Abstract
Human activities have facilitated the introduction of invasive plants worldwide, altering habitat structure and leading to substantial effects on biodiversity. However, the effects of plant invasions on herbivore communities are understudied. Here, we examine factors influencing the occurrence of herbivores in ten coastal sites invaded by Carpobrotus edulis in the northwestern Iberian Peninsula. The aims were to evaluate the distribution and abundance of herbivorous invertebrates in different communities (invaded vs. non-invaded), explore the structure of plant–herbivore interaction networks, and assess whether the presence of herbivores affects the performance and fitness of C. edulis. Our results show that herbivore species composition was altered by the presence of C. edulis. Non-invaded plots had a higher number of plant–herbivore interactions and more specialized herbivore species, resulting in a greater degree of specialization. We also found an increase in the number of damaged flowers (florivory) of C. edulis by the native snails Theba pisana and Cornu aspersum. We conclude that C. edulis alters herbivore communities compared with non-invaded plots by changing plant–herbivore interactions and increasing the abundance of herbivores in invaded coastal sites. Snails might reduce seed production of C. edulis, acting as a natural biological control agent. Understanding the impacts of introduced species over invertebrate species at different community levels is crucial for implementing long-term management strategies that are key to reducing the impact of C. edulis on biodiversity.
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The authors declare that the data supporting the findings of this study are available within the article in its supplementary information. More details that support the findings of this study are available from the corresponding author upon reasonable request.
References
Almeida-Neto M, Ulrich W (2011) A straightforward computational approach for measuring nestedness using quantitative matrices. Environ Model Softw 26:173–178. https://doi.org/10.1016/j.envsoft.2010.08.003
Almeida-Neto M, Guimarães PRJ, Loyota RD, Ulrich W (2008) A consistent metric for nestedness analysis in ecological systems: reconciling concept and measurement. Oikos 117:1227–1239. https://doi.org/10.1111/j.2008.0030-1299.16644.x
Anderson MJ (2006) Distance-based tests for homogeneity of multivariate dispersions. Biometrics 62:245–253. https://doi.org/10.1111/j.1541-0420.2005.00440.x
Barrientos JA (ed) (2004) Curso práctico de Entomología. Asociación Española de Entomología, CIBIO-Centro Iberoamericano de Biodiversidad and Universitat Autònoma de Barcelona, Barcelona
Bascompte J, Jordano P, Olesen JM (2006) Asymmetric coevolutionary networks facilitate biodiversity maintenance. Science 312:431–433. https://doi.org/10.1126/science.1123412
Baselga A (2010) Partitioning the turnover and nestedness components of beta diversity. Glob Ecol Biogeogr 19:134–143. https://doi.org/10.1111/j.1466-8238.2009.00490.x
Baselga A, Orme CDL (2012) Betapart: an R package for the study of beta diversity. Methods Ecol Evol 3:808–812. https://doi.org/10.1111/j.2041-210X.2012.00224.x
Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48. https://doi.org/10.18637/jss.v067.i01
Beck HE, Zimmermann NE, McVicar TR et al (2018) Present and future Köppen–Geiger climate classification maps at 1-km resolution. Sci Data 5:1–12. https://doi.org/10.1038/sdata.2018.214
Bezemer TM, Harvey JA, Cronin JT (2014) Response of native insect communities to invasive plants. Annu Rev Entomol 59:119–141. https://doi.org/10.1146/annurev-ento-011613-162104
Blüthgen N, Menzel F, Blüthgen N (2006) Measuring specialization in species interaction networks. BMC Ecol 6:9. https://doi.org/10.1186/1472-6785-6-9
Bourgeois K, Suehs CM, Vidal E, Médail F (2005) Invasional meltdown potential: facilitation between introduced plants and mammals on French Mediterranean islands. Écoscience 12:248–256. https://doi.org/10.2980/i1195-6860-12-2-248.1
Campoy JG, Acosta ATR, Affre L et al (2018) Monographs of invasive plants in Europe: Carpobrotus. Bot Lett 165:440–475. https://doi.org/10.1080/23818107.2018.1487884
Carballeira A, Devesa C, Retuerto R et al (1983) Bioclimatología de Galicia. Fundación Pedro Barrié de la Maza, A Coruña
