Rodríguez-Ramírez et al.

1 Running Head. -- Dendroclimatic signal of Mexican beeches

3 Title. – Tree-ring research of Fagus grandifolia subsp. mexicana, a relict tree endemic

4 to eastern Mexico

6 Ernesto Chanes Rodríguez-Ramírez1, Isolda Luna-Vega1*, and Vicente Rozas2

7
1
8 Laboratorio de Biogeografía y Sistemática, Facultad de Ciencias, Universidad Nacional

9 Autónoma de México, Mexico City, Mexico.

2
10 Área de Botánica, Departamento de Ciencias Agroforestales, Universidad de Valladolid,

11 E. U. de Ingenierías Agrarias, Campus Duques de Soria, 42004 Soria, Spain

12 *Corresponding author: luna.isolda@gmail.com

13

14

15 ABSTRACT

16 Mexican beech (Fagus grandifolia subsp. mexicana) has been classified as an endangered

17 species due to its restricted distribution. The current distribution of Mexican beech, which

18 is considered a Pliocene relict, is limited to Tropical Montane Cloud Forests (TMCF) in the

19 mountains of the Sierra Madre Oriental in eastern Mexico. We used dendroclimatic

20 techniques to evaluate the effects of climate variability on the growth of Mexican beech

21 within three forest fragments. For this, we constructed independent chronologies for the

22 three sites, which encompassed 152-178 years. We found that, over the last 180 years,

23 Mexican beech trees have had a mean radial growth lower than those exhibited by other

24 Fagus species. Then, we determined the influence of local climatic factors on the

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25 distribution of Mexican beech. Accordingly, we detected important temperature and

26 precipitation fluctuations that had a significant effect on tree growth. These results suggest

27 that the persistence of Fagus-dominated forests in Mexico is dependent on local scale

28 climatic conditions. The plasticity and adaptability of Mexican beech forests are associated

29 to micro-climatic conditions and are crucial factors for the fate of these forests in the face

30 of on-going climate change.

31

32 Keywords: climatic change, endemism, Mexican beech, Sierra Madre Oriental, growth-

33 rings, Tropical Montane Cloud Forest,

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34 INTRODUCTION

35 Fagus grandifolia subsp. mexicana (Martínez) A.E. Murray (Mexican beech) is considered

36 a Pliocene relict and an endangered species under Mexican laws (Webster 1995;

37 SEMARNAT 2010). Mexican beech is endemic to small fragments (1-42.5 ha) of Tropical

38 Montane Cloud Forests (TMCF) of the Sierra Madre Oriental in eastern Mexico. This

39 represents the most southerly distribution of Fagus species around the world (Rowden et al.

40 2004; Téllez-Valdés et al. 2006). Mexican beeches can be found in areas with annual

41 precipitation ranging from 824 to 2458 mm, and mean annual temperature of 14.5-24.4°C.

42 The species usually thrives on steep (43.8°), rocky slopes with low soil water-retention,

43 which increases the probability of water stress in trees (Peters 1992; Williams-Linera et al.

44 2003; Téllez-Valdés et al. 2006). Currently, no information is available on the sensitivity of

45 Mexican beeches to climatic and phenological variability, or to disturbance events that

46 influence forest dynamics (Fritts 1966; Speer 2010; Fang et al. 2012; Villanueva-Díaz et al.

47 2015).

48 Most dendrochronological studies in Mexico have been performed in arid, temperate

49 and montane regions characterized by well-defined dry or cold seasons (Stahle et al. 2000a;

50 González-Elizondo et al. 2005; Villanueva-Díaz et al. 2007; 2015; Franco-Ramos et al.

51 2016). Most of these dendrochronological studies have been carried out in gymnosperms in

52 northeastern and central Mexico, such as Pseudotsuga Carrière (Cleveland et al. 2003;

53 Villanueva-Díaz et al. 2003; Arreola-Ortiz et al. 2010), several species of Pinus L. [e.g.,

54 Pinus lagunae (Rob.-Pass.) Passini (Constante 2007; Pompa-García and Hadad 2016); P.

55 pinceana Gordon & Glend. (Villanueva-Díaz et al. 2009); P. cembroides Zucc. (Santillán-

56 Hernández et al. 2010); P. pseudostrobus Lindl. (Carlón-Allende et al. 2016)], Taxodium

57 mucronatum Ten. (Correa-Díaz et al. 2014) and Abies religiosa (Kunth) Schltdl. & Cham

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58 (West 2011; Carlón-Allende et al. 2016). Other studies have tried to extend the analyses of

59 tree-rings to species inhabiting humid tropical vegetation types, such as tropical rain forests

60 (Ricker et al. 2007; Paredes-Villanueva et al. 2015; Williams et al. 2015). However, these

61 studies have not addressed the effects of climatic variability on the radial growth of

62 individual trees.

63 The radial growth of trees in natural populations has been extensively studied

64 because growth-rate variation among trees appears to be strongly associated with

65 differences in precipitation and with large-scale climatic phenomena such as El Niño

66 Southern Oscilation (ENSO) (Stahle et al. 2000). Recent studies have documented a

67 significant association between climatic variability and rates of radial growth of trees (e.g.,

68 Williams-Linera et al. 2003; Fang and Lechowicz 2006; Ponce-Reyes et al. 2012; Sánchez-

69 Ramos and Dirzo 2014; Cai et al. 2015). In this context, recent trends in climate change

70 and their impact on the radial growth of individual trees can be evaluated through the study

71 of tree-rings in natural populations. Under appropriate climatic conditions, the analysis of

72 tree-rings can be used to make inferences on past climatic conditions beyond the period

73 recorded by meteorological stations (Fritts 1976; Speer 2010). Furthermore, these analyses

74 can also be used to predict the growth of trees under future climate scenarios (Speer 2010;

75 D’Arrigo et al. 2014). However, most of the tree species inhabiting TMCF do not develop

76 reliable and anatomically distinctive annual tree-rings (Stahle et al. 2016; D’Arrigo et al.

77 2014).

