The influence of climate on the masting behavior of Mexican beech: growth rings and xylem anatomy

Abstract

Key message
The Mexican beech undergoes masting events, on average, every 5.5 years. These events depend directly on precipitation.

Abstract
Climate change has considerably impacted the protective functions of tropical montane cloud forests, possibly influencing the synchronicity of phenological processes and the distribution and physiology of plants. In particular, climatic fluctuations cause changes in the distribution of tree species. Mexican beech (Fagus grandifolia subsp. mexicana) is considered an endangered species, due to its restricted distribution and its being a Miocene relict, limited to tropical montane cloud forests in the mountains of the Sierra Madre Oriental in eastern Mexico. We analyzed the influence of temperature and precipitation in prompting changes to tree-ring width, as well as vessel frequency and diameter, of Mexican beech in eastern Mexico. We used growth rings and xylem vessels traits to infer the historical masting events of Mexican beech over the last 128 years. We obtained independent chronologies for Mexican beech in each of the studied sites, dating back 152–178 years. Precipitation was strongly associated with differences in tree-ring width between masting and non-masting years. Our study highlights the use of dendroecological research to detect climate-induced modifications in the vessel frequency and diameter of tree species inhabiting tropical montane cloud forests. This association also explained differences in vessel frequency and diameter recorded before, during, and after masting events. Our results revealed that Mexican beech undergoes masting events every 5.5 years on average, and that these events directly depend on minimum annual precipitation. In conclusion, our results advance our understanding on the plasticity of growth rings and vessels traits (frequency and diameter) in response to fluctuation in precipitation.

Full text

1 23
Trees
Structure and Function
ISSN 0931-1890
Trees
DOI 10.1007/s00468-018-1755-3
The influence of climate on the masting
behavior of Mexican beech: growth rings
and xylem anatomy
Ernesto Chanes Rodríguez-Ramírez,
Teresa Terrazas & Isolda Luna-Vega

1 23
Your article is protected by copyright and
all rights are held exclusively by Springer-
Verlag GmbH Germany, part of Springer
Nature. This e-offprint is for personal use only
and shall not be self-archived in electronic
repositories. If you wish to self-archive your
article, please use the accepted manuscript
version for posting on your own website. You
may further deposit the accepted manuscript
version in any repository, provided it is only
made publicly available 12 months after
official publication or later and provided
acknowledgement is given to the original
source of publication and a link is inserted
to the published article on Springer's
website. The link must be accompanied by
the following text: "The final publication is
available at link.springer.com”.

Vol.:(0123456789)
1 3
Trees
https://doi.org/10.1007/s00468-018-1755-3
ORIGINAL ARTICLE
The influence ofclimate onthemasting behavior ofMexican beech:
growth rings andxylem anatomy
ErnestoChanesRodríguez‑Ramírez1· TeresaTerrazas2· IsoldaLuna‑Vega1
Received: 23 November 2017 / Accepted: 21 August 2018
© Springer-Verlag GmbH Germany, part of Springer Nature 2018
Abstract
Key message The Mexican beech undergoes masting events, on average, every 5.5years. These events depend directly
on precipitation.
Abstract Climate change has considerably impacted the protective functions of tropical montane cloud forests, possibly
influencing the synchronicity of phenological processes and the distribution and physiology of plants. In particular, climatic
fluctuations cause changes in the distribution of tree species. Mexican beech (Fagus grandifolia subsp. mexicana) is con-
sidered an endangered species, due to its restricted distribution and its being a Miocene relict, limited to tropical montane
cloud forests in the mountains of the Sierra Madre Oriental in eastern Mexico. We analyzed the influence of temperature and
precipitation in prompting changes to tree-ring width, as well as vessel frequency and diameter, of Mexican beech in eastern
Mexico. We used growth rings and xylem vessels traits to infer the historical masting events of Mexican beech over the last
128years. We obtained independent chronologies for Mexican beech in each of the studied sites, dating back 152–178years.
Precipitation was strongly associated with differences in tree-ring width between masting and non-masting years. Our study
highlights the use of dendroecological research to detect climate-induced modifications in the vessel frequency and diameter
of tree species inhabiting tropical montane cloud forests. This association also explained differences in vessel frequency
and diameter recorded before, during, and after masting events. Our results revealed that Mexican beech undergoes masting
events every 5.5years on average, and that these events directly depend on minimum annual precipitation. In conclusion, our
results advance our understanding on the plasticity of growth rings and vessels traits (frequency and diameter) in response
to fluctuation in precipitation.
Keywords Climate variables· Dendromastecology· Fagus grandifolia subsp. mexicana· Tropical montane cloud forest·
Xylem vessels· Masting
Introduction
Climate change is likely to have serious impacts on the pro-
tective functions of tropical montane cloud forests world-
wide(Webster 1995). Climatic fluctuations significantly
influence the phenology, distribution and physiology of
plants (Speer 2010; Ming-Lee etal. 2015). Although cycles
of climate change extend over centuries and millennia (e.g.,
climatic variations), current global warming is expected to
generate similar climatic fluctuations over the following dec-
ades. The rapid rate of change is expected to have a direct
effect on the capacity of forest species to adapt to future
climatic conditions (Helama etal. 2004;Tinoco-Rueda etal.
2009; Schoene and Bernier 2012; Rehm etal. 2015). More
specifically, ongoing precipitation and temperature varia-
tions might have a severe impact on tropical montane cloud
forests by influencing the phenology and distribution of sev-
eral plant species in these communities.
Apart from deforestation, current climate change repre-
sents the greatest threat to tropical montane cloud forests,
due to changes in the patterns of precipitation and cloud
Communicated by A. Bräuning.
* Isolda Luna-Vega
luna.isolda@gmail.com;
isolda_luna-vega@ciencias.unam.mx
1 Laboratorio de Biogeografía y Sistemática, Facultad de
Ciencias, Universidad Nacional Autónoma de México,
MexicoCity, Mexico
2 Departamento de Botánica, Instituto de Biología,
Universidad Nacional Autónoma de México, MexicoCity,
Mexico
Author's personal copy

