Materials and methods

Study area. The study was conducted in the Yucatan dry forest and dry forest with columnar cacti near the coastal region, particularly in areas with rock outcrops in the north of the Yucatan peninsula, Mexico (Figure 1). The region is characterized by a strip of arid, warm climate (BS), which includes some climatic subtypes (for details, see ^{Orellana et al. 1999}). Three seasons are characteristic in the region: i) dry, ii) summer rains, and iii) winter rains or “nortes”. The dry season extends from March to May, with an average precipitation up to 30 mm and a maximum temperature of 35.7 ºC. The summer rainy season spans from June to October, with an average precipitation of 141.2 mm, while the winter rainy season ranges from November to early February and is characterized by cooler winds accompanied by low atmospheric pressure, average temperatures of 24.6 ºC, and an average precipitation of 63 mm (^{SMN-CONAGUA 2022}). The geological surface of the Yucatan peninsula is represented by extensive shell-rich deposits of the Quaternary, mainly from the Holocene, that form sandy beaches and marshy sedimentation basins in marshes and estuaries (^{Duch-Gary 1991}). In contrast, the northern Yucatan peninsula, very close to the coastline, is characterized by the exposure of an early Miocene-Pliocene carbonate rock recognized as “coquina”, which is associated with the Carrillo Puerto geological formation. The coquina is characterized by its conspicuous mollusk macrofossils (which lends it the name) and a cracked surface with irregular cavities of different sizes (^{Miranda-Huerta 2005}, ^{Shen et al. 2013}).

Figure 1 Map of Mexico and the Northern Yucatan peninsula. A) Study area located to the north of the Yucatan peninsula (delimited by a rectangle). B) showing the approximate distribution of the Seasonally flooded Coquinal (SFC) (orange shaded area). Red polygons represent selected Coquinal areas, but with improved characterization based on multitemporal LANDSAT remote sensing images. Arrows indicate sites sampled in this study. 

Vegetation classification. The characteristics and criteria for an appropriate classification of this plant association were determined following the system of classification of the vegetation of Mexico SECLAVEMEX (Standardized Hierarchical Mexican Vegetation Classification System) (^{Velázquez et al. 2016}).

Vegetation sampling. We identified areas with exposed coquina-type rock outcrops where vegetation sampling was carried out. Six sites without apparent anthropogenic disturbance were selected covering the entire area where coquina outcrops exist (about 230 km). The average distance between sites was 46 km (range 8-125 km; Figure 1). Although we observed that in the sampled sites the richness and diversity of species are different, the comparison between them was not the objective of this work. We established two linear 50 m transects at each site and perpendicular sub-transects of 10 × 2 m at 10 m intervals on alternate sides of the main transect (six in all, as the first was laid out at 0 m). The identity and quantitative parameters (species richness, abundance, and plant coverage) within each sub-transect were recorded. The two main transects of each site were separated by 50 m. This sampling effort has been previously shown to capture plant species richness and abundance in these sites accurately (^{Espejel 1984}, ^{Torres et al. 2010}, ^{Angulo et al. 2018}). We recorded trees, shrubs, and due to the nature of the site, we were able to discern individuals in clump of grasses. Vines and epiphytes were recorded for richness, but not included in the analysis of abundance and plant coverage.

Taxonomic identification, classification, and species dominance. We used The World Flora Online (www.worldfloraonline.org) and ^{Carnevali et al. (2010}) as a base for correct taxonomic nomenclature. Some scientific names have been updated, such as those related to Caesalpinia Plum. ex L. and Prosopis L. (^{Gagnon et al. 2016}, ^{Hughes et al. 2022}). Plant samples not recognized in the field were identified using specialized literature and/or morphologically comparing them with those housed at herbarium CICY. The first set of vouchers were later deposited at CICY whereas duplicates were sent to GH, MEXU, MO, SEL, UADY, and XAL (acronyms according to ^{Thiers 2023} [continuously updated]). The recorded species were arranged alphabetically; classification and nomenclature closely follow the Angiosperm Phylogeny Group (^{APG IV 2016}). The quantitative parameters previously mentioned were used to estimate the Importance Value Index (IVI; ^{Curtis & McIntosh 1950}) to understand the local ecological value of each species recorded. The IVI was calculated as the sum of the relative values of frequency, density, and coverage (^{Curtis & McIntosh 1951}), where the relative frequency is the number of occurrences of one species as a percentage of the total number of occurrences of all species, whereas the relative density is the number of individuals of one species as a percentage of the total number of individuals of all species and finally the relative dominance is the total area coverage of one species as a percentage of the total area coverage of all species. Coverage was estimated using the formula for the area of an ellipse.