78 Here, we studied the annual tree-rings of individual trees in three populations of

79 Fagus grandifolia. To date, the effects of climate on the radial growth-rates of Mexican

80 beeches have not been analyzed. Thus, the goals of the present study were: (1) to determine

81 whether Fagus grandifolia subsp. mexicana represents a good model for

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82 dendrochronological research; (2) to examine the relationship between tree-ring width and

83 climatic fluctuations and determine the effects of local climatic factors on the growth rates

84 of individual trees.

85

86 MATERIALS AND METHODS

87 Site description

88 The present study was carried out within three fragments of Fagus-dominated

89 TMCF located in the Sierra Madre Oriental in the state of Hidalgo, Mexico: (1) San Bartolo

90 Tutotepec (Medio Monte); (2) Tenango de Doria (El Gosco); and (3) Zacualtipán de

91 Ángeles (La Mojonera) (Table 1; Figure 1). In this three sites, Mexican beeches grow on

92 North-facing slopes within an altitudinal range of 1557-1950 m. The dominant lithological

93 materials at the three sites are Humic (Th) and Vitric Andosols (Tv) (FAO-UNESCO). The

94 soil has a slimy sandy-clay texture with pH values between 4 and 6 (Peters 1995).

95 These beeches are often found in association with other species that can also be

96 found at higher altitudes (Miranda and Sharp 1950; Williams-Linera et al. 2003), such as

97 Pinus patula Schltdl. & Cham, P. teocote Schltdl. & Cham. and different oak species

98 (Quercus spp.). The mid-canopy (10-20 m) of the forest is mostly composed of Befaria

99 aestuans L., Clethra macrophylla M. Martens & Galeotti, rarely Dipholis minutiflora

100 Pittier, Liquidambar styraciflua L., Magnolia schiedeana Schltdl., Ostrya virginiana (Mill.)

101 K. Koch, and Podocarpus matudae Lundell. The low-canopy (2-10 m) of the forest is

102 dominated by Cleyera integrifolia (Benth.) Choisy, Nectandra heydeana Mez & Donn.

103 Sm., Prunus serotina subsp. capuli (Cav,) McVaugh, Symplocos limoncillo Bonpl.,

104 Ternstroemia sylvatica Schltdl. & Cham., Cyathea fulva (M. Martens & Galeotti) Fée,

105 Dicksonia sellowiana Hook., Microtropis schiedeana Loes., and Vaccinium leucanthum

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106 Schltdl.. The understory is dominated by Arisaema macrospathum Benth., Leandra

107 melanodesma (Naudin) Cogn., Miconia glaberrima (Schltdl.) Naudin, M. oligotricha (DC.)

108 Naudin, Piper spp., and Viburnum caudatum L. However, these species are absent in some

109 areas due to the presence of dense clumps of Fagus seedlings. The herbaceous understory is

110 sparse and mainly composed of Elaphoglossum spp., Begonia spp., and Lomariopsis

111 mexicana Holttum.

112 The regional climate varies between the three study sites (Fig. 2). For the

113 Zacualtipán meteorological station (La Mojonera), the average monthly precipitation was

114 recorded for the years 1945 to 2014, whereas the minimum annual precipitation was

115 recorded for 1945 (600 mm) and 2014 (500 mm). For the Tenango de Doria meteorological

116 station (Medio Monte and El Gosco), the maximum annual precipitation was recorded for

117 the years 1944 and 2014 (2800-2900 mm). The average monthly temperature registered in

118 Zacualtipán occurred in two periods: 1942-1951 (23-26°C) and 1994-2004 (23-25°C). For

119 Tenango de Doria, the average monthly maximum temperature was highest for the period

120 1959-1960 (26 and 27°C) (CLICOM-CICESE, http://clicom-mex.cicese.mx).

121

122 Sample collection and chronology development

123 In each site, 20 individuals of Mexican beech were selected following the

124 parameters described by Peters (1992) and Hukusima et al. (2013), who suggested that

125 individual trees of Fagus reach maturity when they achieve: 1) a breast-height diameter >

126 40 cm, and 2) a height > 10 m. Thus, individual trees were selected to meet these two

127 criteria and also to avoid the presence of scars or rot (Olmo-Ruiz en prep.). For each tree,

128 two cores were extracted at a height of 1.30 m with a 40 cm Häglof® drill. The total

129 number of increment cores for the three sites was 120.

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130 The wood cores were dried at room temperature and then mounted and sanded with

131 coarse grit (100 and 360) and fine grit sandpaper (400, 600 and 800). This allowed for a

132 clear recognition of tree-rings that were dated using standard procedures (Stokes and

133 Smiley 1968; Rozas 2001, 2005). Most of the tree species inhabiting TMCF do not develop

134 reliable and anatomically distinctive annual tree-rings (Stahle et al. 2016; D’Arrigo et al.

135 2014). False tree-rings were distinguished from ‘true’ tree-rings by using several cross-

136 sections from fallen trees to complete the chronologies from each site. This also gave

137 support to the information captured with the increment cores (Fritts 1976).

138 The width of tree-rings was measured using a stereoscopic microscope

139 (Stereomaster) and a Velmex Tree Ring Measuring System with a 0.001 mm precision

140 using the software TSAP-Win v. 4.67c (Rinn 2003). The software COFECHA (Holmes

141 1999; Grissino-Mayer 2001) was used to identify missing tree-rings and cross-dating

142 errors. Increment cores with an incorrect alignment of the borer, a very short length of the

143 borer relative to bole radius or showing evidence of rot were excluded from the analyses

144 (Rozas 2001).

145

146 Calculation and assessment of chronologies

147 We calculated ring-width indices (RWI) for each individual using the ARSTAN computer

148 program (Cook and Holmes 1996). Non-climatic trends were removed from each tree-ring

149 series using a cubic spline with a 50% response of 10-year periods, which was flexible

150 enough to maximize high-frequency climatic information (Helama et al. 2004). We used

151 smoothing splines to calculate RWI. In order to produce a standard chronology, the

152 resulting indexed series were averaged using a robust bi-weight mean (Schweingruber

153 1996). Temporal autocorrelation in chronologies is prevalent due to the residual impact of

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154 growing conditions from previous years. Thus, autocorrelation is commonly removed from

155 time series in dendrochronological studies (Speer et al. 2016).

