, Volume 180, Issue 2, pp 519–528 | Cite as

Top predators affect the composition of naive protist communities, but only in their early-successional stage

  • Axel Zander
  • Dominique Gravel
  • Louis-Félix Bersier
  • Sarah M. Gray
Community ecology - Original research


Introduced top predators have the potential to disrupt community dynamics when prey species are naive to predation. The impact of introduced predators may also vary depending on the stage of community development. Early-succession communities are likely to have small-bodied and fast-growing species, but are not necessarily good at defending against predators. In contrast, late-succession communities are typically composed of larger-bodied species that are more predator resistant relative to small-bodied species. Yet, these aspects are greatly neglected in invasion studies. We therefore tested the effect of top predator presence on early- and late-succession communities that were either naive or non-naive to top predators. We used the aquatic community held within the leaves of Sarracenia purpurea. In North America, communities have experienced the S. purpurea top predator and are therefore non-naive. In Europe, this predator is not present and its niche has not been filled, making these communities top-predator naive. We collected early- and late-succession communities from two non-naive and two naive sites, which are climatically similar. We then conducted a common-garden experiment, with and without the presence of the top predator, in which we recorded changes in community composition, body size spectra, bacterial density, and respiration. We found that the top predator had no statistical effect on global measures of community structure and functioning. However, it significantly altered protist composition, but only in naive, early-succession communities, highlighting that the state of community development is important for understanding the impact of invasion.


Aquatic top predators Naive prey Succession Invasion Sarracenia purpurea 



We would like to thank Steve Vissault, Renaud McKinnon, Timothée Poisot, Génika Hulliger, Marie-Amélie Girardet, and Elodie Parain for their aid in marking leaves, collecting samples, and in laboratory preparation. Funding sources for this project are the Swiss National Science Foundation Grant awarded to L. F. B. (31003A_138489), the SNSF International Short Visit Grant awarded to S. M. G., and the NSERC-Discovery Grant awarded to D. G.

Author contribution statement

All authors designed the research; A. Z. and S. M. G. conducted the research; A. Z., L. F. B. and S. M. G. wrote the manuscript; all authors edited the manuscript; D. G., L. F. B. and S. M. G. funded the project.

Supplementary material

442_2015_3476_MOESM1_ESM.pdf (390 kb)
Supplementary material 1 (PDF 390 kb)


