Biological Invasions

, Volume 7, Issue 4, pp 733–746 | Cite as

Invasive plants and their escape from root herbivory: a worldwide comparison of the root-feeding nematode communities of the dune grass Ammophila arenaria in natural and introduced ranges

  • W. H. van der Putten
  • G. W. Yeates
  • H. Duyts
  • C. Schreck. Reis
  • G. Karssen
Article

Abstract

Invasive plants generally have fewer aboveground pathogens and viruses in their introduced range than in their natural range, and they also have fewer pathogens than do similar plant species native to the introduced range. However, although plant abundance is strongly controlled by root herbivores and soil pathogens, there is very little knowledge on how invasive plants escape from belowground enemies. We therefore investigated if the general pattern for aboveground pathogens also applies to root-feeding nematodes and used the natural foredune grass Ammophila arenariaas a model. In the late 1800s, the European A. arenariawas introduced into southeast Australia (Tasmania), New Zealand, South Africa, and the west coast of the USA to be used for sand stabilization. In most of these regions, it has become a threat to native vegetation, because its excessive capacity to stabilize wind-blown sand has changed the geomorphology of coastal dunes. In stable dunes of most introduced regions, A. arenaria is more abundant and persists longer than in stabilized dunes of the natural range. We collected soil and root samples and used additional literature data to quantify the taxon richness of root-feeding nematodes on A.␣arenaria in its natural range and collected samples from the four major regions where it has been introduced. In most introduced regions A. arenaria did not have fewer root-feeding nematode taxa than the average number in its natural range, and native plant species did not have more nematode taxa than the introduced species. However, in the introduced range native plants had more feeding-specialist nematode taxa than A. arenaria and major feeding specialists (the sedentary endoparasitic cyst and root knot nematodes) were not found on A. arenaria in the southern hemisphere. We conclude that invasiveness of A. arenaria correlates with escape from feeding specialist nematodes, so that the pattern of escape from root-feeding nematodes is more alike escape from aboveground insect herbivores than escape from aboveground pathogens and viruses. In the natural range of A. arenaria, the number of specialist-feeding nematode taxa declines towards the margins. Growth experiments are needed to determine the relationship between nematode taxon diversity, abundance, and invasiveness of A. arenaria.

Keywords

Ammophila arenaria Ammophila breviligulata biotic resistance hypothesis enemy escape hypothesis feeding specialist invasive plant root herbivore soil pathogen 

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References

  1. Beckstead, J, Parker, IM 2003Invasiveness of Ammophila arenaria: release from soil-borne pathogens?Ecology8428242831Google Scholar
  2. Bever, JD 1994Feedback between plants and their soil communities in an old field communityEcology7519651977Google Scholar
  3. Bever, JD 2003Soil community feedback and the coexistence of competitors: conceptual frameworks and empirical testsNew Phytologist157465473CrossRefGoogle Scholar
  4. Blossey, B, Hunt-Joshi, TR 2003Belowground herbivory by insects: influence on plants and aboveground herbivoresAnnual Review of Entomology48521547CrossRefPubMedGoogle Scholar
  5. Bongers, T 1988De nematoden van Nederland Stichting Uitgeverij Koninklijke Nederlandse Natuurhistorische VerenigingUtrechtNederlandGoogle Scholar
  6. Brinkman, EP, Veen, JA, Putten, WH 2004Plant recruitment of endoparasitic nematodes may influence, but not regulate, ectoparasitic nematodesApplied Soil Ecology276575CrossRefGoogle Scholar
  7. Brown, VK, Gange, AC 1992Secondary plant succession – how is it modified by insect herbivoryVegetatio101313CrossRefGoogle Scholar
  8. Brzeski, MW 1998Nematodes of Tylenchina in Poland and temperate EuropeMuzeum i Instytut Zoologii Polska Akademia Nauk. WarszawaPoland397Google Scholar
  9. Buell, AC, Pickart, AJ, Stuart, JD 1995Introduction history and invasion patterns of Ammophila arenaria on the north coast of CaliforniaConservation Biology915871593CrossRefGoogle Scholar
  10. Callaway, RM, DeLuca, TH, Belliveau, WM 1999Biological-control herbivores may increase competitive ability of the noxious weed Centaurea maculosaEcology8011961201Google Scholar
  11. Clapp, JP, Stoel, CD, Putten, WH 2000Rapid identification of cyst (Heterodera spp., Globodera spp.) and root-knot (Meloidogyne spp.) nematodes on the basis of ITS2 sequence variation detected by PCR-SSCP (PCR-Single-Strand Conformational Polymorphism) in cultures and field samplesMolecular Ecology912231232CrossRefPubMedGoogle Scholar
  12. Clark, SE, Driesche, RG, Sturdevant, N, Kegly, S 2001bEffect of root feeding insects on spotted knapweed (Centaurea maculosa) stand densitySouthwestern Entomologist26129135Google Scholar
  13. Clark, SE, Driesche, RG, Sturdevant, N, Elkinton, J, Buonaccorsi, JP 2001aEffects of site characteristics and release history on establishment of Agapeta zoegana (Lepidoptera: Cochylidae) and Cyphocleonus achates (Coleoptera: Curculionidae), root-feeding herbivores of spotted knapweed, Centaurea maculosaBiological Control22122130CrossRefGoogle Scholar
  14. Clay, K 1995Correlates of pathogen species richness in the grass familyCanadian Journal of Botany73S42S49Google Scholar
  15. Cook, R 1982Cereal and grass hosts of some gramineous cyst nematodesEPPO Bulletin1299411Google Scholar
  16. Cooper, BA 1955

