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Revista Chapingo serie ciencias forestales y del ambiente

versión On-line ISSN 2007-4018versión impresa ISSN 2007-3828

Rev. Chapingo ser. cienc. for. ambient vol.21 no.1 Chapingo ene./abr. 2015 

Gall (Trioza rusellae Tuthill) insect identification in Brosimum alicastrum Swartz leaves in Yucatán, Mexico


Identificación del insecto agallador (Trioza rusellae Tuthill) en hojas de Brosimum alicastrum Swartz en Yucatán, México


Ada Ascencio-Álvarez1*; Rodolfo Martín-Mex1; Jorge I. Tucuch-Haas2; Jorge Valdez-Carrasco3; Emy G. Huchin-Poot1; Silvia B. Andrade-Canto1; A. Josué Gámez-Vázquez4; Alfonso Larqué-Saavedra1


1 Centro de Investigación Científica de Yucatán. Calle 43, núm. 130, col. Chuburná de Hidalgo. C. P. 97200. Mérida, Yucatán, MÉXICO. Correo-e: Tel.: 045 9991253697 (*Autora para correspondencia).

2 Instituto Nacional de Investigaciones Forestales, Agrícolas y Pecuarias (INIFAP), Campo Experimental Mocochá. km 25 antigua carretera Mérida-Motul. C. P. 97454. Mocochá, Mérida, Yucatán, MÉXICO.

3 Colegio de Postgraduados. km 36.5 carretera México-Texcoco. C. P. 56230. Montecillo, Texcoco, Estado de México. MÉXICO.

4 Instituto Nacional de Investigaciones Forestales, Agrícolas y Pecuarias (INIFAP), Campo Experimental Bajío. km 6.5 carretera Celaya-San Miguel Allende. C. P. 38110. Celaya, Guanajuato, MÉXICO.


Received: August 05, 2014.
Accepted: March 10, 2015.



The insect Trioza rusellae Tuthill (Hemiptera-Triozidae) produces galls on the leaves of the Ramon (Brosimum alicastrum Swartz) tree, species with high nutritional value of the Peninsula of Yucatan. The insect was isolated and identified from collections in the municipalities of Muna and Sacalum, Yucatán. Five to 10 years old trees were sampled selecting branches with leaves showing galls. The samples were placed in plastic bags and taken to the laboratory, and placed in entomological cages. Adult insects were collected using a manual vacuum, while galls were dissected to collect the nymphs directly with a brush (0001). The samples were preserved in alcohol (70 %) and in fixative formalin-alcohol-water (FAW). Nymphs and adult insects from the alcohol samples were mounted and observed on a stereoscopic microscope. The samples in FAW were processed and observed under a scanning electron microscope (SEM). As a result, photographs were obtained and development phases of T. rusellae were identified by entomological keys.

Keywords: Ramon tree, galls, pest, characterization, scanning electron microscope.



El insecto Trioza rusellae Tuthill (Hemiptera-Triozidae) produce agallas en las hojas del árbol de ramón (Brosimum alicastrum Swartz), especie con alto valor nutricional de la península de Yucatán. El insecto fue aislado e identificado a partir de colectas en los municipios de Muna y Sacalum, Yucatán. Los árboles de cinco a 10 años de edad se muestrearon seleccionando ramas con hojas que presentaban agallas. Las muestras se colocaron en bolsas de plástico y se trasladaron al laboratorio confinándolas en jaulas entomológicas. Los adultos se recolectaron con un aspirador manual, mientras que las agallas se disectaron para colectar las ninfas directamente con un pincel (0001). Las muestras se conservaron en alcohol (70 %) y en fijador formol-alcohol-agua (FAA). Las ninfas y adultos de las muestras en alcohol se montaron y observaron en el microscopio estereoscópico. Las muestras en FAA se procesaron y observaron en el microscopio electrónico de barrido (MEB). Como resultado, se obtuvieron fotografías y se identificaron las fases de desarrollo de T. rusellae mediante claves entomológicas.