  1. Addicott JF (1974) Predation and prey community structure: an experimental study of the effect of mosquito larvae on the protozoan communities of pitcher plants. Ecology 55:475–492. doi: 10.2307/1935141 CrossRefGoogle Scholar
  2. Anson J, Dickman C (2013) Behavioral responses of native prey to disparate predators: naiveté and predator recognition. Oecologia 171(367a):171. doi: 10.1007/s00442-012-2424-7 Google Scholar
  3. 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. doi: 10.1890/04-138 CrossRefGoogle Scholar
  4. Belyea LR, Lancaster J (1999) Assembly rules within a contingent ecology. Oikos 86:402–416CrossRefGoogle Scholar
  5. Bledzki LA, Ellison AM (2003) Diversity of rotifers from northeastern USA bogs with new species records for North America and New England. Hydrobiologia 497:53–62CrossRefGoogle Scholar
  6. Bradshaw WE, Holzapfel CM (2001) Genetic shift in photoperiodic response correlated with global warming. Proc Natl Acad Sci USA 98:14509–14511. doi: 10.1073/pnas.241391498 PubMedCentralCrossRefPubMedGoogle Scholar
  7. Bruno JF, Fridley JD, Bromberg K, Bertness MD (2005) Insights into biotic interactions from studies of species invasions. In: Sax DF, Gaines SD, Stachowicz JJ (eds) Species invasions: insights into ecology, evolution and biogeography. Sinauer, Sunderland, pp 13–40Google Scholar
  8. Buckley HL, Miller TE, Ellison AM, Gotelli NJ (2003) Reverse latitudinal trends in species richness of pitcher plant food webs. Ecol Lett 6:825–829. doi: 10.1046/j.1461-0248.2003.00504.x CrossRefGoogle Scholar
  9. Buckley HL, Miller TE, Ellison AM, Gotelli NJ (2010) Local- to continental-scale variation in the richness and composition of an aquatic food web. Glob Ecol Biogeogr 19:711–723. doi: 10.1111/j.1466-8238.2010.00554.x Google Scholar
  10. Carmen C (2007) MicroResp technical manual—a versatile soil respiration system. Macaulay Institute, AberdeenGoogle Scholar
  11. Carpenter SR, Kitchell JF, Hodgson JR (1985) Cascading trophic interactions and lake productivity. Bioscience 35:634–639. doi: 10.2307/1309989 CrossRefGoogle Scholar
  12. Catford JA, Daehler CC, Murphy HT, Sheppard AW, Hardesty BD, Westcott DA, Rejmánek M, Bellingham PJ, Pergl J, Horvitz CC, Hulme PE (2012) The intermediate disturbance hypothesis and plant invasions: implications for species richness and management. Perspect Plant Ecol Evol Syst 14:231–241. doi: 10.1016/j.ppees.2011.12.002 CrossRefGoogle Scholar
  13. Clarke KR, Gorley RN (2006) PRIMER v6: user manual/tutorial. PRIMER-E, PlymouthGoogle Scholar
  14. Clements FE (1916) Plant succession; an analysis of the development of vegetation. Carnegie Institution of Washington, WashingtonCrossRefGoogle Scholar
  15. Connell JH, Slatyer RO (1977) Mechanisms of succession in natural communities and their role in community stability and organization. Am Nat 111:1119–1144. doi: 10.2307/2460259 CrossRefGoogle Scholar
  16. Correvon H (1947) Fleurs des eaux et des marais. Delachaux et Niestlé, NeuchâtelGoogle Scholar
  17. Courchamp F, Chapuis J-L, Pascal M (2003) Mammal invaders on islands: impact, control and control impact. Biol Rev 78:347–383. doi: 10.1017/S1464793102006061 CrossRefPubMedGoogle Scholar
  18. Cox JG, Lima SL (2006) Naiveté and an aquatic-terrestrial dichotomy in the effects of introduced predators. Trends Ecol Evol 21:674–680. doi: 10.1016/j.tree.2006.07.011 CrossRefPubMedGoogle Scholar
  19. del Moral R, Wood DM (1993) Early primary succession on the volcano Mount St. Helens. J Veg Sci 4:223–234. doi: 10.2307/3236108 CrossRefGoogle Scholar