156

157 Climatic records

158 Maximum temperature (Tmax) and monthly precipitation (Prec) are the two most important

159 factors directly affecting the growth of Fagus around the world (Fang and Lechowicz,

160 2006). We obtained data for these two variables directly from nearby weather stations

161 (Zacualtipán, 20.6 N, -98.7 W; Tenango de Doria 20.3 N, -98.2 W), whose records date

162 back to 1942. Data from a single weather station (Tenango de Doria) were used for Medio

163 Monte and El Gosco due to their close geographical proximity. More specifically, we used

164 data for the period 1942-2011 from the CLICOM database (http://clicom-mex.cicese.mx/),

165 which were complemented with data for the period 2012-2015 from INIFAP weather

166 stations (http://clima.inifap.gob.mx/) (Figure 2). These data were corroborated using

167 information provided by Climate-Data (http://es.climate-data.org/).

168 We calculated Spearman rank correlations using SigmaStat v.4 (Jandel Scientific

169 2016) to explore the relationship between climatic data and the growth of F. grandifolia

170 subsp. mexicana. For each growth period (year), we used data on maximum temperature

171 and monthly precipitation (June to September) for the current year and data for every

172 month from the preceding year.

173

174 RESULTS

175 Chronology development and tree growth

176 Compared to other species of Fagus around the world, the estimated RWI (0.99-2.04)

177 indicated a slow radial growth for individuals of Fagus grandifolia subsp. mexicana during

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178 the last 180 years. Although, the mean sensitivity of individual trees was similar across

179 chronologies from the three sites (0.479, Fig. 3; Table 2), the higher signal-to-noise ratio

180 detected in the detrended series from Medio Monte suggest that trees in this site are more

181 sensitive to yearly climatic variation than those at the other two sites. This ratio is not as

182 important for chronology statistics as other indices, but it provides secondary support to the

183 dendroclimatological legitimacy (He et al. 2011).

184 The independent chronologies spanned 178 years for La Mojonera, 168 for Medio

185 Monte and 152 for El Gosco (Figure 3). The average diameter of sampled trees across the

186 three sites was considerably smaller (82.53 cm) than the average diameter reported for the

187 species (134 cm). The tallest trees were located at Medio Monte (28 m) and La Mojonera

188 (25 m). The later also showed the oldest trees on record (187 years). In contrast, individual

189 trees from El Gosco showed a maximum age of 152 years. However, the independent

190 chronologies form the three sites indicated that tree growth responded differently to

191 climatic fluctuations (Figure 3).

192 Fagus grandifolia subsp. mexicana is very susceptible to seasonal and late frosts.

193 Being deciduous, Mexican beeches loose almost all of their leaves during the winter

194 months in response to colder conditions and frosts events (Ern 1976; Lauer 1973).

195 However, late frosts often occur in late winter and early spring (February and March),

196 which can significantly affect the growth of trees and the production of leaves and flowers

197 due to necrosis (Ehnis 1981).

198

199 Relationship between radial growth and climate

200 In the three sites, we detected important temperature and precipitation fluctuations

201 that affected the growth of individual trees. Accordingly, climate data showed significant

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202 associations with the radial growth of trees (Figure 4). More specifically, a decreased radial

203 growth was associated with several drought periods: 1828-30, 1850-66, 1869-1890, 1905,

204 1913, 1918, 1929-30, 1940, 1963, 1970, 1972, 1976, 1983, 1991, 1997, and 2012 (Cardoza-

205 Martínez et al. 2013, Figure 3). Accordingly, Spearman rank correlation coefficients

206 showed that the development of tree-rings during a particular year had a significant

207 association with monthly precipitation during the preceding year (Figure 4-1). However,

208 the correlation between growth and annual precipitation for the preceding year was not

209 significant (P = 0.03). Finally, we found significant correlations between the diameter of

210 tree-rings and the mean maximum temperature for the current year (Figure 4-2). Trees from

211 La Mojonera showed a different response to these climatic fluctuations. This may be the

212 result of trees being more susceptible to sun radiation due to the higher elevation of the site

213 (up to 1950 m) (Table 1). Additionally, differences in tree growth across sites may be a

214 consequence of relatively more stable mean temperatures documented for El Gosco and

215 Medio Monte than those recorded for La Mojonera (Figure 2).

216

217 DISCUSSION AND CONCLUSIONS

218 In this study, the annual tree-rings observed for F. grandifolia subsp. mexicana were

219 associated with climatic variability for the first time. Our results show that Mexican

220 beeches develop annual rings that can be used to confidently estimate the age of trees and

221 rates of radial growth. Furthermore, the inferred sensitivity of Mexican beeches to climatic

222 fluctuations and the observed correlation between growth-ring series across sites indicate

223 that F. grandifolia subsp. mexicana is a useful species for dendrochronological research. In

224 this context, this present study provides relevant new data on the response of TMCF species

225 to regional climatic fluctuations (Figure 3).

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226 The presence of individual trees with maximum ages of 152-178 years allowed us to

227 evaluate the effects of climate on tree growth back to the year 1828. Recently, Williams-

228 Linera et al. (2000) found individual trees of Mexican beech with maximum ages of 117

229 years at Acatlán Volcano in eastern Mexico. Thus, our age estimates for individual

230 Mexican beeches increase the information on how this species has responded to climatic

231 variation during the last two centuries. Nonetheless, given the scarcity of age estimates for

232 Mexican beeches, additional dendrochronological studies should be carried out in other

233 Fagus-dominated forests in the states of Nuevo León, Puebla, Tamaulipas and Veracruz.

234 The growth-ring patterns recorded for F. grandifolia subsp. mexicana are similar to

235 those described for F. grandifolia (Canada and USA), F. sylvatica (Europe) and F.

236 orientalis (Middle East) (Inside Wood, http://insidewood.lib.ncsu.edu/search?5). All these

237 species share a series of anatomical features for water conduction (e.g., xylem vessels) that

238 allow them to inhabit boreal ecosystems with temperate climates. Although Mexican beech

239 is the only species with a tropical distribution, the mountains of the Sierra Madre Oriental

240 inhabited by this species have a prevailing Cb-type climate (sensu García 1988), which

241 corresponds to a temperate climate with a long and mild summer.

