Introduction
Passiflora plants are lianas with axillar tendrils and nectaries; their sexual organs are merged into a structure named the androginophore[1]. Passiflora is a genus with nearly 600 species; 95% of them are American natives, mainly from South America and Mesoamerica (from Central Mexico to Panama)[2]. More than 60 species of Passiflora produce large edible fruits, and nearly 25 species are cultivated. The economically important edible juice producers are Passiflora edulis, P. edulis f. flavicarpa, P. ligularis, P. quadrangularis, and P. tripartita var. mollissima; moreover, the fruits of P. tripartita, P. tarminiana, P. maliformis, P. alata, P. hannii, P. laurifolia, P. popenovii, and P. setacea are consumed locally elsewhere[3]. Approximately 1.5 million tons of passion fruit (Passiflora edulis) are produced worldwide, with Brazil being the main producer and consumer[4].
Although most Passiflora species are American native, research on those species involved worldwide scientific groups. For example, due to their, actual and potential ecological and economic roles, in several world regions, such as China, projects for cropping and breeding Passiflora are being developed[5]. Medical researchers are determining the potential of Passiflora plant organs to recover physical and psychiatric human health[6,7].
In Mexico, 91 Passiflora species, native and introduced, have been reported, indicating that, for this genus, this country is the fifth in worldwide diversity ranking[8]. Within Mexico, one of the areas with greater Passiflora diversity are the areas belonging to the southern states of Campeche, Chiapas, Yucatán, and Quintana Roo[9]. In Chiapas state there are, at least, two endemic species, P. pendens and P. tacanensis[8].
The land area of those southern states is 215,047 km2, representing approximately 10% of the total Mexican territory. Nowadays, its current inhabitants belong to different ethnic groups and mestizo people[10]. Nevertheless, before Spanish irruption in Mexico, this area was inhabited by several groups belonging to ancient Mayan culture, including yucatecos in the states of the Yucatan Peninsula (Campeche, Yucatán, and Quintana Roo), and choles, tsetales, tsotsiles, tojolabanes, and lacandones in Chiapas state[11,12].
As Mexico is one of the main land reserves for Passiflora plants, scientific efforts to claim further national studies on this plant genus must be performed. This review presents a list of the Passiflora species botanically recorded in four southern Mexican states. Then reports related to previous, actual, and potential uses for those species are briefly summarized. This review aims to point out the importance of the conservation of Passiflora genetic resources in southern Mexico.
Passiflora species in southern Mexico
According to the herbaria MEXU[13], HERBANMEX[14], CICY[15], and CHAPA[16], thereafter confirmed in the specialized platform 'Plants of the word on line'[8], in the states under study, there are 55 Passiflora species (Table 1). Chiapas state accounts for 90% of those species, followed by Quintana Roo, Campeche, and Yucatán states[9].
Chiapas state presents five biogeographical provinces related to a specific natural area in relation to its endemic biota. Those five provinces are, the 'Gulf of Mexico lowland', 'Chiapas central plateau', 'Chiapas central depression', 'Madre mountain range', and 'coastal lowland'. In contrast, within the Campeche state area, there are two biographical provinces, the 'Gulf of Mexico lowland' and the 'Yucatán lowland'. Whereas Yucatán and Quintana Roo states belong only to the province named 'Yucatán lowland'[19]. Thus, the presence of different biogeographical provinces, implying different climates and ecological conditions, might influence Passiflora diversity. For example, in Mexico, Chiapas state is known to be the second state with a relatively high total plant diversity, with over 10,000 plant species[20].
For Chiapas state, there are botanical reports of Passiflora in 65 of the 126 municipalities, with a greater presence in Ocosingo (19 species), Unión Juárez (nine species), and Palenque (eight species). Including the four states under study, the municipality of Othón P. Blanco, Quintana Roo state (11 species), follows Ococingo, and then, the list continues with Calakmul, Campeche State (11 species). For Yucatán state, a greater Passiflora presence has been reported in Progreso (five species) (Fig. 1).
