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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.30 no.1 Chapingo ene./abr. 2024  Epub 03-Dic-2024

https://doi.org/10.5154/r.rchscfa.2023.06.030 

Review articles

Systematic Review for Understanding Mexican Biodiversity: The Agaves of Hidalgo

Mario A. García-Montes1 
http://orcid.org/0000-0001-5236-7160

Carmen J. Figueredo-Urbina2 
http://orcid.org/0000-0003-0906-8821

Pablo Octavio-Aguilar3 
http://orcid.org/0000-0002-4636-9773

1Universidad Autónoma del Estado de Hidalgo, Instituto de Ciencias Básicas e Ingeniería, Posgrado en Ciencias en Biodiversidad y Conservación. Ciudad del Conocimiento, Carretera Pachuca-Tulancingo km 4.5, col. Carboneras. C. P. 42184. Mineral de la Reforma, Hidalgo, México.

2Universidad Autónoma del Estado de Hidalgo, Instituto de Ciencias Agropecuarias. Av. Universidad km 1 s/n, Exhacienda Aquetzalpa. C. P. 43600. Tulancingo, Hidalgo, México.

3Universidad Autónoma del Estado de Hidalgo, Instituto de Ciencias Básicas e Ingeniería, Laboratorio de Genética. Ciudad del Conocimiento, Carretera Pachuca-Tulancingo km 4.5, col. Carboneras. C. P. 42184. Mineral de la Reforma, Hidalgo, México.


Abstract

Introduction:

The genus Agave, a biological group of cultural and economic importance, is most diverse in Mexico. However, the exact number of species in the state of Hidalgo remains uncertain.

Objective:

The aim of this study is to conduct a systematic literature review to examine the diversity of agave species found in the state of Hidalgo.

Materials and methods:

A comprehensive literature review was conducted using the PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-analysis) protocol, herbarium collections and digital databases were reviewed. A total of 65 informati0on sources were identified, from which 22 were selected to create a database. Species names were reviewed and updated to avoid synonyms and repetitions.

Results and discussion:

A total of 55 species were identified, with 26 having a ‘very likely’ presence in the region. Agave mitis Mart. was the most frequently recorded maguey (19), followed by A. lechuguilla Torr. (17). The species are primarily concentrated in the Barranca de Metztitlán Biosphere Reserve, Valle del Mezquital, and the central part of the state. Agave peacockii Croucher is subject to special protection according to NOM-059-SEMARNAT-2010.

Conclusions:

Hidalgo can be considered among the states with a considerable number of Agave species. The generated information is useful; however, it should be used with caution, as it may be subject to spatial, temporal, and taxonomic biases in inventory data, collections, and lists.

Keywords: maguey; Asparagaceae; Agavaceae; Agave mitis; Agave lechuguilla

Resumen

Introducción:

El género Agave, grupo biológico de importancia cultural y económica, presenta su mayor riqueza en México, aunque en el estado de Hidalgo aún no es claro el número de especies presentes.

Objetivo:

Analizar el número de especies de magueyes que se distribuyen en el estado de Hidalgo a través de una revisión sistemática de literatura científica.

Materiales y métodos:

Se hizo una revisión exhaustiva de literatura científica mediante el protocolo PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-analysis) y se revisaron colectas de herbarios y bases de datos digitales. Se encontraron 65 fuentes de información, de los cuales se eligieron 22 y con ellos se creó una base de datos. Los nombres de las especies se revisaron y actualizaron para evitar sinonimias y repeticiones.

Resultados y discusión:

Se encontraron 55 especies, de las cuales 26 tienen presencia ‘muy probable’ en la entidad. Agave mitis Mart. fue el maguey con mayor frecuencia de registro (19), seguido de A. lechuguilla Torr. (17). Las especies se concentran principalmente en la Reserva de la Biosfera Barranca de Metztitlán, Valle del Mezquital y el centro de la entidad. Agave peacockii Croucher se encuentra sujeta a protección especial de acuerdo con la NOM-059-SEMARNAT-2010.

Conclusiones:

Hidalgo se puede considerar entre los estados con un número considerable de especies de Agave. La información generada es de utilidad; sin embargo, debe utilizarse con cautela, ya que pueden estar sujetos a sesgos espaciales, temporales y taxonómicos en datos de inventarios, colecciones y listas.

Palabras clave: Maguey; Asparagaceae; Agavaceae; Agave mitis; Agave lechuguilla

Highlights:

  • A total of 55 agave species were recorded, with 26 having 'very likely' presence in Hidalgo.

