Advertisement

Plant Ecology

, Volume 220, Issue 1, pp 125–134 | Cite as

Do novel interactions with local fauna have reproductive consequences for exotic plants? A case study with thistles, ants, aphids, and pollinators

  • Vanina R. ChalcoffEmail author
  • María Natalia Lescano
  • Andrés M. Devegili
Article

Abstract

Exotic plants are involved in different interactions with the fauna of the invaded sites, which can facilitate or limit their successful establishment and spread. Here, we evaluated the impact of native aphid-tending ants on the reproductive consequences of the invasive thistle Carduus thoermeri in NW Patagonia, which is frequently infested by aphids. We estimated the number and proportion of viable seeds, seed weight, germination proportion, and mean germination time of thistles in the presence and absence of aphids and ants, and with or without pollinator access. Aphid-infested thistles had 57% less viable seeds and 29% lower seed weight than non-infested thistles. Although ants and aphids had no effect on germination proportion, the mean germination time was ca. 15% faster in seeds from aphid-infested thistles. Our results suggest that the potential indirect effects of aphid-tending ants on thistles (negative effects via pollinator deterrence and positive effects via driving away non-aphid herbivores) are less important than the direct negative effects of aphids. Interestingly, although harboring aphids and ants has negative reproductive consequences for C. thoermeri plants, it could also generate a competitive advantage by giving rise to small and fast germinated seeds. This study illustrates the complexity of novel interactions among exotic plants and native ants, reinforcing the need for more studies to fully understand the potential impact of ant–plant interactions mediated by Hemiptera on the invasion success of plants.

Keywords

Facilitation Invasion process Reproduction Seed germination 

Notes

Acknowledgements

The authors thank AG Farji-Brener, C Ezcurra, and A Toth for their critical reading and suggestions on an earlier version of this manuscript, and also JP Moreno for field assistance and Lic. PA Suarez for helping in seeds processing. AM Devegili is supported by a doctoral fellowship from the Consejo Nacional de Investigaciones Científicas y Técnicas of Argentina, and MN Lescano and VR Chalcoff are scientific research members of the same institution. This research was partially funded by Agencia Nacional de Promoción Científica y Tecnológica (PICT 2015-0578).

Supplementary material

11258_2019_907_MOESM1_ESM.docx (549 kb)
Supplementary material 1 (DOCX 548 kb)

