Incidence of galls on fruits of Parkinsonia praecox and its consequences on structure and physiology traits in a Mexican semi-arid region

Incidencia de agallas en frutos de Parkinsonia praecox y sus consecuencias sobre atributos morfológicos y fisiológicos en una zona semiárida de México

Estimates of galling insect richness calculates ~133,000 species distributed around the world (Espírito-Santo & Fernandes, 2007). The galling habit is widely spread among insects and is mostly comprised of Diptera, Hymenoptera, Hemiptera, Thysanoptera, Lepidoptera, and Coleoptera (Fernandes & Carneiro, 2009). These organisms induce abnormal structures on the plant, known as galls, cecidias or plant tumors (Fernandes & Carneiro, 2009). These structures are composed of plant tissue characterized by the increase in the number of cells (hyperplasy) and/or the increase in cell size (hypertrophy) (Mani, 1964).

Galls can be induced on any vegetative structure (leaves, stems, branches and roots) or reproductive organ (flowers, fruits and seeds) (Mani, 1964). The growth mechanisms of the plant organs are modified in response to stimuli from the galling insects (e.g., salivary secretion during feeding or maternal secretion in the oviposition), which alters the architecture and physiology of the plant in order to benefit it or its progeny (Oliveira et al., 2016; Raman, 2007; Stone & Schönrogge, 2003). The gall provides food, shelter, and protection against natural enemies for the galling insects (Fernandes & Santos, 2014; Price et al., 1987; Stone & Schönrogge, 2003).

Galling insects are found on specific host plants in natural communities across most biogeographical regions (Fernandes & Price, 1991; Price et al., 1998). However, their species richness has been reported to be higher in tropical regions (Fernandes & Price, 1988; Gonçalves-Alvim & Fernandes, 2001), with more species ocurring in xeric environments (Price et al., 1998) than in temperate and cold regions. At the global scale, most studies addressing the richness of galling insects have been carried out in the Cerrado (Brazilian savanna) (Araújo et al., 2014; Carneiro et al., 2009; Coelho et al., 2009; Fernandes et al., 1997; Gonçalves-Alvim & Fernandes, 2001), but also in tropical savanna (Blanche, 2000) and humid subtropical forests (Blanche & Westoby, 1995) in Australia, tropical humid and dry forests in Panama (Medianero et al., 2003) and in montane forest and shrublands in Texas, USA (Blanche & Ludwing, 2001). In Mexico, there is a scarcity of research studies on the ecology of galling insects. There are only a few studies reporting galling insect richness in 2 tropical rainforests (Los Tuxtlas Biosphere Reserve and in Lacandonia rainforest; Oyama et al., 2003) and in a tropical dry forest (Chamela-Cuixmala Biosphere Reserve; Cuevas-Reyes et al., 2004).

Buds, flowers, and fruits are poorly represented as host organs for galling insects, since these structures depend on the phenological stage of the plant (i.e., they may be unavailable to gallers throughout the year). The phenological dependence is more evident in tropical dry forests and xeric environments (Pezzini et al., 2014). Despite the low number of studies reporting galls on reproductive organs (Fernandes & Santos, 2014), the effects of galling on these organs could pose serious threats to the plants due to the potential impact they would have on plant performance and fitness (Fernandes, 1987). Galls on fruits exhibit noteworthy morphotypes, such as irregular (Santos et al., 2016), spherical (Quintero et al., 2014), amorphous, fusiform, globoid, ovoid, swollen or triangular (Isaias et al., 2014).

The impact of galling insects on their host plants is variable. Galling insects are known to stimulate the metabolism of nearby sources by increasing the sink demand relative to source supply (Fay et al., 1993). This leads to negative effects on the plant, such as a reduction in branch length (Fernandes et al., 1993; Kurzfeld-Zexer et al., 2010; Silva et al., 1996), lower quality seeds that affect germination (Santos et al., 2016; Silva et al., 1996), decrease in CO₂ assimilation (Haiden et al., 2012; Larson, 1998), limitations on flower and fruit production (Fernandes et al., 1993; Silva et al., 1996), and a reduction of entire plant biomass (McCrea et al., 1985). Galls on leaves of Acer sacharum (Sapindaceae) diminish approximately 60% of the stomatal conductance (Patankar et al., 2011). In contrast, the stomatal conductance of leaf galls on Acacia longifolia (Mimosoideae) shows no change in response to light intensity, but the immature galls had higher rates of stomatal conductance (Haiden et al., 2012). To our knowledge, beyond these reports, there are no studies that quantify the stomatal conductance in fruit with galls. Since these structures are physiological sinks and could have a negative effect on the fruit set, studies related to fruit galls become particularly important in order to understand how the presence of galls affects the reproductive input and fitness of the plant. The approach of this study involves the anatomical and physiological features in galled and healthy fruits.

We investigated the effects of galls on fruits of Parkinsonia praecox (Ruiz & Pav. ex Hook.) Hawkins based on morphological traits (length, diameter, thickness, water content and biomass content); anatomical features (trichomes, stomatal, and pavement cells), and physiological characteristics (stomatal conductance, g_s).

Materials and methods

The study was conducted in the Zapotitlán Salinas Valley, located in the Tehuacán-Cuicatlán Biosphere Reserve, Puebla, Mexico. The data sampling was carried out in the nearby surroundings of the “Helia Bravo-Hollis” Botanical Garden (18°20’ N, 97°28’ W, at 1,500 m asl). The main plant association is the tetechera, dominated by the columnar cactus Neobuxbaumia tetetzo (Zavala, 1982); the vegetation corresponds to semi-arid scrubland (Rzedowski, 2006). The mean annual precipitation is 381.21 mm, and the annual mean temperature is 18.04 °C. The dry season is from September to April, and the rainy season is from May to August (Zavala, 1982). The climatic data were obtained from Conagua (2010) for the period 1964-2010.

Parkinsonia praecox (Fabaceae-Caesalpinoideae) is known in the study area as “manteco” or “palo verde”, it is a 7 m tall tree (Fig. 1A). In Mexico, it is distributed in the Northwest (Baja California Sur, Sonora, Chihuahua, Sinaloa, Durango, Zacatecas and Nayarit), East Center (Jalisco, Colima, Michoacán, Guanajuato, Morelos, Guerrero, Puebla, México), East (Tamaulipas and Veracruz), and South (Oaxaca and Chiapas) (Villaseñor, 2016). It is a common species in some vegetal associations in the Zapotitlan Salinas Valley (López-Galindo et al., 2003; Montaña & Valiente-Banuet, 1998). P. praecox fruits are flattened brown pods 10 cm length and 1 cm width, arranged in racemes, generally in pairs (Fig. 1B). Seeds are shiny-brown color and 7 mm mean length (Pennington & Sarukhán, 2005). The flowering season occurs between December-May, and the fruiting period is between January-September (Arias et al., 2001; Pennington and Sarukhán, 2005). Infructescences of P. praecox showed an important incidence of galls (Fig. 1C). Galled fruits had 1 larval chamber located at the center surrounded by parenchymatous tissue (Fig. 1D) (Contreras-Varela pers. obs.). Asphondylia sp. (Diptera: Cecidomyiidae) is the galling insect. From November to March, the branches are leafless when flowering and fruit set occurs (Pavón & Briones, 2001), indicating that it is a totally deciduous species during this period.

The number of fruits affected by galls was determined in 30 randomly selected branches with galls and fruits of 50 cm long (2 per tree) in 15 different trees. In 10 individuals of P. praecox it was determined macroscopical characteristics of galled and healthy fruits, 50 pairs of a galled and a healthy fruit were randomly selected. A digital caliper (CD-s6, Mitutoyo Corp., Kawasaki, Japan) was used to measure length, diameter (distance considered starting in the abscission line in the middle of the fruit) and thickness of galled and healthy fruits. Aditionally, in transversal sections of galled fruits we measured parenchymatous tissue, and larval chamber size. In healthy and galled fruits, we quantified the water and biomass content by recording the fresh weight (FW), and then these were oven-dried for 36 hours at 70 °C. Later, the dry weight (DW) was quantified using a weighing scale (CP-225D, Sartorius, Germany, 0.01 g of accuracy). The water content was calculated as (FW-DW)/FW. The biomass content was defined as DW/FW. The water and biomass contents are expressed as a percentage.