  20. Diamond J, Case TJ (1986) Overview: Introductions, extinctions, exterminations, and invasions. In: Diamond J, Case TJ (eds) Community ecology. Harper and Row, London, pp 65–79Google Scholar
  21. Dickman CR (1996) Impact of exotic generalist predators on the native fauna of Australia. Wildl Biol 2:185–195Google Scholar
  22. Elton CS (1958) The ecology of invasions by animals and plants. Methuen, LondonCrossRefGoogle Scholar
  23. Estes JA, Terborgh J, Brashares JS, Power ME, Berger J, Bond WJ, Carpenter SR, Essington TE, Holt RD, Jackson JBC, Marquis RJ, Oksanen L, OksanenT Paine RT, Pikitch EK, Ripple WJ, Sandin SA, Scheffer M, Schoener TW, Shurin JB, Sinclair RE, Soulé ME, Virtanen R, Wardle DA (2011) Trophic downgrading of planet earth. Science 333:301–306. doi: 10.1126/science.1205106 CrossRefPubMedGoogle Scholar
  24. Fabian Y, Sandau N, Bruggisser OT, Kehrli P, Aebi A, Rohr RP, Naisbit RE, Bersier LF (2012) Diversity protects plant communities against generalist molluscan herbivores. Ecol Evol 2:2460–2473. doi: 10.1002/ece3.359 PubMedCentralCrossRefPubMedGoogle Scholar
  25. Fargione JE, Tilman D (2005) Diversity decreases invasion via both sampling and complementarity effects. Ecol Lett 8:604–611. doi: 10.1111/j.1461-0248.2005.00753.x CrossRefGoogle Scholar
  26. Foster BL, Tilman D (2000) Dynamic and static views of succession: testing the descriptive power of the chronosequence approach. Plant Ecol 146:1–10CrossRefGoogle Scholar
  27. Fragnière Y (2012) Colonisation of Sarracenia purpurea pitchers in Swiss populations. Master thesis, Unit of Ecology and Evolution, University of Fribourg, Fribourg, SwitzerlandGoogle Scholar
  28. Freeman AS, Byers JE (2006) Divergent induced responses to an invasive predator in marine mussel populations. Science 313:831–833CrossRefPubMedGoogle Scholar
  29. Gebühr C, Pohlon E, Schmidt AR, Küsel K (2006) Development of microalgae communities in the phytotelmata of allochthonous populations of Sarracenia purpurea (Sarraceniaceae). Plant Biol 8:849–860. doi: 10.1055/s-2006-924474 CrossRefPubMedGoogle Scholar
  30. Gleason HA (1926) The individualistic concept of the plant association. Bull Torrey Bot Club 53:7. doi: 10.2307/2479933 CrossRefGoogle Scholar
  31. Goldschmidt T, Witte F, Wanink J (1993) Cascading effects of the introduced nile perch on the detritivorous/phytoplanktivorous species in the sublittoral areas of Lake Victoria. Conserv Biol 7:686–700. doi: 10.1046/j.1523-1739.1993.07030686.x CrossRefGoogle Scholar
  32. Gotelli NJ, Ellison AM (2006) Food-web models predict species abundances in response to habitat change. PLoS Biol 4:e324PubMedCentralCrossRefPubMedGoogle Scholar
  33. Gray SM (2012) Succession in the aquatic Sarracenia purpurea community: deterministic or driven by contingency? Aquat Ecol 46:487–499. doi: 10.1007/s10452-012-9417-9 CrossRefGoogle Scholar
  34. Gray SM, Miller TE, Mouquet N, Daufresne T (2006) Nutrient limitation in detritus-based microcosms in Sarracenia purpurea. Hydrobiologia 573:173–181. doi: 10.1007/s10750-006-0265-2 CrossRefGoogle Scholar
  35. Gray SM, Dykhuizen DE, Padilla DK (2014) The effects of species properties and community context on establishment success. Oikos. doi: 10.1111/oik.01550 Google Scholar
  36. Gurevitch J, Padilla DK (2004) Are invasive species a major cause of extinctions? Trends Ecol Evol 19:470–474CrossRefPubMedGoogle Scholar
  37. Hairston NG, Smith FE, Slobodkin LB (1960) Community structure, population control, and competition. Am Nat 94:421–425. doi: 10.2307/2458808 CrossRefGoogle Scholar
  38. Hansson L-A, Bergman E, Cronberg G (1998) Size structure and succession in phytoplankton communities: the impact of interactions between herbivory and predation. Oikos 81:337–345. doi: 10.2307/3547054 CrossRefGoogle Scholar
