response of a freshwater amphipod. Freshw Biol 58:858–865

    Article  Google Scholar 

  • Murdoch WW (1969) Switching in general predators: experiments on predator specificity and stability of prey populations. Ecol Monogr 39(4):335–354

    Article  Google Scholar 

  • Murdoch WW, Oaten A (1975) Predation and population stability. Adv Ecol Res 9:1–131

    Article  Google Scholar 

  • Nestlerode J, Diaz R (1998) Effects of periodic environmental hypoxia on predation of a tethered polychaete, Glycera americana:implications for trophic dynamics. Mar Ecol Prog Ser 172:185–195

    Article  Google Scholar 

  • Ozaki N, Fukushima T, Harasawa H, Kojiri T, Kawashima K, Ono M (2003) Statistical analyses on the effects of air temperature fluctuations on river water qualities. Hydrol Process 17:2837–2853

    Article  Google Scholar 

  • Parkhill KL, Gulliver JS (2002) Effect of inorganic sediment on whole-stream productivity. Hydrobiologia 472:5–17

    Article  Google Scholar 

  • Paterson RA, Dick JTA, Pritchard DW, Ennis M, Hatcher MJ, Dunn AM (2014) Predicting invasive species impacts: a community module functional response approach reveals context dependencies. J Anim Ecol

  • Piscart C, Manach A, Copp GH, Marmonier P (2007) Distribution and microhabitats of native and non-native gammarids (Amphipoda, Crustacea) in Brittany, with particular reference to the endangered endemic sub-species Gammarus duebeni celticus. J Biogeogr 34(3):524–533

    Article  Google Scholar 

  • Pörtner HO, Knust R (2007) Climate change affects marine fishes through the oxygen limitation of thermal tolerance. Science 315:95–97

    Article  PubMed  Google Scholar 

  • Raddum GG, Fjellheim A (1993) Life cycle and production of Baetis rhodani in a regulated river in Western Norway: comparison of pre- and post-regulation conditions. Regul Rivers Res Manag 8:49–61

    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(6):972–981

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Rodda GH, Fritts TH, Conry PJ (1992) Origin and population growth of the brown tree snake, Boiga irregularis, on Guam. Pac Sci 46:46–57

    Google Scholar 

  • Roy HE, Peyton J, Aldridge DC, Bantock T, Blackburn TM, Britton R et al (2014) Horizon scanning for invasive alien species with the potential to threaten biodiversity in Great Britain. Glob Change Biol 20(12):3859–3871

    Article  Google Scholar 

  • Sandberg E (1997) Does oxygen deficiency modify the functional response of Saduria entomon (Isopoda) to Bathyporeia pilosa (Amphipoda)? Mar Biol 129(3):499–504

    Article  Google Scholar 

  • Savidge JA (1987) Extinction of an island forest avifauna by an introduced snake. Ecology 68:660–668

    Article  Google Scholar 

  • Seitz RD, Marshall L, Hines A, Clark K (2003) Effects of hypoxia on predator–prey dynamics of the blue crab Callinectes sapidus and the Baltic clam Macoma balthica in Chesapeake Bay. Mar Ecol Prog Ser 257:179–188

    Article  Google Scholar 

  • Shoji J, Masuda R, Yamashita Y, Tanaka M (2005) Effect of low dissolved oxygen concentrations on behavior and predation rates on red sea bream Pagrus major larvae by the jellyfish Aurelia aurita and by juvenile Spanish mackerel Scomberomorus niphonius. Mar Biol 147:863–868

    Article  Google Scholar 

  • Simberloff D, Martin J-L, Genovesi P, Maris V, Wardle DA, Aronson J, Courchamp F, Galil B, Garcıa-Berthou E, Pascal M, Pyšek P, Sousa R, Tabacchi E, Vila M (2013) Impacts of biological invasions: what’s what and the way forward. Trends Ecol Evol 28:58–66

    Article  PubMed  Google Scholar 

  • Smout S, Rindorf A, Wanless S, Daunt F, Harris MP, Matthiopoulos J (2013) Seabirds maintain offspring provisioning rate despite fluctuations in prey abundance: a multi-species functional response for guillemots in the North Sea (S. Votier, Ed.). J Appl Ecol 50(4):1071–1079

    Article  Google Scholar 

  • Strange CD, Glass GB (1979) The distribution of freshwater Gammarids in Northern Ireland. Proc R Ir Acad 79(11):145–153

    Google Scholar 

  • Taylor DL, Eggleston DB (2000) Effects of hypoxia on an estuarine predator–prey interaction: foraging behavior and mutual interference in the blue crab Callinectes sapidus and the infaunal clam prey Mya arenaria. Mar Ecol Prog Ser 196:221–237

    Article  Google Scholar 

  • Thomsen MS, Wernberg T, Olden JD, Griffin JN, Silliman BR (2011) A framework to study the context-dependent impacts of marine invasions. J Exp Mar Biol Ecol 400:322–327

    Article  Google Scholar 

  • Trexler JC, McCullough CE, Travis J (1988) How can the functional response best be determined? Oecologia 76:206–214

    Article  Google Scholar 

  • Twardochleb LA, Novak M, Moore JW (2012) Using the functional response of a consumer to predict biotic resistance to invasive prey. Ecol Appl 22:1162–1171

    Article  PubMed  Google Scholar 

  • Walther G-R, Roques A, Hulme PE, Sykes MT, Pysek P, Kühn I et al (2009) Alien species in a warmer world: risks and opportunities. Trends Ecol Evol 24(12):686–693

    Article  PubMed  Google Scholar 

  • Whitehead PG, Wilby RL, Battarbee RW, Kernan M, Wade AJ (2009) A review of the potential impacts of climate change on surface water quality. Hydrol Sci 54(1):101–123

    Article  Google Scholar 

  • Wittmann MJ, Gabriel W, Harz E-M, Laforsch C, Jeschke JM (2013) Can Daphnia lumholtzi invade European lakes? NeoBiota 16:39–57

    Article  Google Scholar 

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Acknowledgments

We thank the Department of Employment and Learning (DEL) for funding the Ph.D., with support from ITSligo and the DST-NRF Centre of Excellence for Invasion Biology.

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Authors and Affiliations

  1. School of Biological Sciences, Institute for Global Food Security, Queen’s University Belfast, 97 Lisburn Road, Belfast, BT9 7BL, Ireland

    Ciaran Laverty & Jaimie T. A. Dick

  2. Department of Botany and Zoology, Centre for Invasion Biology, Stellenbosch University, Private Bag X1, Matieland, 7602, South Africa

    Mhairi E. Alexander

  3. Department of Environmental Science, Centre for Environmental Research Innovation and Sustainability, Institute of Technology, Sligo, Ireland

    Frances E. Lucy

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  1. Ciaran Laverty
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  2. Jaimie T. A. Dick
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Correspondence to Ciaran Laverty.

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Laverty, C., Dick, J.T.A., Alexander, M.E. et al. Differential ecological impacts of invader and native predatory freshwater amphipods under environmental change are revealed by comparative functional responses. Biol Invasions 17, 1761–1770 (2015). https://doi.org/10.1007/s10530-014-0832-9

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