An Updated Review of Dendrochronological Investigations in Mexico , a Megadiverse Country with a High Potential for Tree-Ring Sciences

Dendrochronology is a very useful science to reconstruct the long-term responses of trees and other woody plants forming annual rings in response to their environment. The present review considered Mexico, a megadiverse country with a high potential for tree-ring sciences given its high climatic and environmental variability. We reviewed papers considering Mexican tree species that were published from 2001 to 2016. Most of these studies examined tree species from temperate forests, mainly in the pine and fir species. The review included 31 tree species. The most intensively sampled family and species were the Pinaceae and Douglas fir (Pseudotsuga menziessi (Mirb.) Franco), respectively. Some threatened tree species were also studied. Dendrochronological investigations were mainly conducted in northern and central Mexico, with Durango being the most sampled state. The reviewed studies were mostly developed for hydroclimatic reconstructions, which were mainly based on the tree-ring width as a proxy for the climate. Tree-ring studies were carried out in both national and foreign institutions. Our review identified relevant research gaps for dendrochronologists such as: (i) biomes which are still scarcely studied (e.g., tropical dry forests) and (ii) approaches still rarely applied to Mexican forests as dendroecology.


Introduction
Dendrochronology is the science studying annual growth rings in trees and other woody plants by relating characteristics of these rings with the environmental conditions in which they were formed [1].The features of tree rings constitute an indirect source for understanding the historical characteristics of the environment in which trees have grown [2].Usually, sensitive tree species are chosen because they form annual growth rings with certain amount of variability, which allows for synchronizing tree-ring series of different trees growing at the same site.In this way, the targeted tree species should be able to record different types of temporal signals in their rings due to the variability of environment conditions, especially the climate [3][4][5].
One of the first dendrochronological investigations was carried out in America by Andrew E. Douglass, who found a clear dependence between the width of growth rings in pine species from the southwestern part of United States of America (USA) and precipitation [6].Other early contributions to tree-ring sciences in the neotropical regions were based on quantifying the activity of the vascular cambium as related to climate [7] or in the study of specific tree species, often considering their cambium phenology [8,9].In the southern part of America, one of the first tree-ring studies examined Cedrela fissilis [10].As the species and site conditions of the earliest dendrochronological studies developed in the southwestern part of USA are similar to those encountered in many northern Mexico forests, this promoted the theory that Douglass' school, including disciples such as E. Schulman, pioneered tree-ring studies in semi-arid northern American forests [11].
This research along with others stimulated the birth and development of dendrochronology, which promoted the realization of new studies mainly applied to reconstruct climate (dendroclimatology) [12].Some of these studies are being developed in Mexico [13].
Mexico is considered one of the main Latin-American countries with a higher potential for dendrochronological investigations, due to its high environmental and climatic heterogeneity.These conditions result in a high diversity of gymnosperm (pines, firs and cypresses) or angiosperm tree species (oaks), which often show a high longevity [14][15][16].The first dendrochronological studies of Mexico were carried out in places close to El Salto (Durango) city for some species of pines [11].In the last decades, a large number of studies have been carried out, mainly focusing on dendroclimatology [17][18][19].
Although these studies are becoming more numerous in Mexico, we still do not know the state of the art in this scientific field.To our knowledge, there is no report that documents the current situation in the country of dendrochronology and the perspectives offered by dendrosciences.The systematization of this collection in a database would provide an overview to identify the background, knowledge gaps and trends that research has taken depending on the tree species, scientific scope, geographical region and type of ecosystem among other specific data.This constitutes a starting point for researchers interested in further developing dendrosciences in Mexico.
The objective of this study was to analyze the dendrochronological investigations that have been performed in Mexican terrestrial ecosystems, based on an exhaustive literature review to generate a diagnosis and synthesize the dendrochronological perspectives in this megadiverse country with a great tradition in forestry and ecology.In general, we expected to find more conifers and deciduous broadleaf tree species from seasonal climate zones in these studies.This is due to their growth rings being better defined, which facilitates their synchronization or cross-dating and subsequent measurement, compared with tropical forests in which tree-ring delimitation and cross-dating are not so simple [1,20,21].

Materials and Methods
A bibliographic research of scientific articles developed in the subject of dendrochronology was done, using scientific Internet searcher engines (Web of Science-Thomson, Scopus, Science Direct, Google Academic, Redalyc).The research was performed considering studies published between the years of 2001 and 2016.
From the research, a bibliographic database was built and analyzed, containing the following fields of information: vegetation type based on the classification of Land Use and Vegetation of the National Institute of Statistics and Geography (INEGI), studied tree species, site data (state, geographic coordinates and altitude), study objective and scope, journal where the study was published and measured variables (tree-ring width, earlywood and latewood widths, length of the series or chronologies) as well as the institution where the investigation was conducted.