Trees
1 3
immersion (e.g., fog, mist and cloud water), which are asso-
ciated with rising temperatures, habitat fragmentation, and
increasing green-house gas emissions (Price etal. 2011;
Ponce-Reyes etal. 2012). Reduced cloud immersion and
increased evapotranspiration, resulting from global warm-
ing, directly influence several ecological and phenological
processes in tropical montane cloud forests plant species,
such as masting events (Price etal. 2011; Esperón-Rodríguez
and Barradas 2015; FAO 2015).
Masting behavior occurs in many tree species in temper-
ate regions (Harper 1977), serving as an adaptive strategy to
climatic variation and/or as a strategy to avoid seed preda-
tion (Kelly 1994; Pearse etal. 2016). Several studies have
shown that temperature, precipitation, and phenological
events in masting years directly affect growth-ring width
and vessel traits (García-González and Fonti 2008; Fonti
etal. 2010;Speer 2010; González-González etal. 2013).
In recent decades (since 2001), dendroecological research
has provided important tools for describing historical–eco-
logical events and phenological variation in forest species
(Schweingruber 1996;Speer 2010; D´Arrigo etal. 2014;
Hacket-Pain etal. 2015; Amoroso etal. 2017). Such events
are inferred from variation in tree-ring width and vessel
traits, which, in turn, are used to reconstruct the forest his-
tory of relict and endemic tree species (Gareca etal. 2010;
Génova and Moya 2012; Rita etal. 2015). Several authors
have analyzed various environmental factors (e.g., maximum
and minimum temperature and precipitation) associated with
the timing of mass flowering in beech trees (Övergaard etal.
2007; Kon and Noda 2007; Sawada etal. 2008; Latte etal.
2015). Most of these authors suggest that flowering mostly
occurs after years with benign environmental conditions,
such as high temperatures during the summer months.
These environmental conditions promote high rates of car-
bon assimilation by trees, leading to enhanced flower bud
development and beechnut production. Several authors have
studied different factors that trigger flowering and, in conse-
quence, beechnut production. Masting events typically occur
after 2years with high temperature and low precipitation
during the summer months, preceded by a year with low
summer temperature and high precipitation (Matyas 1965;
Norton and Kelly 1988; Piovensan and Adams 2005; Över-
gaard etal. 2007; Burns 2012; Etemad and Sefidi 2017).
Temperature represents one of the most important envi-
ronmental factors affecting the growth of Fagus worldwide
(Fang and Lechowicz 2006). In addition, several authors
have suggested that high summer temperatures (June–July),
in a particular year, are strongly associated with the onset
of masting in Fagus during the following year (Ehnis 1981;
Suzuki etal. 2005; Kon and Noda 2007; Bradshaw etal.
2010; Hacket-Pain etal. 2015). For instance, Bayramza-
deh etal. (2008) and Noyer etal. (2017) reported that
vessels of Fagus trees develop structural modifications in
response to climatic and phenological events. These cli-
matic events (e.g., high temperature and precipitation) are
detected through temporal variations in tree-ring width in
angiosperms and gymnosperms, partly due to the increased
recovery-times of trees after such events (Speer 2010; Bry-
ukhanova and Fonti 2013).
Fagus grandifolia subsp. mexicana (Mexican beech) is a
Miocene relict species that is endemic to the tropical mon-
tane cloud forests of eastern Mexico. This species occurs at
elevations of 1450–1987m and is considered as endangered
under Mexican law (Téllez-Valdés etal. 2006;SEMARNAT
2010; González-Espinosa etal. 2011). Reports suggest that
Mexican beech diverged from Fagus grandifolia Ehrh, which
inhabits the USA and Canada, approximately 7 million years
ago (Manos and Stanford 2001; Denk and Grimm 2009).
Mexican beech exhibits synchronic masting, which might be
the result of autoecological reproductive strategies or a prod-
uct of environmental changes, such as persistent droughts
(Kelly 1994; Piovensan and Adams 2005).
The most extensive and least disturbed Mexican beech
forests are located in the state of Hidalgo, in eastern Mexico
(Rodríguez-Ramírez etal. 2013). These forests are character-
ized by the presence of masting events at every 2- to 8-year
intervals (Ehnis 1981; Pérez-Rodríguez 1999). It was found
that Mexican beech is susceptible to climatic variations,
such as those associated with higher elevations, drought,
and seasonal frosts (Ehnis 1981; Rodríguez-Ramírez etal.
2016, 2018). Natural disturbances, such as strong winds,
hurricanes, and storms, regulate the development of Mexi-
can beech forests (Peters 1992), causing suppression and
release events in tree-ring width (Peters 1995).
The relationship between tree-ring width and vessel traits
in masting events of Mexican beech trees and the climatic
factors that trigger these processes remain largely unknown
(Rodríguez-Ramírez etal. 2018). Because of this, our main
aim is to reconstruct historical masting events of Mexican
beech trees using dendroecological methods. The objec-
tives of this study are: (1) to identify how precipitation and
temperature are associated with masting events, and (2) to
identify if any differences exist in tree-ring widths and ves-
sel traits (e.g., diameter and frequency) between masting
and non-masting years occurring between the years 1980
and 2012.
Materials andmethods
Study area
We selected three fragments of Mexican beech forests
located in the Sierra Madre Oriental, which stretches
in a north–south direction throughout eastern Mexico
(Fig.1). Temperate climate (Cb sensu García 1988)
Author's personal copy

Trees
1 3
was characterized by mild temperatures (14.5–24.4°C),
including a dry cool season from November to January,
a dry warm season from early February to May, cool
summers (June–July) and a wet cool season from August
to October. Humidity levels are in the range of 60–85%
(Peters 1995; Williams-Linera etal. 2002). The soils of
the sites are vitric (Tv) and humic (Th) andosols (FAO-
UNESCO 1988) with light sandy-clay loam texture and
pH values of 4 to 6 (Peters 1995).
The Mexican beech forests are characterized by domi-
nant tree species with Holarctic affinities, such as Mexi-
can beech (F. grandifolia subsp. mexicana), Martínez
spruce (Picea martinezii T. F. Patterson), Mesoameri-
can yew (Taxus globosa Schltdl.), Magnolia (Magnolia
schiedeana Schltdl.), Patula pine (Pinus patula Schltdl.
& Cham.), Aztec pine (Pinus teocote Schltdl. & Cham.),
several oak species (Quercus meavei Valencia-A., Sabás
& Soto, Q. delgadoana S. Valencia, Nixon & L. M. Kelly
and Q. trinitatis Trel.), sweetgum (Liquidambar styraci-
flua L.), and Mexican Clethra (Clethra mexicana DC.).
These species are intermingled with evergreen tree spe-
cies with Neotropical affinities, such as Zapotillo (Sider-
oxylon portoricense subsp. minutiflorum (Pittier) T.D.
Penn.), Tarflower (Befaria aestuans L.), sweetwood
(Nectandra spp.), wild avocado (Persea spp.), and Sabino
(Podocarpus matudae Lundell) (Gual-Díaz and Rendón-
Correa 2014; Rzedowski 2015).
Sample collection andchronology development
At each site, 20 dominant Mexican beech trees were
selected (N = 60) based on the criteria established by Peters
(1992) and Hukusima etal. (2013): (1) diameter at breast
height (DBH) > 40cm; (2) a height of 10–25m; and (3)
no evidence of scars or rot. For each tree, two cores were
sampled at 1.3m (breast height) with a Häglof® borer. We
obtained a total of 120 wood cores from the three sites. At
each site, we revised three complete cross-section discs
from fallen trees as samples of growth patterns of Mexican
beech in each locality and to detect ecological events (e.g.,
fire scars, defoliations, growth suppressions, and releases)
affecting the forests (Fritts 1976). Sampled dominant
Mexican beech trees were selected randomly within each
site, ensuring that they encompassed the greatest possible
variation in habitat characteristics (e.g., slopes ranging
from 0.45° to 43.8° and distances of 30–500m from water
bodies).
The wood cores were dried at room temperature and were
then mounted and polished with successively coarse grits
(100 and 360) and fine grit sandpapers (400, 600, 3800, and
10,000) until the xylem cellular structure was visible in the
transverse plane. Tree-ring series along the cores were dated
by assigning calendar years to the rings through the identi-
fication of characteristic ring sequences (e.g., assigning to
each ring the year in which growth started) as suggested by
Fig. 1 Geographical location of
the three study sites of Fagus
grandifolia subsp. mexicana
(Mexican beech) in the tropical
montane cloud forests of the
Sierra Madre Oriental, Mexico.
A La Mojonera; B Medio
Monte; C El Gosco
20° 38’
98° 36
’
Author's personal copy

