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High resources and infectious disease facilitate invasion by a freshwater crustacean

Abstract

It is well-established that both resources and infectious disease can influence species invasions, but little is known regarding interactive effects of these two factors. We performed a series of experiments to understand how resources and parasites can jointly affect the ability of a freshwater invasive zooplankton to establish in a population of a native zooplankton. In a life history trial, we found that both species increased offspring production to the same degree as algal resources increased, suggesting that changes in resources would have similar effects on both species. In a microcosm experiment simulating an invasion, we found that the invasive species reached its highest densities when there was a combination of both high resources and the presence of a shared parasite, but not for each of these conditions alone (i.e., a significant resource x parasite interaction). This result can be explained by changes in native host population density; high resource levels initially led to an increase in the density of the native host, which caused larger epidemics when the parasite was present. This high infection prevalence caused a subsequent reduction in native host density, increasing available resources and allowing the invasive species to establish relatively dense populations. Thus, in this system, native communities with a combination of high resource levels and parasitism may be the most vulnerable to invasions. More generally, our results suggest that parasitism and resource availability can have interactive, non-additive effects on the outcome of invasions.

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References

  • Alford RA, Wilbur HM (1985) Priority effects in experimental pond communities: competition between Bufo and Rana. Ecology 66:1097–1105

    Article  Google Scholar 

  • Auld SKJR, Brand J (2017) Simulated climate change, epidemic size, and host evolution across host-parasite populations. Glob Change Biol 23:5045–5053

    Article  Google Scholar 

  • Becker DJ, Streicker DG, Altizer S (2015) Linking anthropogenic resources to wildlife-pathogen dynamics: a review and meta-analysis. Ecol Lett 18:483–495

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Boersma M, Spaak P, De Meester L (1998) Predator-mediated plasticity in morphology, life history, and behavior of Daphnia: the uncoupling of responses. Am Nat 152:237–248

    CAS  PubMed  Google Scholar 

  • Brooks JL (1957) The systematics of North American Daphnia. Mem Conn Acad Arts Sci 13:1–180

    Google Scholar 

  • Buck JC, Rohr JR, Blasutein AR (2016) Effects of nutrient supplementation on host-pathogen dynamics of the amphibian chytrid fungus: a community approach. Freshw Biol 61:110–120

    CAS  Article  PubMed  Google Scholar 

  • Byers JE (2002) Impact of non-indigenous species on natives enhanced by anthropogenic alteration of selection regimes. Oikos 97:449–458

    Article  Google Scholar 

  • Callaway RM, Ridenour WM (2004) Novel weapons: invasive success and the evolution of increased competitive ability. Front Ecol Environ 2:436–443

    Article  Google Scholar 

  • Chase JM, Knight TM (2006) Effects of eutrophication and snails on Eurasian watermilfoil (Myriophyllum spicatum) invasion. Biol Invasions 8:1643–1649

    Article  Google Scholar 

  • Civitello DJ, Penczykowski RM, Hite JL, Duffy MA, Hall SR (2013) Potassium stimulates fungal epidemics in Daphnia by increasing host and parasite reproduction. Ecology 94:380–388

    Article  PubMed  Google Scholar 

  • Civitello DJ, Penczykowski RM, Smith AN, Shocket MS, Duffy MA, Hall SR (2015) Resources, key traits and the size of fungal epidemics in Daphnia populations. J Anim Ecol 84:1010–1017

    Article  PubMed  Google Scholar 

  • Clavero M, Garcia-Berthou E (2005) Invasive species are a leading cause of animal extinctions. Trends Ecol Evol 20:110

    Article  PubMed  Google Scholar 

  • Cornet S, Bichet C, Larcombe S, Faivre B, Sorci G (2014) Impact of host nutritional status on infection dynamics and parasite virulence in a bird-malaria system. J Anim Ecol 83:256–265

    Article  PubMed  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 

  • Day K, Kaushik NK (1987) An assessment of the chronic toxicity of the synthetic pyrethroid, fenvalerate, to Daphnia galeata mendotae, using life tables. Environ Pollut 44:13–26

    CAS  Article  PubMed  Google Scholar 

  • Decaestecker E, Verreydt D, De Meester L, Declerck SAJ (2015) Parasite and nutrient enrichment effects on Daphnia interspecific competition. Ecology 96:1421–1430

