Biological Invasions

, Volume 21, Issue 5, pp 1511–1527 | Cite as

Herbivore accumulation on invasive alien plants increases the distribution range of generalist herbivorous insects and supports proliferation of non-native insect pests

  • Jonatan RodríguezEmail author
  • Vinton Thompson
  • Margarita Rubido-Bará
  • Adolfo Cordero-Rivera
  • Luís González
Original Paper


Invasive alien plant species have become dominant components of many landscapes, where they are indicators of ecological disequilibria. They coexist and compete with native plants, disrupting a wide range of trophic interactions, and must cope with a new array of herbivores. We examined factors influencing the occurrence of invertebrate herbivores on two invasive alien plant species, Acacia dealbata and Carpobrotus edulis, and surrounding native vegetation in the northwestern Iberian Peninsula. The aims were to assess the accumulation of herbivorous insects, including the distribution and frequency of herbivorous insects at different invasion levels (low, medium and high), and to evaluate whether introduced plants favour native or exotic, and generalist or specialist herbivorous insects in newly evolving plant–herbivore networks. To achieve these objectives, we surveyed A. dealbata along transects in five mixed pine forests and four shrublands, and C. edulis in nine coastal areas using quadrats. We identified nine herbivore species feeding on one or both of these species and determined that herbivore species composition in forest and coastal areas is directly tied to host preference, as well as related to invasion levels of A. dealbata in forest areas. On average, the introduced species in both the forest and coastal areas had approximately threefold more herbivore species (~ 50% of them exotics) than native plants. The introduced plants in forest areas had approximately eightfold more species interaction strength between herbivores and plants (a measure of the importance of each plant species to each herbivore). Overall, generalist herbivores were favoured by the invasion of the introduced plants. The results also demonstrate that exotic insects are supported by introduced plants, increasing the local occurrence and range of insect pests. Considering our observations, management strategies should be implemented to favour the restoration and protection of native areas for conserving biodiversity.


Acacia dealbata Biotic resistance Carpobrotus edulis Ecological networks Plant–insect interactions Spittlebugs 



This work was funded by Xunta de Galicia, Spain (CITACA Strategic Partnership, Reference: ED431E 2018/07). JR was supported by a research contract (GRC2015/012) from the Xunta de Galicia/FEDER, Consellería de Educación y Ordenación Universitaria. This research was partially carried out within the framework of the project “Retos en la gestión de la planta invasora Carpobrotus edulis. Variabilidad fenotípica y cambios en la relación suelo-planta durante el proceso de invasion” (in Spanish), Reference CGL2013-48885-C2-1-R, funded by the Ministry of Economy and Competence (Spanish Government). The authors are grateful to the staff of the Laboratory of Plant Ecophysiology (University of Vigo) for the field support, Dr. Josefina Garrido for the help in the identification of species, and Dr. Ruben Heleno for help and advice in ecological network analysis. We wish to thank the reviewers and the Editor for their helpful and insightful comments that we feel have substantially improved our manuscript.