Conservation status. The conservation status of the species recorded in the study was estimated based on information about each species from the IUCN Red List database (^{IUCN 2021}) and ^{Carnevali et al. (2021}). Species were assigned to the IUCN categories, depending on their estimated threat level following the IUCN criteria. Species without available information were treated as Not Evaluated (NE) (Table 1).

Results

Floristic characterization and species dominance. Our results recorded a total of 214 species (206 identified to species) belonging to 58 families and 164 genera of vascular plants (Table 1). Marsilea vestita Hook. & Grev. var. vestita was the only fern recorded. Herbs were the group with the highest number of species (46 %), followed by trees (22 %) and shrubs (14 %), while epiphytes and parasites were the least represented groups were the least represented group, with 3 %. Vines and cacti are important and distinctive groups, with 11 and 4 %, respectively. Like most vegetation communities within the Yucatan peninsula, Fabaceae was the most representative plant family, with a higher number of species for trees (21) and shrubs (four), followed by Euphorbiaceae with nine species (three trees and six shrubs). Poaceae (13 species), Cyperaceae, and Malvaceae (seven species each) were the most representative families of herbs (Table 2). Euphorbia L. and Ipomoea L. were the most representative genera, with five species each, followed by Portulaca L. and Eragrostis Wolf with four species each (Table 2).

Five species showed the highest IVI (> 7), with Sida ciliaris L. as the species with the highest IVI value (IVI = 55.58), followed by Haematoxylum campechianum L. (IVI = 16.04), Stachytarpheta angustifolia (Mill.) Vahl (IVI = 8.37), Agave angustifolia var. angustifolia (7.42), and Cienfuegosia yucatanensis Millsp. (IVI = 7.36) (Table 1). Seventy-eight species had an IVI value greater than one, while 107 species recorded an IVI smaller than one (Table 1).

Vegetation classification. We propose the use of the term Seasonally Flooded Coquinal (SFC), to refer to this distinctive plant association. We classified the SFC as a subassociation of the tropical dry forest and particularly of the TDFCC based in the substratum, in which the predominance of the “coquina” stands out, preventing the filtration of water to the subsoil and remaining flooded during the rainy season. The SFC is a mosaic-like assemblage of continuous open, seasonally flooded areas, dominated mainly by herbs, with patches of woody vegetation of small trees and shrubs, including succulent plants (Figures 2A-C, 3A, B, G). Although its plant diversity is very similar to that of other regional dry forests as the tropical dry forest and the TDFCC, at least two species, Zephyranthes orellanae Carnevali, Duno & J.L. Tapia and Ipomoea sororia D.F. Austin & J.L. Tapia are endemic to this plant association. In addition, there are diagnostic plant species that give identity to the SFC such as Cienfuegosia yucatanensis, Portulaca halimoides L., Stachytarpheta angustifolia, Justicia sp. nov. (publication in process), and Angelonia parviflora Barringer. Except for the last two species, which are endemic to the Yucatan Peninsula Biotic Province (YPBP), they are not exclusive to this region. However, in the north of Yucatan the presence of them is commonly associated with the SFC. Furthermore, the SFC is the only type of vegetation where all these taxa occur together, which renders their co-occurrence diagnostic for the vegetation type.

Figure 2 General view of the Seasonally flooded Coquinal (SFC) and some representative species. A. Panoramic view of the SFC in the dry season (Telchac Puerto). B. Panoramic view of the SFC in the wet season with Cienfuegosia yucatanensis Millsp. (Malvaceae), and Stachytarpheta angustifolia (Mill.) Vahl. (Verbenaceae) (El Corchito). C. Panoramic view of the SFC in the wet season with Sesbania herbacea (Mill.) McVaugh (Fabaceae) (El Corchito). D. Justicia sp. nov. (Acanthaceae; in process of publication) E. Angelonia parviflora Barringer (Plantaginaceae). F. Zephyranthes orellanae Carnevali, Duno & J. L. Tapia (Amaryllidaceae). Photos. A; Gustavo A. Romero González. B-E: Claudia J. Ramírez, F: Mayte del R. Aguilar Canche. 