In 3 individuals of P. praecox, 5 galled fruits (n = 15) and 5 healthy fruits (n = 15) were used to determine trichomes, stomatal, and pavement cell density, as well as stomata and pavement cell size. We applied a thin layer of clear nail varnish on the surface of the galled and healthy fruits in order to obtain permanent impressions of trichomes, stomata, and pavement cells. The area covered by the varnish layer was approximately 1 cm². We determined the area of the 150 stomata and 150 pavement cells by measuring microphotographs of the samples with the software ImageJ (Rasband, 2017). The trichomes, stomatal, and pavement cell density were calculated in 2.7 mm² in 3 randomly selected visual fields of an optical microscope per varnish layer (Carl Zeiss Inc., Thornwood, N.Y.).

Measurements of g_s were determined in galled and healthy fruits in field using a porometer (SC-1, Decagon Devices Inc., Washington, USA). The sensor head of the porometer was situated in the middle section of the samples. Galled and healthy fruits were carefully placed on the sensor head without pressing, to avoid an overestimation of the g_s. Seven measurement periods of g_s were made between 07:00 h and 21:00 h on 3 different pairs of galled (n = 21) and healthy fruits (n = 21); 1 pair per individual of P. praecox.

Generalized linear mixed models (GLMMs) were used to evaluate the relationship between galled and healthy fruits in each of the morphological traits (length, diameter, thickness, water content, biomass content) and anatomical features (trichomes, stomata, pavement cells). As fixed effects, we entered the galled and healthy fruits into the model. As random effect, we used intercepts for individuals of P. praecox, as well as random slopes for the effect of galled and healthy fruits.

A GLMM was used to assess the effects of the time of the day, galled and healthy fruits on the g_s. The fixed effects were the galled fruits, healthy fruits and the time of the day (07:00 to 21:00 h), while the random effects were the individuals of P. praecox, as well as random slopes for the effect of galled and healthy fruits. We assumed a gamma distribution for the model.

Visual inspection of residual plots indicates there was no deviation of homoscedasticity or normality. P-values were obtained by a likelihood ratio test of the full model with the effect against the model without the effect (Zuur et al., 2009). All statistical analyses were performed in R version 3.2.2 (R Development Core Team, 2017) with the package lme4 (Bates et al., 2015) and multicomp (Hothorn et al., 2008). For all statistical analyses, we reported the mean ± SE and the differences in magnitude (i.e., mm², %, and density) between galled and healthy fruits, referred as estimated values calculated in the GLMMs.

Results

Twenty percent of the P. praecox fruits had galls, although some affected fruits had a few seeds in the apical portion of the fruit. The branches with only healthy fruits had on average 28.1 ± 1.38 fruits per branch (n = 299), while branches with galled fruits had 21.5 ± 2.04 fruits (fruits ± SE) per branch (n = 138). Galled fruits had a spherical shape and were green-reddish. Each galled fruit was composed of parenchymatous tissue with 0.4 ± 0.06 cm (cm ± SE) of thickness. This tissue surrounds a larval chamber, which was 0.1 ± 0.01 cm of diameter that holds only 1 galling insect larva.

The morphological traits of galled and healthy fruits (length, diameter, thickness, water content, and biomass content) exhibited significant differences. The galled fruits were 2.91 ± 0.17 cm shorter than the healthy fruits (χ² = 51.8, p < 0.001; Fig. 2A). On the other hand, galled fruits had 0.28 ± 0.04 cm larger diameter (χ² = 23.2, p < 0.001; Fig. 2B) and were 0.87 ± 0.03 cm thicker (χ² = 53.1, p < 0.001; Fig. 2C) than the healthy fruits. The water content was 4.24 ± 1.2% higher in the galled fruits (χ² = 7.1, p < 0.01; Fig. 3), while healthy fruits had 4.2 ± 1.3% higher biomass content (χ² = 7.16, p < 0.01; Fig. 3).

The stomatal density (0.28 ± 0.81 stomata mm², χ² = 0.12, p = 0.72; Fig. 4A) did not differ between galled and healthy fruits. Contrarily, trichome density (4.76 ± 1.42 trichomes mm², χ² = 7.43, p = 0.006; Fig. 4C) and pavement cell density (19.4 ± 8.19 pavement cells mm², χ² = 4.34, p < 0.05; Fig. 4D) were statistically different between galled and healthy fruits. The area of pavement cells did not differ between galled and healthy fruits (0.005 ± 0.005 µm², χ² = 0.77, p = 0.37), while the stomatal size was 70.13 ± 21.51 µm² larger in galled fruits than in healthy fruits (χ² = 5.05, p < 0.05; Fig. 4B).

The g_s was higher in galled fruits than in healthy fruits (χ² = 12.6, p = 0.001). The interaction of daytime and the gall presence had a negative effect on the g_s of galled fruits (χ² = 36, p < 0.001). In the galled fruits, the highest values of g_s were recorded at 07:00 h, while the lowest values were found in healthy fruits at 16:00 hrs. Likewise, the g_s exhibited differences during the daytime (χ² = 30, p < 0.001). Values of g_s in galled and healthy fruits decreased throughout the day, with a slight increase in the last 2 records at night (18:00 to 20:00 h) (Fig. 5).

Discussion

In this study, we showed the incidence of galls in P. praceox fruits and its consequences on morphology and physiology. This is the first report of gall incidence on fruits in this semi-arid region of Central Mexico. In general, studies on galled fruits are scarce in the literature. We reviewed studies that report the presence of galls on reproductive structures, and we found 128 host plant species; Fabaceae was the most abundant host family (78 species), followed by Asteraceae (9 species), Boraginaceae (6) and Rubiaceae (6). The 2 most representative genera were Acacia (58 species) and Prosopis (14 species). Of the total number of host plant species found in our revision, 85.15% had galls on flowers (achene, buds, capitula, flowers, inflorescences) and the remaining 14.84% on fruits and seeds (Appendix).

Some species in South America have been reported as hosts of fruit-gall inducing insects, such as Conostegia xalapensis (Melastomataceae) (Chavarría et al., 2009); and Miconia calvescens (Melastomataceae) (Badenes-Perez & Johnson, 2007). Curiously, most studies are developed in the Costa Rican tropical dry forest (Janzen, 1982); Australian seasonally tropical forest (Kolesik et al., 2010), and Brazilian savanna (Santos et al., 2016). There are few studies on xeric environments that report the presence of galls on fruits, i.e. in Brazilian Restinga, Pithecellobium tortum have galls in seeds (de Macêdo & Monteiro, 1989). In our work we reported galls on P. praecox fruits and this is a pioneer study related to the study of galls in this area (Tehuacán-Cuicatlán, Mexico).

The galling insect Asphondylia sp. modifies the natural development of P. praecox fruits and negatively affects the fruit set of the host plant. In our bibliographical revision we found that the most representative taxonomic level of gall-forming insects on reproductive structures corresponded to the order Diptera (92.96%; 119 species) followed by Hymenoptera (6.25%; 8 species). The most important families of dipteran galling insects were Cecydomiidae (89.06%; 114 spp.) and Teprhitidae (3.9%, 5 spp.); of Coleoptera was Curculionidae (0.78%; 1 spp.); of Hymenoptera were Braconiidae (3.12%; 4 spp.), Agaonidae (0.78%; 1 spp.), Pteromalidae (0.78%; 1 spp.), Chalcidoidea (0.78%; 1 spp.) and Euritomidae (0.78%; 1 spp.). The most representative genus of galling insects was Asphondylia (44.87%; 60 spp.); followed by Dasineura (23.43%; 30 spp.), Allorhgas (3.12%; 4 spp.), Clinodiplosis (3.12%; 4 spp.), Urophora (3.12%; 4 spp.), Bruggmanniella (2.34%; 3 spp.), Eschizomia (1.56%; 2 spp.), and 13 genera correspond to 10.93%, each one represented by 1 species (Appendix).

 

Branches of P. praecox had 20% of gall incidence, indicating a high impact on fruit production. In association with pre-dispersal seed predation by coleopterans (Contreras-Varela, pers. obs.) and seed viability (Flores & Briones, 2001) the performance of P. praecox should be largely reduced.

Gall induction on P. praecox fruits should start inside the ovary where the cells are not yet differenciated, consequently the normal structure of the fruit is modified thus producing galls of spherical shape mainly without seeds (Fig. 1C). In general, galling insects require totipotent and undifferentiated tissues to induce galls development (Fernandes & Carneiro, 2009; Fernandes & Santos, 2014).

