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Microscopic Study of Galls Induced by Three Species of Geopemphigus (Hemiptera: Aphididae: Eriosomatinae) on Pistacia Mexicana

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Microscopic Study of Galls Induced by Three Species of Geopemphigus (Hemiptera: Aphididae: Eriosomatinae) on Pistacia Mexicana Arthropod-Plant Interactions (2014) 8:531–538 DOI 10.1007/s11829-014-9333-0 ORIGINAL PAPER Microscopic study of galls induced by three species of Geopemphigus (Hemiptera: Aphididae: Eriosomatinae) on Pistacia mexicana Ana Lilia Mun˜oz-Viveros • Jean-Jacques Itzhak Martinez • Pilar Molist • Silvia Gonza´lez-Sierra • Pedro Gonza´lez Julia´n • Rafael A´ lvarez Received: 20 June 2014 / Accepted: 30 September 2014 / Published online: 17 October 2014 Ó Springer Science+Business Media Dordrecht 2014 Abstract The only genus of the tribe Fordini (Aphididae; without dimples, and a single vascular bundle in the wall Eriosomatinae) that is endemic in the American continent (phloem–xylem). These common microscopic characteris- and that is hosted by plants of the genus Pistacia is Geo- tics show that the genus Geopemphigus is closer to the pemphigus. Galls induced by the species G. morral, G. genera Forda and Paracletus than to Baizongia. torsus and G. blackmani on Pistacia mexicana, a member of the Anacardiaceae family, were studied microscopically. Keywords Microscopic study Á Galls Á Geopemphigus Á The study shows characteristics shared by the three galls Pistacia mexicana and specific differences, lending support to the notion that galls are the extended phenotype of gallicolous aphids. Of the three galls, G. morral shows the smallest degree of Introduction modification and the lowest cellularity, followed by G. torsus. The gall G. blackmani presents the most severe It is well known that insects are among the organisms that modification. On the other hand, the three galls have in are able to induce the formation of galls. Among the gal- common that they are not closed galls and have a mul- licolous insects are aphids, and most aphids that induce the tiseriate epidermis–lumen with cuticle, an interior surface formation of galls in Laurasian regions belong to the sub- family Eriosomatinae Kirkaldy, 1905 (1843) (Blackman and Eastop 1994). In this subfamily and within the tribe Handling Editor: Heikki Hokkanen. Fordini Acloque, 1897, we find the only endemic genus in A. L. Mun˜oz-Viveros Á P. G. Julia´n the American continent that is hosted by plants of the genus Laboratorio de Control de Plagas, Facultad de Estudios Pistacia: Geopemphigus Hille Ris Lambers, 1933. This Superiores Iztacala, Universidad Nacional Auto´noma de Me´xico, genus, which is considered a taxonomic near neighbor to Tlalnepantla, Mexico Baizongia Rondani, 1848, and Aploneura Passerini, 1863, J.-J. I. Martinez induces galls on Pistacia Mexicana, a member of the Department of Zootechnology, Faculty of Sciences and Anacardiaceae family (Mun˜oz Viveros and Remaudie`re Technology, Tel Hai College, Tel Hai, Israel 1999). P. Molist Broadly speaking, there is a direct relationship between Department of Functional Biology and Health Sciences, a particular species of gallicolous aphid and the shape and University of Vigo, Vigo, Spain structure of the gall it induces (Stern 1995; Crespi and Worobey 1998; Stone and Cook 1998; Nyman et al. 2000; S. Gonza´lez-Sierra ´ ´ Laboratorio de Microscopı´a, Centro Nacional de Investigacio´n Inbar et al. 2004; Wool 2004;Alvarez et al. 2009;Alvarez sobre la Evolucio´n Humana (CENIEH), Burgos, Spain 2012). This is so much so that galls are considered as the extended phenotype of gallicolous aphids (Dawkins 1982; ´ & R. Alvarez ( ) Stern 1995; Stone and Scho¨nrogge 2003). For this reason, Departamento Biologı´a Molecular- A´ rea Biologı´a Celular, Universidad de Leo´n, Leo´n, Spain the study of gallicolous species should include the study of e-mail: [email protected] the galls they induce. 123 532 A. L. Mun˜oz-Viveros et al. On P. mexicana, five different galls induced by aphids trichomes present in 250 lm of the closure zone; presence of the genus Geopemphigus have been described. Three of of crystals in the wall. Statistical analysis of data was done these are G. morral, G. torsus and G. blackmani. These are using the statistical package R (v. 3.0.3). The effect of the clearly distinct species, both because of the morphological variable ‘‘species’’ on the response variables was analyzed characteristics of the aphids and because of the type of using one-way ANOVA. When the effect of the species galls they induce (Mun˜oz Viveros and Remaudie`re 1999). was significant (P \ 0.001), a post hoc analysis was carried A fourth species, Geopemphigus sp. ‘‘A’’ (perhaps G. out using Tukey’s ‘‘Honest Significant Difference’’ multi- floccosus (Moreira, 1925)), is of uncertain identity due to ple comparison test. the lack of successful experiments involving transfer to one For scanning electron microscope (SEM) studies, two of its secondary hosts. The possible fifth type of gall is samples of each gall (and of the control leaflets) were morphologically