Trees
1 3
Stokes and Smiley (1968) and Rozas etal. (2015). This dat-
ing was verified with software COFECHA (Holmes 1983;
Grissino-Mayer 2001). We measured tree-ring widths using
a stereoscopic microscope and a Velmex tree-ring measuring
system with 0.001mm accuracy using the software TSAP-
Win v. 4.67c (Rinn 2003). The computer software COFE-
CHA allowed the identification of missing tree rings and
cross-dating errors. For the analyses, we excluded 60 wood
cores that were in poor condition (e.g., cores with evidence
of decay, cores that were not properly mounted, or cores
of short length) following the recommendations of Rozas
(2001).
To obtain the average of detrended tree-ring width indices
(RWI), we standardized raw ring-width series with autore-
gressive modeling to remove serial correlation using the
ARSTAN computer program (Cook and Holmes 1995). We
removed the non-climatic trends from each tree-ring series
using a cubic spline with a 50% response at 10-year periods.
This approach was flexible enough to accentuate high-fre-
quency climatic information and to reduce white noise from
non-climatic variance related to ontogenetic trends and/or
local disturbances (e.g., droughts, strong winds, hurricanes
and storms). Through this, we enhanced inter-annual vari-
ability, possibly related to masting events and the produc-
tion of narrow tree rings (Dittmar and Elling 2007; Gareca
etal. 2010; Drobyshev etal. 2014; Rodríguez-Ramírez etal.
2018).
We performed autoregressive modelling of each stand-
ardized series to remove temporal autocorrelation (Box
and Jenkins 1976) and maximize the climatic signal. To
produce a standardized chronology, the resulting indexed
series were averaged using a bi-weight mean to reduce the
influence of outliers (Cook and Holmes 1995). Temporal
autocorrelation in chronologies was prevalent, due to the
residual impact of growing conditions from previous years
(Speer etal. 2016).
Historical records ofMexican beech masting
We gathered data of past Mexican beech masting events
registered for each studied site for the years 1980, 1990,
1992, 1997, 2004, and 2012 (Ehnis 1981; Pérez-Rodríguez
1999; Godínez-Ibarra etal. 2007; Rodríguez-Ramírez etal.
2013). There are no records on masting events for other
Mexican beech populations along the distribution range of
this species.
Digitalization oftree‑ring width andvessels traits
For each site, we randomly selected five cores to obtain tree-
ring digital images for the recorded masting years, as well
as for the two consecutive years before and after masting
events. The wood cores were prepared using the finest grit
sandpaper (10,000) and eliminating any dust with a hair
drier. Since the ground tissue has very thick-walled fibers
and parenchyma cells with dark deposits, the vessels lumen
have a high contrast. In each digital image, we selected the
area occupied by each tree-ring between two wood rays (an
average of 7.5mm width × 9.1mm length). The area var-
ied with respect to tree-ring width before, during, and after
masting events [e.g., the widest and narrowest rings were
6.6mm width × 8.3mm length (ray to ray) and 2.5mm
width × 1.6mm length (minimum area of 54.7 and 4 mm2,
respectively; Fig.2)]. These digital images were captured
using a stereoscopic microscope (Axio Zoom.V16) with a
36 µm field of depth and saved in TIFF format with a digital
camera (AxioCam MRc 5, Zeiss) to a 1.3 µm resolution. Fig-
ure2 presents an example of a digitized cored with marked
radial tree-ring width and vessel traits (number of vessels/
mm2 and radial vessel diameter, µm); this technique has been
used successfully with other species (Venegas-González
etal. 2015). In each area, we quantified and measured all
the vessels present using the software ImageJ v. 1.5 with
manual detection (Java-based Image Processing, National
Institute of Health).
Reconstruction ofmasting events:
dendromastecology
Mast year reconstruction used two sources of data. We
first delimited the historical masting events in the tree-ring
digital image of trees from Medio Monte according to the
Tree-ring
2012
2013
2014
2011
2010
Mast year
Ray
201220041997 1992 1990 1980
100
mm
6.6 mm
8.3 mm
Fig. 2 Digitized images of a a representative wood-core of Mexi-
can beech. b Micro-section of the representative wood-core show-
ing annual tree rings (white lines) and vessels (white circles). Black
rectangles represent historical masting years and ENSO event (year
2012)
Author's personal copy

Trees
1 3
historical records of Mexican beech masting. This region
is considered as containing the most representative and
best preserved Mexican beech forests studied (Rodríguez-
Ramírez etal. 2013).
Finally, we compare variation in tree-ring width and ves-
sel traits before, during and after masting year. We analyzed
10 randomly selected cores and captured tree-ring digital
images, for the years ranging from 1847 to 2015 in Medio
Monte to reconstruct historical masting events. The reason
for restricting the analyses is because beech masting gener-
ally occurs in trees ≥ 40years in age (Peters 1992; Droby-
shev etal. 2010; Hukusima etal. 2013). Thus, we set 1886
as our initial year in the chronologies.
Earlier studies have suggested 2- to 8-year intervals
between masting events (Rodríguez-Ramírez etal. 2013);
therefore, we used this range of years to identify the tree-ring
patterns around the recorded masting years. We used data on
growth rings, before, during and after masting year to detect
differences in tree-ring width and vessel traits.
Climate data
Several authors have suggested that mass flowering in
beeches worldwide is triggered by two previous years with
high summer temperature and low precipitation, preceded by
a year with low summer temperature and high precipitation
(Piovensan and Adams 2005; Kon and Noda 2007; Över-
gaard etal. 2007; Drobyshev etal. 2010; Ascoli etal. 2017).
To evaluate the association between temperature and
precipitation with the masting data registered for Mexi-
can beech trees, we gathered climate data for the period
1978–2011 (http://clico m-mex.cices e.mx/). These data
included mean monthly values for minimum, average and
maximum temperatures (Tmin, Tavg, and Tmax), as well as total
annual precipitation (Prec) of a single year with the lowest
rainfall. We considered climatic data 2years before each
masting event (e.g., 1978, 1979, 1988, 1989, 1990, 1991,
1995, 1996, 2002, 2003, 2010, and 2011), which were cor-
roborated using information from Climate-data.org (http://
es.clima te-data.org/).
Variation ranges ofthetree‑ring widths andvessel
traits
We analyzed data on mean maximum temperatures and
Prec from climatic reconstructions for the State of Hidalgo
(Cardoza-Martínez etal. 2013). To complete the missing
information, we used the Drought-Net database (http://
www.droug ht-ne t.org/) (Lemoine etal. 2016). This approach
allowed the detection of narrow rings (≤ 1.00mm) in the
tree-ring digital images resulting from drought events, as
suggested by Rozas etal. (2015).
We performed an Analyses of Variance (ANOVA) and
Tukey multiple comparisons to assess if the values of tree-
ring widths and vessel traits (frequency and diameter) dif-
fer significantly between drought years, non-masting years
(NMY) and masting years (MY) in the studied forests. The
analyses were performed using the R-library vegan in R
(Version 2.14.0, http://www.r-proje ct.org; Oksanen etal.
2016).
Influence ofclimate ontree‑ring width andvessels
traits
To test the relationship between climatic variables (Tmax,
Tmin, Tavg and Prec) and tree-ring width and vessels traits,
we performed three non-metric multidimensional scaling
(NMDS) analyses. This approach allowed for the detection
of differences between tree-ring width developed in MY and
NMY, and to identify which climatic variables influence
tree-ring width and vessel traits.
NMDS ordination was based on Bray-Curtis distances
and 20 randomizations to determine the most stable solu-
tion. In addition, Wisconsin double standardization and R2
transformation were used as measures of ecological distance
(Kenkel and Orlóci 1986). An advantage of this method is
that the procedure is less dependent on data distribution than
constrained methods, such as principal component analyses.
The data were computed using the R-library vegan in the
statistical software R.
To evaluate the NMDS, we used the stress-plot function
and the Stress index to estimate R2 values between the vec-
tors and values of the ordination (R). The vectors for cli-
matic factors (Tmin, Tavg, Tmax, and Prec) and centroids were
superimposed using the envfit function. We used the ordisurf
function (within the vegan library) to draw the climatic vari-
ables in the space defined by two NMDS axes. Ordisurf fits
smooth surfaces on the ordination using Generalized Addi-
tive Models (GAMs) with thin-plate splines (Wood 2000;
Kindt and Coe 2005; Borcard etal. 2011). This approach
allowed us to observe the relationship of climatic variables
with tree-ring width and vessels traits. We used the Gener-
alized Cross-Validation statistic (GCV score) to select the
optimum model and minimize prediction error (Arlot and
Celisse 2010).
Results
Dendromastecology ofMexican beech
The independent chronologies for Mexican beech extended
up to 188years for La Mojonera, 168 for Medio Monte,
and 152 for El Gosco. A correlation between the three sites
Author's personal copy