Galled fruits on P. praecox are mainly composed of parenchymatous tissue surrounding the larval chamber. We found that the biomass was greater in healthy fruits than in galled fruits. The water content in galled fruits (ca. 84.16%) suggests that galls are indeed important adaptations to live under harsh environments (Fernandes & Price, 1988; Price et al., 1987). The volumetric growth of fleshy fruits is the result of water and solutes accumulation that involves differences in water potential between the pedicel of the fruit and the rest of the plant (Matthews & Shackel, 2005). The gall formation in P. praecox involves the differentiation of a wide range of tissues that make the fleshy galls to superimpose an overall size. The water storage of galled fruits should be associated to solutes accumulation and to the increase of parenchyma cells turgor, these 2 conditions induce the cell hypertrophy and hyperplasia (Cosgrove, 2000). The parenchyma plays an important role for water and nutrient storage (Evert, 2006). To our knowledge, there is no information about the role of solutes content on the water movement to galls or if the chemical signals from the galling insects regulate the accumulation of solutes in galls. It has been reported that gall formation in vegetative structures comprise mainly the cellular elongation, however, cellular division and elongation has been associated to galls formation in reproductive structures (dos Santos et al., 2014). The sclerified tissue in galls and the high trichome density provide mechanical protection, the parenchymatous layer serves as a water and nutrient reservoir (Oliveira et al., 2014, 2016; Stone & Schönrogge, 2003).

The density of trichomes found on galled fruits of P. praecox was 1.5 times higher than on healthy fruits. In xeric environments, an increase of leaf pubescence leads to reduced water vapor transpiration and increases the thickness of the boundary layer (Evert, 2006; Pallardy, 2008). It has been reported that the pubescence of fruits significantly reduces water loss (Fernández et al., 2011). In P. praecox galled fruits, the high density of trichomes could prevent excessive moisture loss in the larval chamber and may maintain the internal temperature (Oliveira et al., 2014; Price et al., 1987). In addition, an elevated density of trichomes could reduce the vulnerability of the galling insects to potential natural enemies (Fernandes et al., 1987; Stone & Schönrogge, 2003; Woodman & Fernandes, 1991).

Galling insects do not only affect plant architecture and host organ morphogenesis, but also can modify physiological conditions such as stomatal conductance (Fay et al., 1996; Florentine et al., 2005; Larson, 1998), transpiration and CO₂ assimilation (Dorchin et al., 2006). Those modifications influence positively to the gall (Fay et al., 1996) or negatively to the host (Florentine et al., 2005; Larson, 1998). Galled fruits of P. praecox increase the g_s and stomatal size but had lower density of pavement cells in relation to healthy fruits; thus, it is possible that the increase in trichome density is the result of a compensatory mechanism to the high gas exchange of the galls with the environment; otherwise, the g_s could be even higher (Fernández et al., 2011). Stomatal conductance estimates the rate of gases exchange through the stomata; it involves the density and aperture of stomata (Pietragalla & Pask, 2012) to infer transpiration and photosynthesis (Hiyama et al., 2005). According to Lemos-Filho and Isaias (2004), the fruits of Dalbergia miscolombium (Fabaceae) have a photosynthetic activity that contributes to the carbohydrates required for the fruit development. The g_s in both galled and healthy fruits of P. praecox exhibited a similar pattern throughout the day, the higher values were recorded after the sunrise, indicating that the variation in g_s of galls is due to water conditions in stem. The stomatal opening regulates the transpiration and prevents excessive water loss in the environment (Farquhar & Sharkey, 1982).

The g_s in galled fruits was 2.5 times higher than in healthy fruits. Stomatal conductance can vary due to environmental (e.g., light intensity, CO₂ concentration, relative humidity, temperature, wind, atmospheric pressure), anatomical (e.g., foliar area, pubescence, size and stomatal density), and/or endogenous factors (e.g., phytohormones) (Farquhar & Sharkey, 1982; Pallardy, 2008). In our study, the environmental conditions were similar in galled and healthy fruits. We found that galled fruits increased significantly the g_s rates, although the stomatal density was not statistically different. This could be influenced by the production of signaling molecules, like phytohormones that promote the stomata opening and water movement to galls, in order to favor the water and nutrient continuum from host plant to gall. A revision of the abscisic acid (ABA) role in gall formation made by Tooker and Helms (2014) indicates that this phytohormone promotes gall growth. Even though the exact function of this hormone has not been yet fully recognized in gall tissues, ABA has been acknowledged as an endogenous regulator of the transpiration rate that controls the stomatal closing (Xiong & Zhu, 2003). We also suggest that similar endogenous regulation may occur on P. praecox galled fruits, but further phytochemical analysis will be necessary to determine the presence of ABA.

In conclusion, we found an important incidence of galled fruits on P. praecox that negatively affect morphological features of the fruits, with consequences on performance of the fruits. In addition, galled fruits are water sinks for this host plant that inhabits xeric environments. Future research is required to evaluate if the incidence of galled fruits negatively affects the plant fitness at the population level, in the different environmental conditions that occur in the Tehuacán-Cuicatlán Biosphere Reserve.

Acknowledgements

To Facultad de Biología of the Benemérita Universidad Autónoma de Puebla and to the students, for their time and assistance during field work. Special thanks to Dr. Vicente Hernández (Red de Interacciones Multitróficas, INECOL) for his assistance in the identification of the galling insect. To the “Comisariado de Bienes Comunales” of Zapotitlán Salinas for leting us to work within the Botanical Garden “Helia Bravo Hollis” borders. To the Instituto de Ecología, A.C., for the research funds to A.A. (PO-20030-11315). GWF thanks the support of CNPq and FAPEMIG. Finally, thanks to Biól. Rosamond Coates (IB-UNAM) for her English revision. Suggestions of two anonymous reviewers improved the manuscript.

Appendix. Studies related to galls incidence in reproductive structures in plants, highlighting several aspects to the host plants, morphological traits of galls, as well as data of galling insects.

