1. Introduction
Pseudotsuga menziesii (Mirb.) Franco barely survived in Mexico after the last ice age; the gradual increase in temperature forced this species to migrate from south to north and towards higher altitude in the mountains [
1], which resulted in a fragmented and discontinuous distribution. In Mexico, this conifer is mainly distributed in the northern region, although in the central part of the country the species exists in small isolated stands [
2]. At the southernmost limit, two isolated populations are located in the state of Oaxaca [
3,
4].
Added to this, the improper use and exploitation of natural resources affects forest species to the extent that some of them are endangered or threatened [
5,
6]. This is the case of
P. menziesii located in the central region of Mexico, where the species grows in 29 small, fragmented populations suffering high anthropogenic pressure due to land-use changes, overgrazing, forest fires, inappropriate cone collecting, pest attack and illegal tree cutting and timber [
7,
8]. Also, Mexican populations of
P. menziesii are exposed to high environmental stress due to their location at the southern end of its natural distribution [
7,
9]. The above-mentioned situation has caused a reduction in the size and density of populations, as well as low natural recruitment [
8]; these circumstances are causing a reduction in genetic diversity and reproductive capacity associated with increased inbreeding [
2,
10].
P. menziesii is a valuable species for timber and wood production, but in Mexico this conifer is listed as protected by the Mexican government [
11], so it is mainly used for Christmas-tree plantations. Therefore, the protection and proper management of each remaining population of the species is important for both natural recovery and establishment of commercial Christmas-tree plantations. It is imperative to implement
in situ and
ex situ conservation activities to ensure the preservation of the
P. menziesii stands in its natural habitat, thereby allowing continuous evolution of the species and conservation of the remaining gene pool.
When designing conservation strategies for the species, we must understand and prioritize the current extinction risk experienced by the remaining populations. Risk of extinction is related to population viability and can be defined as the probability of the continued existence of populations over specified time periods [
12], which can be estimated by qualitative and quantitative means. It refers to the likelihood of global or local extinction of target taxa. In this sense these authors suggest that no single measure is sufficient to assess population viability (risk) but different pools of data and type of analysis are necessary. Therefore, several methods to assess population risk might exist based on factors that potentially influence the viability of a species and upon its intrinsic characteristics.
The purpose of this study was to estimate, using a multi-criteria analysis technique, the Analytic Hierarchy Process (AHP), the degree of extinction risk faced by each natural P. menziesii population located in Central Mexico (states of Hidalgo, Tlaxcala and Puebla) influenced by anthropogenic, genetic, and environmental factors. Based on AHP, priorities to define a conservation strategy for the species in the region were determined.
3. Results
Four of the twenty-nine evaluated populations (13.8%) had very low risk of extinction showing values less than 0.25 (
Table 6). These populations, Estanzuela, Peñas Cargadas, Presa Jaramillo and Plan del Baile, are influenced to a lesser degree by anthropogenic factors, because the average distance to human population centers is 3.0 km, the average distance to roads is 3.0 km and the main economic activity for the first three populations is tourism and for the last one is forestry. Moreover, there is interest in preserving populations because the owners of the stands established rules for forest use.
Pseudotsuga menziesii is the dominant species in these populations, with healthy trees (free of pests and diseases), ages range from young to mature, and presence of natural regeneration from poor to good.
The average distance to the nearest P. menziesii population is 4.0 km, the average number of trees at reproductive age is over 500, and the average population density is 23 trees ha−1.
Seven
Pseudotsuga populations had low risk with values varying from 0.26 to 0.27, including Cañada El Atajo, Cruz de Ocote, San José Capulines, Capula, Cuatexmola, El Salto, and Villareal (
Table 6). These populations are influenced by anthropogenic factors because the average distance to human population centers is 2.4 km, the average distance to roads is 2.0 km and the main economic activities are agriculture and silviculture. However, the owners have interest in conserving the populations, since 50% of them have a Forest Management Program and the rest are managed under internal rules for forest use. The
P. menziesii trees are young, but some populations are infested by pests and diseases. In these locations, Douglas-fir is the dominant species, but its natural regeneration is scarce, the average distance to the nearest
P. menziesii population is 6.4 km and the average number of trees at reproductive age is 383, while the population density is 18 trees ha
−1.