Trees
1 3
was detected, where the mean sensitivity to climatic varia-
bles was high and similar among sites (Table1). Decreased
radial growth was associated with several historical ENSO
events (e.g., 1828–1830, 1850–1866, 1869–1890, 1905,
1913, 1918, 1929–1930, 1940, 1963, 1970, 1972, 1976,
1983, 1991, 1997, and 2012; Fig.3a).
The climatic reconstruction of Cardoza-Martínez
etal. (2013) for the state of Hidalgo, together with data
from Drought-Net, allowed us to recognize in the tree-
ring digital images of trees from Medio Monte, 15 addi-
tional historical masting events for Mexican beech trees,
to detect short 2-year periods (1955–1956, 1990–1992)
between masting events (Fig.3b). Notwithstanding, the
dendrochronological reconstruction of historical mast-
ing events showed two 8-year periods (1926–1934,
2004–2012) between MY (Fig.3b). Interestingly, these
periods revealed precipitation values ranging from 1748
to 1798mm, with a mean of ≥ 1750mm (Fig.3c). We
estimated a mean of 5.5years between MY recorded for
Mexican beech in the state of Hidalgo. Likewise, we iden-
tify differences between tree-ring digital images and ves-
sel traits formed during drought events, NMY and those
associated with MY. ANOVA showed that statistically sig-
nificant differences were present for vessel frequency and
diameter in the Mexican beech forests studied (Table2).
Vessel frequency and diameter were significantly higher
in NMY and decreased in MY (P < 0.05). Both traits dur-
ing the MY decreased one-fold or more compared to
drought events and NMY, maintaining the negative scaling
between these two variables (rsMY-0.27, P < 0.05). Not-
withstanding, tree-ring widths did not differ significantly
between NMY’s, drought years and MY’s (Fig.4a); the
same pattern was maintained for the reconstructed MY
events (Fig.4b).
Linking climate variation withtree‑ring width
andvessel traits
Ordination using NMDS showed that Prec was significantly
associated with tree-ring width at the three sites (Fig.5a;
GCV score: 0.044; stress: 0.104). In turn, Prec had a consid-
erable effect on vessel diameter and frequency (Fig.5b, c;
GCV score: 0.013, 0.044; stress: 0.120, 0.082). The NMDS2
values did not influence the Tmax for tree-ring width (Fig.5;
Table3). Notwithstanding, NMDS2 was slightly conspicu-
ous for Tmax with respect to vessel diameter and frequency
(Fig.5b, c).
Discussion
Tropical montane cloud forests drive important ecological,
hydrological, and climatological processes (Price etal.
2011). If tropical montane cloud trees begin to experience
drought conditions resulting in cavitation, forest die-off
might occur, leading to substantial changes in the growth
and regeneration capacity of many tree species. This study
shows that the radial growth of Mexican beech has been
affected by specific climatic events such as drought at each
Mexican beech forest studied (Fig.3; Table1). Compared
to the other two sites (La Mojonera and Medio Monte),
the Mexican beech trees at El Gosco were younger and had
lower rates of tree-ring width. This result reinforced the
observation that the Mexican beech forest at El Gosco has
been affected by anthropogenic and natural disturbances in
the recent past (Rodríguez-Ramírez etal. 2013). Possibly,
this effect might correspond to the phase of canopy clo-
sure, with the convergence of individual crowns and initia-
tion of intra-tree competition. This effect was observed by
Podocarpus salignus D. Don. in Chile (Rozas etal. 2016).
Climatic variations at each site might influence the tree-
ring width of beech trees (Gual-Díaz and Rendón-Correa
2014), which is reflected by the presence of narrow rings
(Fig.3).
Our results suggest that Mexican beech trees undergo
masting events, on average, every 5.5years and that these
events might be directly dependent on Prec. The results agree
with those obtained by Drobyshev etal. (2014) for Fagus
sylvatica from Europe. Climate change (e.g., high summer
temperature, ENSO events) involving diminished precipita-
tion might lead to the shortening of masting events (Fig.3).
Minimum annual precipitation plays a key role on tree-ring
width of Mexican beech trees (Fig.4; Table2), rather than
summer temperatures (Fig.3), as for other species of Fagus
Table 1 Growth-ring statistics for Fagus grandifolia subsp. mexi-
cana (Mexican beech) at the three study sites in the Tropical Montane
Cloud Forests of the Sierra Madre Oriental, Mexico
a Values obtained with COFECHA (Holmes 1999b)
b Values statistically different using a Mann–Whitney test (P = 0.01)
c Values obtained with ARSTAN (Cook and Holmes 1999)
Statistics La Mojonera Medio Monte El Gosco
Sampled trees 20 20 20
Crossdated seriesa24 28 28
Master series (years) 1828–2015 1847–2015 1863–2015
Crossdated ringsa2198 3094 2700
Series intercorrelationa0.67 0.68 0.71
Mean sensitivitya0.39 0.33 0.36
Autocorrelationa0.50 0.56 0.51
Mean/median age (years)b93.29/89 110.5/119.5 96.5/92
Common interval 1942–2015 1899–2015 1949–2015
Signal to noise ratioc27.10 16.21 21.72
Author's personal copy

Trees
1 3
(Drobyshev etal. 2014; Hacket-Pain etal. 2015). These cli-
matic fluctuations (temperature and precipitation) are con-
gruent with the patterns observed in other deciduous tree
species in montane forests, such as Quercus ilex Lour., Olea
europea L., and Ilex aquifolium L. (Abrantes etal. 2013;
Rossi etal. 2013; Rita etal. 2015).
Our results revealed no significant associations between
tree-ring width and Tmax (Table3; Fig.5), which has been
proposed as the main factor affecting growth in other
species of Fagus with northern distributions (Suzuki
etal. 2005; Kon and Noda 2007; Bradshaw etal. 2010;
Drobyshev etal. 2014; Hacket-Pain etal. 2015). The par-
ticular growth pattern of Mexican beech is the result of
its southernmost distribution compared with other Fagus
species worldwide. This phenomenon reflects the different
plant associations and climatic conditions in which Mexi-
can beech thrive (Fang and Lechowicz 2006; Rodríguez-
Ramírez etal. 2016, 2018).
Fig. 3 a Ring-width chronolo-
gies for Mexican beech forests.
Black circles represent ENSO
events and gray squares histori-
cal masting. Gray areas indicate
the period (1978–2015) includ-
ing ring-width chronologies for
masting years. b Ring-width
chronologies and masting events
for the Medio Monte site. Black
arrows represent recorded
masting years and white arrows
represent reconstructed masting
years; and c reconstruction of
annual precipitation in eastern
Mexico for the period 1890–
2015 (modified from Cardoza-
Martínez etal. 2013)
ENSO events
Ring-width index (RWI)
0
0.5
1
1.5
2
2.5
3
Historical masting records
Medio Monte
La Mojonera
El Gosco
0
500
1000
1500
2000
2500
3000
3500
Annual precipitation (mm)
0
0.2
0.4
0.6
0.8
1
1.2
1.4
1.6
Ring width-i ndex (RWI)
A
B
Years
C
Author's personal copy

