Introduction

In the tropics of Mexico and Central America, there are little-known fruit species that are distributed in natural vegetation or in backyard orchards, where their fruits are consumed as fresh fruit for their nutritional or medicinal value (^{Alejandro et al., 2020}; ^{Evangelista-Lozano et al., 2021}). The fruits of Garcinia intermedia have a pleasant taste and white pulp; they are used for self-consumption and sold in regional markets in some areas of Mexico. This fruit is mostly harvested in situ, and comes from trees that bear fruit only 2 or 3 years after germination. This fruit tree is from the same family as the mangosteen (Garcinia mangostana L.), which is of Asian origin and highly prized like G. intermedia for its taste and high nutraceutical capacity (^{Navarro-González, Codina-Dia, & Periago, 2015}). According to ^{Einbond et al. (2013)}, G. intermedia also has medicinal uses, since benzophenones extracted from the fruit inhibit the growth of human colon cancer cells.

G. intermedia grows semi-cultivated in home gardens in Santiago Acahuato, Apatzingan, Michoacán, Mexico, at 1,000 m a. s. l. with a warm dry climate. The G. intermedia trees in this locality reach a height of 10 to 20 m, while in Veracruz they reach the same size and are found between 0 and 800 m a. s. l. (^{Martínez y Pérez, Castillo-Campos, & Nicolalde-Morejón, 2015}). In the United States, there are some specimens in Homestead, Florida (^{Einbond et al., 2013}).

Most studies on G. intermedia have been in the ecological and medicinal fields, and little has been addressed in terms of the horticultural aspects of this species. Therefore, studies related to its asexual propagation and the postharvest of its fruits were not found in the literature. The aim of this review was to provide information on the agri-food and medicinal potential of G. intermedia in order to promote its horticultural development in tropical areas.

Methodology

Information was obtained from Agris, Agricola, BioOne, CRC net BASE, CRC Press, ELSEVIER, Google Scholar, Redalyc, SciELO, ScienceOpen, Scopus and Web of Science. The keywords used in the search engines, in addition to the scientific name, were underutilized fruits, Mesoamerican fruit trees, minor fruits, medicinal fruits and native fruits. To select the articles reviewed, horticultural, ecological, agricultural, geographic, environmental, social and medicinal criteria were emphasized.

Botanical classification

The family Clusiaceae is made up of 27 genera and 1,090 species distributed in tropical areas of the world (^{Martínez y Pérez et al., 2015}); in Mexico, 8 genera and 24 species have been recorded (^{Villaseñor, 2004}). The taxonomic classification of G. intermedia is: kingdom Plantae, class Equisetopsida, subclass Magnoliidae, superorder Rosanae, order Malpighiales, family Clusiaceae (Guttiferae), genus Garcinia L., genus Rheedia L. and species Garcinia intermedia (Pittier) Hammel (^{Hammel, 1989}).

Botanical synonyms and common names

The botanical names of G. intermedia are: Rheedia edulis (Seem.), Calophyllum edule (Seem), Rheedia intermedia (Pittier) and Rheedia tonduziana (Engl.) (^{Hammel, 1989}; ^{Martínez y Pérez et al., 2015}). Depending on the region in Mexico, the species is known by several common names, such as ishbastié (Chiapas), limoncillo, naranjillo, patácua, mamellito (Michoacán), zapotillo, toronjil (Oaxaca) (^{Pérez-Pacheco, Rodríguez-Hernández, Lara-Reyna, Montes-Belmont, & Ramírez-Valverde, 2004}), chichi de mono (Puebla), elemuy (Quintana Roo) (^{Quiroz-Carranza, Cantú-Gutiérrez, Quiroz, & Herrera-Vázquez, 2011}), manzanillo (^{Burgos-Hernández & Castillo-Campos, 2018}), guo-guo and wuowo (Veracruz) (^{Martínez y Pérez et al., 2015}). In Panama, it is known as sastra and monkey fruit (^{Murillo et al., 2013}), in the Philippines as chinese santol, lemon drop and mangosteen (^{Chua-Barcelo, 2014}), and in Costa Rica as jorco, mangostán (^{González-Paniagua & Barrantes Lobo, 2018}), sastra and mameyito (^{Irías-Mata et al., 2018}).