Results
A total of 55 articles were found in indexed journals (see the complete list in the Appendix A).These studies were carried out at altitudes ranging from 1300 to 4000 m above sea level (Figure 1).More than half of the studies (53%) were carried out in forests located at more than 3000 m of elevation.Dendrochronological studies have been developed in seven different types of vegetation (Figure 2).Among them, 48% of the studies were developed for the pine species found within pine forests, which were the most studied type of vegetation, followed by the oyamel forest (Abies religiosa (Kunth) Schltdl.& Cham.) in 24% of the studies.The pine-oak forest was found in 14% of the studies and the gallery forest accounted for 8%.The types of vegetation that were less frequently studied included mountain mesophilous forest, coniferous scrubland and subtropical scrubland, with 2% of studies carried out in each one.Dendrochronological studies in Mexico examined 26 tree species, which were distributed in five families.The species of the Pinaceae family accounted for 82% of the studies, those of the Cupressaceae family accounted for 13%.Finally, the families Oleaceae, Fabaceae and Fagaceae were only considered in 2% of the studies for each family (Figure 3).The most studied genera were Pinus, Taxodium, Pseudotsuga and Abies.Pinus was the most intensively studied (16 species), showing concordance with the great diversity of this genus present in Mexico that represents a world center in the diversity of pines [22].The studied species and their frequency are reported in Figure 4.The tree species with a greater number of studies is P. menziesii (16 studies), which is considered as one of the most important species in dendrochronology due to its climate sensitivity, good cross-dating and wide geographical distribution [23].Another tree species frequently studied was Pinus cooperi C.E. Blanco (11 studies), which also has remarkable dendrochronological potential [24][25][26][27].These two species were followed by Pinus hartwegii Lindl.and Taxodium mucronatum Ten.(5 studies).
There were six species studied that fall within a category of risk such as endangered (P) or subject to special protection (Pr) according to the Official Mexican Standard 059 [28]: Abies concolor Lindl.(Pr), Juniperus monticola Martínez (Pr), Pinus jeffreyi Balf.(Pr), Pinus lagunae (Rob.-Pass.)Passini (Pr), P. menziesii (Pr) [29] and Pinus pinceana Gordon & Glend.(P) (Figure 4).This section may be divided by subheadings.It should provide a concise and precise description of the experimental results, their interpretation as well as the experimental conclusions that can be drawn.
From the geographical point of view, dendrochronological studies in Mexico have been carried out in 20 states.Durango is the state most intensively sampled, followed by the states of Mexico, Chihuahua and Coahuila (Figure 5).These studies focused on the northern and central mountainous areas of the country, mostly in the Sierra Madre Occidental complex, which contains many temperate forests.A few studies in tropical ecosystems were found, whose research can be considered incipient in relation to other Latin-American countries [16,21,30,31].Regarding the temporary evolution, we observed an ascending tendency of the number of annual studies (n = 12) in the year 2016, with years 2003 and 2013 having more studies performed compared to the previous ones (n = 4 and 9 studies, respectively) (Figure 6).
In relation to the field of application, most of the studies have been developed with a climatic objective (n = 30 studies), usually for reconstructing precipitation.This is followed by those developed in the ecological (n = 23 studies) and hydrological (n = 3 studies) fields (Figure 7).A few studies were carried out in rarely explored fields, such as dendrogeomorphology or dendrochemistry (see Appendix A).The journals in which the greatest numbers of Mexican dendrochronological studies have been published are mostly national journals covering 40% of the studies, such as: Madera y Bosques (n = 9 studies), Revista Chapingo-Serie Ciencias Forestales y del Ambiente (n = 5 studies), Agrociencia (n = 4 studies).This is followed by international journals, such as Dendrochronologia or Tree-Ring Research, which represent the remaining 60% of the studies (Figure 8).Dendrochronological studies have been carried out including measures of width of earlywood (EW), latewood (LW) and tree-ring width (TRW).A total of 37 studies were found for the case of TRW, while 7 studies were detected for EW.For LW, only 1 study was found.Some studies analyzed several of these variables (Figure 9).A few studies considered other variables, such as carbon and oxygen isotopes, wood density or scars due to fires or volcanic activity (see Appendix A).The studies considered chronologies or mean series of tree-ring variables of different lengths or amplitudes, ranging from 49 to 607 years.Most studies are concentrated in an amplitude of 100 to 300 years (Figure 10).This is because some trees have sufficient longevity to contribute to the reconstruction of climatic events over a wide period of time.This is the case for the earlywood chronologies of up to 554 years of the extension of P. menziesii developed by Villanueva-Díaz et al. for temperate forests located in northern Mexico [24].The species that present a greater climatic sensitivity, quantified as correlations between climatic variables and tree-ring width, were P. menziesii, T. mucronatum and P. cooperi.
A total of 69% of the dendrochronological research was generated in Mexican institutions (Figure 11), with almost 60% concentrated in two of the nine national centers where the research was carried out, namely the National Institute of Forest, Agriculture and Livestock Research (INIFAP) located in Gómez Palacio (Durango) and the Juarez University of Durango State [32,33].Of the national institutions, 71% correspond to educational centers and 31% to research centers.In Mexico, INIFAP is one of the few laboratories with a long tradition in dendrochronology.In other studies, such as Díaz et al. [34], Sheppard et al. [35] or González-Cásares et al. [36], some parts were conducted in overseas laboratories located mainly in United States of America (USA) and Europe.In USA, the universities of Northern Arizona, Arizona and Arkansas were the institutions in which a greater number of studies were carried out.The University of Arizona is considered as a pioneering center in conducting studies of this type in Mexico [8], although it has a smaller number of published studies compared to the University of Arkansas [37,38].