  39. Heard SB (1994) Pitcher-plant midges and mosquitoes: a processing chain commensalism. Ecology 75:1647–1660. doi: 10.2307/1939625 CrossRefGoogle Scholar
  40. Hector A, Dobson K, Minns A, Bazeley-White E, Lawton JH (2002) Community diversity and invasion resistance: an experimental test in a grassland ecosystem and a review of comparable studies. Ecol Res 16:819–831. doi: 10.1046/j.1440-1703.2001.00443.x CrossRefGoogle Scholar
  41. Hoekman D (2007) Top-down and bottom-up regulation in a detritus-based aquatic food web: a repeated field experiment using the pitcher plant (Sarracenia purpurea) inquiline community. Am Midl Nat 157:52–62. doi:10.1674/0003-0031(2007)157[52:TABRIA]2.0.CO;2CrossRefGoogle Scholar
  42. Hoekman D (2010) Turning up the heat: temperature influences the relative importance of top-down and bottom-up effects. Ecology 91:2819–2825. doi: 10.1890/10-0260.1 CrossRefPubMedGoogle Scholar
  43. Hunter MD, Price PW (1992) Playing chutes and ladders: heterogeneity and the relative roles of bottom-up and top-down forces in natural communities. Ecology 73:723–732CrossRefGoogle Scholar
  44. Hutchinson GE (1961) The paradox of the plankton. Am Nat 95:137–145. doi: 10.2307/2458386 CrossRefGoogle Scholar
  45. Istock CA, Wasserman SS, Zimmer H (1975) Ecology and evolution of the pitcher-plant mosquito: 1. population dynamics and laboratory responses to food and population density. Evolution 29:296–312. doi: 10.2307/2407218 CrossRefGoogle Scholar
  46. Jessup CM, Kassen R, Forde SE, Kerr B, Buckling A, Rainey PB, Bohannan BJ (2004) Big questions, small worlds: microbial model systems in ecology. Trends Ecol Evol 19:189–197. doi: 10.1016/j.tree.2004.01.008 CrossRefPubMedGoogle Scholar
  47. Jiang L, Joshi H, Flakes SK, Jung Y (2011) Alternative community compositional and dynamical states: the dual consequences of assembly history. J Anim Ecol 80:577–585. doi: 10.1111/j.1365-2656.2010.01799.x CrossRefPubMedGoogle Scholar
  48. Kadowaki K, Inouye BD, Miller TE (2012) Assembly-history dynamics of a pitcher-plant protozoan community in experimental microcosms. PLoS One 7:e42651. doi: 10.1371/journal.pone.0042651 PubMedCentralCrossRefPubMedGoogle Scholar
  49. Kneitel JM (2012) Are trade-offs among species’ ecological interactions scale dependent? A test using pitcher-plant inquiline species. PLoS One 7:e41809. doi: 10.1371/journal.pone.0041809 PubMedCentralCrossRefPubMedGoogle Scholar
  50. Kneitel JM, Miller TE (2002) Resource and top-predator regulation in the pitcher plant (Sarracenia purpurea) inquiline community. Ecology 83:680–688. doi:10.1890/0012-9658(2002)083[0680:RATPRI]2.0.CO;2CrossRefGoogle Scholar
  51. Kuno E (1987) Principles of predator–prey interaction in theoretical, experimental, and natural population systems. In: Macfadyen A, Ford ED (eds) Advances in ecological research. Academic Press, San Diego, pp 249–337Google Scholar
  52. Lee JJ, Leedale GF, Bradbury P (2000) An illustrated guide to the protozoa, 2nd edn. Society of Protozoologists, LawrenceGoogle Scholar
  53. Legendre P, Legendre L (1998) Numerical ecology, 2nd English edn. Elsevier Science, AmsterdamGoogle Scholar
  54. Lortie CJ, Brooker RW, Choler P, Kikvidze Z, Michalet R, Pugnaire FI, Callaway RM (2004) Rethinking plant community theory. Oikos 107(4337):433. doi: 10.1111/j.0030-1299.2004.13250.x CrossRefGoogle Scholar
  55. Louette G, De Meester L, Declerck S (2008) Assembly of zooplankton communities in newly created ponds. Freshwater Biol 53:2309–2320. doi: 10.1111/j.1365-2427.2008.02052.x Google Scholar