242 Compared to other species inhabiting semiarid environments (Stahle et al. 2000a;

243 Cleveland et al. 2003; Cerano-Paredes et al. 2009; Arreola-Ortiz et al. 2010), we found a

244 weak association between radial growth and climatic variables, namely monthly

245 precipitation and mean maximum temperature (Tmax). We believe this is the result of the

246 high levels of precipitation recorded for Mexican Fagus forests (annual precipitation: 824-

247 2458 mm). The association between climate and tree growth has also been observed in

248 other species. More specifically, Therrell et al. (2002) and West (2011) described the tree-

249 ring chronologies in populations of Douglas fir (Pseudotsuga menziesii (Mirb.) Franco)

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250 within our study region (e.g., El Malpaso, Veracruz; 20.404° N, 98.467° W). These authors

251 observed an extremely weak correlation between late wood production and regional

252 summer precipitation (June-September). In this context, the negative relationship between

253 dry season precipitation and the growth of Fagus (Figures 4-1, 2) can be explained by a

254 reduction in inter-specific competition with other constituent tree species of the forest.

255 On the other hand, the TMCF in the Sierra Madre Oriental has mean maximum

256 temperature ranging from 14.5 to 24.4°C, which has a significant effect on the

257 establishment of Mexican beech forests (Peters 1992; Téllez-Valdés et al. 2006).

258 Accordingly, our results showed significant correlations between radial growth and mean

259 maximum temperature. These observations support Fang and Lechowicz’s (2006)

260 suggestion that regional maximum temperature and monthly precipitation have a great

261 effect on the growth of Fagus in Mexico. Furthermore, mean maximum temperature also

262 appears to be a determinant factor affecting the growth of other tree species restricted to

263 TMCF, such as Austrocedrus chilensis (D. Don) Florin & Boutelje, Magnolia spp.,

264 Nothofagus dombeyi (Mirb.) Oerst., and Pinus contorta Douglas ex Loudon (Price et al.

265 2011). However, our results showed that increased maximum temperatures hindered the

266 radial growth of tress from La Mojonera, but promoted the growth of trees from Medio

267 Monte and El Gosco (Figure 4-2). This discrepancy among sites is may be related to a

268 latitudinal effect or to differences in sun radiation among sites.

269 Bennett (1985) showed that populations of Fagus grandifolia in the United States

270 were adapted to microclimatic conditions. Accordingly, climatic variables did not show

271 coincident influences on the growth of Fagus across sites (Figure 4-1), despite their close

272 geographical proximity (8.94 to 46 km). Overall, there was considerable radial growth of

273 trees during years with high temperatures (mean and maximum) preceding the rainy season

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274 (Fig. 4-2). However, in the case of La Mojonera, mean maximum temperature had a

275 pronounced negative effect on the radial growth of beeches due to the high elevations

276 where this forest develops (up to 2000 m), which makes trees more prone to limiting factors

277 such as frost events.

278 Micro-climatic conditions, together with human and naturally induced disturbances,

279 might be influencing the establishment and growth of trees within Mexican TMCF

280 (Huntley et al. 1989; Rodríguez-Ramírez et al. 2013; Gual-Díaz and Rendón-Correa 2014).

281 In the present case, the radial growth of Mexican beeches appears to be determined, at least

282 partially, by micro-climatic conditions within the three study sites. For example, El Gosco,

283 which is known to have had human and naturally induced disturbances in the recent past

284 (Ortíz-Quijano et al. 2015), showed the youngest and most slow-growing trees among the

285 three study sites. Furthermore, water-flow is scarce at El Gosco, but high humidity levels

286 and abundant bodies of water are prevalent at Medio Monte.

287 Chronologies for species inhabiting TMCF can provide unique and valuable insights

288 into the paleoclimatic history of Mexico (Villanueva-Díaz et al. 2003; Fang and Lechowicz

289 2006). As proposed by Therrell et al. (2002), these chronologies can also be valuable for

290 investigating climatic variability associated to the North American Monsoon. This climatic

291 phenomenon can explain the regional climatic effects occurring in the TMCF in eastern

292 Mexico.

293 Tree growth was slow but continuous and it was affected by specific climatic events

294 occurring at each site (Figure 3). We observe different impacts of climatic fluctuations on

295 the three study sites, generating increased precipitation in one site and increased drought in

296 another. These had considerably different effects on the radial growth of Mexican beeches

297 across sites (Figure 3).

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298 The Mexican TMCF appears to develop under specific micro-climatic conditions

299 (Fang and Lechowicz 2006). More specifically, the TMCF is characterized by sufficient

300 levels of available water throughout the year due to the continuous presence of fog

301 (horizontal precipitation) and a closed canopy that prevent water loss. This results in

302 constant levels of environmental humidity and the absence of a defined dry season.

303 Similar broad-scale climatic conditions facilitate the establishment of Fagus

304 grandifolia subsp. mexicana within TMCF (Godínez-Ibarra et al. 2007), but micro-climatic

305 conditions at each site appear to be affecting the rate of growth of individual trees. Thus,

306 we suggest that the patterns observed in the growth chronologies are dependent on local

307 and regional climatic conditions. Accordingly, the three studied sites were affected by the

308 same climatic fluctuations. In this context, compared to El Gosco, La Mojonera and Medio

309 Monte have the more favorable micro-climatic conditions for the establishment and growth

310 of Mexican beeches. Thus, these two localities had the oldest recorded trees and the highest

311 rates of radial growth.

312 Our results agree with those obtained for other species, such as Pinus cooperi C.E.

313 Blanco in Mexico (Pompa-García et al. 2015) and Tectona grandis L. f. and Pinus caribaea

314 Morelet in Brazil (Venegas-González et al. 2016). These studies showed that favorable

315 micro-climatic conditions allow species to be more resilient to drought. Accordingly,

316 different Mexican beech forests are characterized by particular micro-climatic conditions

317 that produce differential responses in the growth of trees (Rodríguez-Ramírez et al. en

318 prep.) and that lessen effect of regional climatic events, such as those associated ENSO.

319 Therefore, the specific micro-climatic conditions of the TMCF allow for the persistence of

320 Mexican beech populations in the mountains of the Sierra Madre Oriental. Several studies

321 have suggested that Mexican beech forests are greatly dependent on local scale climatic

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322 conditions for their establishment and survival (Godínez-Ibarra et al. 2007). These

323 conditions ultimately allow trees the necessary plasticity (Montiel-Oscura et al. 2013) and

324 adaptability to maintain ecological interactions within TMCF under large-scale climatic

325 fluctuations, which is crucial for the fate of these forests in the face of on-going climate

326 change.

