GALL MAKERS IN PLANTS FROM THE PÉ-DE-GIGANTE CERRADO RESERVE , SANTA RITA DO PASSA QUATRO , SP , BRAZIL

Thirty-six morphologically different types of galls were obtained in leaves, leaflets, veins, petioles, stems, tendrils and flower buds from twenty-five species of plants in the Pé-de-Gigante Reserve, municipality of Santa Rita do Passa Quatro, state of São Paulo, Brazil. The host plant species belong to the closely related families Anacardiaceae, Annonaceae, Asteraceae, Bignoniaceae, Caryocaraceae, Erythroxylaceae, Fabaceae, Malpighiaceae, Melastomataceae, Myrtaceae, Ochnaceae, Polygalaceae, Sapindaceae, Sapotaceae, and Smilacaceae. The most common gall makers included Cecidomyiidae (Diptera), Pteromalidae (Hymenoptera) and Diaspididae (Sternorrhyncha-Hemiptera). This is the first report of galls found in the following plant genera: Gochnatia (Asteraceae), Distictela (Bignoniaceae), Banisteriopsis (Malpighiaceae), Ouratea (Ochnaceae), and Bredemeyera (Polygalaceae). The results of this work contribute to the body of knowledge about the relationship among host plants, gall makers, and the gall morphology of Pé-de-Gigante Cerrado Reserve.


INTRODUCTION
Different gall makers can attack the same vegetal species, causing the reorganization of species-specific characteristics (Hartley, 1998).The manipulation of the host plant by a gall maker can be so great that the latter assumes control of the gall tissue's chemical composition, which can be quite different from the ungalled tissue (Scareli-Santos, 2001).Some authors have commented on the high level of specificity of gall makers and host plant association (Mani, 1964;Abrahamson & Weiss, 1987).
Although gall inducers belong to many different taxa, the gall makers induce galls in relatively few plant groups, and each one is closely related with the host.According to Abrahamson & Weiss (1987), 87% of all cynipids attack specifically certain species of Quercus (Fagaceae).Cynipid (Cynipini, Hymenoptera) -oak (Quercus spp., Fagaceae) interaction is a kind of association that Brooks & McLennan (1991) called association by descent or coevolution.This kind of relationship is well known in the Nearctic region, but its study is still incipient in the Neotropical region because gall maker-host plant systems and the relationships between them are only just beginning.This paper focuses on the determination of the relationship between host plants and gall makers from the Pé-de-Gigante Cerrado Reserve, characterizing the gall morphology, which is very specific to each host plant-gall maker.

Sampling area
Samples were collected in the Pé-de-Gigante Cerrado Reserve, situated in the municipality of Santa Rita do Passa Quatro, SP, southeastern Brazil (Fig. 1), from 1996 through 2001.The site's geographical coordinates are: 21° 35' S and 47°35' W. Samples were collected monthly from 1997 to 1998 and at irregular intervals during the other years.The reserve is situated in the Santa Rita mountains at an altitude of 590 to 740 m.About 98% of the reserve is covered by Cerrado (savanna-like vegetation) with varying physiognomies (Batalha & Mantovani, 2000), which were studied by Pivello et al. (1999) based on Landsat-TM satellite images (Fig. 2).

Treatment of samples
The samples were treated as described by Fernandes et al. (1988).Cecidomiids were  SP, Brazil (Sallis et al., 1995apud Batalha, 1997).identified using keys to immatures of the Nearctic Region (Gagné, 1989), and immatures and adults of the Neotropical region (Gagné, 1994).Vouchers of host plants were deposited in the Botanical Section and galls and insects in the Laboratory of Diphthera at the University of São Paulo Faculty of Philosophy, Sciences and Letters Department of Biology in Ribeirão Preto, SP, Brazil.
All the specimens were given a registration number (RN) which is listed in Appendix.The names and distribution of the plant species were looked up in Lorenzi's book (1992) and/or on the homepage of the Missouri Botanical Garden's VAST (VAScular Tropicos) database at: http://mobot.mobot.org/W3T/Search/vast. html.Urso-Guimarães & Scareli-Santos are the authors of the gall pictures presented in this paper.

RESULTS AND DISCUSSION
Table 1 provides information about the relationship between host plants and gall makers of each gall type, while Table 2 lists information on the gall morphology of each host plant.Appendix contains data on the samples and additional information.The galls are featured in Figs. 3 to 32 .