Supplementary material

10530_2019_1913_MOESM1_ESM.docx (7.4 mb)
Supplementary material 1 (DOCX 7577 kb)


  1. Aguilera N, Guedes LM, Becerra J et al (2015) Morphological effects at radicle level by direct contact of invasive Acacia dealbata Link. Flora Morphol Distrib Funct Ecol Plants 215:54–59. CrossRefGoogle Scholar
  2. Albert M (1995) Portrait of an invader II: the ecology and management of Carpobrotus edulis. Newsl Calif Exot Pest Plant Counc 3:4–6Google Scholar
  3. Almeida RPP, Nunney L (2015) How do plant diseases caused by Xylella fastidiosa emerge? Plant Dis 99:1457–1467. CrossRefGoogle Scholar
  4. Anderson MJ (2006) Distance-based tests for homogeneity of multivariate dispersions. Biometrics 62:245–253. CrossRefPubMedGoogle Scholar
  5. Barbier S, Gosselin F, Balandier P (2008) Influence of tree species on understory vegetation diversity and mechanisms involved—a critical review for temperate and boreal forests. For Ecol Manag 254:1–15. CrossRefGoogle Scholar
  6. Bascompte J, Jordano P, Olesen JM (2006) Asymmetric coevolutionary networks facilitate biodiversity maintenance. Science 312:431–433. CrossRefPubMedGoogle Scholar
  7. Bezemer TM, Harvey JA, Cronin JT (2014) Response of native insect communities to invasive plants. Annu Rev Entomol 59:119–141. CrossRefPubMedGoogle Scholar
  8. Blüthgen N, Menzel F, Blüthgen N (2006) Measuring specialization in species interaction networks. BMC Ecol 6:9. CrossRefPubMedPubMedCentralGoogle Scholar
  9. Burgess TI, Wingfield MJ (2017) Pathogens on the move: a 100-year global experiment with planted eucalypts. Bioscience 67:14–25. CrossRefGoogle Scholar
  10. Callaway RM, Ridenour WM (2004) Novel weapons: invasive success and the evolution of increased competitive ability. Front Ecol Environ 2:436–443.;2 CrossRefGoogle Scholar
  11. Campoy JG, Retuerto R, Roiloa SR (2017) Resource-sharing strategies in ecotypes of the invasive clonal plant Carpobrotus edulis: specialization for abundance or scarcity of resources. J Plant Ecol 10:681–691. CrossRefGoogle Scholar
  12. Carballeira A, Devesa C, Retuerto R et al (1983) Bioclimatología de Galicia. Fundación Pedro Barrié de la Maza, A CoruñaGoogle Scholar
  13. Carroll SP (2007) Natives adapting to invasive species: Ecology, genes, and the sustainability of conservation. Ecol Res 22:892–901. CrossRefGoogle Scholar
  14. Chinery M (1997) Guía de los insectos de Europa. Ediciones Omega, BarcelonaGoogle Scholar
  15. Chiuffo MC, Policelli N, Moyano J et al (2018) Still no evidence that pathogen accumulation can revert the impact of invasive plant species. Biol Invasions 20:9–10. CrossRefGoogle Scholar
  16. Cornara D, Cavalieri V, Dongiovanni C et al (2017a) Transmission of Xylella fastidiosa by naturally infected Philaenus spumarius (Hemiptera, Aphrophoridae) to different host plants. J Appl Entomol 141:1–8. CrossRefGoogle Scholar
  17. Cornara D, Saponari M, Zeilinger AR et al (2017b) Spittlebugs as vectors of Xylella fastidiosa in olive orchards in Italy. J Pest Sci (2004) 90:1–10. CrossRefGoogle Scholar
  18. Correia M, Montesinos D, French K et al (2016) Evidence for enemy release and increased seed production and size for two invasive Australian acacias. J Ecol 104:1391–1399. CrossRefGoogle Scholar
  19. Crous CJ, Burgess TI, LeRous JJ et al (2016) Ecological disequilibrium drives insect pest and pathogen accumulation in non-native trees. Ann Bot 9:plw081. CrossRefGoogle Scholar
  20. D’Antonio C, Flory SL (2017) Long-term dynamics and impacts of plant invasions. J Ecol 105:1459–1461. CrossRefGoogle Scholar
  21. D’Antonio CM, Mahall BE (1991) Root profiles and competition between the invasive exotic perennial, Carpobrotus edulis and two native shrub species in California coastal scrub. Am J Bot 78:885–894. CrossRefGoogle Scholar
  22. de Araújo WS (2016) Global patterns in the structure and robustness of plant–herbivore networks. Front Biogeogr 26:217–220. CrossRefGoogle Scholar
  23. de Araújo WS, Vieira MC, Lewinsohn TM, Almeida-Neto M (2015) Contrasting effects of land use intensity and exotic host plants on the specialization of interactions in plant–herbivore networks. PLoS ONE 10:1–15. CrossRefGoogle Scholar
  24. Didham RK, Tylianakis JM, Gemmell NJ et al (2007) Interactive effects of habitat modification and species invasion on native species decline. Trends Ecol Evol 22:489–496. CrossRefPubMedGoogle Scholar
  25. Dormann MCF, True B (2018) Package ‘bipartite’. Visualising bipartite networks and calculating some (ecological) indices.