Palabras clave: Ramón, agallas, plaga, caracterización, microscopio electrónico de barrido.



Brosimum alicastrum Swartz (Ramón) is a tree that is distributed from Mexico through Central America and the Antilles, to Ecuador and Venezuela in Latin America (Parker, 2008). In Mexico, B. alicastrum is on the side of the gulf, from the south of Tamaulipas to Quintana Roo, along the Sierra Madre Oriental and the Sierra de Chiapas up to an altitude of600 m, and in the Gulf Coastal Plain to the Peninsula of Yucatan. On the Pacific side, the species is distributed from the center of Sinaloa to Chiapas, both in the coastal plains and mountainsides and ravines of the Sierra Madre Occidental from 400 to 800 m above sea level (Pennington & Sarukhan, 2005).

The Academy of Sciences of the United States believes that B. alicastrum is one of the 36 species with greater possibilities of improving the lives of the inhabitants of the tropics (Moreno, 1995). In ancient times, the Mayan population of Guatemala and Mexico used the B. alicastrum seed as part of their diet. Today, the species is used to provide shade for coffee crops and is appreciated for its high nutritional value as forage (Herrera, 1996). B. alicastrum tree is one of the few tropical species which all parts can be used; its wood is used as firewood, fence posts, poles, tool handles and housing construction in rural areas. Forage is used as cattle feed, especially in the dry season. Latex is used as a substitute for milk and it is also used in traditional medicine for asthma, diabetes, tuberculosis and bronchitis treatments. Fruits are used in the production of jams and as livestock feed. Roasted seeds are eaten as chestnuts and boiled as substitute for potatoes (Niembro, Vázquez, & Sánchez, 2010). In one hectare with 400 trees (five years old) up to 15 t of leaves-ha-1 are produced in every cutting, which are acceptable for consumption by goats, sheep and cattle (Larbi, Awojide, Adekunle, Ladipo, & Akinlade, 2000; Sharma, Singh, & Bhat, 2000), because they represent a source with high protein content and adequate digestibility; in addition to improving milk and meat production in ruminants (Geilfus, 1994). However, B. alicastrum tree has several problems; among them, the attack of pests such as the psyllid Trioza rusellae Tuthill is the most important, which produces 400-600 galls per leaf, affecting photosynthesis (Piotto, 2007). Galls are abnormal tissue structures that are developed due to a specific reaction to the activity of an inductor body (Allison & Shultz, 2005; Foss & Rieske, 2004; Price, 2005).

Cuevas-Reyes, Quesada, Hanson, Dirzo and Oyama (2004a) identified gall-inducing plants and insects (GIS) species in trees from the Biosphere Reserve of Chamela-Cuixmala in Jalisco, Mexico, and mention the presence of T. rusellae and B. alicastrum as specific GIS. Cuevas-Reyes, Quesada and Oyama (2006) quantified the damage of gall insects in forest trees, finding that T. rusellae appears on B. alicastrum in a higher percentage in the dry season (15 %) compared to the wet season (9 %).

Different aspects of the Ramon tree have been studied in the state of Yucatan; e.g. productivity for animal consumption (forage), physiological development (Hernández, Vergara, & Larqué, 2014a, 2014b) and the response of roots to salicylic acid (Rosado & Larqué, 2014), but there is no information in the phytosanitary issue. Therefore, in this study we identified and characterized the pest (nymphs and adults) that is causing galls on the leaves of B. alicastrum in the state of Yucatán.



Location of B. alicastrum

The study was performed using B. alicastrum trees located in the municipalities of Muna and Sacalum, Yucatán. Muna is located 20° 25' N and 89° 46' W. Muna has flat topography; rocky or cemented soils; presence of undercurrents (cenotes); warm humid climate (Aw0) with summer rains; annual average temperature of 25 °C, maximum temperature in May (42 °C) and minimum temperature in December (15 °C); annual average rainfall of 946 mm and prevailing winds from the southeast and northwest (Ayala, Krishnamurthy, & Basulto, 2008). Sacalum is located 20° 33' N and 89° 34' W and is characterized by its flat surface; rocky or cemented soil; undercurrents, warm humid climate with summer rains; annual average temperature of 26.5 °C, minimum temperature in January and February (24 °C) and maximum temperature in April and May (31 °C); annual average rainfall of 1,009 mm and prevailing winds from the northeast and southwest.

