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Revista mexicana de ciencias forestales
Print version ISSN 2007-1132
Rev. mex. de cienc. forestales vol.10 n.54 México Jul./Aug. 2019
https://doi.org/10.29298/rmcf.v10i54.502
Articles
Oak gall wasps of Cerro Gordo State Park in the State of Mexico
1Departamento de Preparatoria Agrícola. Universidad Autónoma Chapingo. México.
2Departament de Biologia Evolutiva, Ecologia i Ciències Ambientals, Facultat de Biologia. Universitat de Barcelona. España.
Cerro Gordo State Park is a reserve constituted by ejidos and communal and private areas within the Valley of Mexico. The native vegetation is represented by several unidentified oak species, which are infested with galls, and the identity of causative agent of the disease is unknown. Therefore, the objective of this work was to identify the oak species, as well as the insects associated with the galls. Three sites were selected and marked, oak specimens and galls were collected on a monthly basis from February to July 2017. The plant specimens were dried, identified and integrated into the herbarium collection of the Forest Division of the Universidad Autónoma Chapingo. The galls were placed in emergency chambers under controlled conditions, and the insects were fixed in ethanol for taxonomic identification. The oak species identified were Quercus laurina (register number 69 367), Q. crassipes (69 368), Q. rugosa (69 369) and Q. microphylla (69 370). Andricus carrilloi was found in the galls on the branches of Quercus microphylla, Synergus mexicanus as its inquiline, as well as another species of Synergus that is in the process of being described. Amphibolips hidalgoensis was found in galls collected from Quercus crassipes. These are the first records of both these gall wasps and their oak hosts in the Valley of Mexico.
Key words: Amphibolips hidalgoensis Pujade-Villar y Melika 2011; Andricus carrilloi Pujade-Villar 2013; Cynipidae; Quercus spp.; Synergus mexicanus Gillette 1896
El Parque estatal Cerro Gordo es una reserva constituida por áreas ejidales, comunales y privadas dentro del Valle de México. La vegetación nativa del parque está conformada por diversos taxa de encinos no identificados, y por lo menos dos de ellos están infestados con agallas, sobre todo en brotes y ramas; aunque, se desconoce la identidad del o de sus agentes causales. Por lo tanto, el objetivo de este trabajo consistió en identificar las especies de encinos, así como los insectos asociados a las agallas. Se eligieron y marcaron tres sitios dentro del parque, se colectaron ejemplares botánicos y mensualmente se recolectaron agallas en el periodo de febrero a julio del 2017. Las muestras vegetales se secaron, identificaron e integraron a la colección del herbario de la División de Ciencias Forestales de la Universidad Autónoma Chapingo. Las agallas se colocaron en cámaras de emergencia bajo condiciones controladas; los insectos se fijaron en etanol para su determinación taxonómica. Los encinos correspondieron a: Quercus laurina (número de registro 69 367), Q. crassipes (69 368), Q. rugosa (69 369) y Q. microphylla (69 370). En las agallas de las ramas de Q. microphylla, se registró la presencia de Andricus carrilloi, la de Synergus mexicanus como su inquilino y la de Synergus sp. en Q. crassipes se observó a Amphibolips hidalgoensis. Estos son los primeros registros tanto de los insectos formadores de agallas en la región del Valle de México, como de sus especies hospederas.
Palabras clave: Amphibolips hidalgoensis Pujade-Villar y Melika 2011; Andricus carrilloi Pujade-Villar 2013; Cynipidae; parasitoide; Quercus spp.; Synergus mexicanus Gillette 1896
Introduction
The Cerro Gordo State Park, which has a surface area of approximately 3 027 ha, was decreed as a natural reserve in May, 1977 (SEANPEM, 2016; CEPANAF, 2016). It encompasses three municipalities of the State of Mexico: Axapusco, San Martín de las Pirámides and Temascalapa. It is constituted by ejidos, communal and private lands, and it is the highest elevation in the Valley of Teotihuacán (3 000 masl) (SEANPEM, 2016; CEPANAF, 2016).
The highest part of the mountain has a temperate climate with dry winters and rainy summers (Cw0b(e)g); in its lower areas, the climate is dry with summer rains (BS1K´w(w)(i´)g). The mean annual temperature ranges between 12 and 18 °C, and the mean annual precipitation, approximately between 600 and 700 mm (CEPANAF, 2016).
The native vegetation in the best preserved area in the park consists of oak forests, oak shrubs and grasslands (CEPANAF, 2016), some of which are infested with abundant galls on their shoots and branches.
