Advertisement

Spatial heterogeneity of gall formation in relation to chemotype distribution in Thymus vulgaris

  • John D. Thompson
  • Justin Amiot
  • Christophe Borron
  • Yan B. Linhart
  • Ken Keeefover-Ring
  • Perrine GauthierEmail author
Article
  • 19 Downloads

Abstract

The utilization of host plants by herbivorous insects depends on plant traits and physical environment. The purpose of the present work is to test the hypothesis that spatial variation in the presence of galls of the specialist fly Janetiellathymicola in natural populations of its host plant Thymus vulgaris differ in relation to spatial variation in chemotype presence. We quantified gall infection rates in 59 populations that differ in chemotype presence across a sharp ecological gradient in the South of France. We also quantified spatial aggregation of galls and plants and made a 3-year study of infection, biomass and plant survival in three populations. The proportion of galled plants was significantly higher in populations with non-phenolic chemotypes on deeper soils in sites with cold winter temperatures than in populations of phenolic chemotypes on stony soils in sites with mild winters. In a population with two non-phenolic chemotypes, galls were significantly more present on plants of the chemotype with the highest proportion of galls in the multi-population survey. In a 3-year study, galled plants had a significantly greater probability of being infected by a subsequent generation than non-galled plants. This probability declined with distance. Galls absorbed a significant proportion of vegetative biomass on a shoot, but their presence was unrelated to survival. Host plant chemistry, habitat characteristics and dispersal limitation conjointly affect this host–parasite interaction.

Keywords

Parasitism Gall Chemical polymorphism Dispersal limitation Mediterranean 

Notes

Acknowledgements

We thank Yannis Michalakis for advice, Laure Andrieu, Christian Collin, Marie Maistre, Annabelle Dos Santos, Pierre Reignaud, Muriel Busson and Jérôme Ghesquière for assistance with fieldwork, and the C.N.R.S. for financial support.