  26. Dreistadt SH, Clark JK, Flint ML (2016) Pests of landscape trees and shrubs: an integrated pest management guide, 3rd edn. UC ANR Publication 3359, OaklandGoogle Scholar
  27. Early R, Bradley BA, Dukes JS et al (2016) Global threats from invasive alien species in the twenty-first century and national response capacities. Nat Commun 7:12485. CrossRefPubMedPubMedCentralGoogle Scholar
  28. Earnshaw MJ, Carver KA, Charlton WA (1987) Leaf anatomy, water relations and crassulacean acid metabolism in the chlorenchyma and colourless internal water-storage tissue of Carpobrotus edulis and Senecio mandraliscae. Planta 170:421–432. CrossRefPubMedGoogle Scholar
  29. EFSA (2016) Update of a database of host plants of Xylella fastidiosa: 20 November 2015. EFSA J 14:1–31. CrossRefGoogle Scholar
  30. Ehrenfeld JG (2003) Effects of exotic plant invasions on soil nutrient cycling processes. Ecosystems 6:503–523. CrossRefGoogle Scholar
  31. Eichhorn MP, Ratliffe LC, Pollard KM (2011) Attraction of ants by an invasive Acacia. Insect Conserv Divers 4:235–238. CrossRefGoogle Scholar
  32. Eppinga MB, Rietkerk M, Dekker SC et al (2006) Accumulation of local pathogens: a new hypothesis to explain exotic plant invasions. Oikos 114:168–176. CrossRefGoogle Scholar
  33. European Commission (2017) Commission implementing regulation (EU) 2017/1263—of 12 July 2017—updating the list of invasive alien species of Union concern established by implementing regulation (EU) 2016/1141 pursuant to regulation (EU) No 1143/2014 of the European Parliament. Off J Eur Union L 182:37–39Google Scholar
  34. European Union (2014) Regulation (EU) No 1143/2014 of the European Parliament and of the Council of 22 October 2014 on the prevention and management of the introduction and spread of invasive alien species. Off J Eur Union 317:35–55Google Scholar
  35. Fenollosa E, Roach DA, Munné-Bosch S (2016) Death and plasticity in clones influence invasion success. Trends Plant Sci 21:551–553. CrossRefPubMedGoogle Scholar
  36. Fenollosa E, Munné-Bosch S, Pintó-Marijuan M (2017) Contrasting phenotypic plasticity in the photoprotective strategies of the invasive species Carpobrotus edulis and the coexisting native species Crithmum maritimum. Physiol Plant 160:185–200. CrossRefPubMedGoogle Scholar
  37. Flory SL, Clay K (2013) Pathogen accumulation and long-term dynamics of plant invasions. J Ecol 101:607–613. CrossRefGoogle Scholar
  38. Flory SL, Alba C, Clay K et al (2018a) Emerging pathogens can suppress invaders and promote native species recovery. Biol Invasions 20:5–8. CrossRefGoogle Scholar
  39. Flory SL, Alba C, Clay K et al (2018b) Long-term studies are needed to reveal the effects of pathogen accumulation on invaded plant communities. Biol Invasions 20:11–12. CrossRefGoogle Scholar
  40. Fuentes-Ramírez A, Pauchard A, Cavieres LA, García RA (2011) Survival and growth of Acacia dealbata vs. native trees across an invasion front in south-central Chile. For Ecol Manag 261:1003–1009. CrossRefGoogle Scholar
  41. GEIB (2006) TOP 20: Las 20 especies exóticas invasoras más dañinas presentes en España. GEIB, Serie Técnica N.2. Pp.: 116.