References

  1. Bates D, Mächler M, Bolker B, Walker S (2014) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48.  https://doi.org/10.18637/jss.v067.i01 Google Scholar
  2. Bazzaz FA, Chiariello NR, Coley PD, Pitelka LF (1987) Allocating resources to reproduction and defense. Bioscience 37:58–67.  https://doi.org/10.2307/1310178 CrossRefGoogle Scholar
  3. Blackman R, Eastop V (1984) Aphids on the worlds crops: an identification guide. Wiley, New YorkGoogle Scholar
  4. Blancafort X, Gómez C (2005) Consequences of the Argentine ant, Linepithema humile (Mayr), invasion on pollination of Euphorbia characias (L.) (Euphorbiaceae). Acta Oecol 28:49–55.  https://doi.org/10.1016/J.ACTAO.2005.02.004 CrossRefGoogle Scholar
  5. Bolker B, Skaug H, Magnusson A, Nielsen A (2016) Getting started with the glmmADMB package. R-ForgeGoogle Scholar
  6. Canedo-Júnior EO, Santiago GS, Zurlo LF et al (2017) Isolated and community contexts produce distinct responses by host plants to the presence of ant-aphid interaction: plant productivity and seed viability. PLoS ONE 12:e0170915.  https://doi.org/10.1371/journal.pone.0170915 CrossRefGoogle Scholar
  7. Chamberlain SA, Holland JN (2009) Quantitative synthesis of context dependency in ant–plant protection mutualisms. Ecology 90:2384–2392.  https://doi.org/10.1890/08-1490.1 CrossRefGoogle Scholar
  8. Correa M (1999) Flora patagónica. Colección Científica. INTA, Buenos AiresGoogle Scholar
  9. Crawley MJ (1989) Insect herbivores and plant population dynamics. Annu Rev Entomol 34:531–562.  https://doi.org/10.1146/annurev.en.34.010189.002531 CrossRefGoogle Scholar
  10. Davidson DW, Mckey D (1993) Ant-plant symbioses: stalking the Chuyachaqui. TREE 8:326–332Google Scholar
  11. de Briano AE, Acciaresi HA, Briano JA (2013) Establishment, dispersal, and prevalence of Rhinocyllus conicus (Coleoptera: Curculionidae), a biological control agent of thistles, Carduus species (Asteraceae), in Argentina, with experimental information on its damage. Biol Control 67:186–193.  https://doi.org/10.1016/J.BIOCONTROL.2013.07.009 CrossRefGoogle Scholar
  12. de Vega C, Herrera CM (2013) Microorganisms transported by ants induce changes in floral nectar composition of an ant-pollinated plant. Am J Bot 100:792–800.  https://doi.org/10.3732/ajb.1200626 CrossRefGoogle Scholar
  13. Dimitri M (1962) La flora andino-patagónica. Anales de Parques Nacionales, ArgentinaGoogle Scholar
  14. Elton C (1958) The ecology of invasions by animals and plants. University of Chicago Press, ChicagoCrossRefGoogle Scholar
  15. Farji-Brener AG, Ghermandi L (2008) Leaf-cutting ant nests near roads increase fitness of exotic plant species in natural protected areas. Proc Biol Sci 275:1431–1440.  https://doi.org/10.1098/rspb.2008.0154 CrossRefGoogle Scholar
  16. Farji-Brener AG, Gianoli E, Molina-Montenegro MA (2009) Small-scale disturbances spread along trophic chains: leaf-cutting ant nests, plants, aphids, and tending ants. Ecol Res 24:139–145.  https://doi.org/10.1007/s11284-008-0491-3 CrossRefGoogle Scholar
  17. Fiala B, Meyer U, bin Hashim R, Maschwitz U (2014) Temporary sterilization behavior of mutualistic partner ants in a Southeast Asian myrmecophyte. Ecol Res 29:815–822.  https://doi.org/10.1007/s11284-014-1161-2 CrossRefGoogle Scholar
  18. Floate KD, Whitham TG (1994) Aphid–ant interaction reduces chrysomelid herbivory in a cottonwood hybrid zone. Oecologia 97:215–221.  https://doi.org/10.1007/BF00323152 CrossRefGoogle Scholar
  19. Fox J, Weisberg S, Price B, et al. (2018) Package “car.”Google Scholar
  20. Franzel C, Farji-Brener A (2000) ¿Oportunistas o selectivas? Plasticidad en la dieta de la hormiga cortadora de hojas Acromyrmex lobicornis en el noroeste de la Patagonia. Ecol Austral 10:159–168Google Scholar
  21. Gobbi M, Puntieri J, Calvelo S (1995) Post-fire recovery and invasion by alien plant species in a South American woodland-steppe ecotone. In: Post-fire Recover invasion by alien plant species a South Am woodland-steppe ecotone, p 105–115Google Scholar
  22. Gonzálvez FG, Santamaría L, Corlett RT, Rodríguez-Gironés MA (2013) Flowers attract weaver ants that deter less effective pollinators. J Ecol 101:78–85.  https://doi.org/10.1111/1365-2745.12006 CrossRefGoogle Scholar