very similar to the one just mentioned, but dehydrated in a graded ethanol series and coated with gold. the aphids showed no sound characteristics that allow it to The samples were studied using an FEI Quanta 600 envi- be separated from Geopemphigus sp. ‘‘A’’ (Mun˜oz Viveros ronmental scanning electron microscope (ESEM). and Remaudie`re, 1999). Results Materials and methods The characteristics of the studied galls are summarized in Samples of mature galls induced on P. mexicana by G. Table 1. blackmani, G. morral and G. torsus were collected in the month of July in a village in Hidalgo, Mexico. Leaflets of G. morral P. mexicana were also taken and were used as controls in the histological study. The samples were fixed in situ in Macroscopically it is pouch-shaped and has the size of a FAA (formaldehyde, ethanol and acetic acid) and subse- leaflet (Fig. 1a). In cross section, it appears as a modified quently stored in 70 % ethanol. leaflet. The lamina is folded along the midvein toward the Six samples of each species (and of the leaflets) were adaxial face, with the gall cavity toward the abaxial face of embedded in paraffin: They were dehydrated in a graded the leaflet. The midvein, the modified lamina (that bears no ethanol series, passed through isoamyl acetate as an resemblance to the lamina of the leaflets) and a closure intermediary liquid and embedded in paraplast in an oven zone with trichomes can be recognized (Fig. 1b). at 64 °C to obtain a block of each sample. Of these blocks, The wall is thin, with an average thickness of 251.9 lm. 12-lm-thick serial sections were cut and placed on slides It contains crystals, amyloplasts and tannin inclusions. previously impregnated with Mayer’s albumin. After Crystals are abundant. Specifically, these are druses located removing paraplast, samples were subject to 1/general both in the parenchyma (between the epidermis and the staining with Safranin-Fast Green; 2/Lugol staining to vascular bundles) and associated with the phloem (Fig. 1k). demonstrate the presence of amyloplasts; or 3/left There are few amyloplasts, and these are located in the unstained for observation under an epifluorescence micro- parenchyma. Tannin inclusions are abundant. They are scope. Preparations were then mounted permanently on observed in both epidermi and in the parenchyma (Fig. 1c). microscope slides and were studied using bright field, The inclusions are predominantly homogeneous and dense, polarization and epifluorescence microscopy using a Nikon although they are also observed in strands and as granules. E600 microscope. Photographs were taken of the most The wall of the gall shows: representative microscopic fields. The morphometric study was done on the preparations • Uniseriate epidermis-to-air. Small cells with prominent stained with Safranin-fast green. A bright field microscope cuticle. Stomata and trichomes are not observed with an ocular grid was used. The following measurements (Fig. 1c, d, e). and counts were done: wall thickness; number of cell layers • About 5 layers of parenchymatous cells from the of the epidermis–air; number of stomata in 1 mm of the epidermis to the vascular bundle. They are small cells epidermis–air; number of trichomes in 1 mm of the epi- (average diameter: 25.6 lm). They usually have homo- dermis–air; vascular bundle size; number of cells from the geneous and dense tannin inclusions (Fig. 1c). lumen of the gall to the vascular bundle; distance between • Collateral vascular bundles (Fig. 1c). They are small the lumen of the gall and the phloem; number of cells from (average height: 69.6 lm) and present schizogenous the epidermis–air to the vascular bundle; size of the cell ducts in the phloem. There is a single vascular bundle found to be equidistant to the epidermis–air and the vas- in the wall. The xylem faces the lumen of the gall. The cular bundle in the foregoing measurement; number of average distance between the lumen of the gall and the 123 Microscopic study of galls 533 Table 1 Histological characteristics of the walls of the galls induced Table 1 continued by G. morral, G. torsus and G. blackmani G. morral G. torsus G. blackmani G. morral G. torsus G. blackmani Serrated cuticle ±? ? General Trichomes -- - characteristics Stomata -- - Wall thickness 251.9 ± 10.4c 666.2 ± 19.2b 888.3 ± 39.3a Dimples -- - Crystals ?? ? Closure zone Type of crystals Druses Druses Druses a a a Unicellular ?? ? Number of 1.5 ± 0.4 0.2 ± 0.1 0.1 ± 0.1 trichomes crystals Number of 8.8 ± 0.7A 5.4 ± 0.5b 5.1 ± 0.3b Location of Parenchyma Phloem Phloem trichomes crystals and phloem (parenchyma) (parenchyma) Accumulation -- - Amyloplasts 0/1 2/3 2/3 of crystals Location of Parenchyma Parenchyma Parenchyma Accumulation -- - amyloplasts of tannins Tannin ?? ? inclusions General characteristics (wall thickness, crystals, amyloplasts, and tannins), epidermis–air, parenchyma, vascular bundles, epidermis– Location of Epidermis Epidermis and Epidermis and lumen and closure zone of the galls. Values are expressed as tannins and parenchyma parenchyma mean ± standard error.
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