Study area

The state of Hidalgo is located in central Mexico and has a surface area of 20 905.12 km² (^{INEGI, 2016}) (Figure 1). The relief and climate favor the development of ecosystems such as coniferous and oak forests, gallery forests, mountain mesophyll forests, scrubland, pastureland, rainforest and dry forest (^{Inegi, 2017}).

1.- Claro river, 2.- Calnali river, 3.- Calabozo river, 4.- Beltrán river, 5.- Blanco river, 6.- Venados river (Grande-Tulancingo river), 7.- Amajaque river, 8.- Salado river, 9.- Tula river, 10.- Acayuca river, 11.- San Juan river, 12.- Moctezuma river, 13.- Amajac river.

Figure 1 Taxodium huegelii C. Lawson records and main rivers of the state of Hidalgo. 

Presence database

Records of occurrence for the species were documented from field collections and a search of herbaria of public institutions, including: Facultad de Ciencias, Universidad Nacional Autónoma de México (FC-UNAM); Facultad de Ciencias Naturales, Universidad Autónoma de Querétaro (FCN-UAQ); Escuela de Biología, Benemérita Universidad Autónoma de Puebla (EB-BUAP); Instituto de Biología, Universidad Nacional Autónoma de México (IB-UNAM); Departamento de Botánica, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional (ENCB-IPN) and the Instituto de Ciencias Agropecuarias, Universidad Autónoma del Estado de Hidalgo (ICAp-UAEH). Online records were also obtained (The New York Botanical Garden; The United States National Herbarium; University of South Florida) from databases (SEInet) and from the Global Biodiversity Information Facility (^{GBIF, 2020}), iNaturalist (^{Ueda, 2017}), Enciclovida (^{Conabio, 2020a}) and the Global Biodiversity Information Network (Red Mundial de Información sobre Biodiversidad, REMIB) (^{Conabio, 2020b}).

Presence quality control

Data cleaning was carried out by type of error, based on the methods proposed by ^{Cobos et al. (2018)}. The species was searched for in the databases as both T. mucronatum and T. huegelii in order to consider the change of the scientific name. The potential existence of synonyms, different names, or old names was analyzed.

Naturalista's records were validated by analyzing photographic evidence and by remote verification using Google Earth Pro to corroborate that the altitude and geographic coordinates recorded corresponded with the description of the locality.

Geographic distribution modeling

The 19 monthly bioclimatic variables were drawn from the algorithm BIOCLIM (^{Busby, 1991}) (Table 1) of the database of WorldClim version 2.1 (^{Fick and Hijmans, 2017}), representing data for the 1970-2000 period based on precipitation and minimum and maximum temperature. The topographic variable of elevation from the Shuttle Radar Topography Mission (SRTM) was also used (^{Farr et al., 2007}). The above layers are in generic digital Grid format, made up of pixels with a spatial resolution of 30 seconds (equivalent to ~1 km²). The layers were clipped and standardized to the state boundary and converted to ASCII Grid format using the software ArcGIS® version 10.3. (^{Environmental Systems Research Institute [ESRI], 2016}).

The MaxEnt or Maximum Entropy algorithm (Maximum Entropy Distribution Modeling) (^{Phillips et al., 2006}) version 3.4.1 (^{Phillips et al., 2022}), was used to model the potential distribution; this is considered to be the best modeling approach, because it generates greater value of the Area Under the Curve (AUC) from the analysis of the Receiver Operating Characteristic Curve (ROC), that is, it indicates better discrimination of favorable areas versus unsuitable ones for the species, even with few records. It is an adjustment statistic that estimates the probability of occurrence of species, based on environmental requirements and varies between 0 and -1 (^{Phillips et al., 2006}; ^{Hernández et al., 2006}; ^{Pearson et al., 2007}; ^{Kumar and Stohlgren, 2009}). AUC values ≥0.75 represent good model discrimination of surfaces with and without the presence of the taxon of interest (^{Elith et al., 2006}). The logistic model was used with 500 iterations, and the Do Clamping option was deactivated to avoid extrapolating the extreme values of the variables.