Seven of the
Pseudotsuga populations were at medium risk with values from 0.28 to 0.30, including Axopilco, Buenavista, San Juan, Tlaxco, Barranca Canoita, Cuyamaloya and Zapata (
Table 6). These populations are negatively influenced by anthropogenic and ecological factors. They are at an average distance of 4.2 km away from human population centers and 3.3 km away from roads, but the main economic activity is agriculture. There is interest by owners to conserve the populations, since 50% of these have a Forest Management Program and the others have at least usage rules of the woodlands. Exotic species, pests and diseases are absent;
P. menziesii trees are mature and dominant, but its natural regeneration is scarce to nonexistent. The average distance to the nearest
P. menziesii population is 5.4 km, the average number of trees at reproductive age is 263 and the population density is 14 trees ha
−1, on average.
Six of the
Pseudotsuga populations were at high risk, with values between 0.31 and 0.34, including La Caldera, El Llanete, Apizaquito, La Rosa, Las Antenas and Tlalmotolo (
Table 6). These populations are strongly and negatively influenced by anthropogenic and genetic factors. They are at an average distance of 3.0 km away from human population centers and 1.8 km away from roads; also the main economic activity is agriculture. The populations are on private land; although some of these have a Forest Management Program and others have rules of use, two of the populations do not have any regulation. Three of these populations showed evidence of pests and diseases. Although
P. menziesii trees are young and mature, they are not dominant and its natural regeneration is scarce. The average distance to the nearest
P. menziesii population is 12.8 km, the average number of trees at reproductive age is 299 and the average population density is 11.8 trees ha
−1.
The five remaining populations had a very high risk, showing values above 0.35, including Tonalapa, La Garita, Minatitlán, Morán and Vicente Guerrero (
Table 6). These populations are strongly and negatively influenced by anthropogenic and genetic factors, with an average distance of 1.2 km away from human population centers and 0.88 km away from roads; in addition, the main economic activity is agriculture. Four of these populations are privately owned and the other is part of an ejido, but none of them has a Forest Management Program. Although these stands varied from young to overmature and they are free from pests and diseases, natural regeneration is lacking and
P. menziesii is not the dominant species. In this group are the smallest populations like Morán, La Garita and Vicente Guerrero with less than 20 reproductive trees; Minatitlán has 45 individuals, and Tonalapa shows 166 individuals of reproductive age. The average population density is 4.6 trees per ha, and the distance to nearest
P. menziesii population is greater than 5 km. Furthermore, in these localities exotic pine species have been introduced through reforestation. A special case is the population of Morán, which is at very high risk. This relict of only four reproductive trees was originally described as
Pseudotsuga macrolepis by Flous [
26]. In addition, the owner is considering cutting down the trees because they are growing too close to his home and he is not interested in preserving them.
4. Discussion
The AHP, a mathematical process for measurement and decision-making, was used to evaluate the risk of extinction of fragmented P. menziesii populations in central Mexico. It allowed us to propose a hierarchy model that incorporates information from anthropogenic, genetic, and ecological factors or criteria, and offer a reference for future studies on the extinction risk of forest populations. The model was built considering elements that according to scientific literature and the authors experience on forest conservation practices are important to assess the risk of extinction of the species of interest in central Mexico. Neither the model, nor the criteria included in it are exhaustive or can be applied to other situations, but they might be used as a starting point to generate similar models for other tree species present in other latitudes.
AHP facilitated the task of calculating different weight values (importance) for each of the criteria identified as relevant for the risk assessment carried out, a critical issue in the modeling process. Both tasks, hierarchy model development and criteria weighting, are not trivial and must be carefully realized, AHP has widely demonstrated its value to perform such tasks [
27,
28].