Origen and distribution

G. intermedia is native to Mexico (Jalisco, Michoacán, Oaxaca and Veracruz) and Central America (Belize, Costa Rica, El Salvador, Honduras, Nicaragua and Panama) (^{Lim, 2012}). It grows wild in Veracruz in high evergreen forest (^{Báez-Hernández, Herrera-Meza, Vázquez-Torres, Aquino-Bolaños, & Martínez, 2016}), low deciduous forest, pine-oak forest (^{Martínez y Pérez et al., 2015}), and in the Los Tuxtlas region between 10 and 800 m a. s. l. (^{Lascurain, Avendaño, del Amo, & Niembro, 2010}). It is also distributed in the Lacandon Jungle of Chiapas (^{Sánchez-Gutiérrez, Valdez-Hernández, Hernández-de la Rosa, & Beltrán-Rodríguez, 2018}), and on the Pacific slope in Oaxaca and Chiapas. This species has been collected in the Compostela, Nayarit and Tuito, Jalisco areas. In Michoacán, some trees are found in backyard orchards in the community of Acahuato, located in the north of the municipality of Apatzingan. In Zirimícuaro, municipality of Ziracuaretiro, under subtropical conditions, there is an orchard where fruit is produced for self-consumption.

Outside of Mexico, this fruit grows naturally in Alta Verapas, Guatemala, at 300 m a. s. l. (^{Hammel, 1989}), and in the forests of Panama (^{King, Leigh, Condit, Foster, & Hubbell, 1997}), Ecuador and Colombia (^{Castaño, Carranza, & Pérez-Torres, 2018}). In Costa Rica, in the Central Valley, it is occasionally cultivated as an ornamental and its fruits are consumed (^{Zamora, Jiménez, & Poveda, 2004}). In India, it is a minor fruit tree (^{Dandin, Kencharaddi, Kumar, & Chikkanna, 2019}), and its fruit is used to increase the household income of smallholder farmers (^{Bhat et al., 2015}).

Botanical characteristics

^{Pennington and Sarukhán (2005)} describe G. intermedia as a tree with a cylindrical stem (Figure 1), a height of 20 m, and a trunk with large, spaced bulges. Its outer bark is dark brown, smooth and with abundant lenticels. The inner bark is pink, with drops of intense yellow exudate. The bark is 5 to 8 mm thick. Its wood is yellowish cream colored, with numerous rays, small vessels with vasicentric parenchyma and exudate of yellow drops. Young branches are glabrous, with a bright green color that changes to brownish and produces a yellow latex when cut. They have an oval cross section, with large scars from fallen leaves (^{Martínez y Pérez et al., 2015}).

Figure 1 Tree shape (a) and main stem (b) of Garcinia intermedia 8 years after establishment by seed.  

G. intermedia buds are naked, minute (1 to 2 mm long), acute, glabrous and without stipules. The decussate and simple leaves can reach a size of 13 x 5 cm to 22 x 7.5 cm, which are elliptical or oblong, with the entire margin, an acute to acuminate apex, and an acute base (Figure 2). Their color is dark green and shiny on the upper side, and pale on the underside; in addition, they are glabrous, coriaceous, and with numerous parallel secondary veins and a prominent marginal vein. The petioles are 1.5 to 2 cm long, with a conspicuous bulge at the base on the upper surface, and glabrous (^{Zamora et al., 2004}).

Figure 2 Garcinia intermedia leaves: a) elliptical or oblong shape and b) young reddish leaves. 

G. intermedia trees are evergreen, and their leaves can live for 6 to 8 years on trees growing in a rainforest (^{Lovelock, Kursar, Skillman, & Winter, 1998}). The young leaves are reddish in color (Figure 2), with a high concentration of anthocyanins that protect them from attack by fungi and ants (^{Coley & Aide, 1989}). During the rainy season, this species produces a large number of whitish leaf shoots in their early stages of development, which then turn pink, yellow and light green, until they reach their characteristic dark green color. The leaves are very variable in size; in dry climates, with marked climatic seasonality, they are relatively small, while in very humid climates they are large. Individuals growing in very humid climates are difficult to differentiate from G. madruno, because they have leaves of the same size, although with greenish-brown coloration and without clear rows of resin on the upper surface (^{Zamora et al., 2004}).

