Analysis of the enemy release hypothesis based on the materialof the Central Russia flora

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Дәйексөз келтіру

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Аннотация

The Enemy Release Hypothesis (ERH) is one of the most widespread explanations for the success of invasive species. It proposes that introduced plants are released from phytophages and pathogens in their secondary ranges, facilitating their expansion. However, literature reviews show conflicting results, and empirical support for the hypothesis remains limited. In this study, based on the flora of the Central European part of Russia (2550 species), we tested whether native, alien, and invasive species differ in the number of known natural enemies (herbivores and pathogens). The number of natural enemies was assessed at the genus and family levels using the Plant Parasites of Europe database. We found no significant differences in the number of natural enemies between native and alien plant species, nor between alien and invasive ones. Moreover, plants’ genera and families that include invasive species were characterized by a higher number of native species, which contradicts ERH expectations and supports the preadaptation hypothesis. The proportion of invasive species within a genus was positively correlated with the total number of species in that genus globally, possibly reflecting the influence of phylogenetic and ecological diversity on invasion likelihood. These results highlight the limited explanatory power of the Enemy Release Hypothesis and emphasize the need to consider multiple additional factors when analyzing the success of alien species.

Авторлар туралы

E. Ustinova

Lomonosov Moscow State University, Faculty of Biology, Department of Biological Evolution

Email: ustinolena@ya.ru
Leninskie Gory, 1/12, Moscow, 119234 Russia

S. Lysenkov

Lomonosov Moscow State University, Faculty of Biology, Department of Biological Evolution