    A preliminary key to British species of Heterodera for use in soil examinations

    McE Kevan, DK eds. Soil ZoologyButterworths Scientific PublicationsLondon269280
    Google Scholar
  17. Cooper, JI, Harrison, BD 1973The role of weed hosts and the distribution and activity of vector nematodes in the ecology of tobacco rattle virusAnnals of Applied Biology735366PubMedGoogle Scholar
  18. De Deyn, GB, Raaijmakers, CE, Zoomer, HR, Berg, MP, De Ruiter, PC, Verhoef, HA, Bezemer, TM, Putten, WH 2003Soil invertebrate fauna enhances grassland succession and diversityNature422711713CrossRefPubMedGoogle Scholar
  19. DeRooij-vander Goes, PCEM 1995The role of plant-parasitic nematodes and soil-borne fungi in the decline of Ammophila arenaria (L.) LinkNew Phytologist129611669Google Scholar
  20. Hertling, UM, Lubke, RA 1999Use of Ammophila arenaria for dune stabilisation in South Africa and its current distribution – perceptions and problemsEnvirontal Management24467482CrossRefGoogle Scholar
  21. Hertling, UM, Lubke, RA 2000Assessing the potential for biological invasion – the case of Ammophila arenaria in South AfricaSouth African Journal of Science96520527Google Scholar
  22. Heyligers, PC 1985The impact of introduced plants on foredune formation in south-east AustraliaProceedings of the Ecological Society of Australia142341Google Scholar
  23. Huiskes, AHL 1979Biological flora of the British Isles: Ammophila arenaria (L.) Link (Psamma arenaria (L.) Roem. et Schult.: Calamagrostis arenaria (L.) Roth)Journal of Ecology67363382Google Scholar
  24. Jobin, A, Schaffner, U, Nentwig, W 1996The structure of the phytophagous insect fauna on the introduced weed Solidago altissima in SwitzerlandEntomologia Experimentalis et Applicata793342CrossRefGoogle Scholar
  25. Karssen, G, Aelst, A, Cook, R 1998aRedescription of the root-knot nematode Meloidogyne maritima Jepson, 1987 (Nematoda: Heteroderidae), a parasite of Ammophila arenaria (L.) LinkNematologica44241253Google Scholar
  26. Karssen, G, Aelst, A, Putten, WH 1998bDescription of Meloidogyne duytsi n. sp. (Nematoda: Heteroderidae), a root-knot nematode from Dutch coastal foredunesFundamental and Applied Nematology21299306Google Scholar
  27. Keane, RM, Crawley, MJ 2002Exotic plant invasions and the enemy release hypothesisTrends in Ecology and Evolution17164170CrossRefGoogle Scholar
  28. Kisiel, M 1970On the systematic and geographical distribution of the nematodes inhabiting sand dunes in an Ammophila arenaria plant communityZeszyty Naukowe Wyszej Szkoly Rolniczej w Szczecinie34151193Google Scholar
  29. Kliromonos, JN 2002Feedback with soil biota contributes to plant rarity and invasiveness in communitiesNature4176770Google Scholar
  30. Knevel, IC, Lans, T, Putten, WH, Menting, FBJ, Hertling, UM 2004The role of the enemy release hypothesis and the biotic resistance hypothesis in the establishment of the alien Ammophila arenaria in South AfricaOecologia141502510CrossRefPubMedGoogle Scholar