327

328 ACKNOWLEDGEMENTS

329 We thank Santiago Ramírez-Barahona for his critical observations; David Espinosa

330 for his interesting explanations of climatic phenomena occurring in Mexico; Lorenzo

331 Vazquez Selém and Osvaldo Franco Ramos helped us with the growth-ring measurements

332 and lent some specialized equipment; Othón Alcántara-Ayala and Rodrigo Ortega García

333 for their support during fieldwork. We thank the constructive suggestions and comments of

334 Matthew D. Therrell and Connie Woodhouse. This research was financed by DGAPA

335 PAPIIT IV201015 project. The first author also thanks the financial support granted by the

336 postdoctoral fellowship DGAPA-UNAM 2015-2016.

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346 REFERENCES CITED

347 Arreola-Ortiz, M. R., M. González-Elizondo, and J. J. Návar-Cháidez, 2010.

348 Dendrocronología de Pseudotsuga menziesii (Mirb.) Franco de la Sierra Madre Oriental

349 en Nuevo León, México. Madera y Bosques 16(1):71–84.

350 Bennett, K.D., 1985. The spread of Fagus grandifolia across eastern North America during

351 the last 18 000 years. Journal of Biogeography 12:147–164.

352 Cai, W., A. Santoso., G. Wang., S.W. Yeh., S. I. An., K. M. Cobb., M. Collins., E.

353 Guilyardi, F. F. Jin., J. S. Kung., M. Lengaigne., M. J. McPhaden., K. Takahashi., A.

354 Timmermann., G. Vecchi., M. Watanabe., and L. Wu., 2015. ENSO and greenhouse

355 warming. Nature Climate Change 5:849–859.

356 Cardoza-Martínez, G.F., J. Cerano-Paredes., J. Villanueva-Díaz., R. Cervantes-Martínez.,

357 V. Guerra de la Cruz., and J. Estrada-Ávalos., 2013. Annual precipitation

358 reconstruction of the Eastern region of Tlaxcala state. Revista Mexicana de Ciencias

359 Forestales 5(23):110–127.

360 Carlón-Allende, T., M. E. Mendoza., D. R. Pérez-Salicrup., J. Villanueva-Díaz., and A.

361 Lara., 2016. Climatic responses of Pinus pseudostrobus and Abies religiosa in the

362 Monarch Butterfly Biosphere Reserve, Central Mexico. Dendrochronologia 38:103–

363 116.

364 Cerano-Paredes, J., J. Villanueva-Díaz., P. Z. Fulé., J. G. Arreola-Ávila., I. Sánchez-

365 Cohen., and R. D. Valdez-Cepeda., 2009. Reconstructing 350 years of precipitation

366 in southeast Chihuahua, Mexico. Madera y Bosques 15(2):27–44.

367 Cleveland, M., D. Stahle., M. Therrell., J. Villanueva-Díaz., and B. Burns., 2003. Tree-ring

368 reconstructed winter precipitation and tropical teleconnections in Durango, Mexico,

16
 Rodríguez-Ramírez et al.

369 Climatic Change 59:369–388.

370 Constante, G. V., 2007. Reconstrucción de la precipitación invierno-primavera para los

371 últimos cuatro siglos en el Ejido Cuauhtémoc, Saltillo, Coahuila. Ph. D. Thesis,

372 Departamento Forestal, Universidad Autónoma Agraria Antonio Narro, Saltillo,

373 Coahuila, Mexico City.

374 Cook, E. R., and R. L. Holmes., 1996. Guide for computer program ARSTAN. In The

375 International Tree-Ring Data Bank Program Library Version 2.0 User’s Manual,

376 edited by H. D. Grissino-Mayer, R. L. Holmes, and H. C. Fritts, pp. 75–87.

377 Laboratory of Tree-Ring Research, University of Arizona, Tucson.

378 Correa-Díaz, A., A. Gómez-Guerrero., J. Villanueva-Díaz., L. U. Castruita-Esparza., T.

379 Martínez-Trinidad., and R. Cervantes-Martínez., 2014. Dendroclimatic analysis of

380 Baldcypress (Taxodium mucronatum Ten.) in central Mexico. Agrociencia 48:537–

381 551.

382 D´Arrigo, R., N. Davi., G. Jacoby., R. Wilson., and G. Wiles., 2014. Dendroclimatic studies:

383 tree growth and climate change in northern forests. American Geophysical Union,

384 Wiley, New Jersey, USA.

385 Ehnis, D., 1981. Fagus mexicana Martínez: su ecología e importancia. B. Sc. Thesis,

386 Facultad de Ciencias, Universidad Nacional Autónoma de México, Mexico City.

387 Ern, H., 1976. Descripción de la vegetación montañosa en los estados mexicanos de

388 Puebla y Tlaxcala. Mueller-SAI, Chile.

389 Fang, J., and M. J. Lechowicz., 2006. Climatic limits for the present distribution of beech

390 (Fagus L.) species in the world. Journal of Biogeography 33:1804–1819.

17
 Rodríguez-Ramírez et al.

391 Fang, K., X. Gou., F. Chen., Y. Li., F. Zhang., and M. Kazmer., 2012. Tree growth and its

392 association with climate between individual tree-ring series at three mountain ranges

393 in north central China. Dendrochronologia 30:113–119.

394 Franco-Ramos, O., M. Castillo., and E. Muñiz-Salinas., 2016. Using tree-ring analysis to

395 evaluate intra-eruptive lahar activity in the Nexpayantla Gorge, Popocatépetl

396 volcano (central Mexico). Catena 147:205-215.

397 Fritts, H. C., 1966. Growth-rings of trees: their correlation with climate. Science 154:973–

398 979.