    Article  PubMed  Google Scholar 

  • Duffy MA, Hall SR (2008) Selective predation and rapid evolution can jointly dampen effects of virulent parasites on Daphnia populations. Am Nat 171:499–510

    Article  PubMed  Google Scholar 

  • Duffy MA, Sivars-Becker L (2007) Rapid evolution and ecological host-parasite dynamics. Ecol Lett 10:44–53

    Article  PubMed  Google Scholar 

  • Dzialowski AR, O’Brien WJ, Swaffar SM (2000) Range expansion and potential dispersal mechanisms of the exotic cladoceran Daphnia lumholtzi. J Plankton Res 22:2205–2223

    Article  Google Scholar 

  • Ebert D (1993) The trade-off between offspring size and number in Daphnia magna: the influence of genetic, environmental and maternal effects. Arch Hydrobiol 4(Suppl. 90):453–473

    Google Scholar 

  • Ebert D, Lipsitch M, Mangin KL (2000) The effect of parasites on host population density and extinction: experimental epidemiology with Daphnia and six microparasites. Am Nat 156:459–477

    Article  PubMed  Google Scholar 

  • Fey SB, Cottingham KL (2012) Thermal sensitivity predicts the establishment success of nonnative species in a mesocosm warming experiment. Ecology 93:2313–2320

    Article  PubMed  Google Scholar 

  • Fey SB, Herren CM (2014) Temperature-mediated biotic interactions influence enemy release of nonnative species in warming environments. Ecology 95:2246–2256

    Article  PubMed  Google Scholar 

  • Going BM, Hillerislambers J, Levine JM (2009) Abiotic and biotic resistance to grass invasion in serpentine annual plant communities. Oecologia 159:839–847

    Article  PubMed  Google Scholar 

  • Gross KL, Mittelbach GG, Reynolds HL (2005) Grassland invasibility and diversity: responses to nutrients, seed input, and disturbance. Ecology 86:476–486

    Article  Google Scholar 

  • Guo QF, Fei SL, Dukes JS, Oswalt CM, Iannone BV, Potter KM (2015) A unified approach for quantifying invasibility and degree of invasion. Ecology 96:2613–2621

    Article  PubMed  Google Scholar 

  • Hall SR, Sivars-Becker L, Becker C, Duffy MA, Tessier AJ, Cáceres CE (2007) Eating yourself sick: transmission of disease as a function of foraging ecology. Ecol Lett 10:207–218

    Article  PubMed  Google Scholar 

  • Hall SR, Becker CR, Duffy MA, Caceres CE (2011) Epidemic size determines population-level effects of fungal parasites on Daphnia hosts. Oecologia 166:833–842

    Article  PubMed  Google Scholar 

  • Havel JE, Hebert PDN (1993) Daphnia lumholtzi in North America: another exotic zooplankter. Limnol Oceanogr 38:1823–1827

    Article  Google Scholar 

  • Havel JE, Shurin JB (2004) Mechanisms, effects, and scales of dispersal in freshwater zooplankton. Limnol Oceanogr 49:1229–1238

    Article  Google Scholar 

  • Havel JE, Mabee WR, Jones JR (1995) Invasion of the exotic cladoceran Daphnia lumholtzi into North American reservoirs. Can J Fish Aquat Sci 52:151–160

    Article  Google Scholar 

  • Havel JE, Lee CE, Vander Zanden JM (2005) Do reservoirs facilitate invasions into landscapes? Bioscience 55:518–525

    Article  Google Scholar 

  • Hebert P (1995) The Daphnia of North America: an illustrated fauna. University of Guelph, CyberNatural Software

    Google Scholar 

  • Hiskey RM (1996) The occurrence of the exotic Daphnia lumholtzi in Grand Lake St Marys, Ohio. Ohio J Sci 96:100–101

    Google Scholar 

  • Hudson PJ, Dobson AP (1989) Population biology of Trichostrongylus tenuis, a parasite of economic importance for red grouse management. Parasitol Today 5:283–291

    CAS  Article  PubMed  Google Scholar 

  • Jessop TS, Smissen P, Scheelings F, Dempster T (2012) Demographic and phenotypic effects of human mediated trophic subsidy on a large Australian lizard (Varanus varius): meal ticket or last supper? PLoS One 7:e34069