References

  1. Abrahamson WG, McCrea KD, Whitwell AJ, Vernieri LA (1991) The role of phenolics in goldenrod ball gall resistance and formation. Biochem Syst Ecol 19:615–622CrossRefGoogle Scholar
  2. Achotegui-Castells A, Danti R, Llusia J, Della Rocca G, Barberini S, Penuelas J (2015) Strong induction of minor terpenes in Italian Cypress, Cupressus sempervirens, in response to infection by the Fungus Seiridium cardinale. J Chem Ecol 41(3):224–243CrossRefGoogle Scholar
  3. Akimoto S (1990) Local adaptation and host race formation of a gall-forming aphid in relation to environmental heterogeneity. Oecologia 83:162–170CrossRefGoogle Scholar
  4. Alexander HM (1990) Epidemology of anther smut infection of Silene alba caused by Ustilago violaceae: pattens of spore deposition and disease incidence. J Ecol 78:166–179CrossRefGoogle Scholar
  5. Alexander HM, Antonovics J (1988) Disease spread and population dynamics of anther-smut infection of Silene alba caused by the fungus Ustilago violacea. J Ecol 76:91–104CrossRefGoogle Scholar
  6. Amiot J (2001) Interactions entre facteurs biotiques et types chimiques de Thymus vulgaris: pollinisation, parasitisme et prédation. Unpublished Master Thesis, Agro Montpellier - Université Montpellier 2, MontpellierGoogle Scholar
  7. Amiot J, Salmon Y, Collin C, Thompson JD (2005) Differential resistance to freezing and spatial distribution in a chemically polymorphic plant Thymus vulgaris. Ecol Let 8:370–377CrossRefGoogle Scholar
  8. Bryant JP, Provenza FD, Pastor J, Reichardt PB, Clausen TP, du Toit JT (1991) Interactions between woody plants and browsing mammals mediated by secondary metabolites. Annu Rev Ecol Syst 22:431–446CrossRefGoogle Scholar
  9. Clark L, Dennehy T (1989) Grape Tumid Gallmaker. https://www.nysipm.cornell.edu/factsheets/grapes/pests/gtg/gtg.html
  10. Crawley MJ (1983) Herbivory. The dynamics of animal-plant interactions. Blackwell Scientific Publications, OxfordGoogle Scholar
  11. Cronin JT, Abrahamson WG (2001) Goldenrod stem galler preference and performance: effects of multiple herbivores and plant genotypes. Oecologia 127:87–96CrossRefGoogle Scholar
  12. Croteau R (1987) Biosynthesis and catabolism of monotepenoids. Chem Rev 87:929–954CrossRefGoogle Scholar
  13. David FN, Moore PG (1954) Notes on contagious distributions in plant populations. Ann Bot London 18:47–53CrossRefGoogle Scholar
  14. Dennis RLH, Shreeve TG, Van Dyck H (2003) Towards a functional resource-based concept for habitat: a butterfly biology viewpoint. Oikos 102:417–426CrossRefGoogle Scholar
  15. Egan SP, Ott JR (2007) Host plant quality and local adaptation determine the distribution of a gall-forming herbivore. Ecology 88:2868–2879CrossRefGoogle Scholar
  16. Ehlers BK, Thompson JD (2004) Do co-occuring plant species adapt to one another? The response of Bromus erectus to the presence of different Thymus vulgaris chemotypes. Oecologia 141:511–518CrossRefGoogle Scholar
  17. Ehlers BK, David P, Damgaard CF et al (2016) Competitor relatedness, indirect soil effects and plant coexistence. J Ecol 104:1125–1135CrossRefGoogle Scholar
  18. Ehrlich PR, Raven PH (1964) Butterflies and plants: a study in coevolution. Evolution 18:586–608CrossRefGoogle Scholar
  19. ESRI (1999–2002) ArcMap, Version 8.3, ESRI Inc.Google Scholar
  20. Evans LM, Clark JS, Whipple AV, Whitham TG (2012) The relative influences of host plant genotype and yearly abiotic variability in determining herbivore abundance. Oecologia 168:483–489CrossRefGoogle Scholar
  21. Fay PA, Hartnett DC, Knapp AK (1996) Plant tolerance of gall-insect attack and gall-insect performance. Ecology 77:521–534CrossRefGoogle Scholar
  22. Fraenkel GS (1959) The raison d'être of secondary plant substances. Science 129:1460–1470CrossRefGoogle Scholar
  23. Gouyon PH, Vernet P, Guillerm JL, Valdeyron G (1986) Polymorphisms and environment: the adaptive value of the oil polymorphisms in Thymus vulgaris L. Heredity 57:59–66CrossRefGoogle Scholar
  24. Granger R, Passet J (1973) Thymus vulgaris L. spontané de France: races chimiques et chemotaxonomie. Phytochemistry 12:1683–1691CrossRefGoogle Scholar
  25. Guimarães ALdA, Bizarri CHB, Barbosac LS, Nakamurac MJ, Ramosb MFdS, Vieiraa ACdM (2013) Characterisation of the effects of leaf galls of Clusiamyia nitida (Cecidomyiidae) on Clusia lanceolata Cambess. (Clusiaceae): anatomical aspects and chemical analysis of essential oil. Flora 165–173:162–170Google Scholar
  26. Hartley SE (1998) The chemical composition of plant galls: are levels of nutrients and secondary compounds controlled by the gall-former? Oecologia 113:492–501CrossRefGoogle Scholar
  27. Hartnett DC, Abrahamson WG (1979) The effects of stem gall insects on life history patterns in Solidago canadensis. Ecology 60:910–917CrossRefGoogle Scholar
  28. Horner JD, Abrahamson WG (1992) Influence of plant genotype and environment on oviposition preference and offspring survival in a gallmaking herbivore. Oecologia 90:323–332CrossRefGoogle Scholar
  29. Irwin JT, Lee REJ (2003) Cold winter microenvironments conserve energy and improve overwintering survival and potential fecundity of the goldenrod gall fly, Eurosta solidaginis. Oikos 100:71–78CrossRefGoogle Scholar