Trees
1 3
The observed differences in tree-ring width between MY
and NMY in Mexican beech are indicative of the adaptive
mechanisms of these trees to masting and climatic events
(even ENSO events such as 2012, Figs.2, 4; Table2). The
production of narrow rings in response to masting events,
independent of climatic events (such as droughts), has also
been reported in other Fagus species [e.g., F. grandifolia
Ehrh in USA (Wason etal. 2017); F. crenata Blume in Japan
(Sawada etal. 2008); and F. sylvatica L. in Europe (Hacket-
Pain etal. 2015)]. Our results showed that tree-ring width
within the MY had narrower variation than that of NMY
or drought years. Therefore, instead of growth, resources
are assigned to beechnut production during MY because of
water deficits.
Our study revealed that vessel-related anatomical traits
(frequency and diameter) adjust in response to drought
events, NMY, and MY, corroborating the high plasticity
mentioned for other Fagus species (Bayramzadeh etal.
2008; Pourtahmasi etal. 2011; Yin etal. 2016; Noyer
etal. 2017). When a masting event occurs, Mexican beech
develops fewer and narrower vessels, even narrower than in
drought years (Fig.4), maintaining their negative scaling.
This finding is interesting because Mexican beech produces
narrow vessels during MY to ensure hydraulic safety. Thus,
vascular cambium modifications may be related with a
trade-off between growth (narrow vessels during short peri-
ods of time) and beechnut production (Fig.4). The plasticity
in vessel frequency and diameter regulates water-transport
efficiency, reflecting the ability of tropical montane cloud
trees to adapt to climatic fluctuations as droughts and phe-
nological events (Eller etal. 2017;vonArx etal. 2013;
Rodríguez-Ramírez etal. 2018). Further anatomical studies
of Fagus species worldwide are needed to understand vessel
plasticity during masting events.
Structural modifications were indicated in differences
in vessels traits during MY. These modifications might be
related to hormonal changes (Chan and Cain 1967; Aloni
1987; Tyree and Zimmermann 2002; Rita etal. 2015) and
environmental conditions, such as temperature, precipi-
tation, wind, and inter-annual differences (Kelly 1994;
Pearse etal. 2016). Similar modifications have been
observed in other beech trees species such as Fagus orien-
talis in Middle East (Eşen 2000;Pourtahmasi etal. 2011);
Fagus sylvatica in Europe (Hacket-Pain etal. 2015); and
F. crenata in Japan (Kabeya etal. 2017). In these species,
individual trees structurally modify their vessels before
masting (Speer 2001). However, other biotic and abiotic
factors (e.g., volatile organic chemicals, pathogens, fires,
pollution, environmental factors) are needed to gener-
ate specific structural changes, with carbon distribution
contributing to the modification of vessels traits and the
resulting development of narrow tree rings (Sass and Eck-
stein 1995; Anderegg and Meinzer 2015). Such narrow
tree rings appear to be essential for the onset of masting
events (Övergaard etal. 2007).
We used several dendroecological techniques to detect
differences in tree-ring width between MY and NMY
(Fig.5), which allowed for the reconstruction of historical
masting events that are not on record. Our results suggest
that reduced annual precipitation (814–998mm) directly
influences tree-ring width and vessel traits. This reconstruc-
tion suggests that masting events, both over short (2years)
Table 2 Values (mean ± SD
and CV) for the Mexican beech
forest studied
Bold values represent significant differences among variables as indicated by ANOVA and Tukey post hoc
tests at P < 0.05
Sites Tree-ring width (mm) Vessel frequency (Vessel/
mm2)
Radial vessel diameter
(µm)
Mean CV Mean CV Mean CV
La Mojonera
Drought year 0.81 ± 0.80 1.32 110 ± 103 10.3 85 ± 9.4 2.54
NMY 1.1 ± 1.12 0.8 250 ± 232 18.3 90.2 ± 10.1 5.87
MY 0.7 ± 0.7 1.12 70 ± 69 0.58 49 ± 5.01 1.0
Medio Monte
Drought year 0.80 ± 0.91 2.28 100 ± 112 1.9 91.4 ± 9.1 4.32
NMY 1.13 ± 1.45 3.84 120 ± 132 2.35 82 ± 8.7 4.56
MY 0.77 ± 0.70 1.0 72 ± 71 1.00 53 ± 5.1 3.9
El Gosco
Drought year 0.79 ± 0.79 2.27 150 ± 148 2.18 71 ± 8.1 19.4
NMY 1.0 ± 1.35 1.11 250 ± 249 6.27 92 ± 9.3 36.5
MY 0.81 ± 0.80 1.23 71 ± 72 1.00 48.9 ± 4.3 1.56
F2,22 = 5.00
P ≤ 0.0001 F2,22 = 7.18
P = 0.015 F2,22 = 2.37
P = 0.012
Author's personal copy

Trees
1 3
and long (8years) time intervals, have occurred repeatedly
in the past when the required precipitation is reached (Fig.5)
as suggested by Peters (1995).
This study advances our understanding on the reproduc-
tive strategies of Mexican beech in the face of climatic
fluctuations, which appear to have a strong influence on
phenological events, such as masting synchrony (Vac-
chiano etal. 2016). The observed relationship of Prec with
tree-ring width and vessels traits shows that this species
has adapted to the southern part of its distribution range
by developing narrow rings and using its resources for
beechnut production.
Finally, we suggest that further research should focus
on how climatic phenomena (e.g., El Niño and La Niña
effects) and deforestation affect the masting behavior of
trees (Burns 2012; Fletcher 2015). More specifically,
future studies should address the possible reduction in
reproductive potential and survival of Mexican beech in
the tropical montane cloud forests of the Sierra Madre
Oriental.
0.2
0.4
0.6
0.8
1.0
1.2
1.4
1.6
1.8
2.0
2.2
0
50
100
150
200
250
300
P<0.05
)mm(htdiwgnir-eerT
)²mm(ycneuqerflesseV
*
*Represents a masting and a drought event
Drought yearsNMY MY
20
40
60
80
100
120
140
160
180
*
P<0.05
(retemaidlesseV m)
Tree-ring width (mm)
0.50
0.55
0.60
0.65
0.70
0.75
0.80
0.85
0.90
40
45
50
55
60
65
70
75
Reconstruction of historical MY
32
34
36
38
40
42
44
46
)²mm(ycneuqerflesseV
(retemaidlesseV m)
AB
Fig. 4 Box plots showing the variation ranges of the tree-ring width,
vessel frequency and diameter between drought years, NMY and MY.
The upper and lower limits of the boxes represent the 75 and 25th
percentiles, and whiskers represent the 90 and 10th percentile. Black
circles show outliers. The solid lines within each box indicate statis-
tically significant differences (P < 0.05). a Historical masting years;
and b reconstruction of historical masting events. *Shows masting
and drought events
Author's personal copy