  • Agave mitis was the maguey with the highest frequency of occurrence (19), followed by A. lechuguilla (17).

  • The species are concentrated in the Barranca de Metztitlán Biosphere Reserve and Valle del Mezquital.

  • Agave peacockii is subject to special protection according to NOM-059-SEMARNAT-2010.

  • Taxonomic biases are the main issue for systematic reviews.

Introduction

Since the year 2000, systematic reviews have been incorporated into the field of conservation, and to date, they remain relevant and effective in decision-making, demonstrating their impact in various scientific domains (Berger-Tal et al., 2019; Collaboration for Environmental Evidence [CEE], 2013). These reviews encompass studies on nurse plant conservation, dispersal, invasive species, and distribution models in protected areas (CEE, 2018; Driscoll et al., 2014; Filazzola & Lortie, 2014; Haddaway et al., 2015; Mačić et al., 2018; Ordóñez-Delgado et al., 2019; Robinson et al., 2017; Хапугин, 2020). Systematic review, as a synthesis method, aims to address a specific question with the utmost precision; all relevant evidence available is critically assessed using the PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-analysis) protocol. These guidelines help enhance the reporting of reviews, making them more reliable and solid, such that the final document can be shown as a literature review or a meta-analysis (Haddaway et al., 2015; Liberati et al., 2009; Molina, 2018).

Entities or countries often require reports generated through this type of analysis to ascertain the number of species, the quantity of individuals, and the geographical locations of their populations. Furthermore, these reports serve as foundational information for conservation programs. Integrating this information helps identify which species should be included in specific programs and which areas are crucial for conservation, because evaluations to assign some type of risk to species use criteria of distribution and population characteristics, as well as geographic location data (International Union for the Conservation of Nature [IUCN], 2017; Secretaría de Medio Ambiente y Recursos Naturales [SEMARNAT], 2010).

The genus Agave is endemic to the Americas and is distributed from the southern United States to northern Venezuela. This biologically significant group, with cultural and economic importance, exhibits its greatest diversity in Mexico, although the number of species present in the state of Hidalgo is still unclear. Gentry (1982) identified 15 species of agaves (considering intra-specific varieties) from two subgenera and seven groups in Hidalgo. Later, Granados (1993) listed 13 Agave species in the region. Years afterward, Villavicencio Nieto and Pérez Escandón (2006) documented eight agave species used medicinally for various conditions. Golubov et al. (2007), based on the classification of the Comisión Nacional de Áreas Naturales Protegidas (CONANP), reported the species richness of the genus per state in protected natural areas (NPA) and concluded that 27 Agave species were recorded in four NPAs from Hidalgo, without specifying names. On the other hand, Villaseñor (2016), in his checklist of native vascular plants in Mexico, mentioned the existence of 32 agave species in this state. Subsequently, Thiede (2020) compiled information and identified 20 taxa of this genus in the region, while more recently, Villaseñor et al. (2022), in their work on richness and distribution of vascular flora in the state of Hidalgo, recorded 21 agave species, with 14 of them being endemic to Mexico. These studies note that some records have not been validated or located in the field, cautioning that certain identifications may be incorrect, leading to common data gaps and variability in the reports.

Clearly, there is no unanimous agreement on the precise number of agave species in the state, with significant variations among authors attributed to publication years and taxonomic changes (The Angiosperm Phylogeny Group, 2016; Thiede, 2016). Furthermore, the digital database of the Sistema Nacional de Información sobre Biodiversidad (SNIB) records up to 37 species, subspecies, and varieties (Comisión Nacional para el Conocimiento y Uso de la Biodiversidad [CONABIO], 2022). Some of these are classified as nationally and internationally at risk, underscoring the importance of consolidating and updating this information to develop more effective plans for the use, management, and conservation of this pivotal biological group in Mexico. In this context, the following question arises: How many agave species are officially recorded in Hidalgo? Thus, the primary goal of this study was to comprehensively review the distribution of agave species in the region, employing the synthesis of scientific literature, herbarium collections, and digital databases. This information enhances understanding of the natural resource in the region and proves valuable for proposing management and conservation plans.

Materials and Methods

An exhaustive review of scientific literature and data from publicly accessible databases was undertaken. Using this information, an updated list of accepted scientific names was generated. This process followed the outlined scheme below.

