Oecologia

, Volume 167, Issue 3, pp 701–709 | Cite as

A gall-inducing arthropod drives declines in canopy tree photosynthesis

Plant-Animal interactions - Original Paper

Abstract

Mature forest canopies sustain an enormous diversity of herbivorous arthropods; however, with the exception of species that exhibit large-scale outbreaks, canopy arthropods are thought to have relatively little influence on overall forest productivity. Diminutive gall-inducing mites (Acari; Eriophyoidae) are ubiquitous in forest canopies and are almost always highly host specific, but despite their pervasive occurrence, the impacts of these obligate parasites on canopy physiology have not been examined. We have documented large declines in photosynthetic capacity (approx. 60%) and stomatal conductance (approx. 50%) in canopy leaves of mature sugar maple (Acer saccharum) trees frequently galled by the maple spindle gall mite Vasates aceriscrumena. Remarkably, such large impacts occurred at very low levels of galling, with the presence of only a few galls (occupying approx. 1% of leaf area) compromising gas-exchange across the entire leaf. In contrast to these extreme impacts on the leaves of adult trees, galls had no detectible effect on the gas-exchange of maple saplings, implying large ontogenetic differences in host tolerance to mite galling. We also found a significant negative correlation between canopy tree radial increment growth and levels of mite galling. Increased galling levels and higher physiological susceptibility in older canopy trees thus suggest that gall-inducing mites may be major drivers of “age-dependent” reductions in the physiological performance and growth of older trees.