Email: s_lysenkov@mail.ru
Leninskie Gory, 1/12, Moscow, 119234 Russia

Әдебиет тізімі

  1. Виноградова Ю.К., Майоров С.Р., Хорун Л.В., 2010. Черная книга флоры Средней России: чужеродные виды растений в экосистемах Средней России. М.: Изд-во ГЕОС. 512 с.
  2. Маевский П.Ф., 2014. Флора средней полосы европейской части России. 11-е изд. М.: Т-во науч. изд. КМК. 635 с.
  3. Arora R., 2012. Co-evolution of insects and plants // Theory and Practice of Integrated Pest Management / Eds Arora R., Singh B., Dhawan A.K. Jodhpur: Scientific Publishers (India). P. 49–75.
  4. Ashton I.W., Lerdau M.T., 2007. Tolerance to herbivory and not resistance may explain differential success of invasive naturalized and native North American temperate vines // Divers. Distrib. V. 14. № 2. P. 169–178. https://doi.org/10.1111/j.1472-4642.2007.00425.x
  5. Bennett J.A., 2019. Similarities between invaders and native species: Moving past Darwin’s naturalization conundrum // J. Veg. Sci. V. 30. № 5. P. 1027–1034. https://doi.org/10.1111/jvs.12779
  6. Blossey B., 1996. The search for patterns or what determines the increased competitive ability of invasive non-indigenous plants // Symp. Proc. California Exotic Pest Plant Council. P. 1–7.
  7. Blossey B., 2011. Enemy Release Hypothesis // Encyclopedia of Biological Invasions. Berkeley: Univ. California Press. P. 193–196. https://doi.org/10.1525/9780520948433-049
  8. Blossey B., Notzold R., 1995. Evolution of increased competitive ability in invasive non-indigenous plants: A hypothesis // J. Ecol. V. 83. № 5. P. 887–889. https://doi.org/10.2307/2261425
  9. Blumenthal D.M., 2006. Interactions between resource availability and enemy release in plant invasion // Ecol. Lett. V. 9. № 7. P. 887–895. https://doi.org/10.1111/j.1461-0248.2006.00934.x
  10. Blumenthal D., Mitchell C.E., Pyšek P., Jarošík V., 2009. Synergy between pathogen release and resource availability in plant invasion // Proc. Natl Acad. Sci. V. 106. № 19. P. 7899–7904. https://doi.org/10.1073/pnas.0812607106
  11. Bossdorf O., Auge H., Lafuma L., Rogers W.E., Siemann E., Prati D., 2005. Phenotypic and genetic differentiation between native and introduced plant populations // Oecologia. V. 144. P. 1–11. https://doi.org/10.1007/s00442-005-0070-z
  12. Brändle M., Kühn I., Klotz S., Belle C., Brandl R., 2008. Species richness of herbivores on exotic host plants increases with time since introduction of the host // Divers. Distrib. V. 14. № 6. P. 905–912. https://doi.org/10.1111/j.1472-4642.2008.00511.x
  13. Brian J., Catford J., 2023. A mechanistic framework of enemy release // Ecol. Lett. V. 26. № 12. P. 2147–2166. https://doi.org/10.1111/ele.14329
  14. Cadotte M.W., Campbell S.E., Li S.P., Sodhi D.S., Mandrak N.E., 2018. Preadaptation and naturalization of nonnative species: Darwin’s two fundamental insights into species invasion // Ann. Rev. Plant Biol. V. 69. № 1. P. 661–684. https://doi.org/10.1146/annurev-arplant-042817-040339
  15. Cadotte M.W., Davies T.J., Peres-Neto P.R., 2017. Why phylogenies do not always predict ecological differences // Ecol. Monogr. V. 87. № 4. P. 535–551. https://doi.org/10.1002/ecm.1267
  16. Cappuccino N., Carpenter D., 2005. Invasive exotic plants suffer less herbivory than non-invasive exotic plants // Biol. Lett. V. 1. № 4. P. 435–438. https://doi.org/10.1098/rsbl.2005.0341
  17. Carpenter D., Cappuccino N., 2005. Herbivory, time since introduction and the invasiveness of exotic plants // J. Ecol. V. 93. № 2. P. 315–321. https://doi.org/10.1111/j.1365-2745.2005.00973.x
  18. Chun Y.J., Kleunen M., van, Dawson W., 2010. The role of enemy release, tolerance and resistance in plant invasions: Linking damage to performance // Ecol. Lett. V. 13. № 8. P. 937–946. https://doi.org/10.1111/j.1461-0248.2010.01498.x
  19. Colautti R.I., Ricciardi A., Grigorovich I.A., MacIsaac H.J., 2004. Is invasion success explained by the enemy release hypothesis? // Ecol. Lett. V. 7. № 8. P. 721–733. https://doi.org/10.1111/j.1461-0248.2004.00616.x
  20. Connor E.F., Faeth S.H., Simberloff D., Opler P.A., 1980. Taxonomic isolation and the accumulation of herbivorous insects: A comparison of introduced and native trees // Ecol. Entomol. V. 5. № 3. P. 205–211. https://doi.org/10.1111/j.1365-2311.1980.tb01143.x
  21. Cornell H.V., Hawkins B.A., 2003. Herbivore responses to plant secondary compounds: A test of phytochemical coevolution theory // Am. Nat. V. 161. № 4. P. 507–522. https://doi.org/10.1086/368346
  22. Daehler C.C., 2001. Darwin’s naturalization hypothesis revisited // Am. Nat. V. 158. № 3. P. 324–330. https://doi.org/10.1086/321316
  23. Darwin C.R., 1859. On the Origin of Species by Means of Natural Selection, or the Preservation of Favoured Races in the Struggle for Life. L.: John Murray. 502 p.