  42. González-Muñoz N, Costa-Tenorio M, Espigares T (2012) Invasion of alien Acacia dealbata on Spanish Quercus robur forests: impact on soils and vegetation. For Ecol Manag 269:214–221. CrossRefGoogle Scholar
  43. Guerrieri E, Digilio MC (2008) Aphid-plant interactions: a review. J Plant Interact 3:223–232. CrossRefGoogle Scholar
  44. Hager HA (2004) Competitive effect versus competitive response of invasive and native wetland plant species. Oecologia 139:140–149. CrossRefPubMedGoogle Scholar
  45. Hajek AE, Hurley BP, Kenis M et al (2016) Exotic biological control agents: a solution or contribution to arthropod invasions? Biol Invasions 18:953–969. CrossRefGoogle Scholar
  46. Harvey JA, Bukovinszky T, van der Putten WH (2010) Interactions between invasive plants and insect herbivores: a plea for a multitrophic perspective. Biol Conserv 143:2251–2259. CrossRefGoogle Scholar
  47. Heger T, Jeschke JM (2014) The enemy release hypothesis as a hierarchy of hypotheses. Oikos 123:741–750. CrossRefGoogle Scholar
  48. Hejda M, Hanzelka J, Kadlec T et al (2017) Impacts of an invasive tree across trophic levels: species richness, community composition and resident species’ traits. Divers Distrib 23:997–1007. CrossRefGoogle Scholar
  49. Hodkinson ID, Casson D (1991) A lesser predilection for bugs: Hemiptera (Insecta) diversity in tropical rain forests. Biol J Linn Soc 43:101–109. CrossRefGoogle Scholar
  50. Hokkanen H (1986) Polymorphism, parasites, and the native area of Nezara viridula (Hemiptera, Pentatomidae). Ann Entomol Fenn 52:28–31Google Scholar
  51. Holzinger WE (2002) A review of the European planthopper genus Trirhacus and related taxa, with a key to the genera of European Cixiidae (Hemiptera: Fulgoromorpha). Eur J Entomol 99:373–398CrossRefGoogle Scholar
  52. Horst RK (2008) Westcott’s plant disease handbook, 7th edn. Springer, New YorkCrossRefGoogle Scholar
  53. Hui C, Richardson DM, Landi P et al (2016) Defining invasiveness and invasibility in ecological networks. Biol Invasions 18:971–983. CrossRefGoogle Scholar
  54. Hull-Sanders HM, Clare R, Johnson RH, Meyer GA (2007) Evaluation of the evolution of increased competitive ability (EICA) hypothesis: loss of defense against generalist but not specialist herbivores. J Chem Ecol 33:781–799. CrossRefPubMedGoogle Scholar
  55. Janse JD (2012) Bacterial diseases that may or do emerge, with (possible) economic damage for europe and the mediterranean basin: Notes on epidemiology, risks, prevention and management on first occurrence. J Plant Pathol 94:S4.5–S4.29. CrossRefGoogle Scholar
  56. Janse JD, Obradovic A (2010) Xylella fastidiosa: its biology, diagnosis, control and risks. J Plant Pathol 92:S1.35–S1.48. CrossRefGoogle Scholar
  57. Jonko C (2018) Lepidoptera Mundi. Accessed 28 Aug 2018
  58. Kempel A, Nater P, Fischer M, van Kleunen M (2013) Plant–microbe–herbivore interactions in invasive and non-invasive alien plant species. Funct Ecol 27:498–508. CrossRefGoogle Scholar
  59. Knapp DA (2014) Effects of an exotic plant invasion on arthropod assemblages. PhD thesis, University of California Santa Barbara, Santa BarbaraGoogle Scholar
  60. Kueffer C (2017) Plant invasions in the Anthropocene. Science 358:724–725. CrossRefPubMedGoogle Scholar
  61. Lazzaro L, Giuliani C, Fabiani A et al (2014) Soil and plant changing after invasion: the case of Acacia dealbata in a Mediterranean ecosystem. Sci Total Environ 497–498:491–498. CrossRefPubMedGoogle Scholar
  62. Levine JM, Vila M, Antonio CMD et al (2003) Mechanisms underlying the impacts of exotic plant invasions. Proc R Soc B Biol Sci 270:775–781. CrossRefGoogle Scholar
  63. Litt AR, Cord EE, Fulbright TE, Schuster GL (2014) Effects of invasive plants on arthropods. Conserv Biol 28:1532–1549. CrossRefPubMedGoogle Scholar
  64. Liu H, Stiling P (2006) Testing the enemy release hypothesis: a review and meta-analysis. Biol Invasions 8:1535–1545. CrossRefGoogle Scholar
  65. Lodos N, Kalkandelen A (1981) Preliminary list of Auchenorrhyncha with notes on distribution and importance of species in Turkey IV. Family Issidae Spinola. Türk Bit Kor Derg 5:5–21Google Scholar