Delimiting search and sources

Only the state of Hidalgo was considered as the study area. The search for information on agaves in Hidalgo was conducted in both primary and secondary sources. As primary sources we considered the scientific literature of indexed articles, books with ISBN (International Standard Book Number), gray literature (books without ISBN and articles without DOI [Digital Object Identifier], undergraduate and graduate theses from universities that have repositories (Universidad Nacional Autónoma de México [UNAM], Instituto Politécnico Nacional [IPN], Universidad Autónoma del Estado de Hidalgo [UAEH]), all following the PRISMA protocol (Liberati et al., 2009). As secondary sources of information, some online databases of biological collections were considered, such as the National Herbarium of Mexico (MEXU) of the Institute of Biology of the Universidad Nacional Autónoma de México (IBUNAM, 2021), the Herbarium of the Universidad Autónoma del Estado de Hidalgo (HGOM) was visited, databases of observations and identification were consulted on the website Naturalista (iNaturalist, 2022) and SNIB (CONABIO, 2022).

Search criteria

Keywords and Boolean operators used in the search for information in primary sources were: “Agave”, “Asparagaceae”, “Agavaceae”, “Agavoideae” “Agave* Hidalgo”, “Agave* diversidad”, “Agave*, lista”, “Agave AND Hidalgo, “Agave AND especies”, “Agave AND lista”, “Agave SAME especies SAME Hidalgo”, “Agave SAME especies SAME México”. The "*" operator is used for the search engine to identify the word when it is not complete, "AND" was used to find two different terms and finally "SAME" was used to search for words found in the same sentence. Each search and its combinations were conducted in both Spanish and English. The search engines Google Scholar, Web of Science and Dimensions were chosen. An additional method was the search for articles of interest identified in the reference list of the documents analyzed.

Exclusion criteria

Articles with compatible keywords but not developed in Mexico or in the study area were considered of low relevance and were discarded. At least three databases were consulted and, for the most part, geographic data were taken from these secondary information sources; in addition, data from the visit to the HGOM herbarium were considered. The records of Agave sp. were discarded due to the lack of information they provide for this study.

Collection and systematization of information

Information was filtered by reviewing abstracts and results of articles, particularly focusing on national presence lists, and no restrictions were imposed based on the publication year. These lists were required to include species records per state, their scientific names, and geographical coordinates or the name of the nearest locality. To update the information and avoid synonymies, the scientific name of all recorded species was cross-referenced with the Royal Botanic Gardens Kew website (2022), which displays currently accepted scientific names.

To gather information from secondary sources such as SNIB (CONABIO, 2022) and Naturalista (iNaturalist, 2022), the search included the following criteria: kingdom Plantae, family Asparagaceae, genus Agave, and the state of Hidalgo. Species with a 'degree of investigation' were recorded, indicating proper identification and acceptance by a specialist. For the MEXU (IBUNAM, 2021), the criteria were vascular plant collection, family Asparagaceae, genus Agave, and the state of Hidalgo. Since the search with these parameters yielded no results, the family name was replaced with Agavaceae, resulting in records of specimens collected under that classic denomination.

Based on the gathered information, a data table was constructed, including the following elements: study number, authors, title of the study, publication date, document type (article, thesis, book, list, web), found scientific names, municipality, geographical coordinates, and national and international risk category. The subgenus to which each species belongs, along with the taxonomic descriptor, was also reviewed and included.

Data analysis

A map was created to visualize the species obtained in the review. When a species occurred in more than two locations without georeferences, the geographical coordinates of the municipality with the highest number of records were selected (Figure 1). Subsequently, total number of studies, number of studies with included species lists, overall number of species, and frequency with which these were mentioned in the consulted studies were quantified. Finally, each species with its updated name was cross-referenced with the Mexican Official Standard NOM-059-SEMARNAT-2010 regarding species at risk of extinction (SEMARNAT, 2010), updated as of November 14, 2019, with a modification to normative annex III, as well as the Red List of Threatened Species of the International Union for Conservation of Nature (IUCN, 2023).

Species were considered present in Hidalgo when mentioned in five or more studies. In the same category, some species recorded in four or fewer studies were included if their presence in the region was known from other sources (field validations and herbarium collections). Records with these characteristics were labeled as 'very likely.' A species labeled 'unlikely' was mentioned in one to four studies, and its distribution in the region remained uncertain. Subsequently, a word cloud was generated using the 'wordcloud' package (Fellows et al., 2018) in the R programming language (R Development Core Team, 2012) for visual identification of species with the highest number of records.