Of the total records, 75 % were randomly used for training, and 25 %, for testing (validation); they were resampled by bootstrap, so that the independent covariates were adjusted to the largest number of samples. This technique allows estimating an empirical distribution function by resampling the observed data, and the selected model is not affected by autocorrelation (^{Austin and Tu, 2004}).

The response curves of each variable and their contributions to the habitat model of T. huegelii were calculated using the Jackknife test (^{Phillips et al., 2006}) and Maxent's ROC analysis to evaluate the model.

Maps

In order to prepare the current and potential distribution maps, as well as the calculation of the potential surface area, we used the ArcGIS ^® software, version 10.3. (^{ESRI, 2016}).

Quality control of occurrence records

Of the total number of records, nine (16.36 %) were excluded from the analysis because they did not meet the inclusion criteria. Records for the species were located in 23 of the 84 municipalities of the state (Figure 1). According to the recovered data, Taxodium huegelii is distributed at an altitudinal range of 112-2 472 masl. The documented records are associated with or close to the banks of the Acayuca, Amajaque, San Juan, Tula and Venados rivers (Grande river) (Figure 1).

The potential distribution map (Figure 2) reflects that T. huegelii can be established in 63 municipalities of the state (suitability interval: 0.11-0.92) that coincide with the banks of the rivers: Acayuca, Amajaque, Amajac, Moctezuma, San Juan, Tula and Venados (Grande river).

Figure 2 Potential distribution map of Taxodium huegelii C. Lawson and biogeographic provinces of the state of Hidalgo. 

Estimation of the potential surface area

The potential distribution map (Figure 2) indicated that suitable conditions for the establishment of the species may be present in 1 254.3 km² (6 %) of the total area of the state of Hidalgo, while acceptable conditions exist in 8 362 km² (40 %) (Figure 2).

Biogeographic provinces

According to the map in Figure 2, the presence records and the area where the conditions of suitability for T. huegelii exist are located in the biogeographic provinces of the (Zacatecan-Potosin) Southern Highlands, the Gulf of Mexico, and the Eastern Sierra Madre. In the first, the greatest number of presence records (29) was obtained. In contrast, the biogeographic province of the Trans-Mexican Volcanic Belt lacked records and suitable environmental conditions for the development of the species.

Model evaluation

The model presented an AUC value of 0.921 for the training, and of 0.902 for the test (Figure 3). The environmental variables that contributed most to the prediction (Table 3) were the precipitation of the wettest four-month period (Bio_16), with 24.2 %, precipitation for the coldest four-month period (Bio_19), with 20.5 %, and the minimum temperature of the coldest month (Bio_6), with 20.3 %, followed by the precipitation during the wettest month (Bio_13), with 10.4 %. Altitude (Elev) had little contribution (4.5 %). The results of the Jackknife test indicated that the minimum temperature of the coldest month (Bio_6) was the bioclimatic variable with the highest gain (>0.4) when used independently, followed by the precipitation of the wettest four-month period (Bio_16), the precipitation of the wettest month (Bio_13), and the annual precipitation (Bio_12).

The red line represents the fit of the model to the training data. The blue line represents the fit of the model to the test data, being the actual test of predictive power, and the black line is the expected value if the model were no better than a random one.

Figure 3 ROC analysis. 

The response curves indicated that the habitat suitability of T. huegelii in the state of Hidalgo is high in regions where the minimum temperature of the coldest month (Bio_6) is not lower than 3 °C, and the precipitation of the wettest four-month period (Bio_16), the precipitation of the wettest month (Bio_13), and the annual precipitation (Bio_12) is less than 250 mm, 100 mm and 500 mm, respectively.