Sampling of B. alicastrum

In March 2012 and February 2013, 20 B. alicastrum trees with a height of 5 m were selected. The trees were divided into three layers: lower (1-2 m), medium (2-4 m) and upper (4-5 m) layer. The samples were performed using the medium layer selecting branches of 50 cm in length, which had leaves with galls. The samples were placed in plastic bags marked with date, name of collector and place of origin. The bags were placed in a styrofoam cooler and taken to the laboratory GeMBio (Molecular studies applied to Biology) of the Centro de Investigación Científica de Yucatán A.C.

Sample processing

B. alicastrum branches were placed in entomological wooden cages with organza fabric (1 m x 1 m base x 1.5 m high) to 25 ± 3 °C for 10 days, according to the statements of Tucuch-Haas et al. (2010). Adult insects were collected with a manual vacuum, while galls were dissected to collect the nymphs directly with a brush (0001). All insects were preserved in alcohol (70 %); permanent mounts were made using hair gel and were observed under a stereomicroscope. Adult insects were identified and the nymphal stages of the insect were differentiated with the help of specialized entomological keys (Brown & Hodkinson, 1998; Tuthill, 1944).

Nymphs and adults were observed under a scanning electron microscope (SEM). For this purpose, the samples were fixed in a solution of formalin-alcohol-water (FAW) using the technique of Valdez (1991). A total of 20 insects per phenological stage were selected using a stereoscopic microscope, a thin knife and a brush. The samples were dehydrated using different percentages of alcohol (50, 70 and 90 %) into 1-hr periods, ending at 100 % alcohol. The sample was adhered to an aluminum base and was dried at critical point with CO2, using ethanol (100 %). The samples were initially heated at temperatures of 15 to 20 °C and then at 37 ± 1 °C. The sample was covered with gold and palladium to observe them under the SEM (Nieto, 2010).



T. rusellae galls in B. alicastrum leaves

Figure 1 shows some aspects of galls on B. alicastrum leaves. Galls had elongated shape (Figure 1a) and were classified in sizes: tiny (no insect), small, medium and large (0.2, 0.5 and 0.7 mm, respectively), no relationship was observed between the gall and the insect. It would presume that as the nymph feeds, the gall increases in size; however, this relationship was not observed with T. rusellae nymphs (Figure 1b). This contrasts with that reported by Mani (1992), who indicated that the size of the gall is an indicator of a nymph feeding conditions that produced it. With the SEM, we note that there is formation of trichomes on the opening of the base of the gall (Figure 1c). The increased size and number of cells is a response of the plant to insect feeding; nymphs feed on mesophyll tissue (Cuevas-Reyes et al., 2004b) (Figure 1d).

T. rusellae nymphs

Figure 2 shows some of the most important features of the T. rusellae nymphs. The insect has five nymphal stages (Figure 2a), moulting four times like Diaphorina citri Kuwayama, T. erytreae Del Guercio, T. aguacate Hollis and T. diospyri Ashmead. The difference between T. rusellae and the aforementioned species is that T. rusellae lives and feeds inside the gall, being attached until it becomes an adult insect; the other species actively feed on the surface of leaves, petioles, axillary buds and young stems. All these psyllids have flake shape and are surrounded by waxy filaments in the early stages (Fonseca, Valera, & Vázquez, 2007; Timmer, 2002). Moreover, T. diospyri nymphs have white powder and some filaments on its body (Mead, 2006) and T. aguacate has wing sectors, features that T. rusellae do not show (Burckhardt & Queiroz, 2012). T. rusellae nymphs are pale yellow with red eyes (Figure 2b) and the immature stages are located inside the galls individually (Figure 2c), as reported by Nieves (1993), who concludes that galls are simple structures caused by usually solitary insects. At the immature stages, insects with whitish waxy secretion on the back of their bodies were found. With the SEM, we observed that this secretion is a set of thin threads which on average can be up to 291 nm (Figure 2d). Burckhardt, Alené, Ouvrard, Tamesse, and Messi (2006) indicate that at the species level, psyllids have a very narrow range of host plants, particularly during the nymphal stages.