  56. Lowry E, Rollinson EJ, Laybourn AJ, Scott TE, Aiello-Lammens ME, Gray SM, Mickley J, Gurevitch J (2013) Biological invasions: a field synopsis, systematic review, and database of the literature. Ecol Evol 3:182–196. doi: 10.1002/ece3.431 PubMedCentralCrossRefGoogle Scholar
  57. Manchester SJ, Bullock JM (2000) The impacts of non-native species on UK biodiversity and the effectiveness of control. J Appl Ecol 37:845–864. doi: 10.1046/j.1365-2664.2000.00538.x CrossRefGoogle Scholar
  58. Miller TE, Kneitel JM (2005) Inquiline communities in pitcher plants as prototypical metacommunities. In: Holyoak M, Leibold MA, Holt RD (eds) Metacommunities: spatial dynamics and ecological communities. University of Chicago, Chicago, pp 122–145Google Scholar
  59. Miller TE, terHorst C (2012) Testing successional hypotheses of stability, heterogeneity, and diversity in pitcher-plant inquiline communities. Oecologia 170:243–251. doi: 10.1007/s00442-012-2292-1 CrossRefPubMedGoogle Scholar
  60. Miller TE, Kneitel JM, Burns JH (2002) Effect of community structure on invasion success and rate. Ecology 83:898–905. doi:10.1890/0012-9658(2002)083[0898:EOCSOI]2.0.CO;2CrossRefGoogle Scholar
  61. Mortensen HS, Dupont YL, Olesen JM (2008) A snake in paradise: disturbance of plant reproduction following extirpation of bird flower-visitors on Guam. Biol Conserv 141:2146–2154. doi: 10.1016/j.biocon.2008.06.014 CrossRefGoogle Scholar
  62. Moyle PB (1986) Fish introductions into North America: patterns and ecological impact. In: Mooney H, Drake J (eds) Ecology of biological invasions of North America and Hawaii. Springer, New York, pp 27–43CrossRefGoogle Scholar
  63. Nastase AJ, Rosa CDL, Newell SJ (1995) Abundance of pitcher-plant mosquitoes, Wyeomyia smithii (Coq.) (Diptera: Culicidae) and midges, Metriocnemus knabi Coq. (Diptera: Chironomidae), in relation to pitcher characteristics of Sarracenia purpurea L. Am Midl Nat 133:44–51. doi: 10.2307/2426346 CrossRefGoogle Scholar
  64. Oakley CA, Knox JS (2013) Plant species richness increases resistance to invasion by non-resident plant species during grassland restoration. Appl Veg Sci 16:21–28. doi: 10.1111/j.1654-109X.2012.01202.x CrossRefGoogle Scholar
  65. Odum EP (1969) The strategy of ecosystem development. Science 164:262–270. doi: 10.1126/science.164.3877.262 CrossRefPubMedGoogle Scholar
  66. Paolucci EM, MacIsaac HJ, Ricciardi A (2013) Origin matters: alien consumers inflict greater damage on prey populations than do native consumers. Divers Distrib 19:988–995. doi: 10.1111/ddi.12073 CrossRefGoogle Scholar
  67. Parisod C, Trippi C, Galland N (2005) Genetic variability and founder effect in the pitcher plant Sarracenia purpurea (Sarraceniaceae) in populations introduced into Switzerland: from inbreeding to invasion. Ann Bot 95:277–286. doi: 10.1093/aob/mci023 PubMedCentralCrossRefPubMedGoogle Scholar
  68. Pianka ER (1970) On r- and K-selection. Am Nat 104:592–597. doi: 10.2307/2459020 CrossRefGoogle Scholar
  69. Pomati F, Kraft NJB, Posch T et al (2013) Individual cell based traits obtained by scanning flow-cytometry show selection by biotic and abiotic environmental factors during a phytoplankton spring bloom. PLoS One 8:e71677. doi: 10.1371/journal.pone.0071677 PubMedCentralCrossRefPubMedGoogle Scholar
  70. R Core Team (2013) R: a language and environment for statistical computing. Version 3.0.0. R Foundation for Statistical Computing, Vienna.
  71. Rasband WS (2012) ImageJ. US National Institutes of Health, Bethesda, USA.