Presence record maps

Most of the records and conditions of suitability for the species were concentrated in the biogeographic provinces of the (Zacatecan-Potosin) Southern Highlands and the Eastern Sierra Madre, mainly along the San Juan and Tula rivers; few such records exist in the northern portion, and none in the south of the state despite the presence of rivers (Gulf of Mexico and Trans-Mexican Volcanic Belt biogeographic provinces).

Potential distribution maps

According to the potential distribution map (Figure 2), 23 municipalities have records of the presence of the species, and 31 municipalities have areas of high suitability for its potential distribution (0.59-0.92); of these, 12 have no previous records. There are also suitable conditions for the development of the species along the Amajaque river and other localities; however, no records exist, and therefore it is crucial to carry out more fieldwork in order to verify the veracity of the modeling. The presence of T. huegelii has not been documented along the Beltrán, Blanco, and Claro rivers, consistently with the obtained results, as these areas offer no suitable environmental conditions for the species despite the presence of bodies of water (Figure 2).

The potential distribution of T. huegelii is within the limits of the Eastern Sierra Madre, (Zacatecan-Potosin) Southern Highlands, and Gulf of Mexico biogeographic provinces. The prevailing climate types are Warm humid, Dry warm semi-dry, Dry temperate, Semi-cold semi-dry, and Temperate sub-humid. It has previously been pointed out that T. huegelii is a typical tree of low and semi-warm places, being uncommon in very warm places, at altitudes below 300 m, and at temperatures equal to or above 25 °C (^{Martínez, 1963}), consistently with the results of the present study.

To the north of its distribution in the state, it forms green strips along rivers in dry regions with an arid to semi-arid landscape (^{Farjon, 2017}). In addition to the environmental conditions evaluated in this research, other biotic factors associated with the types of climates in which the species is absent may restrict its geographic distribution.

Evaluation of the AUC model

The model is satisfactory according to the training and test data set (Figure 3), since fit values of 0.921 and 0.902, respectively, were obtained; this implies that the closer the curves are placed, the smaller the error of omission is, and the more appropriate the fit (^{Elith et al., 2006}; ^{Phillips, 2006}). The work of ^{Yi et al. (2016)} cites AUC values of 0.899 for training and 0.840 for testing in Homonoia riparia Lour., a riparian species.

Variables independent contribution to the model

Three of the environmental variables that contributed the most to the prediction are related to precipitation (Bio_16, 24.2 %; Bio_19, 20.5 %, and Bio_13, 10.4 %). Likewise, the response curves indicate that the habitat suitability of T. huegelii in the state of Hidalgo is high in regions where the precipitation of the wettest four-month period (Bio_16), the precipitation of the wettest month (Bio_13), and the annual precipitation (Bio_12) are less than 250, 100 and 500 mm, respectively.

According to the results of this research, most of the documented records are located on the banks of rivers and localities associated with springs in the municipalities of Chapantongo in the El Tanque spa, Epazoyucan in Xolostitla de Morelos, Metztitlán in Zoquizoquipan, Santiago Tulantepec de Lugo Guerrero in Ventoquipa, and Tecozautla in the springs of Taxhido. This is evidence of the close relationship between the development of the species and water sources. The presence of few or only one individual far from water bodies is the result of planting for ornamental purposes.

Since pre-Hispanic times, T. huegelii has been introduced and planted in many locations far from water sources in Mexico and Guatemala; however, all of these places have (or had) water tables that are reached by the deep root system of the trees. Most specimens correspond to planted trees (^{Farjon, 2017}).

^{Villanueva et al. (2010)} point out that the ahuehuetes of Barranca de Amealco, in Querétaro, are very sensitive to the precipitation that occurs in summer and is related to the increase in flow rates that cause an increase in oxygenation and finally greater growth. In addition, seasonal changes of 80 to 90 cm in the water table depth result in temporary reductions in water potential and a maximum net photosynthetic rate of the foliage (^{Campos-Ángeles et al., 2005}).