Trees
1 3
Author contribution statement ECHRR contributed in the
research by designing the experiment, writing the paper
and running the data analyses; TT helped writing the paper,
designing the experiment and running the data analyses; ILV
supervised and revised all the project stages, including the
manuscript writing.
Acknowledgements We wish to thank Osvaldo Franco-Ramos and
Lorenzo Vázquez-Selem for their help with tree-ring measurements
and for lending the necessary equipment; Susana Guzmán Gómez and
María del Carmen Loyola Blanco (Laboratorio de Microscopía y Foto-
grafía de la Biodiversidad II, Instituto de Biología, UNAM) for techni-
cal assistance with the digital photographs; Othón Alcántara-Ayala and
Rodrigo Ortega García for their support during field work; Ana Paola
Martínez-Falcón for assistance with the statistical analyses; Santiago
Ramírez-Barahona and Carlos Solís Hay for his critical observations.
This research was financed by the project PAPIIT IN223218. The first
author thanks the financial support granted by the postdoctoral fellow-
ship DGAPA-UNAM 2015-2016.
Compliance with ethical standards
Conflict of interest The authors declare that they have no conflict of
interest.
References
Abrantes J, Campelo F, García-González I, Nabais C (2013) Envi-
ronmental control of vessel traits in Quercus ilex under Medi-
terranean climate: relating xylem anatomy to function. Trees
27:655–662
Aloni R (1987) Differentiation of vascular tissues. Annu Rev Plant
Physiol 38:179–204
NMDS2
NMDS1
Stress: 0.104
GVC score: 0.044
Stress: 0.120
GVC score: 0.013
Stress: 0.082
GVC score: 0.044
Precipitation
T max
Precipitation
T max
Precipitation
10-1
-0.5
0.0
0.5
-0.5
0.0
0.5
-0.5
0.0
0.5
A
B
C
Fig. 5 Non-metric multidimensional scaling (NMDS) ordination, based
on the relationship of climatic variables (Tmax, Tmin, Tavg and Prec) on the
tree-ring width and xylem vessels. a Tree-ring width, b vessel frequency;
and c vessel diameter in Mexican beech. Labels represent growth rings
for each year and site. LM, La Mojonera; MM, Medio Monte; EG, El
Gosco. Variable values are indicated with bold numbers and dotted lines
Table 3 Climatic variables associated with ring width index (RWI),
vessel frequency and diameter during masting years in Mexican
beech. In bold are represented statistically significant variables (vec-
tors)
Signif. Codes: 0 ‘***’ 0.001 ‘**’ 0.01 ‘*’ 0.05 ‘·’ 0.1 ‘ ’ 1
P values based on 1000 permutations
Metrics Vectors NMDS1 NMDS2 R2Pr (> R)
RWI Tmax 0.756 − 0.024 0.012 0.888
Tmin − 0.177 − 0.984 0.137 0.266
Tavg 0.978 0.209 0.104 0.371
*Precipitation 0.610 − 0.724 0.101 0.054
Vessel fre-
quency
·Tmax 0.443 − 0.896 0.258 0.077
Tmin − 0.147 − 0.895 0.125 0.112
Tavg − 0.124 − 0.795 0.101 0.345
*Precipitation 0.596 − 0.700 0.128 0.062
Vessel diam-
eter
·Tmax 0.396 − 0.918 0.265 0.069
Tmin − 0.168 − 0.887 0.139 0.245
Tavg 0.885 0.210 0.124 0.198
*Precipitation 0.588 − 0.768 0.113 0.084
Author's personal copy

Trees
1 3
Amoroso MM, Daniels LD, Baker PJ, Camarero JJ (2017) Dendroecol-
ogy: tree-ring analyses applied to ecological studies. Springer,
Switzerland
Anderegg WRL, Meinzer FC (2015) Wood anatomy and plant hydrau-
lics in a changing climate. In: Hake U (ed) Functional and eco-
logical xylem anatomy. Springer, Switzerland, pp235–253
Arlot S, Celisse A (2010) A survey of cross-validation procedures for
model selection. Stat Surv 4:40–79
Ascoli D, Vacchiano G, Turco M, Conedera M, Drobyshev I, Mar-
inger J, Motta R, Hacket-Pain A (2017) Inter-annual and decadal
changes in teleconnections drive continental-scale synchroniza-
tion of tree reproduction. Nat Commun 8(2205):1–9
Bayramzadeh V, Funada R, Kubo T (2008) Relationships between ves-
sel element anatomy and physiological as well as morphological
traits of leaves in Fagus crenata seedlings originating from dif-
ferent provenances. Trees 22:217–224
Borcard D, Gillet F, Legendre P (2011) Numerical ecology with R. Use
R! series. Springer, New York
Box GEP, Jenkins GM (1976) Time series analysis: forecasting and
control. Holden-Day, San Francisco
Bradshaw RHW, Kito K, Gieseckre T (2010) Factors influencing the
Holocene history of Fagus. For Ecol Manag 259:2204–2212
Bryukhanova M, Fonti P (2013) Xylem plasticity allows rapid hydrau-
lic adjustment to annual climatic variability. Trees 27:485–496
Burns KC (2012) Masting in a temperate tree: evidence for environ-
mental prediction. Austral Ecol 37:175–182
Cardoza-Martínez GF, Cerano-Paredes J, Villanueva-Díaz J, Cer-
vantes-Martínez R, Guerra de la Cruz V, Estrada-Ávalos J (2013)
Annual precipitation reconstruction of the Eastern region of
Tlaxcala state. Rev Mex Cie Forest 5:110–127
Chan BC, Cain JC (1967) The effect of seed formation on subsequent
flowering in apple. J Am Soc Hortic Sci 91:63–68
Climate-data.org (2016) Historical average temperature. http://clima
te-data.org/. Accessed 10 Oct 2016
Cook ER, Holmes RL (1995) Guide for computer program ARSTAN.
In: Grissino-Mayer HD, Holmes RL, Fritts HC (eds) The Inter-
national tree-ring data bank program library version 2.0 User’s
Manual, Laboratory of Tree-Ring Research. University of Ari-
zona, Arizona, pp75–87
Cook ER, Holmes RL (1999) Program ARSTAN-chronology devel-
opment with statistical analysis (users manual for program
ARSTAN). Laboratory of Tree-Ring Research. University of
Arizona, USA
D´Arrigo R, Davi N, Jacoby G, Wilson R, Wiles G (2014) Dendrocli-
matic studies: trees growth and climate change in northern forest.
American Geophysical Union, Canada
Denk T, Grimm GW (2009) The biogeographic history of beech trees.
Rev Palaeobot Palynol 158:83–100
Dittmar C, Elling W (2007) Dendroecological investigation of the vital-
ity of Common Beech (Fagus sylvatica L.) in mixed mountain
forests of the Northern Alps (South Bavaria). Dendrochronologia
2:37–56
Drobyshev I, Övergaard R, Saygin I, Niklasson M, Hickler T, Karlsson
M, Sykes MT (2010) Masting behaviour and dendrochronology
of European beech (Fagus sylvatica L.) in southern Sweden. For
Ecol Manag 259:2160–2170
Drobyshev I, Niklasson M, Mazerolle MJ, Bergeron Y (2014) Recon-
struction of a 253-year long mast record of European beech
reveals its association with large scale temperature variability
and no long-term trend in mast frequencies. Agric For Meteorol
192–193:9–17
Ehnis DE (1981) Fagus mexicana Martínez: su ecología e importan-
cia. B. Sc. Thesis, Facultad de Ciencias, Universidad Nacional
Autónoma de México, Mexico City
Eller CB, Barros FV, Bittencourt PRL, Rowland L, Mencuccini M,
Oliveira RS (2017) Xylem hidraulic safety and construction costs
determine tropical tree growth. Plant Cell Environ 2018:1–15
Eşen D (2000) Ecology and control of Rhododendron (Rhododendron
ponticum L.) in Turkish eastern beech (Fagus orientalis Lipsky)
forest. Doctoral thesis. Virginia Polytechnic Institute and State
University, Blacksburg, Virginia, USA
Esperón-Rodríguez M, Barradas VL (2015) Comparing environmental
vulnerability in the montane cloud forest of eastern Mexico: a
vulnerability index. Ecol Indic 52:300–310
Etemad V, Sefidi K (2017) Seed production and masting behaviour in
Oriental beech (Fagus orientalis Lipsky) forests of northern Iran.
Forest Ideas 23:65–76
Fang J, Lechowicz MJ (2006) Climatic limits for the present distri-
bution of beech (Fagus L.) species in the world. J Biogeogr
33:1804–1819
FAO (2015) Global forest resources assessment 2015: how are the
world´s forest changing? Food Agriculture Organization of the
United Nations, Rome
FAO-UNESCO (1988) Soil map of the world. Revised legend. World
soil resources report 60. FAO-UNESCO, Rome
Fletcher MS (2015) Mast seeding and the El Niño-Southern Oscilla-
tion: a long-term relationship? Plant Ecol 216:527–533
Fonti P, von Arx G, García-González I, Eilmann B, Sass-Klaassen U,
Gärtner H, Eckstein D (2010) Studying global change through
investigation of the plastic responses of xylem anatomy in tree
rings. New Phytol 185:42–53
Fritts HC (1976) Tree rings and climate. Academic Press, London
García E (1988) Modificaciones al sistema de clasificación climática
de Köppen, México, Offset Larios. Mexico City
García-González I, Fonti P (2008) Ensuring a representative sam-
ple of earlywood vessels for dendroclimatological studies: an
example from two ring-porous species. Trees 22:237–244
Gareca EE, Fernández M, Stanton S (2010) Dendrochronological
investigation of the high Andean tree species Polylepis besseri
and implications for management and conservation. Biodivers
Conserv 19:1839–1851
Génova M, Moya P (2012) Dendroecological analysis of relict pine
forests in the center of the Iberian Peninsula. Biodivers Con-
serv 21:2949–2965
Godínez-Ibarra O, Ángeles-Pérez G, López-Mata L, García-Moya
E, Valdez-Hernández JV, Santos-Posadas H, Trinidad-Santos
A (2007) Lluvia de semillas y emergencia de plántulas de
Fagus grandifolia subsp. mexicana en La Mojonera, Hidalgo,
México. Rev Mex Biodivers 78:117–128
González-Espinosa M, Meave JA, Lorea-Hernández FG, Ibarra-Man-
ríquez G, Newton AC (2011) The Red List of Mexican cloud
forest trees. Fauna & Flora International (FFI), Cambridge
González-González BD, Rozas V, García-González I (2013) Early
vessels of the sub-Meditterranean oak Quercus pyrenaica have
greater plasticity and sensitivity than those of the temper-
ate Q. petrae at the Atlantic-Mediterranean boundary. Trees
28:237–252
Grissino-Mayer HD (2001) Evaluating crossdating accuracy: a manual
and tutorial for the computer program COFECHA. Tree Ring
Res 57:205–221
Gual-Díaz M, Rendón-Correa A (2014) Bosques mesófilos de montaña
de México: diversidad, ecología y manejo. Comisión Nacional
para el Conocimiento y Uso de la Biodiversidad, Mexico City
Hacket-Pain AJ, Friend AD, Lageard JGA, Thomas PA (2015) The
influence of masting phenomenon on growth-climate relation-
ships in trees: explaining the influence of previous summers´
climate on ring width. Tree Physiol 35:319–330
Harper JL (1977) Population biology of plants. Academic Press, London
Helama S, Lindholm M, Timonen M, Eronen M (2004) Detec-
tion of climate signal in dendrochronological data analysis: a
Author's personal copy