Oaks are susceptible to being parasitized by various wasps of the Cynipini tribe (Cynipidae), whose larvae cause the development of galls on any organ of the host tree, always in a specific form (Pujade-Villar et al., 2009). More than 180 species of Cynipidae are cited today for Mexico, parasitizing approximately 30 Quercus taxa (Pujade-Villar et al., 2009; Pujade-Villar and Ferrer-Suay, 2015a). Despite the fact that these insects have been detected in different locations across the country, their study is scarce. On the other hand, the identification of the gall wasps without accurate knowledge of their vegetal hosts or of adult Cynipidae can cause determination errors (Pujade-Villar et al., 2009).
Furthermore, inquiline species may be found in galls induced by Cynipidae (Ronquist et al., 2015). In general, these inquilines have lost the ability to induce galls, but they may modify their feeding site; also, in some cases, they have influence on the size and shape of the galls (Pujade-Villar et al., 2016c).
Because oaks are structurally the most relevant elements of the native vegetation of the Cerro Gordo State Park, it is important to keep them in good health. For this reason, and due to lack of information, the Quercus species were determined, as were the insects associated to the galls and their distribution across the park.
Materials and Methods
Three collection sites were located in the southwest of the Cerro Gordo State Park (Figure 1), in the State of Mexico: site 1 (3 030 masl, 19°45´13.3” N, 098°49´38.4” W); site 2 (2 996 masl, 19°45´07.8” N, 098°49´42.5” W), and site 3 (2 985 masl, 19°45´00.1” N, 098°49´26.5” W).
Oak specimens with the presence of galls, mature leaves in good conditions, and fruits were collected; they were processed for subsequent identification with the aid of taxonomical keys (Zavala, 1995; Romero et al., 2002), and they were compared with the materials kept in the Herbarium of the Forest Division (CHAP) of the Universidad Autónoma Chapingo, where they were finally deposited.
50 × 50 m plots were established at the sites for the sampling of trees, and within them, 10 × 10 m subplots for the sampling of shrubs. In each plot, oaks with a normal diameter above 20 cm (aged 20 to 40 years) were selected and marked, as were shrubs with a height of over 70 cm. 40 galls on shoots and 20 on shrub branches were gathered in five monthly collections during the period of February to July, 2017.
The galls of the shoots and branches were separated and stored in different emergency chambers under controlled conditions (15-22 °C, 12:12 photoperiods). They were checked every other day during two months, and the adult insects obtained were placed in flasks with ethanol at 75 % for transportation to the Universidad de Barcelona, in Spain, where a photographic record of them was made (using a LEICA optic microscope) and they were identified with taxonomical keys (Melika et al., 2011; Pujade-Villar et al., 2013).
Results and Discussion
The oaks belonged to four species: Quercus laurina Bonpl. (herbarium registration number CHAP, 69 367), a somewhat scarce taxon in the area, without representatives at the sampling sites and without galls; Q. rugosa Née (herbarium registration number CHAP, 69 369), with 278 individuals ha-1, and Q. crassipes Humb. & Bonpl (herbarium registration number CHAP, 69 368), with 278 individuals ha-1; Q. microphylla Née (herbarium registration number CHAP, 69 370) is the dominant plant at the open sites located at an altitude interval of 2 700 to 3 000 m; this species forms 1 m tall oak shrubs, with a density of 878 individuals ha-1 at the sampling sites. Q. rugosa and Q. crassipes are distributed in the areas with the highest altitude; they form oak groves with a canopy height between 7 and 8 m. The only species exhibiting galls on the branches were Q. crassipes, where they occurred on the shoots, and Q. microphylla.
Galls of Quercus microphylla
These shrubs exhibited globe shaped, fully lignified galls that partially surrounded the smaller branches (Figure 2a and 2b); 15 to 27 galls were found in each specimen. Three cynipid species emerged during the period of May to July, 2017: Andricus carrilloiPujade-Villar 2013, Synergus mexicanus Gillette 1896 and Syrnergus sp., besides other individuals of the family Eulophidae.
Figure 2 Galls on Quercus microphylla Née and emerged wasps. 1 a and b) Globe-shaped galls. 1 c and d) Andricus carrilloiPujade-Villar 2013 adults associated with the galls.