Gall morphology
The galls showed variations in color and appearance, especially during the maturation period, as depicted for the globoid gall of D. furfuracea (Fig. 4), from green to dark gray, and a scaly aspect when mature.In the maturation period, the structures take on stronger shades, as observed in the polypoid leaf gall of D. furfuracea (Fig. 6), Copaifera langsdorffii (Figs. 16,17), in the leaf bud, leaf vein and stem, and petiole galls of M. bella .When young, the globoid gall of A. peregrina is pale yellow, and turns red after maturation (Fig. 13a).All the sampled galls belong to the closed type.
Galls of Gochnatia pulchra (Fig. 7), Tabebuia ochracea (Fig. 9), Erythroxylum suberosum A. St.-Hil.(Fig. 12), and Pouteria torta (Mart.)Radlk.(Fig. 31) presented large quantities of trichomes, probably formed as a protection for insects inside the gall.Fernandes et al. (1987) stated that the presence of large quantities of trichomes offers a protective barrier for the inducer's insect larvae against attack by parasitoids and small sucking herbivores that feed on gall tissues.
The distribution of galls in plant organs frequently presented an isolated pattern, which Fernandes et al. (1988) proposed is a protective strategy against natural enemies.The isolated oviposition of the inducer generates isolated galls, forcing parasitoids to spend their energy searching for and using the galls in immature stages.This is the first report of galls in the following plant genera: Gochnatia (Asteraceae), Distictela (Bignoniaceae), Banisteriopsis (Malpighiaceae), Ouratea (Ochnaceae), and Bredemeyera Polygalaceae).

Gall makers
One of the most interesting results of this work is the detection of relationships among host plants, gall makers and associated insects, as indicated in Table 2.
About 95% the host plant-gall maker relationships reported here are new to science.The relationships reported so far have been Malpighiaceae-Clinodiplosis from Peru described by Gagné (1994), and Pouteria-Youngomyia-Trotteria, whose relationship was reported by Rübsaamen (1916) and Maia (2001b) in a restinga (coastal sandy plains) environment in Rio de Janeiro, Brazil.Tavares (1918) and Houard (1933) also reported galls of Annona sp.induced by cecidomiids, and Fernandes et al. (1988) and Maia (2001a) described galls in Erythroxylum, albeit without providing the plant's specific identification.
The cecidomiids, one of largest families of Diphthera, are little known in Brazil, particularly in areas of open vegetation.As additional results of this study, three new occurrences of genera and thirteen new occurrences of species of the family Cecidomyiidae were identified, and have been described in other papers (Urso-Guimarães & Amorim, 2005; Urso-Guimarães & Amorim, submitted).In nine cases, the inducer was collected only in immature stages (larvae), despite five years of diligent sample collecting.These nine types of larvae are from cecidomiids, but specific identification at this level is rarely positive.
The cases in which identification was possible are presented with their diagnostic characteristics.Larvae reared in the creamy gall of Anacardium humile (Fig. 3a) probably belong to a new genus of Cecidomyiini.The larvae do not match the key for immatures of the Nearctic Region genera (Gagné, 1989).Anacardium humile also yielded larvae of Contarinia sp.n.1 in a red gall (Fig. 3b).Contarinia is a cosmopolitan genus whose larval diagnostic characteristic is the presence of a pair of corniform papillae in the terminal segment.The new species has two such papillae.
Specimens of the new genus of Lopesiini were collected in the leaf gall of Tapirira guianensis Aubl.occurring together with larvae of Dasineura.Lopesiini is a tribe with six genera, and the specimens found in this work will be described as a new genus based on the separated ovipositor cerci of females.The other Lopesiini have fused cerci.Dasineura belongs to a nonmonophyletic tribe, Oligotrophini (Gagné, 1994), which has nineteen other Neotropical genera.The diagnostic features of Dasineura are clove-shaped larval spatula with six papillae on each side of the spatula and eight terminal papillae in the anal segment.The association with T. guianensis is exclusive to this new species.
Specimens of Oligotrophini induce hairy leaf gall in Erythroxylum suberosum (Fig. 12).This is a new genus since the specimens do not match the key to Neotropical cecidomiids (Gagné, 1994).
Specimens of both genera reared in Pouteria torta belong to a new species.The specimens match the description of Youngomyia except for the female's elongated cerci, which are discoid in other species of this genus.The Trotteria species share mid and hind femora successively larger than the fore femur.The new species has tibial spurs, a feature exclusive to this family.
The 9 th abdominal segment of the specimens of the new species of Bruggmanniella have a pyriform basal portion, two longitudinal sclerotized dorsal bands, otherwise membranous and striated, and the pupa has a pair of distal projections on the 8 th abdominal segment.
The larva of the new Clinodiplosis species has a sclerotized band in the dorsal portion of the thorax, which is exclusive to this species.
As mentioned earlier, the host plant-gall maker relationship is very specific.In the key for the Neotropical Cecidomyiinae, many of the couplets that identify genera are related with the hosts.The species of Asphondylia, Neolasioptera, and the two species of Contarinia were identified as new because this is the first record of these genera, respectively, in galls on Eugenia bimarginata (Myrtaceae), Couepia grandiflora (Chrysobalanaceae), Distictela elongata (Bignoniaceae), and Ouratea spectabilis (Ochnaceae).