Figure 1 Methodological Process Outline for the Systematic Analysis of the State of Knowledge of the Agave Genus in Hidalgo, Mexico. Adapted from Ordóñez-Delgado et al. (2019). ISBN: International Standard Book Number, DOI: Digital Object Identifier, NOM: Mexican Official Standard NOM-059-SEMARNAT-2010; IUCN: International Union for Conservation of Nature. 

Results

Number of studies and records

Table 1 contains data on the diversity of Agave species in Hidalgo, derived from 22 sources of primary and secondary information. Out of the total selected publications, 13 are indexed articles (59 %), mostly presenting lists and catalogs of species per federal entity. Four correspond to digital databases of herbaria and websites (18 %); three are books with ISBNs (14 %), providing information on the presence of some agave species in the region and geographical data. Finally, two referenced studies are undergraduate theses (9 %), primarily focusing on the reproductive biology of some species.

Table 1 Primary and secondary information sources used in the systematic review for understanding the biodiversity of agaves in Hidalgo. 

Study number Species number Reference Title Source of reference
1 15 Gentry (1982) Agaves of continental North America ISBN
2 17 Espejo-Serna and López-Ferrari (1998) Las monocotiledóneas mexicanas: una sinopsis florística ISBN
3 4 Barrios-Rodríguez and Medina-Cota (1996) Estudio florístico de la Sierra de Pachuca, estado de Hidalgo Article
4 8 Villavicencio Nieto and Pérez Escandón (2006) Plantas útiles del estado de Hidalgo Article
5 28 Villaseñor et al. (2016) Checklist of the native vascular plants of Mexico Article
6 11 Peña and Peña (2007) Estudio etnofarmacológico de las diferentes especies endémicas de Agave en la medicina tradicional del estado de Hidalgo Undergraduate thesis
7 7 Pérez-Escandón (2003) Lista de las plantas útiles del estado de Hidalgo ISBN book
8 2 Espejo-Serna (2012) El endemismo en las Lliliopsidas mexicanas Article
9 21 Thiede (2020) Agavaceae: Agave Article
10 1 Villaviencio-Nieto et al. (2010) Plants traditionally used as pesticides in the state of Hidalgo, Mexico Article
11 3 Rojas et al. (2013) Florística y relaciones fitogeográficas del matorral xerófilo en el Valle de Tecozautla, Hidalgo, México Article
12 2 Juárez (2014) The current state of Agave salmiana and A. mapisaga in the valley of Mexico Article
13 10 Rangel (1987) Etnobotánica de los agaves del Valle del Mezquital Undergraduate thesis
14 6 Eguiarte and Sheinvar (2008) Agaves y cactáceas de Metztitlán: Ecología, evolución y conservación Article
15 12 Cornejo-Latorre et al. (2011) Abundancia estacional de los murciélagos herbívoros y disponibilidad de los recursos quiropterófilos en dos tipos de vegetación de la Reserva de la Biosfera Barranca de Metztitlán, Hidalgo, México Article
16 2 Gerardo Salazar (colector, 2009) Herbario de la Universidad Autónoma del Estado de Hidalgo (HGOM) Herbarium specimen
17 35 Comisión Nacional para el Conocimiento y Uso de la Biodiversidad (CONABIO, 2022) Sistema Nacional de Información sobre Biodiversidad (SNIB). Agaves en Hidalgo. Digital database
18 26 iNaturalist (2022) Agaves de Hidalgo Digital database
19 20 Universidad Nacional Autónoma de México-Instituto de Biología (IBUNAM, 2021) IBdata v3 «Helia Bravo Hollis» Herbario Nacional de México (MEXU). Digital herbarium data
20 21 Villaseñor et al. (2022) Riqueza y distribución de la flora vascular del estado de Hidalgo, México Article
21 6 Figueredo-Urbina et al. (2021) Morphological and genetic diversity of traditional varieties of agave in Hidalgo State, Mexico Article
22 37 Villavicencio et al. (1998) Lista florística del estado de Hidalgo Article
Total 293

ISBN (International Standard Book Number).