The main taxon was Andricus carrilloi (Figure 2c and 2d), a gall wasp first detected in Mexico City in 2013, on Q. laeta Liebm. (Pujade-Villar et al., 2013); its galls are similar to those observed in the present study. This insect is characterized for having antennae with 13 flagelomers, a horny scutellum, line of the mesoscutellum, curved propodeal carinae, hyaline wings, and a relatively short radial cell; brown to black antennae and legs, dark (reddish to chestnut brown) body, and reddish to brown metasoma (Pujade-Villar et al., 2013). The genus Andricus is the most numerous in the Cynipidae family, and it produces tuberous galls on oaks; 43 species are cited in Mexico (Pujade-Villar et. al. (2016a and 2016b).
Adults of the genus Synergus have inquiline habits and are associated with the galls of Fagaceae (Ronquist et al., 2015).
A total of 200 taxa of inquiline Cynipidae, belonging to 10 genera and classified into three tribes (Synergini, Ceroptresini and Diastrophini) are known at world level (Ronquist et al., 2015). 87 species have been detected in the Nearctic region, and 15, in the Neotropical region (Pénzes et al., 2012). Ceroptres, Synophromorpha and Synergus have been registered in Mexico (Pujade-Villar et al., 2008).
Of the 125 Synergus taxa in the world (Pénzes et al., 2012; Schweger et al., 2015; Lobato-Vila et al., 2017), 10 have been identified in Mexico: S. cibriani Pujade-Villar & Lobato-Vila 2017; S. citriformis Ashmead 1922; S. equihuai Pujade-Villar & Lobato-Vila 2016; S. estradae Pujade-Villar & Lobato-Vila 2016; S. filicornis Cameron 1883; S. gilletti Pujade-Villar & Lobato-Vila 2017; S. longimalaris Pujade-Villar & Lobato-Vila 2017; S. longiscapus Pujade-Villar & Lobato-Vila 2016; S. mexicanus Gillette and S. striatifrons Pujade-Villar & Lobato-Vila 2017 (Ritchie and Shorthouse, 1987; Pujade-Villar and Melika, 2005; Lobato-Vila and Pujade-Villar, 2017). The present study documents the first detection in Q. microphylla.
Synergus mexicanus (Figure 3) exhibits an open radial cell, whereby it differs from most representatives of the genus and is the only one with this characteristic in Mexico (Figure 3a). Females have 12 flagelomers and frontal lateral carinae that may be complete or incomplete but are always present (Pujade-Villar et al., 2015). Q. rugosa tumor-like galls produced by individuals of Andricus spp. were collected in 2015 (Pujade-Villar et al., 2015).
Figure 3 Adult specimens of Synergus mexicanus Gillette 1896; a) habitus of the female and detail of the radial cell; b) habitus of the male.
Other detected inquiline species were adults of the Eulophidae family, Tetrastichinae subfamily (Figure 4). The Eulophidae (Chalcidoidea) family is one of the most common groups of parasitoids in cynipid galls, and 59 oak species have been detected in Europe (Csóka et al., 1998). The taxonomy of this group is little studied, and therefore the identification of its genera is complex due to its enormous diversity and your morphological uniformity (Gómez et al., 2006).
Figure 4 a) Male and b) female specimens of Eulophidae: Tetrastichinae collected from galls on Quercus microphylla Née.
36 taxa belonging to genera associated with Cynipidae galls have been identified in the Palearctic region (Serrano-Muñoz et al., 2015; 2016); the Eulophidae species developed in oak galls are unknown in Mexico.
Galls on Quercus crassipes
They were located on the buds; their shape was round (Figure 5a), and their size ranged between 7.3 and 8.2 cm; their color was green at the beginning of the collections, and later turned red; its consistency was soft and, when a longitudinal cut was practiced on them, only one larval chamber was observed. In January and February, only 25 to 45 mummified galls were found in each tree individual; however, form March on, their number increased to above 80. Only in the material collected that month, the larval chamber had more than one larva of the inquiline or parasitic species; yet, no adult insects were present. Adult Amphibolips hidalgoensis Pujade-Villar & Melika 2011, cynipids emerged from galls collected from April onward, which were red and larger (Figure 5b); this happened at the end of February and in July (Figure 5c and d).
Figure 5 a) Quercus crassipes Humb. & Bonpl. tree with galls, b) Galls found and collected in May, and c and d) Amphibolips hidalgoensis Pujade-Villar & Melika 2011 adults associated to the galls.