Figure 3 Some species of the Seasonally flooded Coquinal (SFC). A. Acanthocereus tetragonus (L.) Hummelinck (Cactaceae). B. Landscape within the SFC with Agave angustifolia Haw. var. angustifolia (Agavaceae) (Telchac Puerto). C. Cyrtopodium macrobulbon (La Llave & Lex.) G. A. Romero & Carnevali (Orchidaceae) growing under Jatropha gaumeri Greenm. D. Ipomoea sororia D.F. Austin & J.L. Tapia (Convolvulaceae). E. Cuphea gaumeri Koehne (Lythraceae). F. Portulaca rubricaulis Kunth (Portulacaceae). G. Mammillaria gaumeri (Britton & Rose) Orcutt (Cactaceae). H. Jatropha gaumeri Greenm. (Euphorbiaceae). Photos. A, D, E, H. Claudia J. Ramírez. B. Diego F. Angulo. C. Rodrigo Duno de Stefano. F-G. Mayte del R. Aguilar Canche. 

Conservation status. Of the 206 species recorded and identified in this study, 111 have not yet been evaluated by the IUCN, while 84 are listed in the Least Concern (LC) category. Ten species are listed in a risk category: Three (Zephyranthes orellanae, Lobelia yucatana E. Wimm, and Senna pallida (Vahl) H.S. Irwin & Barneby var. gaumeri (Britton & Rose) H.S. Irwin & Barneby are considered Endangered (EN), six have been assigned the Near Threatened (NT) category, and Ipomoea sororia and Gossypium hirsutum Cav. have been classified as Vulnerable (VU). We recorded two endemic species to the SFC (Zephyranthes orellanae and Ipomoea sororia), whereas we also recorded twenty-eight species endemics to the YPBP. Diphysa yucatanensis A.M. Hanan & M. Sousa is quasi-endemic (with a few populations beyond yet near the border of the province (Table 1).

Heteranthera yucatana Carnevali, J.L.Tapia & J.R.Grande was not included as an endemic species of the SFC because it was not collected either in the transects or in surrounding areas. It is rare and seasonal species associated with muddy soils in peripheral areas of the SFC.

Discussion

Seasonally flooded Coquinal. Although this plant association is widely recognized by local botanists (^{Duno 2017}, ^{Pérez-Sarabia et al. 2017}, ^{Carnevali & Tapia-Muñoz 2017}, ^{Ramírez-Morillo 2019}, ^{Aguilar-Canché et al. 2022}), very little has been done to document and thus protect it.

The results in our study clearly suggest that SFC represent an important area of plant biodiversity with local and peninsular endemism, which deserves to be preserved. Based on ^{Velázquez et al. (2016)} we recognize the SFC as a tropical dry deciduous shrubland; sub-spineless, microphyllous, non-succulent, with a series of Fabaceae associations dominating the landscape. Sida ciliaris and Haematoxylum campechianum as dominant floristic subassociation, and Zephyranthes orellanae and Ipomoea sororia as unique and characteristic species, while exposed coquina-type rock outcrops conform substratum subassociation.

Soil Features.- Several classifications of vegetation types have been proposed in Mexico (^{Miranda & Hernández-X 1963}, ^{Gómez-Pompa 1965}, ^{Rzedowski 1978}, ^{González-Medrano 2003}). More recently, efforts have been made to establish criteria that allow better organization and standardization of the types of vegetation proposed over time (e.g., ^{Faber-Langendoen et al. 2014}, ^{Velázquez et al. 2016}).