The distribution of T. huegelii along riverbanks is indicative of riparian vegetation or gallery forest, which is important for maintaining biodiversity (^{Naiman and Decamps, 1997}). During floods, this species traps nutrients and pollutants, in addition to stabilizing sediments, whereby it prevents soil erosion and improves water quality, this is of crucial importance, considering that the Tula river is one of the most polluted rivers in the country (Arredondo et al., 2017). It also reduces the speed of water flow by keeping a sinuous course that favors the recharge of water in the groundwater table at a high level (^{Patten, 1998}); however, when the flow increases, due to prolonged flooding, it can affect regeneration by seeds and shoots (^{Gecy and Wilson, 1990}). Other key factors in the decline of riparian vegetation include soil compaction (^{Kozlowski, 1985}), lack of water, soil infertility, contamination, water scarcity (^{Kozlowski and Pallardy, 1997}), the construction of river terraces (^{Enríquez-Peña and Suzán-Azpiri, 2011}), and climate change.

The suitability of the habitat of T. huegelii in Hidalgo is high in regions where the minimum temperature of the coldest month (Bio_6) is not below 3 °C, consistently with what is cited in the literature in the sense that it is a frost-sensitive species, unlike T. distichum (L.) Rich. which withstands extremely low temperatures (^{Farjon, 2017}), its optimum development interval is between 16 and 22 °C (^{Conafor and Conabio, 2019}). In northern and central Mexico, high temperatures at the end of winter favor its growth during spring (^{Villanueva et al., 2013}). The climatic variables of precipitation and temperature are closely related to the ecophysiology of T. huegelii (^{Fritts, 1976}; ^{Correa et al., 2014}).

Altitude (Elev) contributes 4.5 % to prediction. In this research, the altitudinal range for T. huegelii in the state of Hidalgo was determined to be 112 to 2 472 m, consistently with the previously cited records (^{Martínez, 1963}; ^{Eckenwalder, 2009}; ^{Villanueva et al., 2010}; ^{Farjon, 2017}, ^{Martínez-Sifuentes et al., 2021}).

^{Martínez-Sifuentes et al. (2021)} predict a reduction in the distribution of T. huegelii in Mexico for future climate change scenarios (2050, 2070) under the riparian ecosystem criterion. In Hidalgo, there is no protected natural area that guarantees the conservation of genetic diversity for the species; therefore, the creation of at least one Ecological Conservation Area for the entity should be considered based on future studies of genotypic and phenotypic diversity.

As a riparian species, ahuehuete has a close relationship with bodies of water, which implies that its dispersal maybe much more difficult under climate change scenarios, compared to tree species whose survival does not strictly depend on the presence of bodies of water, therefore, in situ conservation is particularly important for this species.

The location of long-lived organisms is paramount and supports the continuation of efforts for the protection, restoration, formulation of ecotourism projects and conservation of the large extension of unique riparian ecosystems in Mexico in which T. huegelii is distributed (^{Villanueva et al., 2010}; ^{Villanueva et al., 2012}). In Mexico City, it is used as an indicator of surface aquifers (^{Martínez and Chacalo, 1994}). In the case of ahuehuetes, historical records allow to determine the seasonal variation of precipitation based on dendrochronology (^{Cortés et al., 2010}; ^{Correa-Díaz et al., 2014}); such is the case of the climatic conditions prevailing during the establishment, flourishing, and decline of pre-Hispanic civilizations (^{Villanueva et al., 2010}).

The ages of ahuehuete trees in gallery forests in Hidalgo have been little studied (^{Correa-Díaz et al., 2014}) and remain virtually unknown. Among the states in which such data for T. huegelii individuals are available, the following can be cited: Aguascalientes, Chiapas, Coahuila, Guanajuato, Jalisco, Michoacán, Nuevo León, Oaxaca, Querétaro, Tamaulipas and Zacatecas (^{Suzán-Azpiri et al., 2007}; ^{Villanueva et al., 2010}).