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Johnson PTJ, Chase JM, Dosch KL, Hartson RB, Gross JA, Larson DJ, Sutherland DR, Carpenter SR (2007) Aquatic eutrophication promotes pathogenic infection in amphibians. Proc Natl Acad Sci USA 104:15781–15786

    CAS  Article  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 

  • Kelly DW, Paterson RA, Townsend CR, Poulin R, Tompkins DM (2009) Parasite spillback: a neglected concept in invasion ecology? Ecology 90:2047–2056

    CAS  Article  PubMed  Google Scholar 

  • Kestrup AM, Thomas SH, van Rensburg K, Ricciardi A, Duffy MA (2011) Differential infection of exotic and native freshwater amphipods by a parasitic water mold in the St, Lawrence River. Biolo Invasions 13:769–779

    Article  Google Scholar 

  • Kleiven OT, Larsson P, Hobaek A (1992) Sexual reproduction in Daphnia magna requires three stimuli. Oikos 65:197–206

    Article  Google Scholar 

  • Kneitel JM, Chase JM (2004) Disturbance, predator, and resource interactions alter container community composition. Ecology 85:2088–2093

    Article  Google Scholar 

  • Knevel IC, Lans T, Menting FBJ, Hertling UM, van der Putten WH (2004) Release from native root herbivores and biotic resistance by soil pathogens in a new habitat both affect the alien Ammophila arenaria in South Africa. Oecologia 141:502–510

    Article  PubMed  Google Scholar 

  • Kolar CS, Boase JC, Clapp DF, Wahl DH (1997) Potential effect of invasion by an exotic zooplankter, Daphnia lumholtzi. J Freshw Ecol 12:521–530

    Article  Google Scholar 

  • Kotov AA, Taylor DJ (2014) Daphnia lumholtzi Sars, 1885 (Cladocera: Daphniidae) invades Argentina. J Limnol 73:167–172

    Article  Google Scholar 

  • Lennon JT, Smith VH, Dzialowski AR (2003) Invasibility of plankton food webs along a trophic state gradient. Oikos 103:191–203

    Article  Google Scholar 

  • Lockwood JL, Cassey P, Blackburn T (2005) The role of propagule pressure in explaining species invasions. Trends Ecol Evol. 20:223–228

    Article  PubMed  Google Scholar 

  • Martin PH, Marks PL (2006) Intact forests provide only weak resistance to a shade-tolerant invasive Norway maple (Acer platanoides L.). J Ecol 94:1070–1079

    Article  Google Scholar 

  • McKenzie VJ, Townsend AR (2007) Parasitic and infectious disease responses to changing global nutrient cycles. EcoHealth 4:384–396

    Article  Google Scholar 

  • Moyle PB, Light T (1996) Fish invasions in California: do abiotic factors determine success? Ecology 77:1666–1670

    Article  Google Scholar 

  • Paterson RA, Rauque CA, Fernandez MV, Townsend CR, Poulin R, Tompkins DM (2013) Native fish avoid parasite spillback from multiple exotic hosts: consequences of host density and parasite competency. Biol Invasions 15:2205–2218

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Prenter J, MacNeil C, Dick JTA, Dunn AM (2004) Roles of parasites in animal invasions. Trends Ecol Evol 19:385–390

    Article  PubMed  Google Scholar 

  • Price PW, Westoby M, Rice B (1988) Parasite-mediated competition: some predictions and tests. Am Nat 131:544–555

    Article  Google Scholar 

  • Prior NH, Washington CN, Housley JM, Hall SR, Duffy MA, Cáceres CE (2011) Maternal effects and epidemiological traits in a planktonic host–parasite system. Evol Ecol Res 13:401–413

    Google Scholar 

  • R Core Team (2017) R: A language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, Austria. https://www.R-project.org

  • Searle CL, Ochs JH, Cáceres CE, Chiang SL, Gerardo NM, Hall SR, Duffy MA (2015) Plasticity, not genetic variation, drives infection success of a fungal parasite. Parasitology 142:839–848

