Abstract
Plants exhibit a wide array of inert and induced responses in defense against herbivore attack. Among these the abscission of organs has been argued to be a highly effective mechanism, depending, however, on the herbivore’s feeding mode. While consisting of plant tissues, insect induced galls are seen as the extended phenotype of the gall inducer which might circumvent many or most of the plant defenses. There is very little information whether and how far beyond the gall tissue gall inducers might affect plant tissues. A localized impact is likely to leave the abscission of galled organs as a viable defense although at a cost. Here, we report on an instance where the host plant, Neea madeirana (Nyctaginaceae) abscises leaves galled by two species of Bruggmannia (Diptera: Cecidomyiidae), more frequently than ungalled leaves in a rain forest in Amazonia, Brazil. Once on the forest floor the leaves decay quickly, while both gall types show signs of localized maintenance of healthy tissues for a while (the green island effect). However, on the forest floor galls are exposed to a new set of potential natural enemies. Both gall types show a minimum of a five-fold increase in mortality due to pathogens (fungi and bacteria) compared to galls that were retained on the host tree. We discuss the adaptive nature of plant organ abscission as a plant defense against gallers and as a gall inducer adaptive trait.
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References
Abrahamson WG, McCrea KD, Whitwell AJ, Vernieri LA (1991) The role of phenolics in goldenrod ball gall resistance and formation. Biochem Syst Ecol 19:615–622
Abramovitch RB, Martin GB (2004) Strategies used by bacterial pathogens to suppress plant defenses. Curr Opin Plant Biol 7:356–364
Agrawal AA, Fishbein M (2006) Plant defense syndromes. Ecology 87:S132–S149
Allison SD, Schultz JC (2005) Biochemical responses of chestnut oak to a galling cynipid. J Chem Ecol 31:151–166
Arnold TM, Schultz JC (2002) Induced sink strength as a prerequisite for induced tannin biosynthesis in developing leaves of Populus. Oecologia 130:585–593
Azarkan M, Wintjens R, Looze Y, Baeyens-Volant D (2004) Detection of three wound-induced proteins in papaya latex. Phytochemistry 65:525–534
Berland L, Bernard F (1951) Ordre de Hymenopteres. In: P Grassé (ed) Traité de Zoologie, No. 10. Masson et cie, Paris, pp 771–1276
Carneiro MAA, Branco CSA, Braga CED, Almada ED, Costa MBM, Maia VC, Fernandes GW (2008) The reliability of the use of gall morphotypes associated to host plant species as surrogates of gall midge species (Diptera: Cecidomyiidae). Revista Brasileira de Entomologia (in press)
Chapman SK, Hart SC, Cobb NS (2003) Insect herbivory increases litter quality and decomposition: an extension of the acceleration hypothesis. Ecology 84:2867–2876
Crawley MJ (1993) GLIM for ecologists. Blackwell Scientific Publications, London
Egan SP, Ott JR (2007) Host plant quality and local adaptation determine the distribution of a gall-forming herbivore. Ecology 88:2868–2879
Espírito-Santo MM, Fernandes GW (2002) Host plant effects on the development and survivorship of the galling insect Neopelma baccharidis (Homoptera: Psyllidae). Aust Ecol 27:249–257
Faeth SH, Connor EF, Simberloff D (1981) Early abscission: a neglected source of mortality for folivores. Am Nat 117:409–415
Fernandes GW (1987) Gall forming insects: their economic importance and control. Rev Bras Entomol 3:379–398
Fernandes GW (1990) Hypersensitivity: a neglected plant resistance mechanism against insect herbivores. Environ Entomol 19:1173–1182
Fernandes GW (1998) Hypersensitivity as a phenotypic basis of plant induced resistance against a galling insect (Diptera: Cecidomyiidae). Environ Entomol 27:260–267