Keywords

Acer saccharum Eriophyoid mite Galls Herbivory Ontogeny Gas-exchange 

References

  1. Aldea MJ, Hamilton JR, Zangerl AR, Berenbaum MR, Frank T, Delucia EH (2006) Comparison of photosynthetic damage from arthropod herbivory and pathogen infection in understory hardwood saplings. Oecologia 149:221–232PubMedCrossRefGoogle Scholar
  2. Boege K, Marquis RJ (2005) Facing herbivory as you grow up: the ontogeny of resistance in plants. Trends Ecol Evol 20:526CrossRefGoogle Scholar
  3. Dorchin N, Cramer MD, Hoffmann JH (2006) Photosynthesis and sink activity of wasp-induced galls in Acacia pycnantha. Ecology 87:1781–1791PubMedCrossRefGoogle Scholar
  4. Egan SP, Ott JR (2007) Host plant quality and local adaptation determine the distribution of a gall-forming herbivore. Ecology 88:2868–2879PubMedCrossRefGoogle Scholar
  5. Ellsworth DS, Reich PB (1992) Leaf mass per area, nitrogen content and photosynthetic carbon gain in Acer saccharum seedlings in contrasting forest light environments. Funct Ecol 6(4):423–435CrossRefGoogle Scholar
  6. Fay PA, Hartnett DC, Knapp AK (1993) Increased photosynthesis and water potentials in Silphium integrifolium galled by cynipid wasps. Oecologia 93:114–120Google Scholar
  7. Field CB (1991) Ecological scaling of carbon gain to stress and resource availability. In: Mooney HA, Winner WE, Pell EJ (eds) Integrated responses of plants to stress. Academic Press, San Diego, pp 35–65Google Scholar
  8. Florentine SK, Raman A, Dhileepan K (2005) Effects of gall induction by Epiblema strenuana on gas exchange, nutrients, and energetics in Parthenium hysterophorus. Biocontrol 50:787–801CrossRefGoogle Scholar
  9. Fonseca CR, Fleck T, Fernandes GW (2006) Processes driving ontogenetic succession of galls in a canopy. Biotropica 38:514–521CrossRefGoogle Scholar
  10. Hakkarainen H, Roininen H, Virtanen R (2005) Negative impact of leaf gallers on arctic-alpine dwarf willow, Salix herbacea. Polar Biol 28:647–651CrossRefGoogle Scholar
  11. Hartley SE (1998) The chemical composition of plant galls: are levels of nutrients and secondary compounds controlled by the gall-former? Oecologica 113:492–501CrossRefGoogle Scholar
  12. Jeppson LR, Keifer HH, Baker EW (1975) Mites injurious to economic plants. University of California Press, BerkleyGoogle Scholar
  13. Kane NA, Jones CS, Vuorisalo T (1997) Development of galls on leaves of Alnus glutinosa and Alnus incana (Betulaceae) caused by the eriophyid mite Eriophyes laevis (Nalepa). Int J Plant Sci 158:13–23CrossRefGoogle Scholar
  14. Kozlowski TT, Ward RC (1957) Seasonal height growth of deciduous trees. For Sci 3:168–174Google Scholar
  15. Kurz W, Dymond C, Stinson G, Rampley G, Neilson E, Carroll A, Ebata T, Safranyik L (2008) Mountain pine beetle and forest carbon feedback to climate change. Nature 452:987–990PubMedCrossRefGoogle Scholar
  16. Larson KC (1998) The impact of two gall-forming arthropods on the photosynthetic rates of their hosts. Oecologia 115:161–166CrossRefGoogle Scholar
  17. Larson KC, Whitham TG (1991) Manipulation of food resources by a gall-forming aphid: the physiology of sink–source interactions. Oecologia 88:15–21CrossRefGoogle Scholar
  18. Larson KC, Whitham TG (1997) Competition between gall aphids and natural plant sinks: Plant architecture affects resistance to galling. Oecologia 109:575–582CrossRefGoogle Scholar
  19. Lewis SL, Lopez-Gonzalez G, Sonke B, Affum-Baffoe K, Baker TR, Ojo LO, Phillips OL, Reitsma JM, White L, Comiskey JA, Djuikouo MN, Ewango CEN, Feldpausch TR, Hamilton AC, Gloor M, Hart T, Hladik A, Lloyd J, Lovett JC, Makana JR, Malhi Y, Mbago FM, Ndangalasi HJ, Peacock J, Peh KSH, Sheil D, Sunderland T, Swaine MD, Taplin J, Taylor D, Thomas SC, Votere R, Woll H (2009) Increasing carbon storage in intact African tropical forests. Nature 457:1003–1007PubMedCrossRefGoogle Scholar
  20. Luyssaert S, Schulze ED, Borner A, Knohl A, Hessenmoller D, Law BE, Ciais P, Grace J (2008) Old-growth forests as global carbon sinks. Nature 455:213–215PubMedCrossRefGoogle Scholar
  21. Manson DCM, Oldfield GN (1996) Life forms, deuterogyny, diapause and seasonal development. In: Lindquist EE, Sabelis MW, Bruin J (eds) Eriophyoid mites. Their biology, natural enemies and control. Elsevier, Amsterdam, pp 173–183CrossRefGoogle Scholar
  22. Mattson WJ, Addy ND (1975) Phytophagous insects as regulators of forest primary production. Science 190:515–522Google Scholar
  23. McCrea KD, Abrahamson WG, Weis AE (1985) Goldenrod ball gall effects on Solidago altissima—C-14 translocation and growth. Ecology 66:1902–1907CrossRefGoogle Scholar
  24. Moller AP, De Lope F (1999) Senescence in a short-lived migratory bird: age-dependent morphology, migration, reproduction and parasitism. J Anim Ecol 68:163–171CrossRefGoogle Scholar
  25. R Development Core Team (2009) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  26. Ribeiro SP, Basset Y (2007) Gall-forming and free-feeding herbivory along vertical gradients in a lowland tropical rainforest: the importance of leaf sclerophylly. Ecography 30:663–672CrossRefGoogle Scholar
  27. Ryan MG, Phillips N, Bond BJ (2006) The hydraulic limitation hypothesis revisited. Plant Cell Environ 29:367–381PubMedCrossRefGoogle Scholar
  28. Sabelis MW, Bruin J (1996) Evolutionary ecology: life history patterns, food plant choice and dispersal. In: Lindquist EE, Sabelis MW, Bruin J (eds) Eriophyoid mites. Their biology, natural enemies and control. Elsevier, Amsterdam, pp 329–365CrossRefGoogle Scholar
  29. Santos JC, Fernandes GW (2010) Mediation of herbivore attack and induced resistance by plant vigor and ontogeny. Acta Oecol 36:617–625Google Scholar
  30. Sipe TW, Bazzaz FA (1994) Gap partitioning among maples (Acer) in central New England—shoot architecture and photosynthesis. Ecology 75:2318–2332CrossRefGoogle Scholar
  31. Thomas SC (2010) Photosynthetic capacity peaks at intermediate size in temperate deciduous trees. Tree Physiol 30:555–573PubMedCrossRefGoogle Scholar
  32. Thomas SC, Winner WE (2002) Photosynthetic differences between saplings and adult trees: an integration of field results by meta-analysis. Tree Physiol 22:117–127PubMedGoogle Scholar
  33. Thomas SC, Sztaba AJ, Smith SM (2010) Herbivory patterns in mature sugar maple: variation with vertical canopy strata and tree ontogeny. Ecol Entomol 35:1–8CrossRefGoogle Scholar
  34. Vuorisalo T, Walls M, Kuitunen H (1990) Gall mite (Eriophyes laevis) infestation and leaf removal affect growth of leaf area in black alder (Alnus glutinosa) short shoots. Oecologia 84:122–125CrossRefGoogle Scholar
  35. Welter SC (1989) Arthropod impact on plant gas exchange. In: Bernays EA (ed) Insect–plant interactions. CRC, Boca Raton, pp 135–150Google Scholar
  36. Westphal E, Manson DCM (1996) Gall formation and other distortions. In: Lindquist EE, Sabelis MW, Bruin J (eds) Eriophyoid mites. Their biology, natural enemies and control. Elsevier, Amsterdam, pp 231–242CrossRefGoogle Scholar
  37. Wong BL, Baggett KL, Rye AH (2003) Seasonal patterns of reserve and soluble carbohydrates in mature sugar maple (Acer saccharum). Can J Bot 81:780–788CrossRefGoogle Scholar
  38. Woodruff DR, Bond BJ, Meinzer FC (2004) Does turgor limit growth in tall trees? Plant Cell Environ 27:229–236CrossRefGoogle Scholar
  39. Zangerl AR, Hamilton JG, Miller TJ, Crofts AR, Oxborough K, Berenbaum MR, de Lucia EH (2002) Impact of folivory on photosynthesis is greater than the sum of its holes. Proc Natl Acad Sci USA 99:1088–1091PubMedCrossRefGoogle Scholar
  40. Zotz G, Winter K (1993) Short-term photosynthesis measurements predict leaf carbon balance in tropical rain-forest canopy plants. Planta 191:409–412CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Rajit Patankar
    • 1
  • Sean C. Thomas
    • 1
    • 2
  • Sandy M. Smith
    • 1
    • 2
  1. 1.Department of Ecology and Evolutionary BiologyUniversity of TorontoTorontoCanada
  2. 2.Faculty of ForestryUniversity of TorontoTorontoCanada

Personalised recommendations