Abstract
The histological study of galls may provide information on the evolution of the organisms that induce them. The walls of two aphid-induced galls on leaves of Ulmus minor were therefore studied histologically: a globose gall induced by Tetraneura ulmi and a pseudogall induced by Eriosoma ulmi. Galls are regarded as extended phenotypes of aphids, and therefore, they can be used as tools for phylogenetic studies. The walls of the galls induced by T. ulmi are not reminiscent of the ungalled leaf structure of U. minor in any area, showing both cellular hypertrophy and hyperplasia. Galls induced by E. ulmi resemble the leaf structure of U. minor in certain aspects, but in most aspects they do not, showing only cellular hypertrophy. Processes of growth and differentiation are observed in both galls. Based on the findings of this study and other recent publications, we propose to categorize the galls induced by aphids into four types: (1) pseudogalls; (2) closed galls with a “door”; (3) closed galls determined by active processes of growth and differentiation of the lamina of the leaf; and (4) closed galls determined by active processes of growth and differentiation of the midvein.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Allison SD, Schultz JC (2005) Biochemical responses of chestnut oak to a galling Cynipid. J Chem Ecol 31:151–166. doi:10.1007/s10886-005-0981-5
Álvarez R (2011) Initial stages in the formation of galls induced by Geoica Utricularia in Pistacia Terebinthus leaflets: origin of the two vascular bundles which characterize the wall of the galls. A J Plant Sci 2:175–179. doi:10.4236/ajps.2011.22019
Álvarez R (2012) Microscopic study of the walls of galls induced by Geoica utricularia and Baizongia pistaciae in Pistacia terebinthus: a contribution to the phylogeny of Fordini. Arthropod-Plant Interact 6(1):137–145
Álvarez R, Encina A, Pérez Hidalgo N (2009) Histological aspects of three Pistacia terebinthus galls induced by three different aphids: Paracletus cimiciformis, Forda marginata and Forda formicaria. Plant Sci 176:303–314
Aoyama T, Akimoto S-I, Hasegawa E (2012) Gall distribution as a compromise between the optimal gall-site selection and the synchrony to host-plant phenology in the aphid Kaltenbachiella japonica. Arthropod-Plant Interact 6:461–469. doi:10.1007/s11829-012-9196-1
Chakrabarti S (2007) Diversity and biosystematics of gall-inducing aphids (Hemiptera: Aphididae) and their galls in the Himalaya. Orient Insect 41:35–54
Chen J, Qiao G-X (2012) Galling aphids (Hemiptera: Aphidoidea) in China: diversity and host specificity. Psyche 2012: 11. doi:10.1155/2012/621934 (ID 621934)
Crespi B, Worobey M (1998) Comparative analysis of gall morphology in Australian gall thrips: the evolution of extended phenotypes. Evolution 52:1686–1696
Felt EP (1940) Plant galls and gall makers. Comstock Publishing Company, Ithaca, NY
Hartley SE, Lawton JH (1992) Host-plant manipulation by gall insects: a test of the nutrition hypothesis. J Anim Ecol 61:113–119
Inbar M, Wink M, Wool D (2004) The evolution of host plant manipulation by insects: molecular and ecological evidence from gall-forming aphids on Pistacia. Mol Phylogen Evol 32:504–511
Johansen DA (1940) Plant microtechnique. McGraw-Hill Book Company, New York, London
Martinez J-JI (2010) Anti-insect effects of the gall wall of Baizongia pistaciae [L.], a gall-inducing aphid on Pistacia palaestina Boiss. Arthropod-Plant Interact 4:29–34
Nieto-Nafría JM, Mier-Durante MP, Binazzi A, Pérez-Hidalgo N (2002) Hemiptera. Aphididae II. In: Ramos MA et al (ed) Fauna Ibérica. Museo Nacional de Ciencias Naturales, C.S.I.C, Madrid, vol 19, pp 1–351
Price PW, Waring GL, Fernandes GW (1986) Hypotheses on the adaptive nature of galls. Proc Entomol Soc Wash 88:361–363
Price PW, Fernandes GW, Waring WG (1987) Adaptive nature of insect galls. Environ Entomol 16:15–24
Sano M, Akimoto S-Y (2011) Morphological phylogeny of gall-forming aphids of the tribe Eriosomatini (Aphididae: Eriosomatinae). Syst Entomol 36:607–627
Stern DL (1995) Phylogenetic evidence that aphids, rather than plants, determine gall morphology. Proc R Soc Lond B Biol Sci 260:85–89
Stone GN, Schönrogge K (2003) The adaptive significance of insect gall morphology. Trends Ecol Evol 18:512–522
Suzuki DK, Fukushi Y, Akimoto S (2009) Do aphid galls provide good nutrients for the aphids?: comparisons of amino acid concentrations in galls among Tetraneura species (Aphididae: Eriosomatinae). Arthropod Plant Interact 4:241–247. doi:10.1007/s11829-009-9064-9
Wool D (2004) Galling aphids: specialization, biological complexity, and variation. An Rev Entomol 49:175–192
Acknowledgments
The authors are grateful to Ron Hartong of TECcientífica for the English version. We would also like to thank the Junta de Castilla y León for funding project ref. LE006A09.
Author information
Authors and Affiliations
Corresponding author
Additional information
Handling Editor: Heikki Hokkanen.
Rights and permissions
About this article
Cite this article
Álvarez, R., González-Sierra, S., Candelas, A. et al. Histological study of galls induced by aphids on leaves of Ulmus minor: Tetraneura ulmi induces globose galls and Eriosoma ulmi induces pseudogalls. Arthropod-Plant Interactions 7, 643–650 (2013). https://doi.org/10.1007/s11829-013-9278-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11829-013-9278-8