  31. Levine, JM, Vila, M, D’Antonio, CM, Dukes, JS, Grigulis, K, Lavorel, S 2003Mechanisms underlying the impacts of exotic plant invasionsBiological Sciences270775781Proceedings of the Royal Society of London, Series BCrossRefPubMedGoogle Scholar
  32. Little, LR, Maun, MA 1996The ‘Ammophila problem’ revisited: a role for mycorrhizal fungiJournal of Ecology8417Google Scholar
  33. Liebhold, AM, MacDonald, WL, Bergdahl, D, Mastro, VC 1995Invasion by Exotic Forest Pests: A Threat to Forest EcosystemsForest Science Monograph. Society of American ForestersBethesda, MD(No. 30): ii + 49 ppGoogle Scholar
  34. Maun, MA 1998Adaptations of plants to burial in coastal sand dunesCanadian Journal of Botany76713738CrossRefGoogle Scholar
  35. Memmott, J, Fowler, SV, Paynter, Q, Sheppard, , AW, , Syrett, P 2000The invertebrate fauna on broom, Cytisus scoparius, in two native and two exotic habitatsActa Oecologia21213222CrossRefGoogle Scholar
  36. Mitchell, CE, Power, AG 2003Release of invasive plants from fungal and viral pathogensNature421625627CrossRefPubMedGoogle Scholar
  37. Owen, SJ 1996Ecological Weeds on Conservation Land in New Zealand: A DatabaseDepartment of ConservationWellington, New Zealand118Google Scholar
  38. Packer, A, Clay, K 2000Soil pathogens and spatial patterns of seedling mortality in a temperate treeNature404278281CrossRefPubMedGoogle Scholar
  39. Packer, A, Clay, K 2002Soil pathogens and Prunus serotina seedlings and sapling growth near conspecific treesEcology84108119Google Scholar
  40. Pimentel, D 2002Biological Invasions: Economic and Environmental Costs of Alien Plant, Animal, and Microbe SpeciesCRC PressBoca Raton, FL369Google Scholar
  41. Reinhart, KO, Packer, A, Putten, WH, Clay, K 2003Plant-soil biota interactions and spatial distribution of black cherry in its native and invasive rangesEcology Letters610461050CrossRefGoogle Scholar
  42. Rejmanek, M, Richardson, DM 1996What attributes make some plants more invasiveEcology7716651661Google Scholar
  43. Robinson, AF, Orr, CC, Abernathy, JR 1978Distribution of Nothanguina phyllobia and its potential as a biological control agent for silver-leaf nightshadeJournal of Nematology10362366Google Scholar
  44. Robinson, AJ, Stone, AR, Hooper, DJ, Rowe, JA 1996A redescription of Heterodera arenaria Cooper 1955, a cyst nematode from marram grassFundamental and Applied Nematology19109117Google Scholar
  45. Seliskar, DM, Huettel, RN 1993Nematode involvement in die-out of Ammophila breviligulata(Poaceae) on the Mid-Atlantic coastal dunesJournal of Coastal Research997103Google Scholar
  46. Stanton, NL 1988The underground in grasslandsAnnual Review of Ecology and Systematics19573589CrossRefGoogle Scholar
  47. Torchin, ME, Lafferty, KD, Dobson, AP, McKenzie, VJ, Kuris, AM 2003Introduced species and their missing parasitesNature421628630PubMedGoogle Scholar
  48. Putten, WH 2003Plant defense below ground and spatio-temporal processes in natural vegetationEcology8422692280Google Scholar
  49. Putten, WH, Stoel, CD 1998Plant parasitic nematodes and spatio-temporal variation in natural vegetationApplied Soil Ecology10253262CrossRefGoogle Scholar