In the 22 analyzed studies, 293 records were identified, representing 55 species, subspecies, or intraspecific varieties present in the region. The information is summarized in Table 2 and Figure 2. Agave mitis Mart. had the highest frequency of records (19), followed by A. lechuguilla Torr. (17), A. striata Zucc. and A. mapisaga Trel. (15), while A. filifera Salm-Dyck, A. difformis Berger and A. xylonacantha Salm-Dyck had the same number of records (12). Four agaves (A. americana L., A. applanata Hort. ex K. Koch, A. funkiana K. Koch & C. D. Bouché and A. salmiana Otto ex Salm-Dyck) had nine records. On the other hand, there were 10 species with only one record each (A. coetocapnia [M. Roem.] Govaerts & Thiede subsp. coetocapnia, A. debilis Berger, A. horrida Lem. ex Jacobi subsp. horrida, A. parryi Engelm., A. polyacantha Haw., A. scabra Ortega, A. shawii Engelm., A. striata subsp. falcata, A. variegata Jacobi, A. victoria-reginae T. Moore). Nine records were found without identification (Agave sp.) but were excluded. Through a word cloud, Figure 3 illustrates the number of species records based on the size of the font.

Figure 2 Number of articles where Agave species with presence in the state of Hidalgo are mentioned. 

Figure 3 Word cloud of species of agaves recorded in Hidalgo. The symbol ‘-’ was added to subspecies and varieties to recognize them as a single word. 

According to Table 2, most species belong to the subgenus Littaea (28), followed by Agave (20), Manfreda (5), and finally, the natural hybrid Littaea x Agave (1). The information about the group to which A. demeesteriana Jacobi belongs is not clear. Finally, 26 species are classified as 'very likely' to be present in Hidalgo, while 29 are categorized as 'unlikely.' The data reported for species with a 'very likely' distribution include demographic, ecological, and population georeference information that ensures their presence in the region.

Regarding risk categories, A. peacockii Croucher is subject to special protection according to NOM-059-SEMARNAT-2010, and the remaining species are not listed in this standard. In the IUCN Red List (2023), A. albomarginata Gentry and A. macrocantha Zucc. are classified as endangered; A. garciae-mendozae Galván & L. Hern., A. kerchovei Lem., A. peacockii and A. triangularis Jacobi fall under the vulnerable category. Twenty-eight species are classified as least concern, and the remaining 21 species do not have information available in this regard.

Table 2 Species recorded in the systematic review of agave biodiversity in Hidalgo. *Records not considered due to the limited information they provide. 