First stage. Flattened oval body, fused head and thorax, defined eyes, legs developed with few visible segments, abdomen defined with unobvious segments, light yellow body with a length of 0.455 mm and 0.223 mm width.

Second stage. At this stage, the division among head, chest and abdomen is clearly observed. The antennas are visible even antennal segments are not differentiated; red eyes, developed and differentiated legs, creamy yellow defined abdomen. The nymph grows to 0.944 mm long and 0.365 mm wide.

Third stage. Similar to the second stage, but has well-defined wings, slightly marked abdominal segments, presence of anal pores and greenish yellow anal orifice. The nymph can measure 1.125 mm long and 0.455 mm wide.

Fourth stage. The antennas get thinner closer to the middle part and thereafter they become narrower, eyes with very noticeable ommatidia, thorax with segmented legs. The constriction that separates the chest from the abdomen is seen more clearly. At this stage, the nymph can measure 1.474 mm long and 0.591 mm wide.

Fifth stage. Unlike the fourth nymphal stage, the antennae are thickened at the base, reducing progressively towards the apex, cherry eyes and developed wings. The nymph can measure 1.995 mm long and 0.828 mm wide.

T. rusellae adult insects

Figure 3 shows the external appearance of adult insects of T. rusellae. These insects have curved front wing, with vein Rs bifurcated with curved veins reaching the middle portion of the costal edge. The vein R + M has soft trifurcation in the middle portion and extends in veins that look like forked long setae; two reach the costal edge and one to the rear edge of the wing (Figure 3a). Legs with coxa (0.4 mm), trochanter (0.1 mm), femur (0.4 mm), tibia (0.8 mm), tarsus (0.1 mm) and pulvillus (Figure 3b). The last abdominal segment or the anal-genital area of the insect has conical shape and is narrow, ending with a V-shaped point (Figure 3c, 3d).

Adult insects have similar characteristics to the family of psyllids: back-ventral shape with compressed body; color variations ranging from yellow, olive green to dark gray; male insects are smaller than female insects and have blunt-ended point on the abdomen (Figure 4a), while the abdomen of the female insects ends in a sharp point (Figure 4b). Adult insects preserve certain differences compared to D. citri (they are not brown and have no distinctive patterns spots) and T. diospyri (their body has not a shiny black color, excluding the middle and back tibia) insects. In the case of T. erytreae and T. aguacate no significant differences were observed in adult insects, except in their nymphal stages and gregarious habits, so the above characteristics match those of the T. rusellae insect according to the keys of Brown and Hodkinson (1998) and Tuthill (1974). Cuevas-Reyes et al. (2004a) reported the existence of this insect on Ramon trees. Dreger and Sorthouse (1992) and Cuevas-Reyes, Siebe, Martínez-Ramos, and Oyama (2003) said that each gall species has a specific association with a host plant.



The insect producing galls on the leaves of the Ramon (Brosimum alicastrum Swartz) tree is Trioza rusellae Tuthill. These forage injuries limit photosynthesis and growth of the tree, affecting its yield; therefore, identifying this insect will help to plan research in this respect and specific control in the peninsula of Yucatán.



The authors thank and acknowledge for the financial support from CONACYT (grant no. 37517) and thank the Centro de Investigación Científica de Yucatan for providing the equipment and infrastructure during the performance of this work. Finally, independently, the main author thanks the Programa de CATEDRAS CONACYT for assisting in the completion of this work.



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