Trees
1 3
comparison of tree-ring standardization methods. Theor Appl
Climatol 79:239–254
Holmes RL (1983) Computer-assisted quality control in tree-ring dat-
ing and measurement. Tree Ring Bull 43:69–78
Hukusima T, Matsui T, Nishio T, Pignatti S, Yang L, Lu SY etal
(2013) Phytosociology of the beech (Fagus) forest in East Asia.
Springer, Heidelberg
Kabeya D, Inagaki Y, Noguchi K, Han Q (2017) Growth rate reduction
causes a decline in the annual incremental trunk growth in mast-
ing Fagus crenata trees. Tree Physiol 37:1444–1452
Kelly D (1994) The evolutionary ecology of mast seeding. Trees
9:465–470
Kenkel NC, Orlóci L (1986) Applying metric and nonmetric multidi-
mensional scaling to ecological studies: some new results. Ecol-
ogy 67:919–928
Kindt R, Coe R (2005) Tree diversity analysis. A manual and software
for common statistical methods for ecological and biodiversity
studies. World Agroforestry Centre (ICRAF), Nairobi
Kon H, Noda T (2007) Experimental investigation on weather cues for
mast seeding of Fagus crenata. Ecol Res 22:802–806
Latte N, Lebourgeois F, Claessens H (2015) Increased tree-growth syn-
chronization of beech (Fagus sylvatica L.) in response to climate
change in northwestern Europe. Dendrochronologia 33:69–77
Lemoine N, Sheffield J, Dukes JS, Knapp AK, Smith MD (2016) Ter-
restrial precipitation analysis (TPA): a resource for character-
izing long-term precipitation regimes and extremes. Methods
Ecol Evol 7:1396–1401
Manos PS, Stanford AM (2001) The historical biogeography of
Fagaceae: tracking the tertiary history of temperate and sub-
tropical forests of the northern hemisphere. Int J Plant Sci
162:S77–S93
Matyas V (1965) Some ecological factors affecting the periodicity of
fruit in oak and beech. Erdesz Kutatas Budapest 61:99–121 (in
Hungarian with German summary)
Ming-Lee T, Markowitz EM, Howe PD, Ko CY, Leiserowitz AAA
(2015) Predictors of public climate change awareness and risk
perception around the world. Nat Clim Change 5:1014–1020
Norton DA, Kelly D (1988) Mast seeding over 33 years by Dacrydium
cupressinum Lamb. (rimu) (Podocarpaceae) in New Zealand: the
importance of economies of scale. Funct Ecol 2:399–408
Noyer E, Lachenbruch B, Dlouhá J, Collet C, Ruelle J, Ningre F,
Fournier (2017) Xylem traits in European beech (Fagus sylvatica
L.) display a large plasticity in response to canopy release. Ann
For Sci 76:46
Oksanen J, Blanchet FG, Kindt R, Legendre P, Michin PR, Hara RBO´,
Simpson GL, Solymos P, Stevens MHH, Wagner H (2016)
Vegan: community ecology package. R package version 2.3-3.
http://cran.r-proje ct.org. Accessed 20 Nov 2016
Övergaard R, Gemmel P, Karlsson M (2007) Effects of weather condi-
tions on mast year frequency in beech (Fagus sylvatica L.) in
Sweden. Forestry 80:555–565
Pearse IS, Koenig WD, Kelly D (2016) Mechanisms of mast seeding
resources, weather, cues, and selection. New Phytol 212:546–562
Pérez-Rodríguez PM (1999) Las hayas de México, monografía de
Fagus grandifolia spp. mexicana. Universidad Autónoma de
Chapingo, Chapingo, Mexico City
Peters R (1992) Ecology of beech forests in the northern Hemisphere.
Doctoral Thesis, Wageningen Agricultural University, Wagen-
ingen, Germany
Peters R (1995) Architecture and development of Mexican beech forest.
Vegetation science in forestry. In: Box EO, Peet RK, Masuzawa
T, Yamada I, Fujiwara K, Maycock PF (eds) Vegetation science
in forestry. Kluwer Academic Publishers, Dordrecht, pp325–343
Piovensan G, Adams JM (2005) The evolutionary ecology of masting:
does the environmental prediction hypothesis also have a role in
mesic temperate forests? Ecol Res 20:739–743
Ponce-Reyes R, Reynoso-Rosales VH, Watson JEM, Van Der Wal J,
Fuller RA, Pressey RL, Possingham HP (2012) Vulnerability
of cloud forest reserves in Mexico to climate change. Nat Clim
Change 2:448–452
Pourtahmasi K, Lotfiomran N, Bräuning A, Parsapajouh D (2011)
Tree-ring width and vessel characteristics of Oriental beech
(Fagus orientalis) along an altitudinal gradient in the Caspian
forests, Northern Iran. IAWA J 32:461–473
Price MF, Gratzer G, Duguma LA, Kohler T, Maselli D, Rosalaura R
(2011) Mountain forests in a changing world-realizing values,
addressing challenges. FAO/MPS and SDC, Rome
Rehm EM, Olivas P, Stroud J, Feeley KJ (2015) Losing your edge:
climate change and the conservation value of range-edge popula-
tions. Ecol Evol 5:4315–4326
Rinn F (2003) TSAP-Win. Time series analysis and presentation for
dendrochronology and related applications for Microsoft Win-
dows, version 4.64. http://www.rinntech.de/content/view/17/48/
lang,english/index.html. Accessed 15 Dec 2016
Rita A, Cherubini P, Leonardi S, Todaro L, Borghetti M (2015) Func-
tional adjustments of xylem anatomy to climatic variability:
insights from long-term Ilex aquifolium tree-ring series. Tree
Physiol 35:817–828
Rodríguez-Ramírez EC, Sánchez-González A, Ángeles-Pérez G (2013)
Current distribution and coverage of Mexican beech forests
Fagus grandifolia subsp. mexicana in Mexico. Endanger Spe-
cies Res 20:205–216
Rodríguez-Ramírez EC, Sánchez-González A, Ángeles-Pérez G (2016)
Relationship between vegetation structure and microenvironment
in Fagus grandifolia subsp. mexicana forest relicts in Mexico. J
Plant Ecol 138:1–11
Rodríguez-Ramírez EC, Luna-Vega I, Rozas V (2018) Tree-ring
research of Mexican beech (Fagus grandifolia subsp. mexicana)
a relict tree endemic to eastern Mexico. Tree Ring Res 74:1
Rossi L, Sebastiani L, Tognetti R, d´Andria R, Morelli G, Cherubini P
(2013) Tree-ring wood anatomy and stable isotopes show struc-
tural and functional adjustments in olive trees under different
water availability. Plant Soil 372:567–579
Rozas V (2001) Detecting the impact of climate and disturbances
on tree-rings of Fagus sylvatica L. and Quercus robur L. in
a lowland forest in Cantabria, Northern Spain. Ann For Sci
58:237–251
Rozas V, Camarero JJ, Sangüesa-Barreda G, Souto M, García-González
I (2015) Summer drought and ENSO-related cloudiness dis-
tinctly drive Fagus sylvatica growth near the species rear-edge
in norther Spain. Agric For Meteorol 201:153–164
Rozas V, Le Quesne C, Muñoz A, Puchi P (2016) Climate and growth
of Podocarpus salignus in Valdivia. Chile Dendrobiol 76:3–11
Rzedowski J (2015) Catálogo preliminar de las especies de árboles
silvestres de la Sierra Madre Oriental. In: Flora del Bajío y de
regiones adyacentes, fascículo complementario XXX. Instituto
de Ecología. A.C. Centro Regional del Bajío Pátzcuaro, Micho-
acán, Mexico City
Sass U, Eckstein D (1995) The variability of vessel size in beech
(Fagus sylvatica L.) and its ecophysiological interpretation.
Trees 9:247–252
Sawada H, Kaji M, Oomura K, Igarashi Y (2008) Influences of mast
seedling on tree growth dynamics of Fagus crenata and Fagus
japonica in central Honshu, Japan. J Jpn For Soc 90:129–136
Schoene DHF, Bernier PY (2012) Adapting forestry and forest to cli-
mate change: a challenge to change the paradigm. For Policy
Econ 24:12–19
Schweingruber FH (1996) Tree ring and environment: dendroecology.
Paul Haupt AG Berne, Switzerland
SEMARNAT, Secretaría del Medio Ambiente y Recursos Naturales
(2010) Norma Oficial Mexicana NOM-059-SEMARNAT-2010.
Protección ambiental-Especies nativas de México de flora y
Author's personal copy