  50. Putten, WH, Dijk, C, Peters, BAM 1993Plant-specific soil-borne diseases contribute to succession in foredune vegetationNature3625356CrossRefGoogle Scholar
  51. van der Stoel CD (2001) Specificity, Pathogenicity and Population Dynamics of the Endoparasitic Nematode Hederodera arenaria in Coastal Foredunes. PhD thesis Wageningen University, The NetherlandsGoogle Scholar
  52. Stoel, CD, Putten, WH, Duyts, H 2002Development of a negative plant-soil feedback in the expansion zone of the clonal grass Ammophila arenaria following root formation and nematode colonisationJournal of Ecology90978988CrossRefGoogle Scholar
  53. Verschoor, BC, De Goede, RGM, De Vries, FW, Brussaard, L 2001Changes in the composition of the plant-feeding nematode community in grasslands after cessation of fertiliser applicationApplied Soil Ecology17117CrossRefGoogle Scholar
  54. Virginia, RA, Jarell, WM, Whitford, WG, Freckman, DW 1992Soil biota and soil properties in the surface rooting zone of mesquite (Prosopis glandulosa) in historical and recently desertified Chihuahuan Desert habitatsBiology and Fertility of Soils149098CrossRefGoogle Scholar
  55. Wall, JW, Skene, KR, Neilson, R 2002Nematode community and trophic structure along a sand dune successionBiology and Fertility of Soils4293301CrossRefGoogle Scholar
  56. Wardle, DA 2002Communities and Ecosystems: Linking the Aboveground and Belowground ComponentsPrinceton University PressPrinceton, NJGoogle Scholar
  57. Wiedemann, AM, Pickart, AJ 1996The Ammophilaproblem on the Northwest Coast of North AmericaLandscape and Urban Planning34287299CrossRefGoogle Scholar
  58. Williamson, M 1996Biological InvasionsChapman & HallLondonGoogle Scholar
  59. Yeates, GW 1967Studies on nematodes from dune sands. 9. Quantitative comparison of the nematode faunas of six localitiesNew Zealand Journal of Science10927948Google Scholar
  60. Yeates, GW 1968An analysis of annual variation of the nematode fauna in dune sand, at Himatangi Beach, New ZealandPedobiologia8173207Google Scholar
  61. Yeates, GW 1999Effects of plants on nematode community structureAnnual Review of Phytopathology37127149CrossRefPubMedGoogle Scholar
  62. Yeates, GW, Williams, PA 2001Influence of three invasive weeds and site factors on soil microfauna in New ZealandPedobiologia45367383Google Scholar
  63. Yeates, GW, Bongers, T, De Goede, RGM, Freckman, DW, Georgieva, SS 1993Feeding habits in soil nematode families and genera – an outline for soil ecologistsJournal of Nematology25315331Google Scholar

Copyright information

© Springer 2005

Authors and Affiliations

  • W. H. van der Putten
    • 1
  • G. W. Yeates
    • 2
  • H. Duyts
    • 1
  • C. Schreck. Reis
    • 3
  • G. Karssen
    • 4
  1. 1.Department of Multitrophic InteractionsNetherlands Institute of Ecology (NIOO-KNAW)ZG HeterenThe Netherlands
  2. 2.Landcare ResearchPalmerston NorthNew Zealand
  3. 3.Departamento de BotânicaIMAR, Universidade de CoimbraCoimbraPortugal
  4. 4.Plant Protection Service, Nematology sectionHC WageningenThe Netherlands

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