Carboneras C, Genovesi P, Vilà M et al (2018) A prioritised list of invasive alien species to assist the effective implementation of EU legislation. J Appl Ecol 55:539–547. https://doi.org/10.1111/1365-2664.12997
Chinery M (1997) Guía de los Insectos de Europa. Ediciones Omega, Barcelona
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. https://doi.org/10.1007/s10530-017-1519-9
Crous CJ, Burgess TI, Le Roux JJ et al (2016) Ecological disequilibrium drives insect pest and pathogen accumulation in non-native trees. Ann Bot 9:plw081. https://doi.org/10.1093/aobpla/plw081
D’Antonio CM (1990) Seed production and dispersal in the non-native, invasive succulent Carpobrotus edulis (Aizoaceae) in coastal strand communities of central California. J Appl Ecol 27:693–702. https://doi.org/10.2307/2404312
D’Antonio CM, Flory SL (2017) Long-term dynamics and impacts of plant invasions. J Ecol 105:1459–1461. https://doi.org/10.1111/1365-2745.12879
de Araújo WS (2016) Global patterns in the structure and robustness of plant-herbivore networks. Front Biogeogr 26:217–220. https://doi.org/10.5811/westjem.2011.5.6700
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. https://doi.org/10.1371/journal.pone.0115606
Dormann CF, Frund J, Bluthgen N, Gruber B (2009) Indices, graphs and null models: analyzing bipartite ecological networks. Open Ecol J 2:7–24. https://doi.org/10.2174/1874213000902010007
Dormann CF, Fruend J, Gruber B (2020) Package ‘bipartite’. Visualising bipartite networks and calculating some (ecological) indices. https://github.com/biometry/bipartite
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. https://doi.org/10.1038/ncomms12485
Fenollosa E, Roach DA, Munné-Bosch S (2016) Death and plasticity in clones influence invasion success. Trends Plant Sci 21:551–553. https://doi.org/10.1016/j.tplants.2016.05.002
Flory SL, Clay K (2013) Pathogen accumulation and long-term dynamics of plant invasions. J Ecol 101:607–613. https://doi.org/10.1111/1365-2745.12078
Fridley JD, Stachowicz JJ, Naeem S et al (2007) The invasion paradox: Reconciling pattern and process in species invasions. Ecology 88:3–17. https://doi.org/10.1890/0012-9658(2007)88%5b3:tiprpa%5d2.0.co;2
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. https://doi.org/10.1016/j.biocon.2010.03.004
Harvey KJ, Nipperess DA, Britton DR, Hughes L (2012) Australian family ties: does a lack of relatives help invasive plants escape natural enemies? Biol Invasions 14:2423–2434. https://doi.org/10.1007/s10530-012-0239-4
Harvey KJ, Britton DR, Minchinton TE (2014) Detecting impacts of non-native species on associated invertebrate assemblages depends on microhabitat. Austral Ecol 39:511–521. https://doi.org/10.1111/aec.12111
Heger T, Jeschke JM (2014) The enemy release hypothesis as a hierarchy of hypotheses. Oikos 123:741–750. https://doi.org/10.1111/j.1600-0706.2013.01263.x
Horst RK (2008) Westcott’s plant disease handbook, 7th edn. Springer, New York
Hui C, Richardson DM (2019) How to invade an ecological network. Trends Ecol Evol 34:121–131. https://doi.org/10.1016/j.tree.2018.11.003
Hui C, Richardson DM, Landi P et al (2016) Defining invasiveness and invasibility in ecological networks. Biol Invasions 18:971–983. https://doi.org/10.1007/s10530-016-1076-7
Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170. https://doi.org/10.1016/S0169-5347(02)02499-0
Kueffer C (2017) Plant invasions in the Anthropocene. Science 358:724–725. https://doi.org/10.1126/science.aao6371
Lechuga-Lago Y, Sixto-Ruiz M, Roiloa SR, González L (2016) Clonal integration facilitates the colonization of drought environments by plant invaders. AoB Plants 8:plw023. https://doi.org/10.1093/aobpla/plw023
Levine JM, Adler PB, Yelenik SG (2004) A meta-analysis of biotic resistance to exotic plant invasions. Ecol Lett 7:975–989. https://doi.org/10.1111/j.1461-0248.2004.00657.x
Litt AR, Cord EE, Fulbright TE, Schuster GL (2014) Effects of invasive plants on arthropods. Conserv Biol 28:1532–1549. https://doi.org/10.1111/cobi.12350
Liu H, Stiling P (2006) Testing the enemy release hypothesis: a review and meta-analysis. Biol Invasions 8:1535–1545. https://doi.org/10.1007/s10530-005-5845-y
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 106:2230–2241. https://doi.org/10.1111/1365-2745.12986
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:e110430. https://doi.org/10.1371/journal.pone.0110430