  66. Loiola PP, de Bello F, Chytrý M et al (2018) Invaders among locals: alien species decrease phylogenetic and functional diversity while increasing dissimilarity among native community members. J Ecol. CrossRefGoogle Scholar
  67. López-Carretero A, Díaz-Castelazo C, Boege K, Rico-Gray V (2014) Evaluating the spatio-temporal factors that structure network parameters of plant–herbivore interactions. PLoS ONE 9(10):e110430. CrossRefPubMedPubMedCentralGoogle Scholar
  68. López-Carretero A, Díaz-Castelazo C, Boege K, Rico-Gray V (2018) Temporal variation in structural properties of tropical plant–herbivore networks: the role of climatic factors. Acta Oecol 92:59–66. CrossRefGoogle Scholar
  69. Lorenzo P, González L, Reigosa MJ (2010) The genus Acacia as invader: the characteristic case of Acacia dealbata link in Europe. Ann For Sci 67:101. CrossRefGoogle Scholar
  70. Lorenzo P, Pazos-Malvido E, Rubido-Bará M et al (2012) Invasion by the leguminous tree Acacia dealbata (Mimosaceae) reduces the native understorey plant species in different communities. Aust J Bot 60:669–675. CrossRefGoogle Scholar
  71. Lorenzo P, Rodríguez J, González L, Rodríguez- Echeverría S (2017) Changes in microhabitat, but not allelopathy, affect plant establishment after Acacia dealbata invasion. J Plant Ecol 10:610–617. CrossRefGoogle Scholar
  72. Malone M, Watson R, Pritchard J (1999) The spittlebug Philaenus spumarius feeds from mature xylem at the full hydraulic tension of the transpiration stream. New Phytol 143:261–271. CrossRefGoogle Scholar
  73. Marchante H (2006) 100 of the worst invasive species of Europe: Acacia dealbata. In: DASIE Deliv. Eur. Alien Invasive Species Invent. Eur. Online database. Accessed 28 Aug 2018
  74. Marchante H, Morais M, Freitas H, Marchante E (2014) Guia prático para a identificação de plantas invasoras em Portugal. Coimbra University Press, CoimbraCrossRefGoogle Scholar
  75. Maron JL, Bommarco R, Elmendorf S, Beardsley P (2004) Rapid evolution of an invasive plant. Ecol Soc Am 74:261–280. CrossRefGoogle Scholar
  76. Martelli GP, Boscia D, Porcelli F, Saponari M (2016) The olive quick decline syndrome in south-east Italy: a threatening phytosanitary emergency. Eur J Plant Pathol 144:235–243. CrossRefGoogle Scholar
  77. May BM, Attiwill PM (2003) Nitrogen-fixation by Acacia dealbata and changes in soil properties 5 years after mechanical disturbance or slash-burning following timber harvest. For Ecol Manag 181:339–355. CrossRefGoogle Scholar
  78. McGavin GC (2002) Smithsonian handbooks: insects—spiders and other terrestrial arthropods. Dorling Kindersley, DK Publishing, LondonGoogle Scholar
  79. Morrison WE, Hay ME (2011) Herbivore preference for native vs. exotic plants: generalist herbivores from multiple continents prefer exotic plants that are evolutionarily Naïve. PLoS ONE 6:e17227. CrossRefPubMedPubMedCentralGoogle Scholar
  80. Nentwig W, Bacher S, Kumschick S et al (2018) More than “100 worst” alien species in Europe. Biol Invasions 20:1611–1621. CrossRefGoogle Scholar
  81. Novoa A, González L (2014) Impacts of Carpobrotus edulis (L.) N.E.Br. on the germination, establishment and survival of native plants: a clue for assessing its competitive strength. PLoS ONE 9:1–12. CrossRefGoogle Scholar
  82. Novoa A, González L, Moravcová L, Pyšek P (2012) Effects of soil characteristics, allelopathy and frugivory on establishment of the invasive plant Carpobrotus edulis and a co-occuring native, Malcolmia littorea. PLoS ONE 7:e53166. CrossRefPubMedPubMedCentralGoogle Scholar
  83. Novoa A, González L, Moravcová L, Pyšek P (2013) Constraints to native plant species establishment in coastal dune communities invaded by Carpobrotus edulis: implications for restoration. Biol Conserv 164:1–9. CrossRefGoogle Scholar
  84. Novoa A, Rodríguez R, Richardson D, González L (2014) Soil quality: a key factor in understanding plant invasion? the case of Carpobrotus edulis (L.) N.E.Br. Biol Invasions 16:429–443. CrossRefGoogle Scholar