Amphibolips hidalgoensis was first detected in the state of Hidalgo, in Q. candicans, Q. crassifolia and Q. candicans galls (Melika et al., 2011). Its presence in Q. crassipes signifies a new register of a host species. This species has a posterior edge of the mesoscutellum, and a dark line along the anterior edge of the wings, which is interrupted by a light-colored band that crosses the cell delimited by R1+Sc and Rs+M. Its head is black, except for the maxillary and labial palps, which are of a light brown hue. Its antennae, mesosoma, and legs are black, although tarsomers 2-5 are dark brown (Melika et al., 2011).
The wasps of the Amphibolips genus of the Nearctic and Neotropical regions produce galls on the oak trees of the Lobatae section. So far, 50 species have been described, of which 19 are exclusive of Mexico (Pujade-Villar and Ferrer-Suay, 2015b).
Two morphological groups stand out within the genus (Nieves-Aldrey et al., 2012): niger, which consists of adults that have antennae with 14-15 flagelomers and extremely pubescent galls, with an extremely hard central gall, and nassa, characterized by the presence of 11-12 antenomers and galls that are neither pubescent nor hard. Female Amphibolips adults obtained in this research belong to the nassa group. Both groups have a robust body, with a dark, horny head and mesosoma (Melika et al., 2011). Both the sexual and the asexual generation of the Amphibolips species induce galls on the leaves, buds or shoots of red oaks. The nassa group produces galls resembling a spongy globe- or pear-shaped gall with a single larval chamber located at the center of its spongy parenchyma, or attached with radiate filaments (Melika and Abrahamson, 2002; Nieves-Aldrey et al., 2012).
The health of the oak trees of the Cerro Gordo Park is a relevant topic that should be addressed in future papers. According to the known literature, tumor-like galls produced by A. carrilloi on branches cause apparent aesthetic damage. However, Andricus quercuslaurinusMelika and Pujade-Villar 2009 is known to severely affect Quercus laurina Humb and Bonpl. and Q. affinis Scheidw, in Hidalgo (Melika et al., 2009; Pujade-Villar, 2013). Besides, other harmful taxa of this genus have been described in Mexico on Q. laeta (Pujade-Villar et al., 2014). The damage caused to the buds by A. hidalgoensis is well known (Melika et al., 2011). At the state park, galls were observed on all the specimens of Q. crassipes.
Conclusions
The oak species Quercus laurina, Q. crassipes, Q. rugosa and Q. microphylla are found at the Cerro Gordo State park. Q. crassipes and Q. microphylla are new registers of hosts of the endoparasitic wasps A. hidalgoensis and A. carrilloi, respectively. Both these species are the first gall cynipids detected at this park. Associated to these insects, parasitoids of the subfamily Tetrastichinae (Eulophidae) and inquilines of the genus Synergus were identified. The development of globe-shaped galls of A. hidalgoensis harms the buds of Q. crassipes, whereas, according to the literature, the tuberous galls produced by A. carrilloi seem to cause its host, Q. microphylla, only aesthetic damage.
Acknowledgments
The authors wish to express their gratitude to Departamento de Preparatoria Agrícola of the Universidad Autónoma Chapingo for the support with transportation; to the municipal representatives and ejidatarios of San Martín de las Pirámides for their help during the field trips.
REFERENCES
Comisión Estatal de Parques Naturales y de la Fauna (CEPANF). 2016. Fichas técnicas de las áreas naturales protegidas. Parque estatal denominado Cerro gordo. https://cepanaf.edomex.gob.mx/sites/cepanaf.edomex.gob.mx/files/files/Fichas%20Tecnicas/5_%20PARQUE%20ESTATAL%20DENOMINADO%20CERRO%20GORDO.pdf (19 de febrero de 2019). [ Links ]