Conclusions
This is the first systematic review conducted for dendrochronological investigations carried out in Mexico that were published from 2001 until 2016 in indexed journals.Conifers are the most intensively sampled tree species because of their longevity and sensitivity to climate variability.Regarding the measured variables, most studies were based on the measurement of tree-ring width, although measuring earlywood and latewood features may also contribute to improving the reach of some studies.A lack of studies on tropical dry forests has been detected, which is an area of opportunity for the development of projects given the high richness of tree species found in this biome and because these forests experience seasonal droughts.There is a marked tendency in carrying out tree-ring studies focusing on climatic reconstructions, which suggests that it may be beneficial to broaden tree-ring sciences to encompass other research fields, such as ecology (dendroecology) or geomorphology (dendrogeomorphology).Dendrochronological studies are mostly published in international journals.Collaboration with national and international researchers is a great opportunity to promote the future development of dendrochronology in Mexico.

Figure 1 .
Figure 1.Sample sites of the dendrochronological studies carried out in Mexico.The upper right graph indicates the classification of sites based on their elevation.

Figure 2 .
Figure 2. Percentages of studies classified according to the type of ecosystem following the classification of the National Institute of Statistics and Geography (INEGI).

Figure 3 .
Figure 3. Dendrochronological studies performed in Mexico and grouped, according to (a) the taxonomic family and (b) the genus of the studied tree species.

Figure 4 .
Figure 4. Number of dendrochronological studies carried out in Mexico grouped according to the sampled species and its conservation status.Yellow and red bars correspond to those trees species listed within a category in Mexican Official Standard 059[28].According to the Official Mexican Standard 059, "Pr" indicates those tree species subject to special protection and "P" indicates endangered tree species.

Figure 5 .
Figure 5. Dendrochronological studies performed in Mexico and grouped by states.

Figure 6 .
Figure 6.Dendrochronological studies realized in Mexico, grouped by year of publication.

Figure 7 .
Figure 7. Dendrochronological studies performed in Mexico and grouped by its scope of application.

Figure 8 .
Figure 8. Dendrochronological studies on Mexican forests grouped according to the journal where they were published.The impact factor of each journal was estimated for 2015 citation data.

Figure 10 .
Figure 10.Dendrochronological studies performed in Mexico and grouped according to the amplitude or length of the chronologies.

Figure 11 .
Figure 11.Research centers in which work is carried out around dendrochronological issues in Mexico estimated according to the first author of the study).The abbreviations are: National Center of Biological Research of the Northwest (CIBN), College of Postgraduates (CP), National Institute of Forestry, Agriculture and Livestock Research (INIFAP), Pyrenean Institute of Ecology (IPE-CSIC), National Politecnich Institute (IPN), Technological Institute of El Salto (ITES), Antonio Narro Autonomous Agrarian University (UAAAN), Autonomous University of Hidalgo State (UAEH), Juarez University of Durango State (UJED), National Autonomous University of Mexico (UNAM), Northern Arizona University (NAU), The Nature Conservancy (NC), University of Arizona (UAz), University of Arkansas (UAk), University of California (UC), University of Leeds (UL), University of Nevada (UN), University of Rhode Island (URI) and University of Washington (UW).

Table A1 .
List of articles consulted on dendrochronology by species or Mexican forests published in indexed scientific journals.