No. Species/subspecies./var. Subgenus Taxonomic descriptor Municipality with the most records Risk category Source of information1 Presence
NOM-059 IUCN
1 Agave albomarginata Littaea Gentry Huasca No EN 5, 7, 18 Unlikely
2 A. americana Agave Linneo Tizayuca No LC 1, 5, 10, 11, 17, 18, 19, 20, 22 Very likely
3 A. americana subsp. americana Agave Tula No ND 2, 4, 6, 7, 13, 17, 22 Very likely
4 A. americana subsp. protamericana Agave Gentry Eloxochitlán No ND 6, 13, 17, 22 Very likely
5 A. angustifolia Agave Haw Nicolás Flores No LC 5, 17, 18, 19, 20 Very likely
6 A. applanata Agave Hort. ex K. Koch Tulancingo No LC 1,2,5,9,17,18,19,20,22 Very likely
7 A. asperrima Agave Jacobi Ixmiquilpan No LC 17,18 Unlikely
8 A. atrovirens Agave Karw. ex Salm-Dyck Tepeapulco No LC 5,17,18,20,22 Very likely
9 A. atrovirens var. atrovirens Agave Actopan No LC 1, 2, 3, 5, 17, 20, 22 Very likely
10 A. attenuata Littaea Salm-Dyck Metztitlán No LC 5, 18 Unlikely
11 A. coetocapnia subsp. coetocapnia Manfreda Pachuca No ND 9 Unlikely
12 A. debilis Manfreda Berger Zempoala No ND 9 Unlikely
13 A. demeesteriana Jacobi Alfajayucan No ND 17, 18 Unlikely
14 A. difformis Littaea Berger Metztitlán No LC 1, 2, 5, 9, 14, 15, 17, 18, 19, 20, 22 Very likely
15 A. ensifera Littaea Jacobi Pachuca No ND 2, 5, 22 Unlikely
16 A. filifera Littaea Salm-Dyck Zempoala No LC 1, 2, 3, 5, 9, 15, 17, 18, 19, 20, 22 Very likely
17 A. funkiana Littaea K. Koch & C. D. Bouché Alfajayucan No LC 1, 2, 5, 9, 17, 18, 19, 20, 22 Very likely
18 A. garciae-mendozae Littaea Galván & L. Hern. Metztitlán No VU 9, 14, 17, 18, 19, 20 Very likely
19 A. gentryi Agave B. Ullrich Zimapán No LC 5, 9, 18, 19 Unlikely
20 A. ghiesbreghtii Littaea Verschaff. Zapotlán No LC 4, 22 Unlikely
21 A. guttata Manfreda Jacobi & C. D. Bouché Zimapán No ND 9 Unlikely
22 A. “hidalguensis” Littaea No publicado Metztitlán No ND 14, 15, 19 Very likely
23 A. horrida Littaea Lem. ex Jacobi Mixquiahuala No LC 5, 17, 18, 22 Unlikely
24 A. horrida subsp. horrida Littaea Metztitlán No ND 15 Unlikely
25 A. inaequidens Agave K. Koch San Agustín Tlaxiaca No LC 5, 9, 22 Unlikely
26 A. kerchovei Littaea Lem. Metztitlán No ND 1, 2, 5, 15, 17, 18, 20, 22 Very likely
27 A. lechuguilla Littaea Torr. Metzquititlán No LC 1, 2, 3, 4, 5, 6, 7, 9, 11, 13, 15, 16, 17, 18, 19, 20, 22 Very likely
28 A. lophantha Littaea Schiede San Salvador No LC 22 Unlikely
29 A. macroacantha Agave Zucc. Metztitlán No EN 5, 15 Unlikely
30 A. mapisaga Agave Trel. El Cardonal No ND 1, 2, 4, 5, 6, 7, 9, 12, 13, 17, 18, 19, 20, 21 Very likely
31 A. mitis Littaea Mart. Metztitlán No LC 1, 2, 4, 5, 6, 7, 8, 9, 13, 14, 15, 17, 18, 19, 20, 22 Very likely
32 A. obscura Littaea Schiede ex Schltdl. El Cardonal No LC 2, 5 Unlikely
33 A. parryi Agave Engelm. Pachuca No LC 5 Unlikely
34 A. peacockii Littaea x Agave Croucher Mixquiahuala Pr VU 5, 6, 13, 15, 17, 19, 20 Very likely
35 A. polyacantha Littaea Haw. Tepeapulco No LC 17 Unlikely
36 A. salmiana Agave Otto ex Salm-Dyck Epazoyucan No ND 5, 6, 12, 15, 17, 18, 19, 20, 21 Very likely
37 A. salmiana subsp. crassispina Agave Mineral del Monte No ND 1, 2, 3, 6, 7, 9, 13, 17, 21 Very likely
38 A. salmiana subsp. salmiana Agave San Salvador No ND 1, 2, 4, 6, 9, 13, 17, 21, 22 Very likely
39 A. salmiana var. ferox Agave Eloxochitlán No ND 14, 17, 21 Very likely
40 A. scabra Manfreda Ortega Mineral del Chico No ND 9, 20, 22 Unlikely
41 A. schidigera Littaea Lem. Mineral del Monte No LC 17, 18 Unlikely
42 A. shawii Agave Engelm. Pachuca No LC 18 Unlikely
43 A. sisalana Agave Perrine Metztitlán No ND 5, 17, 19, 20 Unlikely
* Agave sp. - - Chilcuautla - - 6, 13, 19 -
44 A. spicata Littaea Cav. Mineral del Monte No ND 2, 5, 8 Unlikely
45 A. striata Littaea Zucc. Mineral del Monte No LC 2,4,5,6,7,9,11,14, 15, 16, 17, 18, 19, 20 Very likely
46 A. striata subsp. falcata Littaea Metztitlán No ND 17 Very likely
47 A. striata subsp. striata Littaea Ixmiquilpan No ND 1, 9, 13, 17 Very likely
48 A. stricta Littaea Salm-Dyck Metztitlán No LC 17, 18, 20 Unlikely
49 A. tenuifolia Littaea Zamudio & E. Sánchez Metztitlán No LC 5, 9 Unlikely
50 A. tequilana Agave F. A. C. Weber Atotonilco de Tula No ND 17, 18 Unlikely
51 A. triangularis Littaea Jacobi Huasca No VU 17, 18 Unlikely
52 A. variegata Manfreda Jacobi El Cardonal No ND 9 Unlikely
53 A. victoria-reginae Littaea T. Moore Zapotlán No LC 17 Unlikely
54 A. x gromeruliflora Littaea (Engelm.) A. Berger Zempoala No ND 20 Very likely
55 A. xylonacantha Littaea Salm-Dyck Metztitlán No LC 1, 2, 5, 7, 9, 14, 15, 17, 18, 19, 20, 22 Very likely

NOM: Official Mexican Standard NOM-059-SEMARNAT-2010 (Pr = special protection); IUCN: International Union for Conservation of Nature (EN = endangered, VU = vulnerable, LC = least concern, ND = no data). 1Source of information corresponding to the list indicated in Table 1.