The number of Passiflora species recorded in Ocosingo is greater than the number of Passiflora species reported in each of the other 18 states in Mexico[9]. Additionally, Unión Juárez must be valorized for its Passiflora richness, as the municipality area is only 62 km2[10].
Passiflora species grow mainly in family orchards and jungle systems[12,21]; the latter system is very sensitive to overexploitation of natural resources, pollution, and climatic change. Moreover, it is very responsive to demographic changes, public policies, and local technological projects[22].
Former and actual uses
To our knowledge, there are no reports of the use of Passiflora plants by ancient Mayan culture. However, ethnobotanical reports, written in the last three decades, indicate that in the Lacandón forest, native people eat the fruits of 'ch'um ak'' (P. ambigua), 'ch'ink ak'il' (Passiflora sp.) 'poochin' (P. serratifolia) and P. hahnii[12,13]. A recent review confirmed the consumption of P. ambigua, P. bicornis, P. ciliata, P. foetida, P. hahnii, P. ligularis, P. mayarum, P. serratifolia, and P. yucatensis fruits in communities of Chiapas and the Yucatan Peninsula[23].
In Yucatán state, the P. ciliata plant is used to treat hysteria, sleeplessness, and child convulsion; local people assign this species narcotic and sedative properties[24]. In the Chiapas High Valleys, P. membranacea liana is used as a rope to tie tools or help build rudimentary houses[21].
In the municipality of Solidaridad, Quintana Roo State, the staff of the butterfly pavilion of a theme park, crop at least two Passiflora species, one allegedly to be P. lobata ('pata de gallo' in Spanish), to raise butterfly larvae. The information within the park, mentions that they raise the butterflies Agraulis vanillae, Dryas iulias, Heliconius erato, and H. charithonia. Scientific literature supports the preference of butterfly larvae for P. lobata[25].
Potential uses
For centuries, some effects on the human body have been assigned to Passiflora plants. Moreover, in the Spanish language, the name of passion fruit was misunderstood, and many people have given aphrodisiac properties to Passiflora species, instead of relating its name to the passion of Christ[1]. Moreover, in plants of this genus, several molecules with spasmolytic, sedative, anxiolytic, and blood pressure modulation properties have been identified. One of those molecules is passicol, which has antibacterial properties. P. foetida leaf extracts reduce the growth of Pseudomonas putida, Vidrio cholerae, Shigella flexneri, and Streptococcus pyogenes, supporting the use of this plant in ethnopharmacology to treat fiber, diarrhea, stomach and throat pains, and ear and skin infections[26].
It has been suggested that the anthocyanin present in the peel of P. biflora might be used as an additive to increase color and antioxidant capacity in some human foods[27]. Additionally, pectin can be extracted from the Passiflora peel for human consumption[28], and it has been proposed to transform peel into biofuels[29]. As Brazil is a high yellow passion fruit producer, it has been proposed to produce passion fruit seed oil there. The oil might be used in human foods or transformed into creams, shampoos, and pharmacology products[30]. In addition, among the seed components, there are stilbenes, which are excellent antioxidants, enhance human skin conditions, and present hypoglycemic properties[31].
Conservation
In the Yucatan Peninsula, Passiflora is among the top five plant genera with relatively high diversity[17]. This richness might be used to breed, aiming for genotypes producing high-quality fruits and suitable for cropping in new areas[5,32]. Nevertheless, land use change represents one of the greatest risks to conserving actual biodiversity; this factor also contributes to increasing the rate of climatic change and affects ecosystem sustainability[33].
Quintana Roo state is one of the main tourist region's in Mexico, Cancun resort area is located there, and further luxury resorts are still planned. Mexican environmental law protects approximately 30% of the land of the municipality of Othón P. Blanco, Quintana Roo state[34]; and this municipality started policy programs for sustainable bay management, keeping its vegetation, including several medicinal plants[35]. In this sense, recently, the Mexican government involved some institutes in flora conservation. In the municipality of Solidaridad, Quintana Roo state, the Botanical Garden 'Dr. Alfredo Barrera Marín' belonging to the 'Centro de Investigaciones de Quintana Roo' is the repository of the flora native of the section North 5 of the project Maya Railway.