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. https://doi.org/10.1016/j.actao.2018.08.002
Maron JL, Vilà M (2001) When do herbivores affect plant invasion? Evidence for the natural enemies and biotic resistance hypotheses. Oikos 95:361–373. https://doi.org/10.1034/j.1600-0706.2001.950301.x
McCary MA, Mores R, Farfan MA, Wise DH (2016) Invasive plants have different effects on trophic structure of green and brown food webs in terrestrial ecosystems: a meta-analysis. Ecol Lett 19:328–335. https://doi.org/10.1111/ele.12562
McGavin GC (2002) Smithsonian handbooks: insects—spiders and other terrestrial arthropods. Dorling Kindersley, DK Publishing, London
Nentwig W, Bacher S, Kumschick S et al (2018) More than “100 worst” alien species in Europe. Biol Invasions 20:1611–1621. https://doi.org/10.1007/s10530-017-1651-6
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. https://doi.org/10.1371/journal.pone.0107557
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-ccuring native, Malcolmia littorea. PLoS ONE 7:e53166. https://doi.org/10.1371/journal.pone.0053166
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. https://doi.org/10.1016/j.biocon.2013.04.008
Núñez-Farfán J, Fornoni J, Valverde PL (2007) The evolution of resistance and tolerance to herbivores. Annu Rev Ecol Evol Syst 38:541–566. https://doi.org/10.1146/annurev.ecolsys.38.091206.095822
Oksanen AJ, Blanchet FG, Friendly M, et al (2019) Package ‘vegan’. Community Ecology Package. https://CRAN.R-project.org/package=vegan
Olden JD, LeRoy Poff N, Douglas MR et al (2004) Ecological and evolutionary consequences of biotic homogenization. Trends Ecol Evol 19:18–24. https://doi.org/10.1016/j.tree.2003.09.010
Olesen JM, Bascompte J, Dupont YL, Jordano P (2007) The modularity of pollination networks. Proc Natl Acad Sci 104:19891–19896. https://doi.org/10.1073/pnas.0706375104
Oliver I, Beattie AJ (1996) Designing a cost-effective invertebrate survey: a test of methods for rapid assessment of Biodiversity. Ecol Appl 6:594–607. https://doi.org/10.2307/2269394
Parker JD, Hay ME (2005) Biotic resistance to plant invasions? Native herbivores prefer non-native plants. Ecol Lett 8:959–967. https://doi.org/10.1111/j.1461-0248.2005.00799.x
Parker JD, Burkepile DE, Hay ME (2006) Opposing effects of native and exotic herbivores on plant invasions. Science 311:1459–1461. https://doi.org/10.1126/science.1121407
Policelli N, Chiuffo MC, Moyano J et al (2018) Pathogen accumulation cannot undo the impact of invasive species. Biol Invasions 20:1–4. https://doi.org/10.1007/s10530-017-1439-8
Prasad AV, Hodge S (2013) The diversity of arthropods associated with the exotic creeping daisy (Sphagneticola trilobata) in Suva, Fiji Islands. Entomol Mon Mag 149:155–161
Prior KM, Robinson JM, Meadley Dunphy SA, Frederickson ME (2015) Mutualism between co-introduced species facilitates invasion and alters plant community structure. Proc R Soc B Biol Sci 282:20142846. https://doi.org/10.1098/rspb.2014.2846
R Development Core Team (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org/
Richard M, Tallamy DW, Mitchell AB (2019) Introduced plants reduce species interactions. Biol Invasions 21:983–992. https://doi.org/10.1007/s10530-018-1876-z
Richardson DM, Holmes PM, Esler KJ et al (2007) Riparian vegetation: degradation, alien plant invasions, and restoration prospects. Divers Distrib 13:126–139. https://doi.org/10.1111/j.1472-4642.2006.00314.x
Rodríguez J, Calbi M, Roiloa SR, González L (2018) Herbivory induced non-local responses of the clonal invader Carpobrotus edulis are not mediated by clonal integration. Sci Total Environ 633:1041–1050. https://doi.org/10.1016/j.scitotenv.2018.03.264
Rodríguez J, Thompson V, Rubido-Bará M et al (2019) Herbivore accumulation on invasive alien plants increases the distribution range of generalist herbivorous insects and supports proliferation of non-native insect pests. Biol Invasions 21:1511–1527. https://doi.org/10.1007/s10530-019-01913-1
Rodríguez J, Cordero-Rivera A, González L (2020a) Characterizing arthropod communities and trophic diversity in areas invaded by Australian acacias. Arthropod Plant Interact 14:531–545. https://doi.org/10.1007/s11829-020-09758-5