Appendix. Continued
Host	Galls
Family plant	Species	Organ	Shape	Color	Galling insect	Order/family	Reference
Host	Galls
Family plant	Species	Organ	Shape	Color	Galling insect	Order/family	Reference
Anacardiaceae	Mangifera indica	Flower	Elliptical	unknown	Procontarina mangiferae	Diptera-Cecidomyiidae	Tavares, 1917; Gagné, 2004; Carneiro et al., 2009
Apocynaceae	Peplonia asteria	Flower	Ovoid	Green	Asphondylia peplonidae	Diptera-Cecidomyiidae	Gagné, 2004; Carneiro et al., 2009
Apocynaceae	Oxypetalum banksii	Flower bud	–	–	Asphondylia peploniae	Diptera-Cecidomyiidae	Gagné, 2004; Flor & Maia, 2017
Arecaceae	Geonoma cuneata	Inflorescence	Cylindrical	Green-reddish	Contarinia geonomae	Diptera-Cecidomyiidae	Gagné et al., 2018
Asteraceae	Porophyllum sp.	Stem/flower	Elliptical	Purple	Zalepidota ituensis	Diptera-Cecidomyiidae	Tavares, 1917; Gagné, 1994, 2004; Carneiro et al., 2009
Asteraceae	Chromolaena odorata	Achene	Swollen	unknown	Asphondylia corbulae	Diptera-Cecidomyiidae	Möhn, 1959; Gagné, 1994, 2004; Carneiro et al., 2009
Asteraceae	Fleischmannia microstemon	Achene	Swollen	unknown	Asphondylia corbulae.	Diptera-Cecidomyiidae	Möhn, 1959; Gagné, 1994, 2004; Carneiro et al., 2009
Asteraceae	Chromolaena odorata	Bud	Swollen	unknown	Perasphondylia reticulata	Diptera-Cecidomyiidae	Möhn, 1959; Gagné, 1977; Carneiro et al., 2009
Asteraceae	Sonchus arvensis	Flower heads	–	–	Tephritis dilacerata	Diptera-Tephritidae	Harris & Shorthouse, 1996
Asteraceae	Centaurea maculosa	Floral receptacule	–	–	Urophora affinis	Diptera-Tephritidae	Crowe & Bourchier, 2006
Asteraceae	Carduus nutans	Flower heads	–	–	Urophora solstitialis	Diptera-Tephritidae	Groenteman et al., 2007
Asteraceae	Centaurea stoebe subsp. micranthos	Flower heads	–	–	Urophora quadrifasciata	Diptera-Tephritidae	Duguma et al., 2009
Asteraceae	Centaurea solstitialis	Flower heads	–	–	Urophora sirunaseva	Diptera-Tephritidae	Woods et al., 2008
Boraginaceae	Cordia alba	Flower	Swollen	unknown	Asphondylia cordiae	Diptera-Cecidomyiidae	Gagné, 1994, 2004; Carneiro et al., 2009
Boraginaceae	Cordia dentata	Flower	Swollen	unknown	Asphondylia cordiae	Diptera-Cecidomyiidae	Gagné, 1994, 2004; Carneiro et al., 2009
Boraginaceae	Cordia verbenacea	Flower	Ovoid	Green	Asphondylia cordiae	Diptera-Cecidomyiidae	Maia, 2001; Carneiro et al., 2009
Boraginaceae	Tournefortia angustifolia	Fruit	Elongated sheroid	unknown	Asphondylia tournefortiae	Diptera-Cecidomyiidae	Houard, 1933; Möhn, 1960; Gagné 1994, 2004; Carneiro et al., 2009
Boraginaceae	Tournefortia volubilis	Fruit	Elongated sheroid	unknown	Asphondylia tournefortiae	Diptera-Cecidomyiidae	Houard, 1933; Möhn, 1960; Gagné 1994, 2004; Carneiro et al., 2009
Boraginaceae	Varronia curassavica	Inflorescence	Ovoid, hairy	Green-yellow	Asphondylia cfr. cordia	Diptera-Cecidomyiidae	Gagné, 1994; Maia et al., 2008; Flor & Maia, 2017
Brassicaceae	Cakile maritima	Bud		Brown	Gephyraulus zewaili	Diptera-Cecidomyiidae	Elsayed et al., 2017
Calophyllaceae	Kielmeyera coriaceae	Flower bud	Swollen	unknown	Arcivena kielmeyera	Diptera-Cecidomyiidae	Gagné, 2004; Carneiro et al., 2009
Calophyllaceae	Kielmeyera rosea	Flower bud	Swollen	unknown	Arcivena kielmeyera	Diptera-Cecidomyiidae	Gagné, 2004; Carneiro et al., 2009
Calophyllaceae	Kielmeyera petiolaris	Flower bud	Swollen	unknown	Arcivena kielmeyera	Diptera-Cecidomyiidae	Gagné, 2004; Carneiro et al., 2009
Calophyllaceae	Kielmeyera variata	Flower bud	Swollen	unknown	Arcivena kielmeyera	Diptera-Cecidomyiidae	Gagné, 2004; Carneiro et al., 2009
Calophyllaceae	Kielmeyera speciosa	Flower bud	Swollen	unknown	Arcivena kielmeyera	Diptera-Cecidomyiidae	Gagné, 2004; Carneiro et al., 2009
Calophyllaceae	Kielmeyera rubiflora	Flower bud	Swollen	unknown	Arcivena kielmeyera	Diptera-Cecidomyiidae	Gagné, 2004; Carneiro et al., 2009
Calophyllaceae	Kielmeyera corymbosa	Flower bud	Swollen	unknown	Arcivena kielmeyera	Diptera-Cecidomyiidae	Gagné, 2004; Carneiro et al., 2009
Celastraceae	Maytenus obtusifolia var. obovata	Fruit	Ovoid	Red	Bruggmanniella maytenuse	Diptera-Cecidomyiidae	Maia, 2001; Gagné, 1994, 2004; Carneiro et al., 2009
Convolvulaceae	Jacquemontia holosericea	Flower	Ovoid	Green/reddish	Schizomyia santosi	Diptera-Cecidomyiidae	Maia, 2001; Carneiro et al., 2009
Erythroxilaceae	Erythroxylum ovalifolium	Flower	Ovoid	Greenish	Asphondylia sp.	Diptera-Cecidomyiidae	Maia, 2001; Carneiro et al., 2009
Fabaceae	Senna bicapsularis	Flower	Spherical	Yellow	Asphondylia sennae	Diptera-Cecidomyiidae	Maia et al., 1992; Gagné, 2004; Carneiro et al., 2009
Fabaceae	Mimosa caesalpinifolia	Fruit	Unknown	unknown	Tavaresomyia mimosae	Diptera-Cecidomyiidae	Möhn, 1961; Gagné, 1994, 2004; Carneiro et al., 2009
Fabaceae	Inga vera	Seeds	–	–	Allorhogas sp.	Hymenoptera-Braconidae	Morales-Silva & Modesto-Zampiero, 2018
Fabaceae	Acacia longifolia	Inflorescence	–	–	Trichilogaster acaciaelongifoliae	Hymenoptera-Pteromalidae	Dennill, 1988
Fabaceae	Acacia aneura	Open flowers	–	–	Dasineura glauca	Diptera-Cecidomyiidae	Kolesik et al., 2010
Fabaceae	Acacia baileyana	Open flowers	–	–	Dasineura pilífera	Diptera-Cecidomyiidae	Kolesik et al., 2010
Fabaceae	Acacia baileyana	Flower buds	–	–	Asphondylia pilogerminis	Diptera-Cecidomyiidae	Kolesik et al., 2010
Fabaceae	Acacia cyclops	Flower buds, fruit	–	–	Asphondylia acaciae	Diptera-Cecidomyiidae	Kolesik et al., 2010
Fabaceae	Acacia cyclops	Open flowers	–	–	Dasineura dielsi	Diptera-Cecidomyiidae	Kolesik et al., 2010
Fabaceae	Acacia dealbata	Open flowers	–	–	Dasineura pilífera	Diptera-Cecidomyiidae	Kolesik et al., 2010
Fabaceae	Acacia dealbata	Flower buds	–	–	Asphondylia pilogerminis	Diptera-Cecidomyiidae	Kolesik et al., 2010
Fabaceae	Acacia deanei	Flower buds	–	–	Asphondylia glabrigerminis	Diptera-Cecidomyiidae	Kolesik et al., 2010
Fabaceae	Acacia deanei	Open flowers	–	–	Dasineura glomerata	Diptera-Cecidomyiidae	Kolesik et al., 2010
Fabaceae	Acacia deanei	Fruit	–	–	Asphondylia bursicola	Diptera-Cecidomyiidae	Kolesik et al., 2010
Fabaceae	Acacia decurrens	Open flowers	–	–	Dasineura pilífera	Diptera-Cecidomyiidae	Kolesik et al., 2010
Fabaceae	Acacia decurrens	Fruit	–	–	Asphondylia bursicola	Diptera-Cecidomyiidae	Kolesik et al., 2010
Fabaceae	Acacia divergens	Flower buds	–	–	Asphondylia germinis	Diptera-Cecidomyiidae	Kolesik et al., 2010
Fabaceae	Acacia elata	Open flowers	–	–	Dasineura glomerata	Diptera-Cecidomyiidae	Kolesik et al., 2010
Fabaceae	Acacia floribunda	Flower buds, fruit	–	–	Asphondylia acaciae	Diptera-Cecidomyiidae	Kolesik et al., 2010
Fabaceae	Acacia genistifolia	Flower buds	–	–	Asphondylia germinis	Diptera-Cecidomyiidae	Kolesik et al., 2010
Fabaceae	Acacia hakeoides	Open flowers	–	–	Dasineura glomerata	Diptera-Cecidomyiidae	Kolesik et al., 2010
Fabaceae	Acacia implexa	Open flowers	–	–	Dasineura acaciaelongifoliae	Diptera-Cecidomyiidae	Kolesik et al., 2010
Fabaceae	Acacia irrorata	Open flowers	–	–	Dasineura fistulosa	Diptera-Cecidomyiidae	Kolesik et al., 2010
Fabaceae	Acacia irrorata	Fruit	–	–	Asphondylia bursicola	Diptera-Cecidomyiidae	Kolesik et al., 2010
Fabaceae	Acacia irrorata	Flower buds	–	–	Asphondylia pilogerminis	Diptera-Cecidomyiidae	Kolesik et al., 2010
Fabaceae	Acacia littorea	Flower buds	–	–	Asphondylia germinis	Diptera-Cecidomyiidae	Kolesik et al., 2010
Fabaceae	Acacia littorea	Fruit	–	–	Asphondylia occidentalis	Diptera-Cecidomyiidae	Kolesik et al., 2010
Fabaceae	Acacia longifola	Open flowers	–	–	Dasineura acaciaelongifoliae	Diptera-Cecidomyiidae	Kolesik et al., 2010
Fabaceae	Acacia mearnsii	Open flowers	–	–	Dasineura fistulosa	Diptera-Cecidomyiidae	Kolesik et al., 2010
Fabaceae	Acacia mearnsii	Flower buds	–	–	Asphondylia glabrigerminis	Diptera-Cecidomyiidae	Kolesik et al., 2010
Fabaceae	Acacia mearnsii	Open flowers	–	–	Dasineura glomerata	Diptera-Cecidomyiidae	Kolesik et al., 2010
Fabaceae	Acacia mearnsii	Fruit	–	–	Asphondylia bursicola	Diptera-Cecidomyiidae	Kolesik et al., 2010
Fabaceae	Acacia mearnsii	Flower buds	–	–	Asphondylia pilogerminis	Diptera-Cecidomyiidae	Kolesik et al., 2010
