Cloud forest dynamics in the Mexican neotropics during the last 1300 years: CLOUD FOREST DYNAMICS IN...

Cloud forest dynamics in the Mexican neotropics duringthe last 1300 years

B L A N C A L . F I G U E R O A - R A N G E L *, K AT H Y J . W I L L I S w z and M I G U E L O LV E R A - VA R G A S *

*Departamento de Ecologıa y Recursos Naturales-IMECBIO, Centro Universitario de la Costa Sur, Universidad de Guadalajara,

Apartado Postal 108, Autlan de Navarro, Jalisco, C.P. 48900, Mexico, wOxford Long-Term Ecology Laboratory, Oxford University

Centre for the Environment, School of Geography, South Parks Road, Oxford OX1 3QY, UK, zDepartment of Biology, University of

Bergen, N-5007 Bergen, Norway

Abstract

Key questions for understanding the resilience and variability of Mexican Neotropical

cloud forest assemblages in current and future climate change include: How have human

disturbances and climate change affected the dynamics of the cloud forest assemblage?

What are the predominant processes responsible for its present day composition and

distribution? Are the current conservation strategies for the cloud forest in accordance

with preserving its natural variability through time? In this study, the temporal dynamics

of the cloud forest in west-central Mexico over the last � 1300 years were reconstructed

using palaeoecological techniques. These included analyses of fossil pollen, microfossil

charcoal, and sediment geochemistry. Results indicated that a cloud forest assemblage

has been the predominant vegetation type in this region over the last � 1300 years.

During this time, however, there have been changes in the vegetation with an apparent

expansion of cloud forest from � 832 to 620 cal years BP and a decline from 1200 to 832 cal

years BP. Climate change (intervals of aridity) and human disturbances through anthro-

pogenic burning appear to have been the main factors influencing the dynamics of this

cloud forest. The spatial heterogeneity reported for high-altitude forests in this region, in

concert with high beta diversity, appears to be a manifestation of the high temporal

variability in species composition for these forests. Greater turnover in cloud forest taxa

occurred during intervals of increased humidity and is probably representative of a

higher temporal competition for resources among the cloud forest taxa. The present

results support the current protection scheme for cloud forests in west-central Mexico

where areas are kept in exclusion zones to avoid timber extraction, grazing, and

agriculture; this will maintain diversity within these forests, even if there are only a

few individuals per species, and enable the forests to retain some resilience to current

and future climate change.

Keywords: conservation, fire, forest ecology, logging, palaeoecology

Received 6 March 2009; revised version received 16 June 2009 and accepted 24 June 2009

Introduction

Cloud forest is recognized as the terrestrial ecosystem

with the highest diversity per unit area in Mexico and

includes 10% of the Mexican flora and 12% of terrestrial

vertebrates (Pineda & Halffter, 2004). This forest is

characterized by a complex biogeographical history that

combines temperate and tropical elements and has

specific environmental requirements including constant

levels of humidity, usually provided through the pre-

sence of fog, a precipitation range 1000 and 3000 mm,

and temperatures from 12 to 23 1C (Rzedowskii, 1981).

In terms of geographical distribution, cloud forest is

more continuous on the Atlantic than on the Pacific

slopes and it is mainly restricted to humid ravines

(Rzedowskii, 1996) located between 800 and 2700 m

a.s.l. The west-central region of Mexico, in particular,

contains several cloud forest blocks discontinuously

distributed within the Pacific part of the Serranias

Meridionales province (Luna Vega et al., 1999). Pre-

sently cloud forests in Mexico are extremely fragmentedCorrespondence: Blanca Figueroa-Rangel, tel. 1 317 38 25010 ext.

7045, fax 1 317 38 11425, e-mail: [email protected]

Global Change Biology (2010) 16, 1689–1704, doi: 10.1111/j.1365-2486.2009.02024.x

r 2009 Blackwell Publishing Ltd 1689

mailto:[email protected]

(Luna Vega et al., 2000) covering o1% of the country.

Suggested causes of fragmentation are climate change

and human activities such as clearing for agriculture,

livestock grazing and logging (Bubb et al., 2004). How-

ever, very little data exists to determine the relative

importance of each of these on fragmentation of the

cloud forest.

Several stands of cloud forest comprising � 4500 ha

are located inside the Sierra de Manantlan Biosphere

Reserve (SMBR) in west-central Mexico, an area pro-

tected by government decree since 1987. Cloud forest

in the SMBR represents mature communities and con-

tains � 23% of all plant species in the area and the

highest taxonomic richness (Cuevas-Guzman et al.,

2004); these characteristics, in concert with its fragmen-

ted character, high beta diversity (Vazquez-Garcıa &

Givnish, 1998), complex vertical and horizontal struc-

ture and high endemism (Rzedowskii, 1996) make this

forest of high conservation priority.