399 Fritts, H. C., 1976. Tree rings and climate. Academic Press, London.

400 García, E., 1988. Modificaciones al sistema de clasificación climática de Köppen, México,

401 Offset Larios. Mexico City.

402 Godínez-Ibarra, O., G. Ángeles-Pérez., L. López-Mata., E. García-Moya., J. I. Valdez-

403 Hernández., H. De los Santos-Posadas., and A. Trinidad-Santos., 2007. Seed rain

404 and seedling emergence of Fagus grandifolia subsp. mexicana at La Mojonera,

405 Hidalgo, Mexico. Revista Mexicana de Biodiversidad 78:117−128.|

406 González-Elizondo, M., E. Jurado., J. Návar., M. S. González-Elizondo., J. Villanueva-

407 Díaz., O. Aguirre., and J. Jiménez., 2005. Tree-rings climate relationships for

408 Douglas-fir chronologies from the Sierra Madre Oriental, Mexico: a 1681-2001 rain

409 reconstruction. Forest Ecology and Management 213:39−53.

410 Grissino-Mayer, H. D., 2001. Evaluating cross-dating accuracy: a manual and tutorial for the

411 computer program COFECHA. Tree-Ring Research 57:205–221.

18
 Rodríguez-Ramírez et al.

412 Gual-Díaz, M., and A. Rendón-Correa., 2014. Bosques mesófilos de montaña de México:

413 diversidad, ecología y manejo. Comisión Nacional para el Conocimiento y Uso de

414 la Biodiversidad. México.

415 He, D., M. X. Jiang., and X. Z. Wei., 2011. A dendroclimatic investigation of radial

416 growth-climate relationships for the riparian species Cercidiphyllum japonicum in

417 the Shennongjia area, central China. Trees 26:503–512.

418 Helama, S., M. Lindholm., M. Timonen., M. Eronen., 2004. Detection of climate signal in

419 dendrochronological data analysis: a comparison of tree-ring standardization

420 methods. Theoretical and Applied Climatology.79:239–254.

421 Holmes, R., 1999. Program COFECHA, cross-dating and measurement quality control.

422 Laboratory of tree-ring research, University of Arizona, Tucson, USA.

423 Hukusima, T., T. Matsui., T. Nishio., S. Pignatti., L. Yang., S. Y. Lu., M. H. Kim., M.

424 Yoshikawa., H. Honma., and Y. Wang., 2013. Phytosociology of the beech (Fagus)

425 forest in East Asia. Springer, Heidelberg, New York.

426 Huntley, B., P. J. Bartlein., and I. C. Prentice., 1989. Climatic control of the distribution and

427 abundance of beech (Fagus L.) in Europe and North America. Journal of Biogeography

428 16:551–560.

429 Jandel Scientific., 2016. SigmaStat, release 4. Jandel Scientific, San Rafael, California, USA.

430 Lauer, W., 1973. Problemas climatoecológicos de la vegetación de la región montañosa

431 oriental de México. Comunicaciones 7:37–44.

432 Miranda, F., and Sharp A. J., 1950. Characteristics of the vegetation in certain temperate

433 regions of eastern Mexico. Ecology 31:313−33.

19
 Rodríguez-Ramírez et al.

434 Montiel-Oscura, D., C. Ramírez-Herrera., G. Ángeles-Pérez., J. López-Upton., P. Antonio-

435 López., 2013. Allozyme variation and population size of haya mexicana (Fagus

436 grandifolia subsp. mexicana) in the Sierra Madre Oriental. Revista Fitotecnia

437 Mexicana 36(4):413–420.

438 Ortíz-Quijano, B., M. C. Cuevas-Carmona., A. Sánchez-González., 2015. Historia

439 ambiental de tres bosques de haya del estado de Hidalgo, México, 1935-2014.

440 Historia 2.0 5(10):25–41.

441 Paredes-Villanueva, K., L. López., M. Brookhouse., and R. M. N. Cerillo., 2015. Rainfall

442 and temperature variability in Bolivia derived from the tree-ring width of Amburana

443 cearensis (Fr. Allem.) A.C. Smith. Dendrochronologia 35:80–86.

444 Peters, R., 1992. Ecology of beech forests in the northern Hemisphere. Ph. D. Thesis,

445 Wageningen Agricultural University, Wageningen, Netherlands.

446 Peters, R., 1995. Architecture and development of Mexican beech forest. Vegetation

447 science in forestry. In: Vegetation science in forestry, edited by E. O. Box, R. K.

448 Peet, T. Masuzawa, I. Yamada, K. Fujimara, and P. F. Maycock, pp. 325–343.

449 Klumer Academic Publishers, Dorbrecht.

450 Pompa-García, M., L. Miranda-Aragón., and C. A. Aguirre-Salado., 2015. Tree growth

451 response to ENSO in Durango, Mexico. International Journal of Biometeorology

452 59:89–97.

453 Pompa-García, M., and M. A. Hadad., 2016. Sensitivity of pines in Mexico to temperature

454 varies with age. Atmósfera 29(3):209-219.

20
 Rodríguez-Ramírez et al.

455 Ponce-Reyes, R., V. H. Reynoso-Rosales., J. E. M. Watson., J. VanDerWal., R. A. Fuller.,

456 R. L. Pressey., and H. P. Possingham., 2012. Vulnerability of cloud forest reserves

457 in Mexico to climate change. Nature Climate Change 2:448–452.

458 Price, M.F., G. Gratzer., L. A. Duguma., T. Kohler., D. Maselli., and R. Rosalaura., 2011.

459 Mountain forests in a changing world-realizing values, addressing challenges.

460 FAO/MPS and SDC, Rome.

461 Ricker, M., G. Gutiérrez-García., and D. C. Daly., 2007. Modeling long-term tree growth

462 curves in response to warming climate: test cases from a subtropical mountain forest

463 and a tropical rainforest in Mexico. Canadian Journal of Forest Research 37:977–

464 989.

465 Rinn, F., 2003. TSAP-Win. Time series analysis and presentation for dendrochronology

466 and related applications. Version 4.64 for Microsoft Windows. User Reference.

467 Rinntech, Heidelberg, Germany.

468 Rodríguez-Ramírez, E.C., A. Sánchez-González., and G. Ángeles-Pérez., 2013. Current

469 distribution and coverage of Mexican beech forests Fagus grandifolia subsp.

470 mexicana in Mexico. Endangered Species Research 20:205–216.

471 Rowden, A., A. Robertson., T. Allnutt., S. Heredia., G. Williams-Linera., and A. C.

472 Newton., 2004. Conservation genetics of Mexican beech, Fagus grandifolia var.

473 mexicana. Conservation Genetics 5:475−484.