Trees
1 3
fauna silvestres-Categorías de riesgo y especificaciones para
su inclusión, exclusión o cambio-Lista de especies en riesgo.
Diario Oficial de la Federación. Segunda Sección, México, Dis-
trito Federal [online]. http://www.profe pa.gob.mx/innov aport
al/file/435/1/NOM_059_SEMAR NAT_2010.pdf. Accessed 06
Apr 2016
Speer JH (2001) Oak mast history from dendrochronology: a new tech-
nique demonstrated in the southern Appalachian region. Disser-
tation, University of Tennessee, Knoxville, USA
Speer JH (2010) Fundamentals of tree ring research. University of
Arizona Press, Tucson
Speer JH, Bräuning A, Zhang Q, Pourtahmasi K, Gaire NP, Dawadi
B etal (2016) Pinus roxburghii stand dynamics at a heavily
impacted site in Nepal: research through an educational field-
week. Dendrochronologia 41:2–9
Stokes MA, Smiley TL (1968) An introduction to tree-ring dating.
University of Chicago Press, Chicago
Suzuki W, Osumi K, Masaki T (2005) Mast seeding and its spa-
tial scale in Fagus crenata in northern Japan. For Ecol Manag
205:105–116
Téllez-Valdés O, Dávila-Aranda P, Lira-Saade R (2006) The effects of
climate change on the long-term conservation of Fagus grandi-
folia var. mexicana, an important species of the cloud forest in
eastern Mexico. Biodivers Conserv 15:1095–1107
Tinoco-Rueda JA, Toledo-Medrano ML, Carrillo-Negrete IJ,
Monterroso-Rivas I (2009) Clima y variabilidad climática en
los municipios de Hidalgo con presencia de bosque mesófilo
de montaña. In: Monterroso-Rivas AJ (ed) El bosque mesófilo
en el estado de Hidalgo. Perspectiva ecológica frente al cam-
bio climático. Universidad Autónoma Chapingo, Mexico City,
pp71–98
Tyree MT, Zimmermann MH (2002) Xylem structure and the ascent
of sap. Springer, Berlin
Vacchiano G, Hacket-Pain A, Turco M, Motta R, Maringer J, Conedera
M, Drobyshev I, Ascoli D (2016) Spatial patterns and broad-
scale weather cues of beech mast seeding in Europe. New Phytol
215:595–608
Venegas-González A, von Arx G, Chagas MP, Filho MT (2015) Plastic-
ity in xylem anatomical traits of two tropical species in response
to intra-seasonal climate variability. Trees 29:423–435
von Arx G, Kueffer C, Fonti P (2013) Quantifying plasticity in vessel
grouping added value from the image analysis tool Roxas. IAWA
J 34:433–445
Wason JW, Dovciak M, Beier CM, Battles JJ (2017) Tree growth is
more sensitive than species distributions to recent changes in
climate and acidic deposition in the northeastern United States.
J Appl Ecol 54:1648–1657
Webster GL (1995) The panorama of Neotropical cloud forest. In:
Churchill SP, Balslev H, Forero E, Luteyn JL (eds) Biodiversity
and conservation of Neotropical Montane Forests. The New York
Botanical Garden, New York, pp53–57
Williams-Linera G, Rowden A, Newton AC (2002) Distribution and
stand characteristics of relict populations of Mexican beech
(Fagus grandifolia var. mexicana). Biol Cons 109:27–36
Wood SN (2000) Modelling and smoothing parameter estimation with
multiple quadratic penalties. J R Stat Soc Ser B 62:413–428
Yin J, Fridley JD, Smith MS, Bauerle TL (2016) Xylem vessel traits
predict the leaf phenology of native and non-native understorey
species of temperate deciduous forests. Funct Ecol 30:206–214
Author's personal copy