Csóka, G., W. Mattson J., N. Stone G. and W. Price P. 1998. The biology of gall-inducing arthropods. Gen. Tech. Rep. NC-199. Department of Agriculture, Forest Service, North Central Research Station. St. Paul, MN USA. 329 p. [ Links ]
Gómez J., F., N. Hernández M., T. A. Garrido M., R. Askew R. and J. Nieves-Aldrey L. 2006. Los Chalcidoidea (Hymenoptera) asociados con agallas de cinípidos (Hymenoptera, Cynipidae) en la comunidad de Madrid. Graellsia 62:293-331. doi: 10.3989/graellsia.2006.v62.iExtra.122. [ Links ]
Lobato-Vila, I. and J. Pujade-Villar. 2017. Description of five new species of inquiline oak gall wasps of the genus Synergus Hartig (Hymenoptera, Cynipidae: Synergini) with partially smooth mesopleurae from Mexico. Zoological Studies 56(36): 1-28. doi:10.6620/ZS.2017.56-36. [ Links ]
Lobato-Vila, I. , S. Fernández-Garzón, R. Rojas C., M. González A. and J. Pujade-Villar. 2017. Synergus pedroi n. sp. from Colombia (Hymenoptera: Cynipdae: Synergini). Folia Entomológica Mexicana 3(3):106-113. [ Links ]
Melika, G. and W. Abrahamson G. 2002. Review of the World Genera of Oak Cynipid Wasps (Hymenoptera: Cynipidae: Cynipini). In: Melika, G. and Cs Thuróczy (eds.). Parasitic Wasps: Evolution, Systematics, Biodiversity and Biological Control. Agroinform, Budapest, Hungary. pp. 150-190. [ Links ]
Melika, G. , D. Cibrián-Tovar, V. Cibrián-Llanderal D., J. Tormos and J. Pujade-Villar. 2009. New species of oak gallwasp from Mexico (Hymenoptera: Cynipidae: Cynipini) - a serious pest of Quercus laurina (Fagaceae). Dugesiana 16(2): 67-73. [ Links ]
Melika, G. , A. Equihua-Martínez, E. Estrada-Venegas G., D. Cibrián-Tovar, V. Cibrián-Llanderal D. and J. Pujade-Villar. 2011. New Amphibolips gallwasp species from Mexico (Hymenoptera: Cynipidae). Zootaxa 3105: 47-59. [ Links ]
Nieves-Aldrey, J., L. Pascual, E. Maldonado-Lopez, Y. Medianero E. and K. Oyama. 2012. Revision of the Amphibolips species of Mexico excluding the “niger complex” Kinsey (Hymenoptera: Cynipidae), with description of seven new species. Zootaxa 3545: 1-40. [ Links ]
Pénzes, Z., T. Chang-Ti, P. Bihari, M. Bozsó, S. Schwéger and G. Melika, 2012. Oak associated inquilines (Hymenoptera, Cynipidae, Synergini). Tiscia Monograph. Series 11. Deparment of Ecology, University of Szeged. Szeged, Hungary. 76 p. [ Links ]
Pujade-Villar, J. and G. Melika. 2005. Synergus castanopsidis (Beutenmüller, 1918) and Synergus mexicanus Gillette, 1896, two conflictive cynipid inquilines species from America (Hymenoptera, Cynipidae: Synergini). Boletín de la Sociedad Entomológica Aragonesa 37: 215-218. [ Links ]
Pujade-Villar, J., A. Equihua-Martínez , E. G. Estrada-Venegas y P. Ros-Farré. 2008. Los Cinípidos mexicanos no asociados a encinos (Hymenoptera: Cynipidae), perspectivas de estudio. Orsis 23: 87-96. [ Links ]
Pujade-Villar, J. , A. Equihua-Martínez , E. G. Estrada-Venegas y C. Changoyán-Garcia. 2009. Estado del Conocimiento de los Cynipini (Hymenoptera: Cynipidae) en México: Perspectivas de Estudio. Neotropical Entomology 38(6): 809-821. [ Links ]
Pujade-Villar, J. 2013. Las agallas de los encinos: un ecosistema en miniatura que hace posible estudios multidisciplinares. Entomología mexicana 12(1): 1-20. [ Links ]
Pujade-Villar, J. , A. G. Pérez-García, A. Equihua-Martínez , E. G. Estrada-Venegas, D. Cibrián-Tovar, U.M. Barrera-Ruíz and M. Ferrer-Suay. 2013. Review of Andricus species (Hymenoptera, Cynipidae) producing woody tuberous oak galls in México and bordering areas of United States of America. Dugesiana, 20(2): 183-208. [ Links ]
Pujade-Villar, J. , Y. Wang, X. Chen and J. He. 2014. Taxonomic review of East Palearctic species of Synergus section I, with description of a new species from China (Hymenoptera: Cynipidae: Cynipinae). Zoological Systematics 39(4): 534-544. [ Links ]