  85. Oksanen AJ, Blanchet FG, Kindt R et al (2018) Package ‘vegan.’ Community Ecology Package.
  86. Ouvrard D (2018) The world Psylloidea database. Accessed 28 Aug 2018
  87. Parker JD, Hay ME (2005) Biotic resistance to plant invasions? native herbivores prefer non-native plants. Ecol Lett 8:959–967. CrossRefGoogle Scholar
  88. Parker JD, Burkepile DE, Hay ME (2006) Opposing effects of native and exotic herbivores on plant invasions. Science 311:1459–1461. CrossRefPubMedGoogle Scholar
  89. Policelli N, Chiuffo MC, Moyano J et al (2018) Pathogen accumulation cannot undo the impact of invasive species. Biol Invasions 20:1–4. CrossRefGoogle Scholar
  90. Pyšek P, Pergl J, Essl F et al (2017) Naturalized alien flora of the world: species diversity, taxonomic and phylogenetic patterns, geographic distribution and global hotspots of plant invasion. Preslia 89:203–274. CrossRefGoogle Scholar
  91. R Development Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna.
  92. Rodríguez J, Lorenzo P, González L (2017) Different growth strategies to invade undisturbed plant communities by Acacia dealbata Link. For Ecol Manag 399:47–53. CrossRefGoogle Scholar
  93. Roiloa SR, Rodriguez-Echeverria S, López-Otero A et al (2014) Adaptive plasticity to heterogeneous environments increases capacity for division of labor in the clonal invader Carpobrotus edulis (Aizoaceae). Am J Bot 101:1301–1308. CrossRefPubMedGoogle Scholar
  94. Roy HE, Lawson Handley L-J, Schönrogge K et al (2011) Can the enemy release hypothesis explain the success of invasive alien predators and parasitoids? Biocontrol 56:451–468. CrossRefGoogle Scholar
  95. Salisbury A, Booth RG (2004) Rodolia cardinalis (Mulsant), the Vedalia ladybird (Coleoptera: Coccinellidae) feeding on Icerya purchasi Maskell, cottony cushion scale (Hemiptera: Margarodidae) in London’s gardens. Br J Entomol Nat Hist 17:103–104Google Scholar
  96. Sanz-Elorza M, Dana-Sánchez ED, Sobrino-Vesperinas E (2004) Atlas de las plantas alóctonas invasoras en España. Dirección General para la Biodiversidad, MadridGoogle Scholar
  97. Schaffner U, Ridenour WM, Wolf VC et al (2011) Plant invasions, generalist herbivores, and novel defense weapons. Ecology 92:829–835. CrossRefPubMedGoogle Scholar
  98. Schlaepfer MA, Sherman PW, Blossey B, Runge MC (2005) Introduced species as evolutionary traps. Ecol Lett 8:241–246. CrossRefGoogle Scholar
  99. Seebens H, Blackburn TM, Dyer E et al (2017) No saturation in the accumulation of alien species worldwide. Nat Commun. CrossRefPubMedPubMedCentralGoogle Scholar
  100. Sheppard AW, Shaw RH, Sforza R (2006) Top 20 environmental weeds for classical biological in Europe: a review of opportunities, regulations and other barriers to adoption. Weed Res 46:93–117. CrossRefGoogle Scholar
  101. Siemann E, Rogers WE, Dewalt SJ (2006) Rapid adaptation of insect herbivores to an invasive plant. Proc R Soc B 273:2763–2769. CrossRefPubMedGoogle Scholar
  102. Singer MC, Parmesan C (2018) Lethal trap created by adaptive evolutionary response to an exotic resource. Nature 557:238–241. CrossRefPubMedGoogle Scholar
  103. Smith-Ramesh LM (2017) Invasive plant alters community and ecosystem dynamics by promoting native predators. Ecology 98:751–761. CrossRefPubMedGoogle Scholar
  104. Souza-Alonso P, Rodríguez J, González L, Lorenzo P (2017) Here to stay. Recent advances and perspectives about Acacia invasion in Mediterranean areas. Ann For Sci 74:55. CrossRefGoogle Scholar
  105. Stricker KB, Harmon PF, Goss EM et al (2016) Emergence and accumulation of novel pathogens suppress an invasive species. Ecol Lett 19:469–477. CrossRefPubMedGoogle Scholar