Rodríguez J, Novoa A, Cordero-Rivera A et al (2020b) Biogeographical comparison of terrestrial invertebrates and trophic feeding guilds in the native and invasive ranges of Carpobrotus edulis. NeoBiota 56:49–72. https://doi.org/10.3897/neobiota.56.49087
Roiloa SR, Rodríguez-Echeverría S, de la Peña E, Freitas H (2010) Physiological integration increases the survival and growth of the clonal invader Carpobrotus edulis. Biol Invasions 12:1815–1823. https://doi.org/10.1007/s10530-009-9592-3
Roiloa SR, Rodríguez-Echeverría 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. https://doi.org/10.3732/ajb.1400173
Ruiz A, Cárcaba Á, Porras. AI, Arrébola JR (2006) Caracoles terrestres de Andalucía. Guía y manual de identificación. Fundación Gypaetus, Consejería de Medio Ambente de la Junta de Andalucia
Sánchez-Bayo F, Wyckhuys KAG (2019) Worldwide decline of the entomofauna: a review of its drivers. Biol Conserv 232:8–27. https://doi.org/10.1016/j.biocon.2019.01.020
Schultheis EH, Berardi AE, Lau JA (2015) No release for the wicked: enemy release is dynamic and not associated with invasiveness. Ecology 96:2446–2457
Siemann E, Rogers WE, Dewalt SJ (2006) Rapid adaptation of insect herbivores to an invasive plant. Proc R Soc B 273:2763–2769. https://doi.org/10.1098/rspb.2006.3644
Smith-Ramesh LM (2017) Invasive plant alters community and ecosystem dynamics by promoting native predators. Ecology 98:751–761. https://doi.org/10.1002/ecy.1688/suppinfo
Souza-Alonso P, González L (2017) Don’t leave me behind: viability of vegetative propagules of the clonal invasive Carpobrotus edulis and implications for plant management. Biol Invasions 19:2171–2183. https://doi.org/10.1007/s10530-017-1429-x
Stricker KB, Harmon PF, Goss EM et al (2016) Emergence and accumulation of novel pathogens suppress an invasive species. Ecol Lett 19:469–477. https://doi.org/10.1111/ele.12583
Sugiura S, Tsuru T, Yamaura Y (2013) Effects of an invasive alien tree on the diversity and temporal dynamics of an insect assemblage on an oceanic island. Biol Invasions 15:157–169. https://doi.org/10.1007/s10530-012-0275-0
ter Braak CJF, Verdonschot PFM (1995) Canonical correspondence analysis and related multivariate methods in aquatic ecology. Aquat Sci 57:255–289. https://doi.org/10.1007/BF00877430
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. https://doi.org/10.1111/1365-2745.12176
Vázquez DP, Melián CJ, Williams NM et al (2007) Species abundance and asymmetric interaction strength in ecological networks. Oikos 116:1120–1127. https://doi.org/10.1111/j.2007.0030-1299.15828.x
Vieites-Blanco C (2018) Effects on soil and alternatives for biological control of the invasive plant Carpobrotus edulis. Ph.D. Thesis, Universidade de Santiago de Commpostela, Santiago de Compostela
Villa-Galaviz E, Boege K, del-Val E (2012) Resilience in plant-herbivore networks during secondary succession. PLoS ONE 7:e53009. https://doi.org/10.1371/journal.pone.0053009
Zhang Y, Meng H, Wang Y, He Q (2018) Herbivory enhances the resistance of mangrove forest to cordgrass invasion. Ecology 99:1382–1390. https://doi.org/10.1002/ecy.2233
Acknowledgements
This work was funded by Xunta de Galicia, Spain (CITACA Strategic Partnership, Reference: ED431E 2018/07) and 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 Competitiveness (Spanish Government). JR was supported by a research contract (GRC2015/012) from the “Xunta de Galicia/FEDER, Consellería de Educación y Ordenación Universitaria” and a research contract from “Plan de mellora do Centro de Investigacións Agroalimentarias CIA3 do Campus de Ourense, Universidade de Vigo”. JR also acknowledges funding from the Czech Science Foundation (Project No. 19-13142S) and supported by long-term research development Project No. RVO 67985939 of the Czech Academy of Sciences. We thank Alba Ferreiro-Martínez, Mariasole Calbi, Yaiza Lechuga-Lago and Marga Rubido-Bará for fieldwork assistance. We are most grateful for the valuable and constructive comments from the Editor and two anonymous referees that have substantially improved our manuscript.
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Rodríguez, J., Cordero-Rivera, A. & González, L. Impacts of the invasive plant Carpobrotus edulis on herbivore communities on the Iberian Peninsula. Biol Invasions 23, 1425–1441 (2021). https://doi.org/10.1007/s10530-020-02449-5
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DOI: https://doi.org/10.1007/s10530-020-02449-5