Fabaceae	Acacia mearnsii	Open flowers	–	–	Dasineura rubiformis	Diptera-Cecidomyiidae	Kolesik et al., 2010
Fabaceae	Acacia maidenii	Open flowers	–	–	Dasineura acaciaelongifoliae	Diptera-Cecidomyiidae	Kolesik et al., 2010
Fabaceae	Acacia melanoxylon	Flower buds, fruit	–	–	Asphondylia acaciae	Diptera-Cecidomyiidae	Kolesik et al., 2010
Fabaceae	Acacia melanoxylon	Open flowers	–	–	Dasineura furcata	Diptera-Cecidomyiidae	Kolesik et al., 2010
Fabaceae	Acacia melanoxylon	Open flowers	–	–	Dasineura glomerata	Diptera-Cecidomyiidae	Kolesik et al., 2010
Fabaceae	Acacia oldfieldii	Open flowers	–	–	Dasineura oldfieldii	Diptera-Cecidomyiidae	Kolesik et al., 2010
Fabaceae	Acacia omalophylla	Open flowers	–	–	Dasineura glauca	Diptera-Cecidomyiidae	Kolesik et al., 2010
Fabaceae	Acacia oshanesii	Open flowers	–	–	Dasineura oshanesii	Diptera-Cecidomyiidae	Kolesik et al., 2010
Fabaceae	Acacia paradoxa	Flower buds, fruit	–	–	Asphondylia acaciae	Diptera-Cecidomyiidae	Kolesik et al., 2010
Fabaceae	Acacia pendula	Open flowers	–	–	Dasineura glauca	Diptera-Cecidomyiidae	Kolesik et al., 2010
Fabaceae	Acacia pentadenia	Fruit	–	–	Asphondylia occidentalis	Diptera-Cecidomyiidae	Kolesik et al., 2010
Fabaceae	Acacia pycnantha	Open flowers	–	–	Dasineura glomerata	Diptera-Cecidomyiidae	Kolesik et al., 2010
Fabaceae	Acacia ramulosa	Open flowers	–	–	Dasineura glauca	Diptera-Cecidomyiidae	Kolesik et al., 2010
Fabaceae	Acacia ramulosa	Fruit	–	–	Asphondylia occidentalis	Diptera-Cecidomyiidae	Kolesik et al., 2010
Fabaceae	Acacia retinoides	Flower buds, fruit	–	–	Asphondylia acaciae	Diptera-Cecidomyiidae	Kolesik et al., 2010
Fabaceae	Acacia retinoides	Open flowers	–	–	Dasineura glomerata	Diptera-Cecidomyiidae	Kolesik et al., 2010
Fabaceae	Acacia rostellifera	Fruit	–	–	Asphondylia occidentalis	Diptera-Cecidomyiidae	Kolesik et al., 2010
Fabaceae	Acacia saligna	Open flowers	–	–	Dasineura sulcata	Diptera-Cecidomyiidae	Kolesik et al., 2010
Fabaceae	Acacia schinoides	Open flowers	–	–	Dasineura glomerata	Diptera-Cecidomyiidae	Kolesik et al., 2010
Fabaceae	Acacia longifolia subsp. sophorae	Flower buds, fruit	–	–	Asphondylia acaciae	Diptera-Cecidomyiidae	Kolesik et al., 2010
Fabaceae	Acacia longifolia subsp. sophorae	Open flowers	–	–	Dasineura acaciaelongifoliae	Diptera-Cecidomyiidae	Kolesik et al., 2010
Fabaceae	Acacia sophorae x oxycedrus	Open flowers	–	–	Dasineura acaciaelongifoliae	Diptera-Cecidomyiidae	Kolesik et al., 2010
Fabaceae	Acacia stricta	Open flowers	–	–	Dasineura acaciaelongifoliae	Diptera-Cecidomyiidae	Kolesik et al., 2010
Fabaceae	Acacia ulicifolia	Flower buds, fruit	–	–	Asphondylia acaciae	Diptera-Cecidomyiidae	Kolesik et al., 2010
Fabaceae	Acacia urophylla	Flower buds	–	–	Asphondylia germinis	Diptera-Cecidomyiidae	Kolesik et al., 2010
Fabaceae	Acacia verticillata	flower buds, fruit	–	–	Asphondylia acaciae	Diptera-Cecidomyiidae	Kolesik et al., 2010
Fabaceae	Acacia xanthina	Flower buds	–	–	Asphondylia germinis	Diptera-Cecidomyiidae	Kolesik et al., 2010
Fabaceae	Acacia cavenia	Bud	–	–	Chalcidoidea sp.	Hymenoptera-Chalcidoidea	Maia, 2012
Fabaceae	Gourliea decorticans	Bud and stem	–	–	Proseurytoma gallarum	Hymenoptera-Eurytomidae	Maia, 2012
Fabaceae	Inga laurina	Fruit	–	–	Allorhogas sp.	Hymenoptera-Brachonidae	Santos et al., 2016
Fabaceae	Enterolobium cyclocarpum	Fruit	–	–	Asphondylia enterolobi	Diptera-Cecidomyiidae	Janzen, 1982
Fabaceae	Prosopis alba	Flower	–	–	Asphondylia sp. nr. prosopidis	Diptera-Cecidomyiidae	Mc Kay & Gandolfo, 2007
Fabaceae	Prosopis caldenia	Flower	–	–	Asphondylia sp. nr. prosopidis	Diptera-Cecidomyiidae	Mc Kay & Gandolfo, 2007
Fabaceae	Prosopis chilensis	Flower	–	–	Asphondylia sp. nr. prosopidis	Diptera-Cecidomyiidae	Mc Kay & Gandolfo, 2007
Fabaceae	Prosopis flexuosa	Flower	–	–	Asphondylia sp. nr. prosopidis	Diptera-Cecidomyiidae	Mc Kay & Gandolfo, 2007
Fabaceae	Prosopis nigra	Flower	–	–	Asphondylia sp. nr. prosopidis	Diptera-Cecidomyiidae	Mc Kay & Gandolfo, 2007
Fabaceae	Prosopis kuntzei	Flower	–	–	Asphondylia sp. nr. prosopidis	Diptera-Cecidomyiidae	Mc Kay & Gandolfo, 2007
Fabaceae	Prosopis ruscifolia	Flower	–	–	Asphondylia sp. nr. prosopidis	Diptera-Cecidomyiidae	Mc Kay & Gandolfo, 2007
Fabaceae	Prosopis affinis	Unriped pods	–	–	Asphondylia sp. nr. prosopidis	Diptera-Cecidomyiidae	Mc Kay & Gandolfo, 2007
Fabaceae	Prosopis alba	Unriped pods	–	–	Asphondylia sp. nr. prosopidis	Diptera-Cecidomyiidae	Mc Kay & Gandolfo, 2007
Fabaceae	Prosopis caldenia	Unriped pods	–	–	Asphondylia sp. nr. prosopidis	Diptera-Cecidomyiidae	Mc Kay & Gandolfo, 2007
Fabaceae	Prosopis chilensis	Unriped pods	–	–	Asphondylia sp. nr. prosopidis	Diptera-Cecidomyiidae	Mc Kay & Gandolfo, 2007
Fabaceae	Prosopis flexuosa	Unriped pods	–	–	Asphondylia sp. nr. prosopidis	Diptera-Cecidomyiidae	Mc Kay & Gandolfo, 2007
Fabaceae	Prosopis kuntzei	Unriped pods	–	–	Asphondylia sp. nr. prosopidis	Diptera-Cecidomyiidae	Mc Kay & Gandolfo, 2007
Fabaceae	Prosopis nigra	Unriped pods	–	–	Asphondylia sp. nr. prosopidis	Diptera-Cecidomyiidae	Mc Kay & Gandolfo, 2007
Lamiaceae	Hyptis sp.	Flower	Spherical	unknown	Asphondylia canastrae	Diptera-Cecidomyiidae	Gagné, 2004; Carneiro et al., 2009
Loranthaceae	Struthanthus sp.	Fruit	Globular	unknown	Asphondylia struthanthi	Diptera-Cecidomyiidae	Gagné, 1994, 2004; Carneiro et al., 2009
Loranthaceae	Psittacanthus robustus	Flower	Unknown	unknown	Schizomyia sp.	Diptera-Cecidomyiidae	Gagné, 1994; Carneiro et al., 2009
Malpghiaceae	Byrsonima sericea	Inflorescence	Ovoid	Brown	Bruggmanniella byrsonimae	Diptera-Cecidomyiidae	Maia, 2001; Gagné 1994, 2004; Carneiro et al., 2009
Malphigiaceae	Byrsonima sericea	Bud	Cylindrical	Green	Bruggmanniella byrsonimae	Diptera-Cecidomyiidae	Guimarães et al., 2014
Malpighiaceae	Heteropteris sp.	Flower	Swelling		Cantarinia sp.	Diptera-Cecidomyiidae	Gagné, 1994; Carneiro et al., 2009
Malpighiaceae	Heteropterys nitida	Flower	Elliptical	Yellow	Clinodiplosis floricola	Diptera-Cecidomyiidae	Maia, 2001; Carneiro et al., 2009
Malvaceae	Waltheria indica	Leaf/inflorescence	Spherical	yellow/brown	Anisodiplosis praecox	Diptera-Cecidomyiidae	Maia & Fernandes, 2005; Almeida et al., 2006; Carneiro et al., 2009
Melastomataceae	Conostegia xalapensis	Fruit	–	–	Allorhogas conostegia	Hymenoptera-Braconidae	Chavarria et al., 2009
Melastomataceae	Miconia calvescens	Fruit	–	–	Apion sp.	Coleoptera-Curculionidae	Badenes-Perez & Johnson, 2007
Melastomataceae	Miconia calvescens	Fruit	–	–	Allorhogas sp.	Hymenoptera-Braconidae	Badenes-Perez & Johnson, 2007
Moraceae	Chlorophora tinctoria	Flower	Swollen	unknown	Clinodiplosis chlorophorae	Diptera-Cecidomyiidae	Rübsaamen, 1905; Gagné, 1994; Carneiro et al., 2009
Moraceae	Ficus sp.	Flower	–	–	Agaonidae sp.	Hymenoptera-Aganoidae	Maia, 2012
Myrtaceae	Eugenia buxifolia	Fruit	Subglobular	Green	Dasineura eugeniae	Diptera-Cecidomyiidae	Gagné, 1994, 2004; Carneiro et al., 2009
Rubiaceae	Undetermined	Flower	Subovoid	Green	Asphondylia bahiensis	Diptera-Cecidomyiidae	Houard, 1933; Gagné 1994, 2004; Carneiro et al., 2009
Rubiaceae	Undetermined	Flower	Subovoid/elliptical	Green	Asphondylia parva	Diptera-Cecidomyiidae	Gagné 1994, 2004; Carneiro et al., 2009
Rubiaceae	Diodia gymnocephala	Flower	Elliptical	Green	Clinodiplosis diodiae	Diptera-Cecidomyiidae	Maia,2001; Gagné, 2004; Carneiro et al., 2009
Rubiaceae	Borreria sp.	Flower	Swollen	unknown	Asphondylia borreriae	Diptera-Cecidomyiidae	Gagné, 1994, 2004; Carneiro et al., 2009
Rubiaceae	Diodia sp.	Flower	Swollen	unknown	Asphondylia borreriae	Diptera-Cecidomyiidae	Gagné, 1994, 2004; Carneiro et al., 2009
Rubiaceae	Borreria verticillata	Inflorescence	Fusiform	Green	Asphondylia borreriae	Diptera-Cecidomyiidae	Maia et al., 1992; Carneiro et al., 2009
Solanaceae	Solanum sp.	Fruit	Spherical	Green	Asphondylia fructicolo	Diptera-Cecidomyiidae	Flor & Maia, 2017
Verbenaceae	Lantana sp.	Flower	Ovoid	Pink	Clinodiplosis pulchra	Diptera-Cecidomyiidae	Tavares, 1918; Houard, 1933; Gagné, 1994, 2004; Carneiro et al., 2009