^{Miranda (1958)} classified some characteristic plant associations of the Yucatan peninsula as non-optimal primary associations (“edaphic associations” of ^{Holdridge 1967}), referring to plant associations that grow on soils or localities with less than favorable conditions. The SFC is undoubtedly a non-optimal ecosystem sensu^{Miranda (1958)}, and a tropical dry deciduous shrubland according to ^{Velázquez et al. (2016)} determined by the edaphic conditions and local climate (i.e., rock outcrops or rock outcrops + floods). Other non-optimal ecosystems sensu^{Miranda (1958)} or subassociations sensu ^{Velázquez et al. (2016)} are also associated with the coast (e.g., tintal, associated mainly with the presence of Haematoxylum campechianum; carrizal, associated mainly to Phragmites australis (Cav.) Trin. ex Steud., saibal, associated mainly with Cladium mariscus subsp. jamaicense (Crantz) Kiik., and tular, associated mainly with Typha domingensis). However, no previously described vegetation association in Mexico matches the characteristics and conditions of the SFC. ^{Beard (1944}, ¹⁹⁵⁵⁾ proposed a classification system for tropical vegetation in America, which describes a plant association in the Guianas called "Rock Pavement Vegetation", growing on hard sandstone rock plates and granite outcrops (the Roraima formation) with scattered herbaceous and woody plants of less than two meters of height. In contrast, the SFC has shallow soils with outcrops of a highly permeable carbonated rock shell associated with the Carrillo Puerto geological formations, including bound stones or wackestones containing embedded fossils of mollusks, mainly bivalves and gastropods (^{Miranda-Huerta 2005}, ^{Shen et al. 2013}). Rocks show surface cracks and cavities of different sizes, along with slight depressions and elevations that possibly determine the vegetation dynamics in the area.

Environmental conditions and plant associations.- The seasonality that characterizes the Yucatan peninsula with a dry season, a summer rainy season, and a winter rainy season influenced the dynamics of its plant populations (^{Flores & Espejel 1994}, ^{Islebe et al. 2018}, ^{SMN-CONAGUA 2022}). This seasonality has a greater impact on the SFC, where the rainy season starts slightly later and, therefore, receives lower rainfall averages compared to the surrounding communities (^{Flores & Espejel 1994}).

Two main structural elements can be recognized within the SFC. First, an open area with rock outcrops; during the rainy season, this area is flooded by a water layer of approximately 10-50 cm depth in which Cyperaceae and Poaceae thrive, along with other herbs and suffrutices up to one-meter high. In these flood-prone areas, hydrophilic or flood-resistant species grow seasonally, giving a distinctive profile to the area (see Figure 2 B, C). Species adapted to anaerobic or hydric stress conditions, such as Zephyranthes orellanae, Cienfuegosia yucatanensis, Ipomoea sororia, and Stachytarpheta angustifolia, are abundant in flooded soils during the rainy season, but are difficult to observe during the dry season since they have either an annual life cycle (e.g., S. angustifolia) or persist through underground storage structures such as bulbs (e.g., Z. orellanae) and specialized roots (e.g., C. yucatanensis). Sesbania herbacea (Mill.) McVaugh is infrequent within the SFC, but can be highly abundant in flood-prone areas where it is usually found. The second structural element comprises patches of different sizes (commonly from 1 to 5 m in diameter, occasionally larger) on “islands” of imperceptibly higher microrelief that do not flood, with shrubs and trees such as Bursera simaruba Sarg., Ipomoea carnea Jacq. subsp. carnea, Jatropha gaumeri Greenm., Neltuma juliflora (Sw.) Raf. var. juliflora, and Pithecellobium unguis-cati. These species frequently serve as nurse plants for cacti, including species such as Acanthocereus tetragonus, Opuntia inaperta (A. Schott ex Griffiths) D.R. Hunt, and Opuntia stricta (Haw.) Haw., and the orchids Cyrtopodium macrobulbon (La Llave & Lex.) G.A. Romero & Carnevali and Myrmecophila christinae Carnevali & M. Gómez, all of which frequently grow on the periphery of these vegetation patches where light irradiance is higher. Agave angustifolia var. angustifolia is an abundant and distinctive species, particularly when in its reproductive phase, due to its long, conspicuous inflorescences and flowers, which can be found in both environments just described (Figure 3B).