  72. Rees M, Condit R, Crawley M et al (2001) Long-term studies of vegetation dynamics. Science 293:650–655. doi: 10.1126/science.1062586 CrossRefPubMedGoogle Scholar
  73. Rodriguez L (2006) Can invasive species facilitate native species? Evidence of how, when, and why these impacts occur. Biol Invasions 8:927–939. doi: 10.1007/s10530-005-5103-3 CrossRefGoogle Scholar
  74. Salo P, Korpimäki E, Banks PB et al (2007) Alien predators are more dangerous than native predators to prey populations. Proc R Soc Lond B Biol Sci 274:1237–1243. doi: 10.1098/rspb.2006.0444 CrossRefGoogle Scholar
  75. Savidge JA (1984) Guam: paradise lost for wildlife. Biol Conserv 30:305–317. doi: 10.1016/0006-3207(84)90049-1 CrossRefGoogle Scholar
  76. Savidge JA (1987) Extinction of an island forest avifauna by an introduced snake. Ecology 68:660–668. doi: 10.2307/1938471 CrossRefGoogle Scholar
  77. Schmitz OJ, Kalies EL, Booth MG (2006) Alternative dynamic regimes and trophic control of plant succession. Ecosystems 9:659–672CrossRefGoogle Scholar
  78. Shurin JB, Borer ET, Seabloom EW, Anderson K, Blanchette CA, Broitman B, Cooper SD, Halpern BS (2002) A cross-ecosystem comparison of the strength of trophic cascades. Ecol Lett 5:785–791. doi: 10.1046/j.1461-0248.2002.00381.x CrossRefGoogle Scholar
  79. Sih A, Bolnick DI, Luttbeg B, Orrock JL, Peacor SD, Pintor LM, Preisser E, Rehage JS, Vonesh JR (2010) Predator–prey naïveté, antipredator behavior, and the ecology of predator invasions. Oikos 119:610–621. doi: 10.1111/j.1600-0706.2009.18039.x CrossRefGoogle Scholar
  80. Simon M, Cho B, Azam F (1992) Significance of bacterial biomass in lakes and the ocean: comparison to phytoplankton biomass and biogeochemical implications. Mar Ecol Prog Ser 86:103–110CrossRefGoogle Scholar
  81. Smith JB (1902) Life-history of Aëdes smithii Coq. J NY Entomol Soc 10:10–15. doi: 10.2307/25002970 Google Scholar
  82. Sommer U, Gliwicz ZM, Lampert W, Duncan A (1986) The PEG-model of seasonal succession of planktonic events in fresh waters. Arch Hydrobiol 106:433–471Google Scholar
  83. Sousa WP (1979) Experimental investigations of disturbance and ecological succession in a rocky intertidal algal community. Ecol Monogr 49:227–254. doi: 10.2307/1942484 CrossRefGoogle Scholar
  84. Srivastava DS, Kolasa J, Bengtsson J, Gonzalez A, Lawler SP, Miller TE, Munguia P, Romanuk T, Schneider DC, Trzcinski MK (2004) Are natural microcosms useful model systems for ecology? Trends Ecol Evol 19:379–384. doi: 10.1016/j.tree.2004.04.010 CrossRefPubMedGoogle Scholar
  85. Streble H, Krauter D (2002) Das Leben im Wassertropfen: Mikroflora und Mikrofauna des Süßwassersm, 9th edn. Kosmos (Franckh-Kosmos), StuttgartGoogle Scholar
  86. Walls M, Kortelainen I, Sarvala J (1990) Prey responses to fish predation in freshwater communities. Ann Zool Fenn 27:183–199. doi: 10.2307/23736038 Google Scholar
  87. Wiles GJ, Bart J, Beck RE, Aguon CF (2003) Impacts of the brown tree snake: patterns of decline and species persistence in Guam’s avifauna. Conserv Biol 17:1350–1360. doi: 10.1046/j.1523-1739.2003.01526.x CrossRefGoogle Scholar
  88. Wootton JT (1993) Size-dependent competition: effects on the dynamics vs. the end point of mussel bed succession. Ecology 74:195–206. doi: 10.2307/1939514 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Axel Zander
    • 1
  • Dominique Gravel
    • 2
  • Louis-Félix Bersier
    • 1
  • Sarah M. Gray
    • 1
  1. 1.Unit of Ecology and Evolution, Department of BiologyUniversity of FribourgFribourgSwitzerland
  2. 2.Département de biologie, chimie et géographieUniversité du Québec à RimouskiRimouskiCanada

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