Time frame of studies and geographic distribution

With respect to the temporal scale, most studies relevant to this research were published between 2004 and 2014. The most recent data corresponds to 2022, and digital databases were only reviewed in 2021. Some of the most recent studies and database records provide relevant information. Figure 4 shows that the species are distributed throughout the entire state but are concentrated mainly in the Biosphere Reserve Barranca de Metztitlán, Valle del Mezquital, and the central part of the region. Specifically, Metztitlán, Ixmiquilpan, and some municipalities near the state capital have the highest number of recorded species. The northeast region (Huejutla, Huehuetla, and Atlapexco) lacks records due to its warm-humid climate (Figure 5).

Figure 4 The frequency of 293 records of Agave species by municipalities in Hidalgo. 

Figure 5 Distribution of the 55 Agave species in the state of Hidalgo according to the records from 22 analyzed sources of information. A: Central Zone; B: Barranca de Metztitlán; C: Valle del Mezquital 

Discussion

This study marks the initial systematic exploration of agave diversity in Hidalgo, based on the review of scientific literature, although the topic has already been addressed in other places (Arulnayagam et al., 2021; Jakobsson et al., 2018; Spafford et al., 2013; Szewczyk & McCain, 2016; Yan & Yang, 2017). These reviews analyzed the available evidence regarding a specific, structured and specific research question, either only in scientific literature (primary) or in any available source such as databases, books, web pages and theses (secondary). The systematic review is qualitative because it shows the evidence in a descriptive way, without a statistical analysis (meta-analysis). Systematic reviews have an explicit and reproducible methodology, provide an accurate and reliable evaluation, and also allow comparison of results between studies; however, they are time-consuming and limited by the quantity and quality of the studies (Aguilera-Eguía & Arroyo-Jofre, 2016). On the other hand, updated species inventories provide information about the distribution of their richness for macroecological analysis and provide tools for planning priority conservation areas. With respect to online databases, their use has expanded rapidly, as the number of species that can be consulted in electronic format has increased since the beginning of the year 2000.

In the present study, one of the advantages of considering both primary and secondary sources of information is that it led to the recording of a greater number of species; in addition, it was visualized which type of source provided more information on the number of records. The primary source providing the highest number of records was the article by Villaseñor et al. (2016), who initially mention 32 species. However, when reviewing the valid and updated names, it was reduced to 28 species reported for Hidalgo; in this case, considering one or the other number will depend on the researcher's criteria. The secondary source of information that provided the most species records was the SNIB online database (CONABIO, 2022) with 35 species; however, this high number is because it includes species outside their natural distribution and, sometimes, these records are an individual of the species in a garden or on a walkside. For instance, A. tequilana Weber serves as an example, being naturally present in Jalisco and less common in Sonora, Sinaloa, Michoacán and Oaxaca (Thiede, 2020). Similar cases occur with A. shawii, as this species is naturally distributed in Sonora, Baja California, Baja California Sur, in addition to California in the United States (Morin et al., 2015). In the case of A. demeesteriana, the species is considered native to Veracruz and Sinaloa, so its presence in other states is still doubtful. Agave ghiesbreghtii Verschaff. according to García-Mendoza (2011), is an agave distributed in Estado de México, Puebla, Oaxaca, and even Guatemala. In the same study, A. triangularis is reported only in the southwest of the country, in Puebla, Oaxaca, and Guerrero.

Finally, A. sisalana Perrine is exclusively recorded in the Yucatán Peninsula (Brown, 2002). For some agaves with one to four records, such as A. victoriae-reginae, A. coetocapnia subsp. coetocapnia, A. parryi, A. debilis, A. guttata Jacobi & C. D. Bouché, A. gentryi Ullrich, A. obscura Schiede ex Schltdl., A. albomarginata y A. ensifera Jacobi field validations of natural populations and more rigorous identifications are recommended. This is particularly crucial for species like A. gentryi, as there are botanical collections deposited in the MEXU herbarium, which were consulted on its website.