Species dominance.- The Importance Value Index (IVI) has been used in different research areas such as pharmacology and ethnobiology (e.g., ^{Dhar et al. 2000}, ^{Guèze et al. 2014}), but is most widely used for assessing the ecological importance of plant species (e.g., ^{Tadele et al. 2014}). In the present study, the species featuring high IVI values cover a large proportion of the area in the plant community (Table 1). For example, Sida ciliaris, which yielded the highest IVI value, is a small herb that is common and widespread in open areas, while the logwood tree (“palo de tinte”; Haematoxylum campechianum), the species with the second highest IVI value, is a medium height erect to prostrate shrub or tree with a wide crown that is common in the seasonally flooded patches of the SFC. Other species with high IVI values were Ipomoea carnea subsp. carnea, a shrubby vine that can cover extensive areas, growing from suberect to prostrate on the ground or on bushes, and Cienfuegosia yucatanensis, that remains leafless for most of the year but that is conspicuous in flooded sites, within the SFC, during the rainy season. Species endemic to the YPBP and listed as Threatened, such as Mammillaria gaumeri, Ipomoea sororia, and Zephyranthes orellanae, had a relatively high IVI values, so they are species ecologically important within the YC. However, more than 70 % of the endemic species to YPBP had an IVI less than one, which indicates that they are ecologically scarce or rare (^{Rabinowitz 1981}, ^{Ahmed et al. 2020}). Likewise, endemic species to YPBP included in the Least Concern category, such as Jatropha gaumeri, Opuntia inaperta, Havardia albicans, and Cuphea gaumeri Koehne, also obtained high IVI values (Table 1). These endemic species occur in the north of the Yucatan peninsula, not only in the SFC, but also in surrounding vegetation, mainly the TDFCC and the coastal dune shrubland.

Conservation status and threats to the SFC. The Yucatan peninsula contains a remarkable concentration of tropical dry forest (^{Miles et al. 2006}, ^{Carnevali et al. 2021}), which has been referred to as probably the most threatened forest type, with projected low climatic stability (unstable climatic conditions) in the next 20 years (^{Janzen 1988}, Miles et al. 2006, ^{Pennington et al. 2018}, ^{Mesa-Sierra et al. 2022}). Moreover, tropical dry forest is one of the least protected biomes in Mexico (^{Koleff et al. 2009}, ^{Mesa-Sierra et al. 2022}), so actions to increase our knowledge and improve its conservation are necessary to warrant its short, medium, and long-term survival. In addition, the SFC is among the most highly threatened natural plant communities within the YPBP for several reasons. It is located between Merida -one of the main cities- and Progreso -one of the most important harbors- in the southeast of Mexico. In recent decades, both the city and the port have been growing vigorously, exerting increasing pressure on the TDFCC and, particularly, the SFC. The advancing coastal urbanization and, therefore, the growing population living in coastal cities is a global trend that has advanced exponentially in recent decades (^{Barragán & de Andrés 2015}). On the other hand, the increasing socioeconomic importance of coastal areas, mainly associated with the recent expansion of tourism (^{Elliott et al. 2020}), has also had adverse consequences on natural ecosystems. The Yucatan coasts are no exception to this issue, particularly in the geographically restricted SFC, currently being a major tourist attraction for locals and foreigners that has promoted urban growth, causing adverse environmental impacts on the plant and animal communities of the coast and adjacent areas (unpublished data). Finally, small-scale cattle-ranching and “traditional agriculture systems” = (Cucurbita spp.) and, along with natural events such as storms and hurricanes and the high incidence of natural and arson fires, cause adverse impacts on the natural communities of the SFC.

Despite its small geographic area (900 km² approximately), the SFC hosts a high diversity of plant species, two of which are endemic to the SFC and some 25 endemics to the YPBP, some of which are featured in the IUCN red list. However, the lack of its acknowledgement as a highly threatened plant associations, coupled with the fact that has it has mistakenly been thought of as a highly degraded successional stage of the tropical dry forest and of the TDFCC, has made it difficult to establish mechanisms and policies for its protection and conservation. Although there are some sites featuring coquina outcrop in the northwestern edge of the SFC that are located within the “Ciénegas y Manglares de la Costa Norte de Yucatán” state reserve, to date, the TDFCC and the most of the SFC areas are not included in any Mexican conservation initiatives, and their ecological fragility merits high priority for conservation to prevent the loss and extinction of its unique assemblage of species.