Fernandes GW, Negreiros D (2001) The occurrence and effectiveness of hypersensitive reaction against galling herbivores across host taxa. Ecol Entomol 26:46–55
Fernandes GW, Price PW (1992) The adaptive significance of insect gall distribution: survivorship of species in xeric and mesic habitats. Oecologia 90:14–20
Fernandes GW, Whitham TG (1989) Selective fruit abcission by Juniperus monosperma as an induced defense against predators. Am Midl Nat 121:389–392
Fernandes GW, Castro FMC, Marques ESA (1999) Leaflet abscission caused by a gall induced by Melaphis rhois (Aphididae) on Rhus glabra (Anarcadiaceae). Int J Ecol Environ Sci 25:63–69
Fernandes GW, Cornelissen TG, Isaias RMS, Lara AF (2000) Plants fight gall formation: hypersensitivity. Ciênc Cult 52:49–54
Fisch G, Marengo JA, Nobre CA (1998) Uma revisão geral sobre o clima da Amazônia. Acta Amaz 28:101–126
Harper LJ, Schönrogge K, Lim KY, Francis P, Lichtenstein CP (2004) Cynipid galls: insect-induced modifications of plant development create novel plant organs. Plant Cell Environ 27:327–335
Hartley SE (1998) The chemical composition of plant galls: are the levels of nutrients and secondary compounds controlled by the gall-former? Oecologia 113:492–501
Hough JS (1953) Studies on the common spangle gall of oak I: the developmental history. New Phytol 52:149–177
Hull R (2002) Mathews’ plant virology, 4th edn. Academic Press—A Harcourt Science and Technology Company, New York
Karban R, Thaler JS (1998) Plant phase change and resistance to herbivory. Ecology 80:510–517
Kirst GO, Rapp H (1974) Zur Physiologie der Galle von Mikiola fagi Htg. auf Blättern von Fagus sylvatica L. 2. Transport 14C-markierter Assimilate aus dem befallenen Blatt und aus Nachbar-blättern in die Galle. Biochem Physiol Pflanz 165:445–455
Larson KC, Whitham TG (1991) Manipulation of food resources by a gall-forming aphid: the physiology of sink–source interactions. Oecologia 88:15–21
Lovejoy TE, Bierregaard RO Jr (1990) Central Amazonian Forest and the minimum critical size of ecosystems project. In: Gentry AW (ed) Four neotropical rainforests. Yale University Press, London
Mani MS (1964) The ecology of plant galls. Junk, The Hague, The Netherlands
Mapes CC, Davies PJ (2001) Cytokinins in the ball gall of Solidago altissima and in the gall forming larvae of Eurosta solidaginis. New Phytol 151:203–212
Nyman T, Bokma F, Kopelke J-P (2007) Reciprocal diversification in a complex plant–herbivore–parasitoid food web. BMC Biol 5:49
Oliveira AA (1997) Diversidade, estrutura e dinámica de Manaus, Amazonas. Unpublished PhD dissertation, Universidade de São Paulo, São Paulo
Preszler RW, Price PW (1993) The influence of Salix leaf abscission on leaf-miner survival and life-history. Ecol Entomol 18:150–154
Raman A, Madhavan S, Florentine SK, Dhileepan K (2006) Metabolite mobilization in the stem galls of Parthenium hysterophorus induced by Epiblema strenuana inferred from the signatures of isotopic carbon and nitrogen and concentrations of total non-structural carbohydrates. Entomol Exp Appl 119:101–107
Ribeiro JELS, Hopkins MJG, Vincenti A, Sothers CA, Costa MAS, Brito JM, Souza MAD, Martins LH, Lohmann LG, Assunção PACL, Pereira EC, Silva CF, Mesquita MR, Procopio LC (1999) Flora da Reserva Ducke—Guia de identificação das plantas vasculares de uma floresta de terra-firme na Amazonia central. INPA, 796 p
Rohfritsch O (1997) Morphological and behavioural adaptations of the gall midge Lasioptera arundinis (Schiner) (Diptera, Cecidomyiidae) to collect and transport conidia of its fungal symbiont. Tijdschr Entomol 140:59–66
Rohfritsch O, Shorthouse JD (1982) Insect galls. In: Kall G, Schell JS (eds) Molecular biology of plant tumors. Academic Press, New York, pp 132–151
Schönrogge K, Crawley MJ (2000) Quantitative webs as a means of assessing the impact of alien insects. J Anim Ecol 69:841–868