Pujade-Villar, J. , M. Serrano-Muñoz,G. A. Villecas-Guzmán y M. Roca-Cusachs. 2015. Synergus mexicanus Gillette, 1896: una especie que incrementa el conflicto genérico (Hym., Cynipidae: Synergini). Butlletí de la Institució Catalana d’Història Natural 79: 145-148. [ Links ]
Pujade-Villar, J. and M. Ferrer-Suay. 2015a. Andricus protuberans n. sp. (Hymenoptera: Cynipidae: Cynipini), a new species of oak gallwasp from Mexico. Dugesiana 22(2): 115-120. DOI: http://dx.doi.org/10.32870/dugesiana.v22i2.4717. [ Links ]
Pujade-Villar, J. and M. Ferrer-Suay. 2015b. Adjudicació genèrica d’espècies mexicanes d’ubicació dubtosa descrites per Kinsey i comentaris sobre la fauna mexicana (Hymenoptera: Cynipidae: Cynipini). Butlletí de la Institució Catalana d’Història Natural 79: 7-14. [ Links ]
Pujade-Villar, J. , J. A. Acuña-Soto, E. Ruíz-Cancino and J. M. Coronado-Blanco. 2016a. Andricus tamaulipensis Pujade-Villar nom. nov. para Disholcaspis mexicana (Beutenmüller, 1911) (Hymenoptera: Cynipidae). Butlletí de la Institució Catalana d’Història Natural 80: 127-130. [ Links ]
Pujade-Villar, J. , A. Equihua-Martínez , E. G. Estrada-Venegas, D. Cibrián-Tovar and U.M. Barrera-Ruíz. 2016b. New records and new hosts of Andricus sphaericus Pujade-Villar. 2016. (Hymenoptera: Cynipidae). Butlletí de la Institució Catalana d’Història Natural 80: 135-136. [ Links ]
Pujade-Villar, J. , M. Roca-Cusachs y I. Lobato-Vila. 2016c. Descripción de las primeras especies de Synergus con hembras de 13 antenómeros para México (Hymenoptera: Cynipidae: Synergini). Dugesiana 23(2): 109-116. [ Links ]
Ritchie A., J. and J. Shorthouse D.1987. A review of the species of Synergus from Guatemala, with notes on Cynips guatemalensis Cameron (Hymenoptera: Cynipidae). Proc Entomol Soc Wash, 89(2): 230-241. [ Links ]
Romero R., E. C. Rojas y M. de L. Aguilar. 2002. El género Quercus (Fagaceae) en el Estado de México. Annals of the Missouri Botanical Garden 89:551-593. [ Links ]
Ronquist, F., J. L. Nieves-Aldrey, M. L. Buffington, Z. Liu, J. Liljeblad and J. A. Nylander A . 2015. Phylogeny, Evolution and Classification of Gall Wasps. The Plot Thickens. PLoS ONE 10(5): e0123301. doi: 10.1371/journal.pone.0123301. [ Links ]
Schwéger, S., G. Melika, C. Tang T., P. Bihari, M. Bozsó, G. Stone S., J. Nicholls A. and Z. Pénzes. 2015. New species of cynipid inquilines of the genus Synergus (Hymenoptera: Cynipidae: Synergini) from the Eastern Palaearctic. Zootaxa 3999(4): 451-497. doi: 10.11646/zootaxa.3999.4.1. [ Links ]
Serrano-Muñoz, M., A. Villegas G., A. Callejas-Chavero, J. R. Lomeli-Flores, S. Romero-Rangel y J. Pujade. 2015. Sinergini y chalcidoidea (Hymenoptera) asociados a una agalla inducida por Atrusca sp. (Hymenoptera: Cynipidae: Cynipini) de la región noroeste de Sierra de Guadalupe, Estado de México. Entomología Mexicana 2: 155-160. [ Links ]
Serrano-Muñoz, M. , G.A. Villegas-Guzmán, A. Callejas-Chavero, J. R. Lomeli-Flores, U.M. Barrera-Ruiz, J. Pujade y M. Ferrer-Suay. 2016. Himenópteros asociados a las agallas de Andricus quercuslanigera (Hymenoptera: Cynipidae, Chalcidoidea) de Sierra de Guadalupe, estado de México. Entomología Mexicana 3: 177-182. [ Links ]
Sistema Estatal de Áreas Naturales Protegidas Estado de México (SEANPEM). 2016. Parque Estatal Cerro Gordo. Recuperado de Recuperado de http://sma.edomex.gob.mx/parque_estatal_cerro_gordo (5 de febrero de 2019). [ Links ]
Zavala, F. 1995. Encinos hidalguenses. Universidad Autónoma Chapingo. División de Ciencias Forestales. Chapingo, Edo. de Méx., México. 133 p. [ Links ]
Received: February 20, 2019; Accepted: June 26, 2019
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