Nomenclature Updates

Espejo-Serna (2012) identifies two agave species as endemic to Hidalgo. One of them is A. scabra, and the accepted names database of the Royal Botanic Gardens, Kew, confirms the exclusivity of this plant to the region. The other species is A. mitis var. albidior, but due to recent changes in the nomenclature and taxonomy of this species and subspecies complex, only the name A. mitis is currently considered valid. Consequently, the notion that this species is endemic to the state is dismissed. The decision not to impose restrictions on the publication year was crucial to observe the increasing studies on agaves in the state based on seasonality. On the other hand, this strategy allowed for the observation of changes in some scientific names and rearrangements over the years. However, it also reflects that these taxonomic updates are not always accepted by some more conservative scientists.

The earliest study recorded 15 species distributed in the region (Gentry, 1982) and showed some changes in the nomenclature of only one of them. In contrast, more recent studies (excluding online databases) reported 21 species for Hidalgo (Thiede, 2020; Villaseñor et al., 2022), which also exhibit taxonomic errors. However, these studies assert that their findings are grounded in classifications and nomenclatures. As evident, the magnitude of differences among recorded species is not directly proportional to the difference in years between them, given the 38-year gap between the studies. A. mitis had the highest number of records, being mentioned in 19 out of the 22 sources consulted. Recently, this species has been cataloged with an expanded distribution range, and its name has been modified to account for its subspecies and varieties; it was previously recognized under the name A. celsii Hook (Thiede, 2016).

Geographic Distribution of Agaves in Hidalgo

The georeferences of each record reveal the collecting trends and how geographic information systems are employed for species analysis in the region (Greene & Pick, 2012). In this study, the Metztitlán ravine and the Mezquital Valley have the highest concentration of records.

Out of the 55 species records for Hidalgo, 26 have a category of ‘very likely’ and are naturally distributed in the state. As mentioned, A. lechuguilla was the second most common species in the studies and databases, which is due to its natural history, because of its natural history, as it is a widely distributed, abundant species with large population densities (Gentry, 1982). Furthermore, this species is of importance to some communities in the region, as there is evidence of the use of its fiber to produce bags and cleaning utensils. Agave hidalguensis is also included, which, despite having few records and no formal description, has specimens deposited in herbarium and has been the subject of a study (Eguiarte & Sheinvar, 2008). Other examples of this type are A. salmiana var. ferox and A. americana subsp. protoamericana, since they obtained three and four records respectively, which may be due to a taxonomic bias, but these data are considered reliable due to the information source; in addition, it is known from other sources that these two species of magueys are harvested and managed in the state. Similarly, A. striata subsp. falcata, despite having only one mention, was included in the ‘very likely’ category, because the information source presented field validation of natural populations and other necessary information (Table 2). Finally, the species in the article published by Thiede (2020) do not show detailed geographic information, but despite this, almost all of them fall into the ‘very likely’ category, so they could be a very good reference when consulting about magueyes in Mexico and Hidalgo. Similarly, the digital database of MEXU (IBUNAM, 2021) and the social network Naturalista (iNaturalist, 2022) show a similar number of species.

The results of this review stem from information sources that, despite being useful, should be approached with caution, as they may be subject to three types of bias in inventory data, collections, and lists.1) Spatial Bias: There is a clear tendency for collections to be strongly associated with roads, protected natural areas, and large human settlements. Additionally, less accessible sites are generally less collected and, consequently, less known. 2) Temporal Bias: collected only once at any given locality, making it very challenging to track the presence/absence of the species over time. 3) Taxonomic Bias: There is a clear pattern of collecting and studying the ‘preferred’ species of researchers or the most common and abundant species of economic or cultural importance compared to a collection that includes many species of the same genus. Sometimes dubious or erroneous identifications are made, due to the complexity of distinguishing between species, subspecies and varieties; in addition, synonymies and recently described or not yet formally described species are part of these taxonomic biases (Golubov et al., 2007; Soberón, 1999). If we take these already refined data, Hidalgo can be considered among the states with a considerable number of Agave species (26) if we compare it with Oaxaca, the state with the greatest richness (35 species) of the genus in the country (García-Mendoza & Franco-Martínez, 2018).

Conclusions

Twenty-six species of Agave have a ‘very likely’ distribution in the state of Hidalgo, according to the information available in the records. On the contrary, 29 species mentioned in different studies have 'unlikely' distribution, due to the omission of important data to corroborate their presence. This could be attributed to the fact that they are mentioned only once in older works or included for ornamental purposes.

Acknowledgments

Corresponding authors thank CONAHCYT for their support during the study program.

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Received: June 01, 2023; Accepted: January 19, 2024

*Corresponding author: ga238881@uaeh.edu.mx; tel.: +52 552 092 4118.

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