  24. Diez J.M., Sullivan J.J., Hulme P.E., Edwards G., Duncan R.P., 2008. Darwin’s naturalization conundrum: Dissecting taxonomic patterns of species invasions // Ecol. Lett. V. 11. № 7. P. 674–681. https://doi.org/10.1111/j.1461-0248.2008.01178.x
  25. Ehrlich P.R., Raven P.H., 1964. Butterflies and plants: A study in coevolution // Evolution. V. 18. P. 586–608. https://doi.org/10.1111/j.1558-5646.1964.tb01674.x
  26. Elton C.S., 1958. The Ecology of Invasions by Animals and Plants. L.: T. Methuen and Co. 261 p.
  27. Futuyma D.J., Agrawal A.A., 2009. Macroevolution and the biological diversity of plants and herbivores // Proc. Natl Acad. Sci. V. 106. № 43. P. 18054–18061. https://doi.org/10.1073/pnas.0904106106
  28. Gruntman M., Segev U., Glauser G., Tielbörger K., 2017. Evolution of plant defences along an invasion chronosequence: Defence is lost due to enemy release – but not forever // J. Ecol. V. 105. P. 255–264. https://doi.org/10.1111/1365-2745.12660
  29. Hahn P.G., Keefover-Ring K., Nguyen L.M.N., Maron J.L., 2021. Intraspecific correlations between growth and defence vary with resource availability and differ within and among populations // Funct. Ecol. V. 35. № 11. P. 2387–2396. https://doi.org/10.1111/1365-2435.13878
  30. Harvey J.A., Fortuna T.M., 2012. Chemical and structural effects of invasive plants on herbivore–parasitoid/predator interactions in native communities // Entomol. Exp. Appl. V. 144. № 1. P. 14–26. https://doi.org/10.1111/j.1570-7458.2012.01252.x
  31. Harvey K.J., Nipperess D.A., Britton D.R., et al., 2013. Does time since introduction influence enemy release of an invasive weed? // Oecologia. V. 173. P. 493–506. https://doi.org/10.1007/s00442-013-2633-8
  32. Hawkes C.V., 2007. Are invaders moving targets? The generality and persistence of advantages in size, reproduction, and enemy release in invasive plant species with time since introduction // Am. Nat. V. 170. № 6. P. 832–843. https://doi.org/10.1086/522842
  33. Heger T., Jeschke J.M., 2014. The enemy release hypothesis as a hierarchy of hypotheses // Oikos. V. 123. P. 741–750. https://doi.org/10.1111/j.1600-0706.2013.01263.x
  34. Heger T., Jeschke J.M., Bernard-Verdier M., Musseau C.L., Mietchen D., 2024. Hypothesis description: Enemy release hypothesis // Res. Ideas Outcomes. V. 10. Art. e107393. https://doi.org/10.3897/rio.10.e107393
  35. Huang W., Siemann E., Wheeler G.S., Zou J., Carrillo J., Ding J., 2010. Resource allocation to defense and growth are driven by different responses to generalist and specialist herbivory in an invasive plant // J. Ecol. V. 98. № 5. P. 1157–1167. https://doi.org/10.1111/j.1365-2745.2010.01704.x
  36. Jermy T., 1976. Insect–host-plant relationships: Coevolution or sequential evolution? // Symp. Biol. Hung. V. 16. P. 109–113. https://doi.org/10.1007/978-1-4613-4274-8_16
  37. Jermy T., 1984. Evolution of insect/host plant relationships // Am. Nat. V. 124. № 5. P. 609–630. https://doi.org/10.1086/284302
  38. Jeschke J.M., Heger T. (eds.), 2018. Invasion Biology: Hypotheses and Evidence. Boston: CABI. 187 p. https://doi.org/10.1079/9781780647647.0000
  39. Jogesh T., Carpenter D., Cappuccino N., 2008. Herbivory on invasive exotic plants and their non-invasive relatives // Biol. Invasions. V. 10. P. 797–804. https://doi.org/10.1007/s10530-008-9236-z
  40. Jones E.I., Nuismer S.L., Gomulkiewicz R., 2013. Revisiting Darwin’s conundrum reveals a twist on the relationship between phylogenetic distance and invasibility // Proc. Natl Acad. Sci. V. 110. № 51. P. 20627–20632. https://doi.org/10.1073/pnas.1310247110
  41. Keane R.M., Crawley M.J., 2002. Exotic plant invasions and the enemy release hypothesis // Trends Ecol. Evol. V. 17. P. 164–170. https://doi.org/10.1016/s0169-5347(02)02499-0
  42. Lind E.M., Parker J.D., 2010. Novel weapons testing: Are invasive plants more chemically defended than native plants? // PLoS One. V. 5. № 5. Art. e10429. https://doi.org/10.1371/journal.pone.0010429
  43. Liu H., Stiling P., 2006. Testing the enemy release hypothesis: A review and meta-analysis // Biol. Invasions. V. 8. P. 1535–1545. https://doi.org/10.1007/s10530-005-5845-y
  44. Liu H., Stiling P., Pemberton R.W., 2007. Does enemy release matter for invasive plants? Evidence from a comparison of insect herbivore damage among invasive, non-invasive and native congeners // Biol. Invasions. V. 9. P. 773–781. https://doi.org/10.1007/s10530-006-9074-9
  45. Ma C., Li S.P., Pu Z., Tan J., Liu M., et al., 2016. Different effects of invader–native phylogenetic relatedness on invasion success and impact: A meta-analysis of Darwin’s naturalization hypothesis // Proc. R. Soc. Lond. B Biol. Sci. V. 283. № 1838. P. 20160663. https://doi.org/10.1098/rspb.2016.0663
  46. Marx H.E., Giblin D.E., Dunwiddie P.W., Tank D.C., 2016. Deconstructing Darwin’s naturalization conundrum in the San Juan Islands using community phylogenetics and functional traits // Divers. Distrib. V. 22. № 3. P. 318–331. https://doi.org/10.1111/ddi.12401