In general, in the four states under study herein, there are important archeological and touristic venues; thus, Passiflora conservation in southern Mexico might involve ethno-tourism, ecotourism, and other local developmental projects. Moreover, in the Yucatan Peninsula and Chiapas there are almost 17 areas named Nature Reserves. They are: 'Pantanos de Centla', 'Río Celestum', 'Río Lagartos', 'Sian Ka'an' 'Chinchorro', 'Caribe Mexicano', 'Tiburón ballena', 'El triunfo', 'La Encrucijada', 'La Sepultura', 'Lacan tún', 'Montes azules', 'Selva El Ocote', 'Volcán Tacaná', 'Calakmul', 'Balam ku', and 'Los Peténes'. Therefore, according to UNESCO, in nature reserves, effective fauna and flora protection policies might be observed[36].
The role of Passiflora plant species in conserving local fauna, and, by a consequence, help to keep the ecosystem balance, must be carefully understood. Several Passiflora species included in Table 1 have been reported to be good feed sources for animals. For example, P. biflora may play a role in conserving bats in the Lacandón forest[9]. For Passiflora species being bat-pollinated, it has been observed that their flowers are well adapted to bat behavior, as their flowers secrete nectar at night[37]. Moreover, it has been reported that some years after introducing Passiflora plants, the population of butterflies and bees was increased[9]. Some studies have revealed that P. suberosa is a good feed source for A. vanillae maculosa larvae, although less preferred by D. iulia caterpillar, who prefers leaves of P. misera[38,39].
Although tropical forest regeneration is possible, the predicted growth of urban areas is a risk factor[33] in reducing Passiflora diversity. On the other hand, some researchers have suggested that rural families contribute strongly to maintaining plant species[40]. Thus, reducing the poverty factor might be included in national, state, and municipality politics to recognize the importance of native and original communities in conserving plant genetic resources. For example, within the three municipalities with the greatest presence of Passiflora species, only Othón P. Blanco has less than 45% of its population living in poverty, whereas over 80% of the populations of Ocosingo and Calakmul live in poverty. In five of the six municipalities with a greater presence of Passiflora, the human population living in poverty is greater than 70%[41].
Although some countries offer payments to conserve plant genetic resources, they are limited to plant species presenting economic importance[42]. Thus, to involve local people in plant genetic conservation, projects aimed at sustainability, environment conservation, prosperity, and human welfare must be offered. The municipality, state, and national governments must establish laws and regulations to save jungles and mangroves. Further efforts to keep flora and fauna, in this case Passiflora species, in the areas with a higher presence of this genus, are expected to keep its holistic value and diversity.
Conclusions
The high diversity of Passiflora plants in Chiapas state seems to be related to the presence of five biographical provinces: 'Gulf of Mexico lowland', 'Chiapas central plateau', 'Chiapas central depression', 'Madre mountain range', and 'coastal lowland'. Within Chiapas state, Ococingo is the municipality with the highest Passiflora diversity.
Although there are no reports of the use of Passiflora in ancient Maya culture living in Chiapas, Campeche, Yucatán, or Quintana Roo states, the actual use of Passiflora suggests inherited knowledge. On the other hand, the agro-industrial and pharmacological potential of this plant genus might help promote sustainable regional development. The rescue of traditional fruit species and their ancient knowledge might enhance the local economy and maintain ecological balance.
The authors confirm contribution to the paper as follows: study conception and design: Franco-Mora O; data collection: Franco-Mora O, Moreno-Jiménez A; analysis and interpretation of results: Franco-Mora O, Sánchez-Pale JR; draft manuscript preparation: Franco-Mora O, Castañeda-Vildózola Á. All authors reviewed the results and approved the final version of the manuscript.
The herbarium MEXU, HERBANMEX, and CICY offers free access to their on line database; they are cited in the References section[13−15]. Data from herbaria CHAPA (16) is available at the Institute.
The herbaria exemplars, consulted herein, represent the work of several botanists. The picture of Passiflora ciliata was kindly donated by Prof. Elia Ballesteros-Rodríguez (CICY, Yucatán, Mexico).
The authors declare that they have no conflict of interest.