    CAS  Article  PubMed  Google Scholar 

  • Searle CL, Cortez MH, Hunsberger KK, Grippi DC, Oleksy IA, Shaw CL, de la Serna SB, Lash CL, Dhir KL, Duffy MA (2016a) Population density, not host competence, drives patterns of disease in an invaded community. Am Nat 188:554–566

    Article  PubMed  Google Scholar 

  • Searle CL, Shaw CL, Hunsberger KK, Prado M, Duffy MA (2016b) Salinization decreases population densities of the freshwater crustacean, Daphnia dentifera. Hydrobiologia 770:165–172

    CAS  Article  Google Scholar 

  • Settle WH, Wilson LT (1990) Invasion by the variegated leafhopper and biotic interactions: parasitism, competition, and apparent competition. Ecology 71:1461–1470

    Article  Google Scholar 

  • Shulman MJ, Ogden JC, Ebersole JP, McFarland WN, Miller SL, Wolf NG (1983) Priority effects in the recruitment of juvenile coral reef fishes. Ecology 64:1508–1513

    Article  Google Scholar 

  • Smilanich AM, Mason PA, Sprung L, Chase TR, Singer MS (2011) Complex effects of parasitoids on pharmacophagy and diet choice of a polyphagous caterpillar. Oecologia 165:995–1005

    Article  PubMed  Google Scholar 

  • Stachowicz JJ, Byrnes JE (2006) Species diversity, invasion success, and ecosystem functioning: disentangling the influence of resource competition, facilitation, and extrinsic factors. Mar Ecol Prog Ser 311:251–262

    Article  Google Scholar 

  • Strauss A, White A, Boots M (2012) Invading with biological weapons: the importance of disease-mediated invasions. Funct Ecol 26:1249–1261

    Article  Google Scholar 

  • Symons CC, Arnott SE (2014) Timing is everything: priority effects alter community invasibility after disturbance. Ecology and Evolution 4:397–407

    Article  PubMed  PubMed Central  Google Scholar 

  • Therneau T (2015) A package for survival analysis in S. Version 2.38. Url: https://CRAN.R-project.org/package=survival. Accesed 6 June 2017

  • Tilman D (2004) Niche tradeoffs, neutrality, and community structure: a stochastic theory of resource competition, invasion, and community assembly. Proc Natl Acad Sci USA 101:10854–10861

    CAS  Article  PubMed  Google Scholar 

  • Tuttle LJ, Sikkel PC, Cure K, Hixon MA (2017) Parasite-mediated enemy release and low biotic resistance may facilitate invasion of Atlantic coral reefs by Pacific red lionfish (Pterois volitans). Biol Invasions 19:563–575

    Article  Google Scholar 

  • Tyler AC, Lambrinos JG, Grosholz ED (2007) Nitrogen inputs promote the spread of an invasive marsh grass. Ecol Appl 17:1886–1898

    Article  PubMed  Google Scholar 

  • Venesky MD, Parris MJ, Storfer A (2009) Impacts of Batrachochytrium dendrobatidis infection on tadpole foraging performance. EcoHealth 6:565–575

    Article  PubMed  Google Scholar 

  • Winsor GL, Innes DJ (2002) Sexual reproduction in Daphnia pulex (Crustacea: Cladocera): observations on male mating behaviour and avoidance of inbreeding. Freshw Biol 47:441–450

    Article  Google Scholar 

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Acknowledgements

We would like to thank M.A. Duffy and M.R. Christie for feedback on the manuscript. This project was funded by the Department of Biological Sciences at Purdue University, Purdue Honors College research funds for JKI, a McAtee stipend for BRH, and a Cable-Silkman award to BRH.

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Contributions

CLS designed the experiments and analyzed the data. BRH, AMM, JKI, and MAW performed the experiments. CLS wrote the manuscript; all other authors provided editorial advice.

Corresponding author

Correspondence to Catherine L. Searle.

Additional information

Communicated by Pieter Johnson.

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Searle, C.L., Hochstedler, B.R., Merrick, A.M. et al. High resources and infectious disease facilitate invasion by a freshwater crustacean. Oecologia 188, 571–581 (2018). https://doi.org/10.1007/s00442-018-4237-9

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  • DOI: https://doi.org/10.1007/s00442-018-4237-9

Keywords

  • Daphnia dentifera
  • Daphnia lumholtzi
  • Eutrophication
  • Invasive species
  • Pathogen