Schönrogge K, Stone GN, Cockrell B, Crawley MJ (1994) The communities associated with the galls of Andricus quercuscalicis (Hymenoptera: Cynipidae) an invading species in Britain: a geographical view. In: Williams MAJ (ed) Plant galls: organisms, interactions, populations. Clarendon Press, Oxford, pp 369–390
Schönrogge K, Harper LJ, Lichtenstein CP (2000) The protein content of tissues in cynipid galls (Hymenoptera: Cynipidae): similarities between cynipid galls and seeds. Plant Cell Environ 23:215–222
Shorthouse JD, Rohfritsch O (1992) Biology of insect-induced galls. Oxford University Press, New York
Shorthouse JD, Wool D, Raman A (2005) Gall inducing insects—nature’s most sophisticated herbivores. Basic Appl Ecol 6:407–411
Sitch TA, Grewcock DA, Gilbert FS (1988) Factors affecting components of the fitness in a gall-making wasp (Cynips divisa Hartig). Oecologia 76:371–375
Sopow SL, Shorthouse JD, Strong W, Quiring DT (2003) Evidence for long-distance, chemical gall induction by an insect. Ecol Lett 6:102–105
Stiling P, Cattell M, Moon DC (2002) Elevated atmospheric CO2 lowers herbivore abundance, but increases leaf abscission rates. Glob Chang Biol 8:658–667
Stone GN, Schönrogge K (2003) The adaptive significance of insect gall morphology. TREE 18:512–522
Stone GN, Schönrogge K, Crawley MJ, Fraser S (1995) Geographic and between generation variation in the parasitoid communities associated with an invading gallwasp, Andricus quercuscalicis (Hymenoptera:Cynipidae). Oecologia 104:207–217
Stone GN, Schönrogge K, Atkinson RJ, Bellido D, Pujade-Villar J (2002) The population biology of oak gall wasps (Hymenoptera: Cynipidae). Annu Rev Entomol 47:633–668
Stromgren ES, Lanciani CA (2001) Early abscission in hackberry leaves bearing Pachypsylla galls (Homoptera: Psyllidae). Fla Entomol 84:727–728
Taper ML, Case TJ (1986) Sources of mortality for a cynipid gall-wasp (Dryocosmus dubiosus (Hymenoptera: Cynipidae)): the importance of the tannin/fungus interaction. Oecologia 68:437–445
Van Zandt PA, Agrawal AA (2004) Specificity of induced plant responses to specialist herbivores of the common milkweed Asclepias syriaca. Oikos 104:401–409
Wilson D (1995) Fungal endophytes which invade insect galls—insect pathogens, benign saprophytes, or fungal inquilines. Oecologia 103:255–260
Wilson D, Carroll GC (1997) Avoidance of high-endophyte space by gall-forming insects. Ecology 78:2153–2163
Whitham TG (1978) Habitat selection by Pemphigus aphids in response to resource limitation and competition. Ecology 59:1164–1176
Whitham TG (1979) Territorial behaviour of Pemphigus gall-aphids. Nature 279:324–325
Williams AG, Whitham TG (1986) Premature leaf abscission: an induced plant defense against gall aphids. Ecology 67:1619–1627
Wool D, Bogen R (1999) Ecology of the gall-forming aphid, Slavum wertheimae, on Pistacia atlantica: population dynamics and differential herbivory. Isr J Zool 45:247–260
Yukawa J, Tsuda K (1986) Leaf longevity of Quercus glauca Thumb., with reference to the influence of gall formation by Contarinia sp (Diptera: Cecidomyiidae) on the early mortality of fresh leaves. Mem Fac Agric Kagos Univ 22:73–77
Zar JH (1996) Biostatistical analysis. Prentice-Hall, Englewood Cliffs, New Jersey
Acknowledgments
This manuscript was improved by the comments of A. Raman, M.A.C. Carneiro, G.N. Stone and an anonymous referee. We thank A. Oliveira for the species identification and field assistance. This research was supported by CNPq (472491/2003-2, 30 4851/2004-3).
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Fernandes, G.W., De Marco Júnior, P. & Schönrogge, K. Plant organ abscission and the green island effect caused by gallmidges (Cecidomyiidae) on tropical trees. Arthropod-Plant Interactions 2, 93–99 (2008). https://doi.org/10.1007/s11829-008-9031-x
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DOI: https://doi.org/10.1007/s11829-008-9031-x