  47. McEvoy P.B., 2002. Insect-plant interactions on a planet of weeds // Entomol. Exp. Appl. V. 104. № 1. P. 165–179. https://doi.org/10.1046/j.1570-7458.2002.01004.x
  48. Meijer K., Schilthuizen M., Beukeboom L., Smit C., 2016. A review and meta-analysis of the enemy release hypothesis in plant–herbivorous insect systems // Peer J. V. 4. Art. e2778. https://doi.org/10.7717/peerj.2778
  49. Mitchell C.E., Blumenthal D., Jarošík V., Puckett E.E., Pyšek P., 2010. Controls on pathogen species richness in plants’ introduced and native ranges: Roles of residence time, range size and host traits // Ecol. Lett. V. 13. № 12. P. 1525–1535. https://doi.org/10.1111/j.1461-0248.2010.01543.x
  50. Mitchell C.E., Power A.G., 2003. Release of invasive plants from fungal and viral pathogens // Nature. V. 421. № 6923. P. 625–627. https://doi.org/10.1038/nature01317
  51. Park D.S., Feng X., Maitner B.S., Ernst K.C., Enquist B.J., 2020. Darwin’s naturalization conundrum can be explained by spatial scale // Proc. Natl Acad. Sci. V. 117. № 20. P. 10904–10910. https://doi.org/10.1073/pnas.1918100117
  52. Parker I.M., Gilbert G.S., 2007. When there is no escape: The effects of natural enemies on native, invasive, and noninvasive plants // Ecology. V. 88. № 5. P. 1210–1224. https://doi.org/10.1890/06-1377
  53. Parker J.D., Burkepile D.E., Hay M.E., 2006. Opposing effects of native and exotic herbivores on plant invasions // Science. V. 311. P. 1459–1461. https://doi.org/10.1126/science.1121407
  54. Parker J.D., Torchin M.E., Hufbauer R.A., Lemoine N.P., Alba C., et al., 2013. Do invasive species perform better in their new ranges? // Ecology. V. 94. № 5. P. 985–994. https://doi.org/10.1890/12-1810.1
  55. Pellock S., Thompson A., He K.S., Mecklin C.J., Yang J., 2013. Validity of Darwin’s naturalization hypothesis relates to the stages of invasion // Commun. Ecol. V. 14. P. 172–179. https://doi.org/10.1556/comec.14.2013.2.7
  56. Procheş Ş., Wilson J.R., Richardson D.M., Rejmánek M., 2008. Searching for phylogenetic pattern in biological invasions // Global Ecol. Biogeogr. V. 17. № 1. P. 5–10. https://doi.org/10.1111/j.1466-8238.2007.00333.x
  57. Qian H., Sandel B., 2017. Phylogenetic relatedness of native and exotic plants along climate gradients in California, USA // Divers. Distrib. V. 23. P. 1323–1333. https://doi.org/10.1111/ddi.12620
  58. Ricciardi A., Mottiar M., 2006. Does Darwin’s naturalization hypothesis explain fish invasions? // Biol. Invasions. V. 8. P. 1403–1407. https://doi.org/10.1007/s10530-006-0005-6
  59. Rotter M.C., Holeski L.M., 2018. A meta-analysis of the evolution of increased competitive ability hypothesis: Genetic-based trait variation and herbivory resistance trade-offs // Biol. Invasions. V. 20. P. 2647–2660. https://doi.org/10.1007/s10530-018-1724-1
  60. Schultheis E.H., Berardi A.E., Lau J.A., 2015. No release for the wicked: Enemy release is dynamic and not associated with invasiveness // Ecology. V. 96. № 9. P. 2446–2457. https://doi.org/10.1890/14-2158.1
  61. Siemann E., Rogers W.E., 2001. Genetic differences in growth of an invasive tree species // Ecol. Lett. V. 4. P. 514–518. https://doi.org/10.1046/j.1461-0248.2001.00274.x
  62. Siemann E., Rogers W.E., Dewalt S.J., 2006. Rapid adaptation of insect herbivores to an invasive plant // Proc. R. Soc. Lond. B Biol. Sci. V. 273. № 1602. P. 2763–2759. https://doi.org/10.1098/rspb.2006.3644
  63. Stricker K.B., Stiling P., 2014. Release from herbivory does not confer invasion success for Eugenia uniflora in Florida // Oecologia. V. 174. P. 817–826. https://doi.org/10.1007/s00442-013-2798-1
  64. Thellung A., 1915. Pflanzenwanderungen unter dem Einfluß des Menschen // Beiblatt zu den Botanischen Jahrbüchern. V. 53. № 116. S. 37–66.
  65. Wang Y., Siemann E., Wheeler G.S., Zhu L., Gu X., Ding J., 2012. Genetic variation in anti-herbivore chemical defences in an invasive plant // J. Ecol. V. 100. № 4. P. 894–904. https://doi.org/10.1111/j.1365-2745.2012.01980.x
  66. Williams V.R.J., Sahli H.F., 2016. A comparison of herbivore damage on three invasive plants and their native congeners: Implications for the enemy release hypothesis // Castanea. V. 81. № 2. P. 128–137. https://doi.org/10.2179/15-069
  67. Williamson M., Fitter A., 1996. The varying success of invaders // Ecology. V. 77. № 6. P. 1661–1666. https://doi.org/10.2307/2265769
  68. Xu M., Mu X., Zhang S., Dick J.T., Zhu B., et al., 2020. A global analysis of enemy release and its variation with latitude // Global Ecol. Biogeogr. V. 30. № 1. P. 277–288. https://doi.org/10.1111/geb.13229
  69. Zhang Z.J., Pan X.Y., Blumenthal D., Kleunen M., van, Liu M., Li B., 2018. Contrasting effects of specialist and generalist herbivores on resistance evolution in invasive plants // Ecology. V. 99. № 4. P. 866–875. https://doi.org/10.1002/ecy.2155

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