  30. Keefover-Ring K, Thompson JD, Linhart YB (2009) Beyond six scents: defining a seventh Thymus vulgaris chemotype by ethanol extraction new to southern France. Flavour and Frag J 24:117–122CrossRefGoogle Scholar
  31. Linhart YB, Thompson JD (1995) Terpene-based selective herbivory by Helix aspersa (Mollusca) on Thymus vulgaris (Labiatae). Oecologia 102:126–132CrossRefGoogle Scholar
  32. Linhart YB, Thompson JD (1999) Thyme is of the essence: biochemical polymorphism and multi-species deterrence. Evol Ecol Res 1:151–171Google Scholar
  33. Linhart YB, Gauthier P, Keefover-Ring K, Thompson JD (2015) Variable phytotoxic effects of terpenes of Thymus vulgaris (lamiaceae) upon associated species. Int J Plant Sci 176:20–30CrossRefGoogle Scholar
  34. McCrea KD, Abrahamson WG (1987) Variation in herbivore infestation: historical versus genetic factors. Ecology 68:822–827CrossRefGoogle Scholar
  35. Overton JM (1994) Dispersal and infection in mistletoe populations. J Ecol 82:711–723CrossRefGoogle Scholar
  36. Passet J (1971) Thymus vulgaris L.: Chémotaxonomie et biogénèse monoterpénique. Unpublished Ph.D. Thesis, Faculté de Pharmacie, Montpellier.Google Scholar
  37. Peñuelas J, Sardans J, Stefanescu C, Parella T, Filella I (2006) Lonicera implexa leaves bearing naturally laid eggs of the specialist herbivore Euphydryas aurinia have dramatically greater concentrations of iridoid glycosides than other leaves. J Chem Ecol 32:1925–1933CrossRefGoogle Scholar
  38. Rand K, Bar E, Ari MB, Davidovich-Rikanati R, Dudareva N, Inbar M, Lewinsohn E (2017) Differences in monoterpene biosynthesis and accumulation in Pistacia palaestina leaves and aphid-induced galls. J Chem Ecol 43:143–152CrossRefGoogle Scholar
  39. Redfern M (2011) Plant galls. Collins New Naturalist, LondonGoogle Scholar
  40. Rocha S, Branco M, Boas LV, Almeida MH, Protasov A, Mendel Z (2013) Gall induction may benefit host plant: a case of a gall wasp and eucalyptus tree. Tree Physiol 33:388–397CrossRefGoogle Scholar
  41. SAS Institute (1999–2000) SAS/STAT Users guide, Version 6, SAS Institute Inc., Cary, NC, USA.Google Scholar
  42. Strong DR, Lawton JH, Southwood R (1984) Insects on plants. Blackwell Scientific Publishers, OxfordGoogle Scholar
  43. Tarayre M, Thompson JD, Escarré J, Linhart YB (1995) Intra-specific variation in the inhibitory effects of Thymus vulgaris (Labiatae) monoterpenes on seed germination. Oecologia 101:110–118CrossRefGoogle Scholar
  44. Thompson JN (1994) The coevolutionary process. The University of Chicago Press, ChicagoCrossRefGoogle Scholar
  45. Thompson JD (2002) Population structure and the spatial dynamics of genetic polymorphism in thyme. In: Stahl-Biskup E, Sáez F (eds) Thyme: the genus Thymus. Taylor & Francis, London, pp 44–74Google Scholar
  46. Thompson JD, Chalchat JC, Michet A, Linhart YB, Ehlers B (2003) Qualitative and quantitative variation in monoterpene co-occurrence and composition in the essential oil of Thymus vulgaris chemotypes. J Chem Ecol 29:859–880CrossRefGoogle Scholar
  47. Thompson JD, Tarayre M, Gauthier P, Litrico I, Linhart YB (2004) Multiple genetic contributions to plant performance in Thymus vulgaris. J Ecol 92:45–56CrossRefGoogle Scholar
  48. Thompson JD, Gauthier P, Amiot J, Ehlers BK, Collin C, Fossat J, Barrios V, Arnaud-Miramont F, Keefover-Ring K, Linhart YB (2007) Ongoing adaptation to Mediterranean climate extremes in a chemically polymorphic plant. Ecol Monogr 77:421–439CrossRefGoogle Scholar
  49. Tija B, Houston DB (1975) Phenolic constituents of Norway spruce resistant or susceptible to the eastern spruce gall aphid. For Sci 21:180–184Google Scholar
  50. Traveset A (1994) Reproductive biology of Phillyrea angustifolia L. (Oleaceae) and effect of galling insects on its reproductive output. Bot J Linn Soc 114:153–166CrossRefGoogle Scholar
  51. Vernet P, Guillerm JL, Gouyon PH (1977a) Le polymorphisme chimique de Thymus vulgaris L. (Labiée) I. Repartition des formes chimiques en relation avec certains facteurs écologiques. Oecol Plant 12:159–179Google Scholar
  52. Vernet P, Guillerm JL, Gouyon PH (1977b) Le polymorphisme chimique de Thymus vulgaris L. (Labiée) II. Carte à l'echelle 1/25000 des formes chimiques dans la région de Saint-Martin-de-Londres (Herault-France). Oecol Plant 12:181–194Google Scholar
  53. Vernet P, Gouyon PH, Valdeyron G (1986) Genetic control of the oil content in Thymus vulgaris L.: a case of polymorphism in a biosynthetic chain. Genetica 69:227–231CrossRefGoogle Scholar
  54. Weis AE, Abrahamson WG (1986) Evolution of host-plant manipulation by gall makers: ecological and genetic factors in the Solidago-Eurosta system. Am Nat 127:681–695CrossRefGoogle Scholar
  55. Whitham TG (1979) Territorial behaviour of Pemphis gall aphids. Nature 279:324–325CrossRefGoogle Scholar
  56. Zucker WV (1982) How aphids choose leaves: the roles of phenolics in host selection by a galling aphid. Ecology 63:972–981CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.UMR 5175 Centre D’Ecologie Fonctionnelle et Evolutive, 1919 Route de MendeCNRSMontpellier Cedex 5France
  2. 2.Department of Ecology and Evolutionary BiologyUniversity of ColoradoDenverUSA
  3. 3.Department of Botany and GeographyUniversity of Wisconsin-MadisonMadisonUSA

Personalised recommendations