Insect galls of the Parque Nacional das Emas ( Mineiros , GO , Brazil )

In this study we perform an inventory of the insect leaf galls of the Parque Nacional das Emas, Goias State, Brazil. We found 97 gall morphotypes, distributed on 24 botanical families comprising 37 genera and 55 species. The plant taxa that showed the greatest richness of galls were the families Myrtaceae, with 17 morphotypes and Fabaceae with 14, and the genera Myrcia (Myrtaceae) and Qualea (Vochysiaceae) with 10 and eight morphotypes, respectively. The plant species Andira cujabensis Benth. (Fabaceae) and Myrcia guianensis (Aubl.) DC., with four morphotypes each, were the most diverse. We found galling insects belonging to Diptera, Hemiptera and Lepidoptera. The galling insects of family Cecidomyiidae (Diptera) were the most common inducing 38.1% of the gall morphotypes. All recorded gall morphotypes are first records to Parque Nacional das Emas. Among the 55 host plant species listed in the survey, 16 species (20%) have the first report of hosting galls.


Introduction
Insect galls can be defined as modifications in the vegetal tissues by hypertrophy and hyperplasia of cells caused by galling insect presence (Shorthouse and Rohfritsch 1992).Although galling insects are globally well distributed, several studies have showed that the Neotropical region is one of the most diverse in galling insect species (Gagné 1994;Espírito-Santo and Fernandes 2007;Carneiro et al. 2009).Much of this high diversity in the Neotropic is due to the high complexity of xeric physiognomies of Cerrado Biogeographic Region, a hotspot of galling diversity (Araújo et al. 2014).
In this paper, we perform an inventory of the insect leaf galls of Parque Nacional das Emas (PARNA-EMAS) located in Mineiros, Goiás State, Midwest Region of Brazil.The PARNA-EMAS is one of the largest and most important reserves in the Cerrado region with 132,941 ha.Its importance for the conservation of the fauna and flora of the Cerrado has been recognized by UNESCO in 2001 which declared the park as a World Heritage.The park exhibits almost all types of vegetation occurring in the Cerrado region (França et al. 2007).Floristic studies record the occurrence of 601 species and 80 families of vascular plants, being Fabaceae, Myrtaceae and Malpighiaceae the most important plant families in the woody vegetations of PARNA-EMAS (Batalha and Martins 2007).
In this study we found galling insects belonging to Diptera, Hemiptera and Lepidoptera (Table 3).The galling insects of family Cecidomyiidae (Diptera) were the most common inducing 38.1% of the gall morphotypes.Galling of Lepidoptera and Hemiptera were found in 5.2% and 2.0% of the morphotypes, respectively.In 54.6% of the gall morphotypes we did not find the gall-inducing insects.
All recorded gall morphotypes are first records to PARNA-EMAS.Among the 55 host plant species listed in the survey, 16 species (20%) have the first report of hosting galls: A.

Discussion
We recorded 97 gall morphotypes in PARNA-EMAS, which is relatively high when compared to other similar vegetations.For example, 62 gall morphotypes were recorded in savannas and forests of the Parque Estadual da Serra dos Pireneus (Araújo et al. 2011).In others studies were recorded 47 morphotypes in the Parque Estadual da Serra do Cabral (Coelho et al. 2013) and 38 gall types in the Parque Estadual Paulo César Vinha (Bregonci et al. 2010).These results indicate that PARNA-EMAS have a great diversity of galling insects.
Our main explanation to high gall diversity in the PARNA-EMAS is the dominance of xeric vegetations, which cover most of 90% of the reserve area (Ramos-Neto and Pivello 2000).Comparisons between different types of vegetations have pointed to a higher galling insect richness in the xeric plants (Gonçalves-Alvim and Fernandes 2001;Araújo et al. 2011).This differential distribution of galling insects in sclerophyllous vegetation can be due to three ecological mechanisms: plant stress, nutritional robustness and relationships with natural enemies (Araújo et al. 2014).Plants in xeric environments are under stress conditions, as water and nutrient scarcity that result in physiological changes and low protein production (Araújo et al. 2014).Galling insects have developed the ability to circumvent the toxic and nutritional restrictions of sclerophyllous plants under stress conditions (Wright and Samways 1998).In addition, at xeric environments, galling insects obtains protection from natural enemies, given the low diversity and frequency of parasitoids on harsh abiotic factors (Fleck and Fonseca 2007).The most diverse host family recorded in our study was Myrtaceae with 17 gall morphotypes.This result is different from most inventories on gall diversity in the Cerrado that indicate that Fabaceae (Gonçalves-Alvim and Fernandes 2001; Maia and Fernandes 2004;Santos et al. 2010;Araújo et al. 2011) and Asteraceae (Fernandes et al. 1996, Carneiro et al. 2009) are the most important host families.The high richness of galls in Myrtaceae can be attributed to high local number of host plant species recorded (18% of total).Myrtaceae is among the three most important plant families in the woody vegetations of PARNA-EMAS, together with Fabaceae and Malpighiaceae (Batalha and Martins 2007).We recorded Fabaceae as the second most important host family with 14 gall morphotypes, followed by Vochysiaceae with nine morphotypes.This latter family, have been pointed as an important host of galls in the Cerrado, even with a low diversity of plant species (Araújo et al. 2013).
The plant genera with the highest gall diversity in this study were Myrcia and Qualea, with 10 and eight gall morphotypes, respectively.The genus Myrcia was recorded with 10 gall morphotypes in restingas of Bertioga (Maia et al. 2008).Araújo et al. (2013) recorded 18 galling species on Qualea (Vochysiaceae) and eight on Qualea parviflora in different Brazilian savannas.About the high gall diversity on the plant species A. cujabensis and M. guianensis, the most important host species in the present study, there are no reports in the literature.
The galling insects of family Cecidomyiidae were the most important in the fauna studied, representing 84% of the obtained gall-makers.This result corroborate previous studies that pointed the dominance of Cecidomyiidae in the Neotropical savannas (Gonçalves-Alvim and Fernandes 2001;Maia and Fernandes 2004;Santos et al. 2010;Araújo et al. 2011).According to Araújo et al. (2014) the adaptive radiation strongly opportunistic of Cecidomyiidae associated to highly diverse flora are the main responsible by high diversity of group in the Cerrado.
To the best of our knowledge, this is the first systematic survey of insect galls realized in the PARNA-EMAS.The fact that 24% of the plant species listed in this study never have been recorded as gall-hosts demonstrates the need to increase the sampling efforts of insect galls in new areas, mainly areas highly conserved as the studied reserve.We believe that future studies in the park in other months of year (seasonal inventories) and other vegetation types may be important for understanding their regional galling fauna.

Table 2 .
Host plants (family and species) and insect gall morphotypes recorded in the Parque Nacional das Emas in Mineiros, GO, Brazil.