The white G. intermedia flowers are actinomorphic, 7 to 8 mm in diameter (Figure 3a) and appear in fascicles on small bumps in the leaf axils. Pedicels are 1.5 to 2.5 cm long and glabrous. The sepals are whitish-green, elliptical, cuculate and glabrous, 2 to 3 mm long. The petals are white, obovate and glabrous, 4 to 5 mm long. The stamens are numerous, white and 3 to 5 mm long with small rounded anthers. The ovary is approximately 2 mm long, ovoid and glabrous. In Veracruz, the tree blooms from February to April, while in Ziracuaretiro, Michoacán, it blooms from July to August in cultivated form, and intermittently throughout the year.

The fruits are glabrous, ovoid, yellow berries when ripe (^{Hammel, 1989}) (Figure 3b), and when cut they produce a yellow latex. The fruits have a thin yellow, orange or red rind around a white pulp; they are edible and have an attractive sweet and sour taste.

The fruits ripen from June to September, and at elevations of 1,600 m (Zirimíuaro, Michoacán), the trees can bear fruit throughout the year. In San Andrés Tuxtla, Veracruz, Mexico, the fruits can be found in local markets between August and November (^{Ibarra-Manríquez, Ricker, Ángeles, Sinaca-Colín, & Sinaca-Colín, 1997}). In Chimalapas, Oaxaca, the fruits are consumed by the spider monkey (Ateles geoffroyi) (^{Ortíz-Martínez & Ramos-Fernández, 2012}), and in Santa Rosa de Cabal, Colombia, they are consumed by bats (^{Castaño et al., 2018}).

Some insects that are potential pests of G. intermedia fruit are the lepidopteran Eriosocia guttifera (^{Brown et al., 2020}), the lobate lac scale Paratachardina pseudolobata Kondo & Gullan (Hemiptera: Coccoidea: Kerriidae) (^{Segarra-Carmona & Cabrera-Asencio, 2010}) and the fruit fly Anastrepha suspensa (^{Jenkins & Goenaga, 2008}).

Figure 3 a) Flowers, b) fruits and c) seeds of Garcinia intermedia. 

Seeds measure 2.8 x 1.2 cm (Figure 3c), can take up to six months to germinate and show growth of two types of roots: primary and secondary, which cross the seed lengthwise. This can be an advantage if their root system needs to be regenerated (^{Di Stefano, Marín, & Díaz, 2006}).

Individuals for transplanting are found under adult trees. Most Garcinias are apomictic (^{Murthy et al., 2018}), although there is no information on G. intermedia. The juvenility of this tree is short, as it produces fruits two years after germination.

From the home gardens of Santiago Acahuato, Michoacán, G. intermedia fruits were collected, seeds were extracted and plants were established beginning in 2008 in a small orchard located in Zirimícuaro, Ziracuaretiro, Michoacán. In 10 trees, 8 ripe fruits were randomly sampled in 2018, with the following characteristics evaluated: fruit weight (g), polar length (cm), equatorial diameter (cm), peel firmness (kg·cm-2; with a 1 cm diameter texturometer), total soluble solids (°Brix), number of seeds, total seed weight (g), peel weight (g), peel plus seed weight (g), pulp percentage (%), pedicel length (cm), roundness index (polar length/equatorial diameter), and fruit color (visual) (Table 1).

The average fruit mass was 71.8 g and ranged from 24 to 140 g. Polar and equatorial lengths were 4.6 and 5.3 cm, respectively. Peel firmness was 5.1 kg·cm-2. Solids reached 18.6 °Brix at consumption maturity, which is a high value compared to that of other fruits, such as feijoa (Acca sellowiana Berg), which is bittersweet and reaches 14 °Brix (^{González-García, Guerra-Ramírez, del Ángel-Coronel, & Cruz-Castillo, 2018}). The fruits presented one to four seeds, with an average of two, which resulted in 52 % pulp, and the rest seeds and peel. The roundness index was 0.98, showing almost round or oval fruits (Table 1). Data on these characteristics in G. intermedia fruit were not found in the literature.