  23. Gosper CR, Vivian-Smith G (2006) Selecting replacements for invasive plants to support frugivores in highly modified sites: a case study focusing on Lantana camara. Ecol Manag Restor 7:197–203.  https://doi.org/10.1111/j.1442-8903.2006.00309.x CrossRefGoogle Scholar
  24. Heil M, McKey D (2003) Protective ant–plant interactions as model systems in ecological and evolutionary research. Annu Rev Ecol Evol Syst 34:425–553.  https://doi.org/10.1146/annurev.ecolsys.34.011802.132410 CrossRefGoogle Scholar
  25. Hoffmann JH, Moran VC (1998) The population dynamics of an introduced tree, Sesbania punicea, in South Africa, in response to long-term damage caused by different combinations of three species of biological control agents. Oecologia 114:343–348.  https://doi.org/10.1007/s004420050456 CrossRefGoogle Scholar
  26. Hull A, Evans J (1973) Musk thistle (Carduus nutans): an undesirable range plant. J Range Manag 26:383–385.  https://doi.org/10.2307/3896865 CrossRefGoogle Scholar
  27. Ibarra-Isassi J, Oliveira PS (2018) Indirect effects of mutualism: ant–treehopper associations deter pollinators and reduce reproduction in a tropical shrub. Oecologia 186:691–701.  https://doi.org/10.1007/s00442-017-4045-7 CrossRefGoogle Scholar
  28. Ito F, Higashi S (1991) An indirect mutualism between oaks and wood ants via aphids. J Anim Ecol 60:463.  https://doi.org/10.2307/5291 CrossRefGoogle Scholar
  29. Jensen JM, Six DL (2006) Myrmecochory of the exotic plant, Centaurea maculosa: a potential mechanism enhancing invasiveness. Environ Entomol 35:326–331.  https://doi.org/10.1603/0046-225X-35.2.326 CrossRefGoogle Scholar
  30. Lach L (2007) A mutualism with a native membracid facilitates pollinator displacement by argentina ants. Ecology 88:1994–2004.  https://doi.org/10.1890/06-1767.1 CrossRefGoogle Scholar
  31. Lach L (2008) Floral visitation patterns of two invasive ant species and their effects on other hymenopteran visitors. Ecol Entomol 33:155–160.  https://doi.org/10.1111/j.1365-2311.2007.00969.x CrossRefGoogle Scholar
  32. Lach L, Parr CL, Abbott KL (2010) Ant ecology. Oxford University Press, OxfordGoogle Scholar
  33. Lenth R, Love J (2018) Package “lsmeans” Title Least-Squares Means.  https://doi.org/10.1080/00031305.1980.10483031
  34. Lescano MN, Farji-Brener AG (2011) Exotic thistles increase native ant abundance through the maintenance of enhanced aphid populations. Ecol Res 26:827–834.  https://doi.org/10.1007/s11284-011-0842-3 CrossRefGoogle Scholar
  35. Lescano MN, Farji-Brener AG, Gianoli E (2015) Outcomes of competitive interactions after a natural increment of resources: the assemblage of aphid-tending ants in northern Patagonia. Insectes Soc 62:199–205.  https://doi.org/10.1007/s00040-015-0393-7 CrossRefGoogle Scholar
  36. LeVan KE, Holway DA (2015) Ant–aphid interactions increase ant floral visitation and reduce plant reproduction via decreased pollinator visitation. Ecology 96:1620–1630.  https://doi.org/10.1890/14-0058.1 CrossRefGoogle Scholar
  37. LeVan KE, Hung K-LJ, McCann KR et al (2014) Floral visitation by the Argentine ant reduces pollinator visitation and seed set in the coast barrel cactus, Ferocactus viridescens. Oecologia 174:163–171.  https://doi.org/10.1007/s00442-013-2739-z CrossRefGoogle Scholar
  38. Maillet J, Lopez-Garcia C (2000) What criteria are relevant for predicting the invasive capacity of a new agricultural weed? The case of invasive American species in France. Weed Res 40:11–26CrossRefGoogle Scholar
  39. Memmott J, Waser NM (2002) Integration of alien plants into a native flower-pollinator visitation web. Proc Biol Sci 269:2395–2399.  https://doi.org/10.1098/rspb.2002.2174 CrossRefGoogle Scholar
  40. Messina FJ (1981) Plant protection as a consequence of an ant-membracid mutualism: interactions on goldenrod (Solidago Sp.). Ecology 62:1433–1440.  https://doi.org/10.2307/1941499 CrossRefGoogle Scholar
  41. Mitchell CE, Agrawal AA, Bever JD et al (2006) Biotic interactions and plant invasions. Ecol Lett 9:726–740.  https://doi.org/10.1111/j.1461-0248.2006.00908.x CrossRefGoogle Scholar