Despite being a mature decision analysis methodology, the AHP is only one of many possible combinations of methods to standardize, weight, and rank available decision alternatives [
18]. Other approaches to evaluate extinction risk exist, such as the so called population viability analysis [
29]; however, it is also fair to mention that owing to its simplicity, ease of use, and theoretical foundation, the AHP has found wide acceptance among decision-makers [
28]. It helps structure the decision problem in a manner that is simple to follow and analyze. Further, it has proved to be a methodology capable of producing results that agree with the decision-maker’s expectations; that is the case of the study here reported.
Extinction of native forest tree species is caused by various processes, including reduction of and fragmentation of suitable environment, spread of diseases, genetic erosion and inbreeding [
6]. The extinction of species also modifies and alters ecological processes involving it, affecting other species and causing changes in communities and ecosystems [
20]. In the case of the
P. menziesii populations in central Mexico, there is evidence of the effects of fragmentation and isolation by distance (9.4 km average distance between populations) as well as small size, from 4 to 1450 adult trees and 307 trees on average.
It is estimated that coniferous species require a population size of at least 180 reproductive trees to reduce the negative effects caused by low pollen levels and inbreeding, and to maintain seed production at sufficient levels [
30]. In several of the stands included in the current study low natural regeneration of
P. menziesii was observed [
8]. In addition, seeds showed low germination and primary dormancy [
7,
31]. Moreover, a reduced level of genetic diversity with a high proportion of self-fertilization was found [
10,
32].
Habitat fragmentation in most of these populations is due to anthropogenic factors, but there is evidence that other factors such as environment and genetics play important roles in increasing the risks of extinction. The analysis conducted shows the relative effect of each of these factors over the current risks for each population, which is an important step to outline strategies for species conservation in the region. Risk factors for Pseudotsuga menziesii in the study area have their primary origin in the enormous social pressure that persists over populations as a result of historical changes in land use to fulfill human needs in the region, thereby increasing the fragmentation process of habitat.
One way to increase the genetic variability to counteract the effects of inbreeding over reproductive capacity [
33,
34] is through the promotion of gene flow between neighboring populations growing in similar environments (assisted gene flow as defined by Aitken and Whitlock [
35]), which in turn could reduce adaptation problems (outbreeding depression). Populations from similar environments can also exchange genes through assisted migration by creating plantations that use more likely adaptable trees [
32]; an action like this one is certainly possible to be carried out in central Mexico, which would increase genetic diversity by transferring new alleles or increasing the frequency of rare alleles in the recipient populations [
23,
33], and would provide long-term genetic stability to each population and a greater ability for adaptation to climate change or other risk factors. Performing movement of genetic material between related populations would counteract the effects of geographic isolation and fragmentation.
Conservation of remnant populations of
Pseudotsuga menziesii in the central region of Mexico should be carried out in the natural environment where the species develops (
in situ), because this would preserve the natural evolution processes of the species and its interactions with other organisms and ecological processes [
22]. Such a conservation strategy is feasible in central Mexico due to the growing interest in managing the populations of the species as a genetic reserve—due to its current legal protection status. In this sense, the Mexican National Forestry Commission (CONAFOR), a federal agency, is currently promoting local and regional programs in order to enhance forest conservation to preserve the country’s genetic resources.
The five populations with very high extinction risk and the six populations at high risk should have priority for conservation, due to the real possibility of losing their gene pool in case of extreme events. The populations at medium and low risk would also require protective actions such as grazing prevention, pest control and other actions to reduce current risks. Ex situ conservation should be considered as an alternative or complementary resource for populations at high and very high risk.
Other tree species present in central Mexico that are potentially relevant in this context and require studies of extinction risks include: Pinus chiapensis, Fagus sylvatica, and Taxus globosa, all of which have spatial distribution patterns and life history similar to that shown by Pseudotsuga menziesii.