  106. Thompson V (1994) Spittlebug indicators of nitrogen-fixing plants. Ecol Entomol 19:391–398. CrossRefGoogle Scholar
  107. Thompson V (1999) Spittlebugs associated with actinorhizal host plants. Can J Bot 77:1387–1390Google Scholar
  108. Tittensor DP, Walpole M, Hill SLL et al (2014) A mid-term analysis of progress toward international biodiversity targets. Science 346:241–244. CrossRefPubMedGoogle Scholar
  109. Todd JW (1989) Ecology and behavior of Nezara viridula. Annu Rev Entomol 34:273–292. CrossRefGoogle Scholar
  110. van Hengstum T, Hooftman DAP, Oostermeijer JGB, van Tienderen PH (2014) Impact of plant invasions on local arthropod communities: a meta-analysis. J Ecol 102:4–11. CrossRefGoogle Scholar
  111. van Kleunen M, Dawson W, Essl F et al (2015) Global exchange and accumulation of non-native plants. Nature 525:100–103. CrossRefPubMedGoogle Scholar
  112. Vasquez EC, Meyer GA (2011) Relationships among leaf damage, natural enemy release, and abundance in exotic and native prairie plants. Biol Invasions 13:621–633. CrossRefGoogle Scholar
  113. Villa-Galaviz E, Boege K, Del-Val E (2012) Resilience in plant–herbivore networks during secondary succession. PLoS ONE 7:1–6. CrossRefGoogle Scholar
  114. Washburn JO, Frankie GW (1985) Biological studies of iceplant scales, Pulvinariella mesembryanthemi and Pulvinaria delottoi (Homoptera: Coccidae), in California. Hilgardia 53:1–27CrossRefGoogle Scholar
  115. Weaver C, King D (1954) Meadow spittlebug, Philaenus leucophthalmus (L.). Ohio Agric Exp Station Res Bull 741:1–99Google Scholar
  116. Wiegert R (1964) Population energetics of meadow spittlebugs (Philaenus spumarius L.) as affected by migration and habitat. Ecol Monogr 34:217–241. CrossRefGoogle Scholar
  117. Wingfield MJ, Roux J, Wingfield BD (2011) Insect pests and pathogens of Australian acacias grown as non-natives—an experiment in biogeography with far-reaching consequences. Divers Distrib 17:968–977. CrossRefGoogle Scholar
  118. Winter K (1973) NaCl-induzierter Crassulaceensäurestoffwechsel bei einer weiteren Aizoacee: Carpobrotus edulis. Planta 115:187–188. CrossRefPubMedGoogle Scholar
  119. Ximenes Pinho B, Dáttilo W, Leal IR (2017) Structural breakdown of specialized plant–herbivore interaction networks in tropical forest edges. Glob Ecol Conserv 12:1–8. CrossRefGoogle Scholar
  120. Yates CN, Murphy SD (2008) Observations of herbivore attack on garlic mustard (Alliaria petiolata) in Southwestern Ontario, Canada. Biol Invasions 10:757–760. CrossRefGoogle Scholar
  121. Yoon S, Read Q (2016) Consequences of exotic host use: impacts on Lepidoptera and a test of the ecological trap hypothesis. Oecologia 181:985–996. CrossRefPubMedGoogle Scholar
  122. Yurtsever S (2000) On the polymorphic meadow spittlebug, Philaenus spumarius (L.) (Homoptera: Cercopidae). Turk J Zool 24:447–459. CrossRefGoogle Scholar
  123. Zenner G, Stöckmann M, Niedringhaus R (2005) Preliminary key to the nymphs of the families and subfamilies of the German Auchenorrhyncha fauna (Hemiptera, Fulgoromorpha et Cicadomorpha). Beitr Zikadenkd 8:59–78Google Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Plant Ecophysiology Group, Department of Plant Biology and Soil ScienceUniversity of VigoVigoSpain
  2. 2.CITACA, Agri-Food Research and Transfer Cluster, Campus da AugaUniversity of VigoOurenseSpain
  3. 3.ECOEVO Lab, E. E. ForestalUniversity of VigoPontevedraSpain
  4. 4.Division of Invertebrate ZoologyAmerican Museum of Natural HistoryNew YorkUSA

Personalised recommendations