21
 Rodríguez-Ramírez et al.

474 Rozas, V., 2001. Detecting the impact of climate and disturbances on tree-rings of Fagus

475 sylvatica L. and Quercus robur L. in a lowland forest in Cantabria, Northern Spain.

476 Annals of Forest Science 58:237–251.

477 Rozas, V., 2005. Dendrochronology of pedunculate oak (Quercus robur L.) in an old-

478 growth pollarded woodland in northern Spain: tree-ring growth responses to

479 climate. Annals of Forest Science 62:209–218.

480 Sánchez-Ramos, G., and R. Dirzo., 2014. El bosque mesófilo de montaña: un ecosistema

481 prioritario amenazado. In: Bosques mesófilos de montaña en México: diversidad,

482 ecología y manejo, edited by M. Gual-Díaz, and A. Rendón-Correa, pp. 109–139.

483 Comisión Nacional para el Conocimiento y Uso de la Biodiversidad, México.

484 Santillán-Hernández, M., E. H. Cornejo-Oviedo., J. Villanueva-Díaz., J. Cerano-Paredes.,

485 S. Valencia-Manzo., and M. A. Capó-Arteaga., 2010. Potencial dendroclimático de

486 Pinus pinceana Gordon en la Sierra Madre Oriental. Madera y Bosques 16(1):17–

487 30.

488 Schweingruber, F. H., 1996. Tree rings and environment: dendroecology. Swiss Federal

489 Institute for Forest, Snow and Landscape Research. Paul Haupt Verlag, Bern.

490 SEMARNAT, Secretaría del Medio Ambiente y Recursos Naturales., 2010. Norma Oficial

491 Mexicana NOM-059-SEMARNAT-2010. Protección ambiental-Especies nativas de

492 México de flora y fauna silvestres -Categorías de riesgo y especificaciones para su

493 inclusión, exclusión o cambio-Lista de especies en riesgo. Diario Oficial de la

494 Federación. Segunda Sección, México City, www.profepa.gob.mx/innovaportal

495 /file/435/1/ NOM_059_SEMARNAT_2010.pdf

22
 Rodríguez-Ramírez et al.

496 Speer, J. H., 2010. Fundamentals of tree ring research. University of Arizona Press,

497 Tucson, Arizona.

498 Speer, J.H., A. Bräuning., Q. Zhang., K. Pourtahmasi., N. P. Gaire., B. Dawadi., P. Rana.,

499 Y. B. Dhakal., R. H. Acharya., D. L. Adhikari., S. Adhikari., P. C. Aryal., D.

500 Bagale., B. Baniya., S. Bhandari., N. Dahal., S. Dahal., N. Ganbaatar., A. Giri., D.

501 B. Gurung., Y. Khandu., B. Maharjan., R. Maharjan., R. A. Malik., C. D. Nath., B.

502 Nepal., J. Ngoma., R. Pant., M. L. Pathak., H. Paudel., B. Sharma., M. S. Hossain.,

503 B. Soronzonbold., T. Swe., I. Thapa., and A. Tiwari., 2016. Pinus roxburghii stand

504 dynamics at a heavily impacted site in Nepal: Research. Dendrochronologia. in

505 press.

506 Stahle, D. W., E. R. Cook., M. K. Cleveland., M. D. Therrell., D. M. Meko., H. D.

507 Grissino-Mayer., E. Watson., and B. H. Luckman., 2000. Tree-Ring data document

508 16th century Megadrought over North America, Eos, Transactions, American

509 Geophysical Union 81:21−125.

510 Stahle, D. W., E. R. Cook., D. J. Burnette., J. Villanueva-Díaz., J. Cerano., J. N. Burns., D.

511 Griffin., B. I. Cook., R. Acuña., M. C. Torbenson., P. Sjezner., and I. M. Howard.,

512 2016. The Mexican Drought Atlas: Tree-ring reconstructions of the soil moisture

513 balance during the late pre-Hispanic, colonial, and modern eras. Quaternary Science

514 Reviews 149:34−60.

515 Stahle, D. W., J. Villanueva-Díaz., M. K. Cleaveland., M. D. Therrell., G. J. Paull., B. T.

516 Burns., W. Salinas., H. Suzan., and P. Z. Fule., 2000a. Recent tree-ring research in

23
 Rodríguez-Ramírez et al.

517 Mexico. In Dendrocronología en América Latina, edited by F. A. Roig, pp. 285–

518 306. EDIUNC, Mendoza, Argentina.

519 Stokes, M.A., and T. L. Smiley., 1968. An introduction to tree-ring dating. University of

520 Chicago Press, Chicago, USA.

521 Téllez-Valdés, O., P. Dávila-Aranda., and R. Lira-Saade., 2006. The effects of climate

522 change on the long-term conservation of Fagus grandifolia var. mexicana, an

523 important species of the cloud forest in eastern Mexico. Biodiversity and

524 Conservation 15:1095−1107.

525 Therrell, M. D., D. W. Stahle., M. K. Cleaveland., J. Villanueva-Díaz., 2002. Warm season

526 tree growth and precipitation over Mexico. Journal of Geophysical Research

527 107:4205−4212.

528 Venegas-González, A., M. Peres-Chagas., C. R. Anholetto-Júnior., C. A. Alvares., F. A.

529 Roig., and M. T. Filho., 2016. Sensitivity of tree ring growth to local and large-scale

530 climate variability in a region of Southeastern Brazil. Theoretical and Applied

531 Climatology 123:233–245.

532 Villanueva-Díaz, J., P. Z. Fulé., J. Cerano-Paredes., J. Estrada-Ávalos., and I. Sánchez-

533 Cohen., 2009. Reconstrucción de la precipitación estacional para el barlovento de la

534 Sierra Madre Oriental con anillos de crecimiento de Pseudotsuga menziesii (Mirb.)

535 Franco. Revista Ciencia Forestal en México 34(105):39–71.

536 Villanueva-Díaz, J., D. W. Stahle., M. K. Cleveland., M. D. Therrell., 2003. Estado actual

537 de la dendrocronología en México. Ciencia Forestal en México 25:5–35.