  42. Moles AT, Westoby M (2004) Seedling survival and seed size: a synthesis of the literature. J Ecol 92:372–383.  https://doi.org/10.1111/j.0022-0477.2004.00884.x CrossRefGoogle Scholar
  43. Morales CL, Aizen MA (2002) Does invasion of exotic plants promote invasion of exotic flower visitors? A case study from the temperate forest of southern Andes. Biol Invasions 4:87–100CrossRefGoogle Scholar
  44. Ness JH (2006) A mutualism’s indirect costs: the most aggressive plant bodyguards also deter pollinators. Oikos 113:506–514.  https://doi.org/10.1111/j.2006.0030-1299.14143.x CrossRefGoogle Scholar
  45. Noble IR, Weiss PW (2006) Movement and modelling of buried seed of the invasive perennial Chrysanthemoides monilifera in coastal dunes and biological control. Aust J Ecol 14:55–64.  https://doi.org/10.1111/j.1442-9993.1989.tb01008.x CrossRefGoogle Scholar
  46. Pinheiro J, Bates D, DebRoy S, Sarkar D (2014) nlme: linear and nonlinear mixed effects models. R package version 3.1-117. http://cran.r-project.org/web/packages/nlme/inde
  47. Pirk GI, Lopez de Casenave J (2017) Ant interactions with native and exotic seeds in the Patagonian steppe: influence of seed traits, disturbance levels and ant assemblage. Plant Ecol 218:1255–1268.  https://doi.org/10.1007/s11258-017-0764-4 CrossRefGoogle Scholar
  48. Pirk GI, Farji-Brener AG (2012) Foliar herbivory and its effects on plant growth in native and exotic species in the Patagonian steppe. Ecol Res 27:903–912.  https://doi.org/10.1007/s11284-012-0968-y CrossRefGoogle Scholar
  49. Popay A, Medd R (1995) Carduus nutans L. ssp. nutans. Biol Aust weeds 1:29–49Google Scholar
  50. R Development Core Team (2016) R: a language and environment for statistical computingGoogle Scholar
  51. Ranal MA, de Santana DG, Ferreira WR, Mendes-Rodrigues C (2009) Calculating germination measurements and organizing spreadsheets. Rev Bras Bot 32:849–855.  https://doi.org/10.1590/S0100-84042009000400022 CrossRefGoogle Scholar
  52. Rejmanek M, Richardson DM (1996) What attributes make some plant species more invasive? Ecology 77:1655–1661.  https://doi.org/10.2307/2265768 CrossRefGoogle Scholar
  53. Renault CK, Buffa LM, Delfino MA (2005) An aphid–ant interaction: effects on different trophic levels. Ecol Res 20:71–74.  https://doi.org/10.1007/s11284-004-0015-8 CrossRefGoogle Scholar
  54. Richardson D, Allsopp N, D’antonio C et al (2000) Plant invasions—the role of mutualism. Biol Rev 75:65–93CrossRefGoogle Scholar
  55. Sallabanks R (1993) Hierarchical mechanisms of fruit selection by an avian frugivore. Ecology 74:1326–1336.  https://doi.org/10.2307/1940063 CrossRefGoogle Scholar
  56. Shea K, Kelly D (1998) Estimating biocontrol agent impact with matrix models: Carduus nutans in New Zealand. Ecol Appl 8:824–832.  https://doi.org/10.1890/1051-0761(1998)008%5b0824:EBAIWM%5d2.0.CO;2 CrossRefGoogle Scholar
  57. Shea K, Kelly D, Sheppard AW, Woodburn TL (2005) Context-dependent biological control of an invasive thistle. Ecology 86:3174–3181.  https://doi.org/10.1890/05-0195 CrossRefGoogle Scholar
  58. Sidhu CS, Rankin EEW (2016) Honey bees avoiding ant harassment at flowers using scent cues. Environ Entomol 45:420–426.  https://doi.org/10.1093/ee/nvv230 CrossRefGoogle Scholar
  59. Skarpaas O, Silverman EJ, Jongejans E, Shea K (2011) Are the best dispersers the best colonizers? Seed mass, dispersal and establishment in Carduus thistles. Evol Ecol 25:155–169.  https://doi.org/10.1007/s10682-010-9391-4 CrossRefGoogle Scholar
  60. Styrsky JD, Eubanks MD (2010) A facultative mutualism between aphids and an invasive ant increases plant reproduction. Ecol Entomol 35:190–199.  https://doi.org/10.1111/j.1365-2311.2009.01172.x CrossRefGoogle Scholar
  61. Tsuji K, Hasyim AH, Nakamura K (2004) Asian weaver ants, Oecophylla smaragdina, and their repelling of pollinators. Ecol Res 19:669–673.  https://doi.org/10.1111/j.1440-1703.2004.00682.x CrossRefGoogle Scholar
  62. Zuur A, Leno E, Walker N et al (2009) Mixed effects models and extensions in ecology with R. Spring, New YorkCrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Laboratorio EcotonoINIBIOMA (CONICET - UNCOMA)BarilocheArgentina

Personalised recommendations