 

References

Almeida, F. V. M., Santos, J. C., Silveira, F. A. O., & Fernandes, G. W. (2006). Distribution and frequency of galls induced by Anisodiplosis waltheriae Maia (Diptera: Cecidomyiidae) on the invasive plant Waltheria indica L. (Sterculiaceae). Neotropical Entomology, 35, 435–439.

Araújo, W. S., Sobral, F. L., & Maracahipes, L. (2014). Insect galls of the Parque Nacional das Emas (Mineiros, GO, Brazil). Check List, 10, 1445–1451.

Arias, A. A., Valverde, M. T., & Reyes, J. (2001). Las plantas de la región de Zapotitlán de Salinas, Puebla. Mexico D.F.: Instituto Nacional de Ecología.

Badenes-Perez, F. R., & Johnson, M. T. (2007). Ecology and impact of Allorhogas sp. (Hymenoptera: Braconidae) and Apion sp. (Coleoptera: Curculionoidea) on fruits of Miconia calvescens DC (Melastomataceae) in Brazil. Biological Control, 43, 317–322.

Bates, D., Maechler, M., Bolker, B., & Walker, S. (2015). Fitting linear mixed-effects models using lme4. Journal of Statistical Software, 67, 1–48.

Blanche, K. R. (2000). Diversity of insect-induced galls along a temperature -rainfall gradient in the tropical savannah region of the Northern Territory, Australia. Austral Ecology, 25, 311–318.

Blanche, K. R., & Ludwig, J. A. (2001). Species richness of gall-inducing insects and host plants along an altitudinal  gradient in Big Bend National Park, Texas. The American Midland Naturalist Journal, 145, 219–232.

Blanche, K. R., & Westoby, M. (1995). Gall-forming insect diversity is linked to soil fertility via host plant taxon. Ecology, 76, 2334–2337.

Carneiro, M. A. A., Branco, C. S. A., Braga, C. E. D., Almada, E. D., Costa, M. B. M., Maia, V. C. et al. (2009). Are gall midge species (Diptera, Cecidomyiidae) host plant-specialists? Revista Brasileira de Entomologia, 53, 365–378.

Chavarría, L., Hanson, P., Marsh, P., & Shaw, S. (2009). A phytophagous branconid, Allorhogas conostegia sp. nov. (Hymenoptera: Braconidae), in the fruits of Conostegia xalapensis (Bonpl.) D. Don (Melastomataceae). Journal of Natural History, 43, 2667–2689.

Coelho, M. S., Almada, E., Fernandes, G. W., Carneiro, M. A. A., Santos, R. M., Quintino, A. V. et al. (2009). Gall inducing arthropods from a seasonally dry tropical forest in Serra do Cipó, Brazil. Revista Brasileira de Entomologia, 53, 404–14.

Conagua (Comisión Nacional del Agua). (2010). Datos de precipitación y temperatura de estaciones meteorológicas. Sección Puebla, Puebla. Puebla: Conagua.

Cosgrove, D. J. (2000). Loosening of plant cell walls by expansins. Nature, 407, 321–326.

Crowe, M. L., & Bourchier, R. S. (2006). Interspecific interactions between the gall-fly Urophora affinis Frfld. (Diptera: Tephritidae) and the weevil Larinus minutus Gyll. (Coleoptera: Curculionidae), two biological control agents released against spotted knapweed, Centaurea stobe L. ssp. micranthos. Biocontrol Science and Technology, 16, 417–430.

Cuevas-Reyes, P., Quesada, M., Hanson, P., Dirzo, R., & Oyama, K. (2004). Diversity of gall-inducing insects in a Mexican tropical dry forest: the importance of plant species richness, life-forms host plant age and plant density. Journal of Ecology, 92, 707–716.

de Macêdo, M. V., & Monteiro, R. T. (1989). Seed predation by a braconid wasp, Allorhogas sp. (Hymenoptera). Journal of the New York Entomological Society, 97, 358–362.

Dennill, G. B. (1988). Why a gall former can be a good biocontrol agent: the gall wasp Trichilogaster acaciaelongifoliae and the weed Acacia longifolia. Ecological Entomology, 13, 1–9.

Dorchin, N., Cramer, M. D., & Hoffmann, J. H. (2006). Photosynthesis and sink activity of wasp-induced galls in Acacia pycnantha. Ecology, 87, 1781–1791.

dos Santos, I. R. M., de Oliveira, D. C., da Silva, C. R. G., & Kraus, J. E. (2014). Developmental anatomy of galls in the Neotropics: arthropods stimuli versus host plant constraints. In G. W. Fernandes, & C. J. Santos (Eds.), Neotropical insect galls (pp. 429–463). Dordrecht: Springer.

Duguma, D., Kring, T. J., & Wiedenmann, R. N. (2009). Seasonal dynamics of Urophora quadrifasciata on spotted knapweed in the Arkansas Ozarks. The Canadian Entomologist, 141, 70–79.