The white pulp fruit is aromatic, yellow or greenish-yellow when ripe for consumption, and keeps well at 7 °C for up to 30 days. These characteristics are horticulturally important for a tropical fruit with potential in the agri-food trade and can be adapted to the subtropics. There are advances in the breeding of other little-known Garcinia species such as G. indica, but not for G. intermedia (^{Murthy et al., 2018}).

The fruits, once harvested, can be left to ripen for seven days at 20 °C and acquire a bright yellow-greenish color, which indicates their ripeness for consumption.

Current and potential uses

G. intermedia wood resists termite attack and is used to make posts and tool handles. In Veracruz, it grows as a backyard tree and is used for housing construction (^{Álvarez-Buylla, Lazos-Chavero, & García-Barrios, 1989}). This species is ideal as a permanent shade tree, and for establishing hedges, living fences and windbreaks. In addition, it is a drought-tolerant species (^{Engelbrecht & Kursar, 2003}), and to optimize water use it could be evaluated as a rootstock for other Garcinia species.

Because the tree has attractive leaves and fruit, in Costa Rica it is used as an ornamental plant, especially when it has fruit (^{Zamora et al., 2004}). Likewise, its foliage can be used for floral arrangements, and the fruit is used in the preparation of liquors, jams, ice cream, yogurt, and fresh drinks, although there is no information on its processing.

Garcinia species have great medicinal potential (^{Spontoni-do Espirito Santo et al., 2020}). G. intermedia fruit is rich in benzophenones, such as 32-hydroxy-ent-gutiferone M (1) and 6-epi-guttiferona J (2) (^{Muñoz-Acuña et al., 2010}), which have been used in the treatment of colon cancer in vitro (^{Einbond et al., 2013}). Several carotenoids such as zeaxanthin, b-carotene, lutein and b-cryptoxanthin have been identified in G. intermedia fruit (^{Murillo et al., 2013}). Due to the high content of these compounds (especially lutein and zeaxanthin), it is suggested to consume this fruit to prevent eye diseases (^{Fernández-Araque, Guiaquinta-Aranda, Laudo-Pardos, & Rojo-Aragüés, 2017}).

G. intermedia fruit has a higher antioxidant capacity and a higher concentration of total phenols than G. mangostana (^{Muñoz-Acuña, Dastmalchi, Basile, & Kennelly, 2012}). In addition, some flavonoids (podocarpusflavone A and amentoflavone) extracted from the leaves of G intermedia can be used to combat Chagas disease (^{Abe et al., 2004}; ^{Nabavi et al., 2017}), which is produced by triatomine insects that transmit the Trypanosoma cruzi parasite. For therapeutic purposes, this fruit tree could become as valuable as the white sapote (Casimiroa edulis Llave & Lex.), which is native to Mexico and with which several studies have been conducted (^{Agustin, Soto, Famiani, & Cruz-Castillo, 2017}).

Prospects

The medicinal and commercial production potential of G. intermedia fruit requires further exploration. The medicinal properties of this species’ fruits have been emphasized, and the phytochemical characteristics of its leaves require further evaluation. Studies on the nutraceutical and medicinal potential of the flowers and seeds were not found in the literature. Therefore, the integral utilization of this fruit tree could position it as a new and important arboreal horticultural product of the tropical zones. Ex situ conservation of this fruit tree is not being carried out, and collections of this fruit tree in tropical zones of Mexico and Central America could be carried out. The selection of individuals with high fruit quality would be advantageous for its commercialization, since it has the potential to be adapted in high elevation tropical areas and it could be a new fruit tree for the 21st century.

Conclusions

The lemon drop mangosteen (Garcinia intermedia (Pittier) Hammel) is a species with potential for fruit use in the tropics of Mexico. Studies on its propagation and postharvest handling are needed. Due to deforestation, many individuals have been lost; therefore, its ex situ and in situ conservation is necessary. Collections of this species could be carried out in Veracruz, Puebla and Oaxaca in Mexico and in Alta Verapaz, Guatemala. Its medicinal potential is high due to its high concentrations of benzophenones and flavonoids.

The selection of trees that produce large, sweet fruits with small seeds would offer the possibility of their commercial use in the food sector and in the health sector as an alternative product to prevent or attack colon cancer.