24
 Rodríguez-Ramírez et al.

538 Villanueva-Díaz, J., D. W. Stahle., B. H. Luckman., J. Cerano-Paredes., M. D. Therrell.,

539 and M. K. Cleveland., 2007. Winter-spring precipitation reconstructions from tree

540 rings for northeast Mexico. Climatic Change 83:117–131.

541 Villanueva-Díaz, J., J. Cerano-Paredes., L. Vázquez-Selem., D. W. Stahle., P. Z. Fulé., L.

542 L. Yocom., O. Franco-Ramos., and J. A. Ruíz-Corral., 2015. Red dendrocronológica

543 del pino de altura (Pinus hartwegii Lindl.) para estudios dendroclimáticos en el

544 noreste y centro de México. Investigaciones Geográficas, Boletín del Instituto de

545 Geografía, UNAM 86:5–14.

546 Walker, L. R., K. Mehltreter., and J. M. Sharpe., 2010. Current and future directions in fern

547 ecology. In: Fern ecology, edited by K. Mehltreter, L. Walker, and J. M. Sharpe, pp.

548 360–378. Cambridge University Press, USA,

549 Webster, G. L., 1995. The Panorama of Neotropical Cloud Forests. In. Biodiversity and

550 Conservation of Neotropical Montane Forests, edited by S. P. Churchill, H. Balslev,

551 E. Forero, and J. L. Luteyn, pp. 53–57. The New York Botanical Garden, USA,

552 West, G. H., 2011. Defining the regional and seasonal climatic response of long Douglas-

553 fir tree-ring chronologies in central Mexico. M.A. Thesis, University of Arkansas,

554 USA.

555 Williams, R. E., M. H. Gagen., E. P. D. Walsh., and K. Bidin., 2015. On the development

556 of a drill-borer for sampling tropical supra-hardwoods: an example using the Borneo

557 ironwood Eusideroxylon zwageri. Dendrochronologia 35:99–104.

558 Williams-Linera, G., M. S. Devall., and C. Álvarez-Aquino., 2000. A relict population of

559 Fagus grandifolia var. mexicana at the Acatlan Volcano, Mexico: structure, litterfall,

560 phenology and dendroecology. Journal of Biogeography 27:1297–1309.

25
 Rodríguez-Ramírez et al.

561 Williams-Linera, G., A. Rowden., and A. C. Newton., 2003. Distribution and stand

562 characteristics of relict populations of Mexican beech (Fagus grandifolia var.

563 mexicana). Biological Conservation 109:27−36.

564

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565 TABLES

566 Table 1. Geographic characteristics of Tropical Montane Cloud Forests at the three sites of

567 Fagus grandifolia subsp. mexicana (Mexican beech) in the mountains of the Sierra Madre

568 Oriental of eastern Mexico.

La Mojonera Medio Monte El Gosco

Latitude (N) 20°38´33´´ 20° 24´50´´ 20° 19´37.8´´

Longitude (W) 98° 36´51.8´´ 98° 14´24´´ 98° 14´57.1´´

Elevation (m a.s.l.) 1780-1950 1800-1944 1557-1864

Slope (degrees) Max 37.8 21.5 43.8

Min 1.8 0.45 16.1

Diameter at breast height Max 118 110 225

(cm)
Min 54 43 50

Height (m) Max 25 28 20

Min 14 15 12

569
570

571

572

573

574

575

576

577

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 Rodríguez-Ramírez et al.

578 Table 2. Growth ring statistics for Fagus grandifolia subsp. mexicana (Mexican beech) in

579 Tropical Montane Cloud Forests at the three study sites in the mountains of the Sierra

580 Madre Oriental of eastern Mexico.

581 Statistics La Mojonera Medio Monte El Gosco

582 Sampled trees 20 20 20

Crossdated seriesa 24 28 28
583
Master series (years) 1828-2015 1847-2015 1863-2015
584 Crossdated ringsa 2198 3094 2700

585 Series intercorrelationa 0.679 0.689 0.716

586
Mean sensitivitya 0.395 0.334 0.363
587
Autocorrelationa 0.504 0.569 0.518
588
Mean/median age (years)b 93.29/89 110.5/119.5 96.5/92
589
Common interval 1942-2015 1899-2015 1949-2015
590
Signal-to-noise ratioc 27.10 16.21 21.72
591 a
Values obtained with COFECHA (Holmes, 1999)
b
592 Values statistically different using a Mann-Whitney test (P = 0.01)
c
Values obtained with ARSTAN (Cook and Holmes, 1999)
593

594

595

596

597

598

599

600

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 Rodríguez-Ramírez et al.

601 FIGURE LEGENDS

602 Figure 1. Geographical location and extent of Tropical Montane Cloud Forests at the three

603 study sites of Fagus grandifolia subsp. mexicana (Mexican beech) in the mountains of the

604 Sierra Madre Oriental of eastern Mexico. Light green surfaces represent sampled polygons

605 of Tropical Montane Cloud Forests dominated by Mexican beech (A= La Mojonera, B=

606 Medio Monte, C= El Gosco).

607

608

609

610

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 Rodríguez-Ramírez et al.

611 Figure 2. The climatic characteristics at the Zacualtipán (La Mojonera, A) and Tenango de

612 Doria (Medio Monte, B and El Gosco, C) meteorological stations (1941-2015). Average

613 monthly temperature and average total monthly precipitation were based on CLICOM

614 database (http://clicom-mex.cicese.mx/).

615

616

617

618

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 Rodríguez-Ramírez et al.

619 Figure 3. Ring-width chronologies for Fagus grandifolia subsp. mexicana (Mexican

620 beech), in Tropical Montane Cloud Forests at the three study sites in the mountains of the

621 Sierra Madre Oriental of eastern Mexico.

622

623

624

625

626

627

628

629

630

631

632

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 Rodríguez-Ramírez et al.

633 Figure 4. Estimated correlation coefficients between ring-width chronologies for Fagus

634 grandifolia subsp. mexicana (Mexican beech), total precipitation (1) and mean monthly

635 temperature (2) in Tropical Montane Cloud Forests at the three study sites in the mountains

636 of the Sierra Madre Oriental of eastern Mexico (A= La Mojonera, B= Medio Monte, C= El

637 Gosco). Horizontal lines represents 95% confidence intervals: *P< 0.05.

638

32