Elsayed, A. K., Karam, H. H., & Tokuda, M. (2017). A new Gephyraulus species (Diptera: Cecidomyiidae) inducing flower bud galls on the European sea rocket Cakile maritima Scop. (Brassicaceae). Applied Entomology and Zoology, 52, 553–558.

Espírito-Santo, M. M., & Fernandes, G. W. (2007). How many species of gall-inducing insects are there on earth, and where are they? Annals of the Entomological Society of America, 100, 95–99.

Evert, R. F. (2006). Esau’s plant anatomy. Meristems, cells, and tissues of the plant body: their structure, function, and development. New Jersey: John Wiley, & Sons.

Farquhar, G. D., & Sharkey, T. D. (1982). Stomatal conductance and photosynthesis. Annual Review of Plant Physiology, 33, 317–345.

Fay, P. A., Harnett, D. C., & Knapp, A. K. (1993). Increased photosynthesis and water potentials in Silphium integrifolium galled by cynipid wasps. Oecología, 93, 114–120.

Fay, P. A., Hartnett, D. C., & Knapp, A. K. (1996). Plant tolerance of gall insect attack and gall-insect performance. Ecology, 77, 521–534.

Fernandes, G. W. (1987). Gall forming insects: their economic importance and control. Revista Brasileira de Entomologia, 31, 379–398.

Fernandes, G. W., Araújo, R. C., Araújo, S. C., Lombardi, J. A., Paula, A. S., Loyola Jr., R. et al. (1997). Insect galls from savanna and rocky fields of the Jequitinhonha Valley, Minas Gerais, Brazil. Naturalia, 22, 221–244.

Fernandes, G. W., & Carneiro, M. A. A. (2009). Insetos galhadores. In A. R. Panizzi, & J. R. P. Parra (Eds.), Bioecologia e nutrição de insetos: base para o manejo integrado de pragas (pp. 597–639). Brasilia: Embrapa Informação Tecnológica.

Fernandes, G. W., Martins, R. P., & Neto, T. (1987). Food web relationships involving Anadiplosis sp. galls (Diptera: Cecidomyiidae) on Machaerium aculeatum (Leguminosae). Revista Brasileira de Botanica, 10, 117–123.

Fernandes, G. W., & Price, P. W. (1988). Biogeographical gradientes in galling species richness. Oecologia, 76, 161–167.

Fernandes, G. W., & Price, P. W. (1991). Comparison of tropical and temperate galling species richness: the roles of environmental harshness and plant nutrient status. In P. W. Price, T. M. Lewinsohn, G. W. Fernandes, & W. W. Benson (Eds.), Plant-animal interactions: evolutionary ecology in tropical and temperate regions (pp. 91–115). New Jersey: John Wiley, & Sons.

Fernandes, G. W., & Santos, J. C. (2014). Neotropical insect galls. New York: Springer.

Fernandes, G. W., Souza, A., & Sacchi, C. (1993). Impact of a Neolasioptera (Diptera: Cecidomyiidae) stem galler on its host plant, Mirabilis linearis (Nyctaginaceae). Phytophaga, 5, 1–6.

Fernández, V., Khayet, M., Montero-Prado, P., Heredia-Guerrero, J. A., Liakopoulos, G., Karabourniotis, G. et al. (2011). New insights into the properties of pubescent surfaces: peach fruit as a model. Plant Physiology, 156, 2098–2108.

Florentine, S. K., Raman, A., & Dhileepan, K. (2005). Effects of gall induction by Epiblema strenuana on gas exchange, nutrients, and energetics in Parthenium hysterophorus. BioControl, 50, 787–801.

Flores, J., & Briones, O. (2001). Plant life-form and germination in a Mexican inter-tropical desert: effects of soil water potential and temperature. Journal of Arid Environments, 47, 485–497.

Gagné, R. J. (1977). The Cecidomyiidae (Diptera) associated with Chromolaena odorata (L.) K. and R. (Compositae) in the Neotropical Region. Brenesia, 12/13, 113–131.

Gagné, R. J. (1994). The gall midges of the Neotropical Region. New York: Cornell University Press.

Gagné, R. J. (2004). A catalog of the Cecidomyiidae (Diptera) of the world. Memoirs of the Entomological Society of Washington, 25, 1–408.

Gagné, R. J., Ley-López, J. M., & Hanson, P. E. (2018). First New World record of a gall midge from palms: a new species of Contarinia (Diptera: Cecidomyiidae) from Geonoma cuneata in Costa Rica. Proceedings of the Entomological Society of Washington, 120, 51–61.

Gonçalves-Alvim, S. J., & Fernandes, G. W. (2001). Comunidades de insetos galhadores (Insecta) em diferentes fisionomias do cerrado em Minas Gerais, Brasil. Revista Brasileira de Zoologia, 18, 289–305.

Guimarães, A. L. A., Cruz, S. M. S., & Vieira, A. C. M. (2014). Structure of floral galls of Byrsonima sericea (Malpighiaceae) induced by Bruggmanniella byrsonimae (Cecidomyiidae, Diptera) and their effects on host plants. Plant Biology, 16, 467–475.

Haiden, S., Hoffmann, J., & Cramer, M. (2012). Benefits of photosynthesis for insects in galls. Oecologia, 170, 987–997.

Harris, P., & Shorthouse, J. D. (1996). Effectiveness of gall inducers in weed biological control. The Canadian Entomologist, 128, 1021–1055.

Hiyama, T., Kochi, K., Kobayashi, N., & S. Sirisampan. (2005). Seasonal variation in stomatal conductance and physiological factors observed in a secondary warm-temperate forest. Ecological Restoration, 20, 333–346.

Hothorn, T., Bretz, F., & Westfall, P. (2008). Simultaneous inference in general parametric models. Biometrical Journal, 50, 346–363.

Houard, C. (1933). Les Zoocécidies des Plantes de l ́Amérique du Sud e de l ́Amérique Central. Paris: Hermann et Cie. 519.

Isaias, R. M. S., Carneiro, R. G. S., Santos, J. C., & Oliveira, D. C. (2014). Gall morphotypes in the Neotropics and the need to standardize them. In G. W. Fernandes, & C. J. Santos (Eds.), Neotropical insect galls (pp. 51–67). Dordrecht: Springer.

Janzen, D. H. (1982). Variation in average seed size and fruit seediness in a fruit crop of a Guanacaste tree (Leguminosae: Enterolobium cyclocarpum). American Journal of Botany, 69, 1169–1178.

Kolesik, P., Adair, R. J., & Eick, G. (2010). Six new species of Asphondylia (Diptera: Cecidomyiidae) damaging flower buds and fruit of Australian Acacia (Mimosaceae). Systematic Entomology, 35, 250–267.

Kurzfeld-Zexer, L., Wool, D., & Inbar, M. (2010). Modification of tree architecture by a gall-forming aphid. Trees-Structure and Function, 24, 13–18.

Larson, K. C. (1998). The impact of two gall-forming arthropods on the photosynthetic rates of their hosts. Oecologia, 115, 161–166.

Lemos-Filho, J. P., & Isaias, R. M. S. (2004). Comparative stomatal conductance and chlorophyll a fluorescence in leaves vs. fruits of the Cerrado legume tree, Dalbergia miscolobium. Brazilian Journal of Plant Physiology, 16, 89–93.

López-Galindo, F., Munóz-Iniestra, D., Hernández-Moreno, M., Soler-Aburto, A., Castillo-López, M. C., & Hernández-Arzate, I. (2003). Análisis integral de la toposecuencia y su influencia en la distribución de la vegetación y la degradación del suelo en la subcuenca de Zapotitlán Salinas, Puebla. Boletín de la Sociedad Geológica Mexicana, 56, 19–41.

Maia, V. C. (2001). The gall midges (Diptera, Cecidomyiidae) from three restingas of Rio de Janeiro State, Brazil. Revista Brasileira de Zoologia, 8, 583–630.

Maia, V. C. (2012). Richness of hymenopterous galls from South America. Papéis Avulsos de Zoologia (São Paulo), 52, 423–429.

Maia, V. C., Couri, M. S., & Monteiro, R. F. (1992). Sobre seis espécies de Asphondylia Loew, 1850 do Brasil (Diptera, Cecidomyiidae). Revista Brasileira de Entomologia, 36, 653–661.

Maia, V. C., & Fernandes, G. W. (2005). Two new species of Asphondylinii (Diptera: Cecidomyiidae) associated with Bahuinia brevipes (Fabaceae) in Brazil. Zootaxa, 1091, 27–40.

Maia, V. C., Silveira, F. A. O., Oliveira, L. A., & Xavier, M. F. (2008). Asphondylia gochnatiae, a new species of gall midge (Diptera: Cecidomyiidae) associated with Gochnatia polymorpha (Less.) Cabrera (Asteraceae). Zootaxa, 1740, 53–58.

Mani, M. S. (1964). Ecology of plant galls. Dordrecht: Springer Science.

Matthews, M. A., & Shackel, K. A. (2005). Growth and water transport in fleshy fruit. En N. M. Holbrook, & M. A. Zwieniecki (Eds.), Vascular transport in plants (pp. 181–197). Burlington, California: Academic Press.

McCrea, K. D., Abrahamson, W. G., & Weis, A. E. (1985). Goldenrod ball gall effect on Solidago altissima: 14C translocation and growth. Ecology, 66, 1902–1907.

Mc Kay, F., & Gandolfo, D. (2007). Phytophagous insects associated with the reproductive structures of mesquite (Prosopis spp.) in Argentina and their potential as biocontrol agents in South Africa. African Entomology, 15, 121–131.

Medianero, E., Valderrama, A., & Barrios, H. (2003). Diversidad de insectos minadores de hojas y formadores de agallas en el dosel y sotobosque del bosque tropical. Acta Zoológica Mexicana, 89, 153–168.

Möhn, E. (1959). Gallmücken (Diptera, Cecidomyiidae) aus El Salvador. 1. Teil. Senckenbergiana Biologica, 40, 297–368.

Möhn, E. (1960). Gallmücken (Diptera, Cecidomyiidae) aus El Salvador. 2. Teil. Senckenbergiana Biologica, 41, 197–240.

Möhn, E. (1961). Neue Asphondyliidi-Gattungen (Diptera, Itonididae). Stuttgarter Beiträge zur Naturkunde, 49, 1–14.

Montaña, C., & Valiente-Banuet, A. (1998). Floristic life-form diversity along an altitudinal gradient in an intertropical semiarid Mexican region. Southwest Naturalist, 43, 24–39.

Morales-Silva, T., & Modesto-Zampieron, S. L. (2018). Occurrence of Allorhogas sp. (Hymenoptera: Braconidae: Doryctinae) associated with galls on seeds of Inga vera (Fabaceae) in Brazil. Brazilian Journal of Biology, 78, 178–179.

Oliveira, D. C., Isaias, R. M. S., Fernandes, G. W., Ferreira, B. G., Carneiro, R. G. S., & Fuzaro, L. (2016). Manipulation of host plant cells and tissues by gall-inducing insects and adaptive strategies used by different feeding guilds. Journal of Insect Physiology, 84, 103–113.

Oliveira, D. C., Moreira A. S. F. P., & Isaias, R. M. S. (2014). Functional gradients in insect gall tissues: studies on Neotropical host plants. En G. W. Fernandes, & C. J. Santos (Eds.), Neotropical insect galls (pp. 51–67). Dordrecht: Springer.

Oyama, K., Pérez-Pérez, M., Cuevas-Reyes, P., & R. Luna-Reyes. (2003). Regional and local species richness of gall-forming insects in two tropical rain forest in México. Journal of Tropical Ecology, 19, 595–598.

Pallardy, S. G. (2008). Physiology of woody plants. Burlington, California: Academic Press.

Patankar, R., Thomas, S. C., & Smith, S. M. (2011). A gall-inducing arthropod drives declines in canopy tree photosynthesis. Oecologia, 167, 701–709.

Pavón, N. P., & Briones, O. (2001). Phenological patterns of nine perennial plants in an intertropical semi-arid Mexican scrub. Journal of Arid Environments, 49, 265–277.

Pennington, T. D., & Sarukhán, J. (2005). Árboles tropicales de México: manual para la identificación de las principales especies. México D.F.: Fondo de Cultura Económica.

Pezzini, F., Ranieri, B. D., Brandao, D. O., Fernandes, G. W., Quesada, M., Espirito-Santo, M. M. et al. (2014). Changes in tree phenology along natural regeneration in a seasonally dry tropical forest. Plant Biosystematics, 148, 1–10.

Pietragalla, J., & Pask, A. (2012). Stomatal conductance. En A. Pask, J. Pietragalla, D. Mullan, & M. Reynolds (Eds.), Physiological breeding II: a field guide to wheat phenotyping (pp. 15–17). México D.F.: CIMMYT.

Price, P. W., Fernandes, G. W., Lara, A. C. F., Brawn, J., Barrios, H., Wright, M. G. et al. (1998). Global patterns in local number of insect galling species. Journal of Biogeography, 25, 581–91.

Price, P. W., Fernandes, G. W., & Waring, G. L. (1987). Adaptive Nature of insect galls. Environmental Entomology, 16, 15–24.

Quintero, C., Garibaldi, L. A., Grez, A., Polidori, C., & Nieves-Aldrey, J. L. (2014). Galls on the temperate forest of southern South America: Argentina and Chile. En G. W. Fernandes, & C. J. Santos (Eds.), Neotropical insect galls (pp. 429–463). Dordrecht: Springer.

R Development Core Team. (2017). R: a language and environment for statistical computing, version 3.3.0. Vienna, Austria. Retrieved on March 11th., 2017, from: https://www.r-project.org/

Raman, A. (2007). Insect-induced plant galls of India: unresolved questions. Current Science, 92, 748–757.

Rasband, W. S. (2017). ImageJ. National Institutes of Health, USA. Retrieved on March 11th., 2017, from: http://imagej.nih.gov/ij/

Rübsaamen, E. H. (1905). Beiträge zur Kenntnis aussereuropäischer Zoocecidien. II. Beitrag: Gallen aus Brasilien und Peru. Marcellia, 4, 65–85.

Rzedowski, J. (2006). Vegetación de México. México D.F.: Comisión Nacional para el Conocimiento y Uso de la Biodiversidad.

Santos, J. C., De Araujo, N. A. V., Venancio, H., Andrade, J. F., Alves-Silva, E., Almeida, W. R. et al. (2016). How detrimental are seed galls to their hosts? Plant performance, germination, developmental instability and tolerance to herbivory in Inga laurina, a leguminous tree. Plant Biology, 18, 962–972.

Silva, I. M., Andrade, G. I., Fernandes, G. W., & Lemos-Filho, J. P. (1996). Parasitic relationships between a gall-forming insect Tomoplagia rudolphi (Diptera: Tephritidae) and its host plant (Vernonia polyanthes, Asteraceae). Annals of Botany, 78, 45–48.

Stone, G. N., & Schönrogge, K. (2003). The adaptive significance of insect gall morphology. Trends in Ecology and Evolution, 18, 512–522.

Tavares, J. S. (1917). Cecidias brazileiras que se criam em plantas das Compositae Rubiaceae, Tiliaceae, Lythraceae e Artocarpaceae. Broteria: Série Zoológica, 15, 113–181.

Tavares, J. S. (1918). Cecidologia brazileira. Cecidias que se criam em plantas das famílias das Verbenaceae, Euphorbiaceae, Malvaceae, Anacardiaceae, Labiatae, Rosaceae, Anonaceae, Ampelidaceae, Bignoniaceae, Aristolochiaceae e Solanaceae. Brotéria: Série Zoológica, 16, 21–68.

Tooker, J. F., & Helms, A. M. (2014). Phytohormone dynamics associated with gall insects, and their potential role in the evolution of the gall-inducing habitat. Journal of Chemical Ecology, 40, 742–753.

Villaseñor, J. L. (2016). Checklist of the native vascular plants of Mexico. Revista Mexicana de Biodiversidad, 87, 559–902.

Woodman, R. L., & Fernandes, G. W. (1991). Differential mechanical defense: herbivory, evapotranspiration, and leaf-hairs. Oikos, 60, 11–19.

Woods, D. M., Pitcairn, M. J. Joley, D. B., & Turner, C. E. (2008). Seasonal phenology and impact of Urophora sirunaseva on yellow starthistle seed production in California. Biological Control, 47, 172–179.

Xiong, L., & Zhu, J. K. (2003). Regulation of abscisic acid biosynthesis. Plant Physiology, 133, 29–36.

Zavala, A. (1982). Estudios ecológicos en el Valle semiárido de Zapotitlán, Puebla I. Clasificación numérica de la vegetación basada en atributos binarios de presencia o ausencia de las especies. Biotica, 7, 99–120.

Zuur, A., Leno, E. N., Walker, N., Saveliev, A. A., & Smith, G. M. (2009). Mixed effects models and extensions in ecology with R. New York: Springer-Verlag.