Many of the tree types in the SMBR cloud forest

(e.g. Quercus, Tilia, Clethra, Dendropanax, Carpinus) have

generation times 450 years. In order to fully appreciate

the natural variability of this important vegetation

type and factors responsible for its fragmentation, a

longer-term perspective is essential. At present, the

longest perspective of cloud forest dynamics in

Mexico are data spanning no more than one decade

(Williams-Linera, 2002; Ramırez-Marcial, 2003; Alvarez-

Aquino et al., 2004; Suarez Guerrero & Equihua, 2005);

longer studies of several decades and centuries are still

very patchy in Mexico and centered in the Yucatan

Peninsula in lowland vegetation (Curtis et al., 1996;

Hodell et al., 2001, 2005a, b) or in central Mexico mainly

in Pine, Pine-Oak and Fir forests (Gonzalez-Quintero,

1986; Lozano-Garcıa et al., 1993; Metcalfe, 1995; Arnauld

et al., 1997; Almeida-Lenero et al., 2005; Metcalfe et al.,

2007).

The aim of this study, therefore, was to reconstruct

the long-term dynamics of the cloud forest in the SMBR

in order to address the following key questions: What

have been the long-term dynamics of the cloud forest in

this biosphere reserve? How have past human distur-

bances and climate change affected its present day

composition and distribution? Are conservation strate-

gies currently in place for the cloud forest in this region

in accordance with its long-term dynamics?

The temporal vegetation dynamics of the cloud

forest are reconstructed using fossil pollen, microfossil

charcoal and inorganic and organic sediments. The

data span the last � 1300 years covering Pre- and

Post-Hispanic occupation periods and a crucial time

of important climatic change in Mexico (Hodell

et al., 1995, 2001, 2005a, b; Curtis et al., 1996; Beach

et al., 2006).

Materials and methods

Study area

The cloud forest stand selected for this study is located

at 1913503200N, 10411605600W approximately 1820–1890 m

a.s.l. in the SMBR in west-central Mexico (Fig. 1). The

environmental characteristics most influential in deter-

mining the distribution of the cloud forest in the SMBR

are a temperate subhumid climate with temperatures

from 8 to 25 1C, rainfall range of 1000–1700 mm, and the

constancy of fog and humidity throughout the year

(Vazquez-Garcıa et al., 1995). The cloud forest in the

SMBR is a highly diverse community with at least 483

plant taxa identified (Cuevas-Guzman et al., 2004). Of

the arboreal component, predominant trees include

Carpinus tropicalis, Clethra vicentina, Cornus disciflora, Ilex

brandegeana, Magnolia iltisiana, Ostrya virginiana, Persea

hintonii, Pinus douglasiana, Quercus xalapensis, Quercus

candicans, Quercus castanea, Q. xalapensis, Tilia americana

var. mexicana and Zinowiewia concinna. In the understory

Parathesis villosa and Euphorbia sp. are the most common

shrubs (Vazquez-Garcıa et al., 1995). The nonarboreal

component of the cloud forest includes terrestrial

herbs, terrestrial and epiphytic ferns, climbers, mosses,

lichens, orchids and bromeliads with the following

families being the most representative: Adiantaceae,

Aspleniaceae, Grammitidaceae, Hymenophyllaceae,

Lycopodiaceae, Orchidaceae and Polypodiaceae.

In the early 1900s the cloud forests of the SMBR were

extensively logged until 1987 when they became pro-

tected in core zones of the biosphere reserve. This

protection scheme excluded most human activities such

as grazing, timber harvesting and agriculture (SEMAR-

NAP, 2000) from these zones.

Archaeology and culture. One of the nearest

archaeological sites to the cloud forest is located in

Autlan (1914600500N, 10412105900W) (Fig. 1) which, at

present, is the largest population centre close to the

SMBR (53,269 inhabitants). Kelly (1945, 1995) explored

43 archaeological sites in Autlan spanning from � AD

1200 to 1500. Human activities, mainly based on

agriculture, have been continuous in this region since

before the Spanish conquest in AD 1521; maize and chilli

were the main staples while clothing was manufactured

using cotton and maguey (Kelly, 1945).

Climate change. Most palaeo-reconstructions of climate

change in Mexico have focused on central Mexico and

the Yucatan Peninsula. From these studies based on

pollen records, stable isotopes, microfossil charcoal,

sedimentology, geomorphology and stratigraphy,

diatoms and historical records it is apparent that in

1690 B . L . F I G U E R O A - R A N G E L et al.

r 2009 Blackwell Publishing Ltd, Global Change Biology, 16, 1689–1704

central Mexico humid conditions prevailed from 4000 to

around 2500 BP (Gonzalez-Quintero, 1986; Lozano-

Garcıa et al., 1993; Metcalfe et al., 2000; Almeida-

Lenero et al., 2005) and arid conditions from 2500 to

1900 BP (O’Hara et al., 1993). Another period of

pronounced aridity also occurred around 1000 BP

(O’Hara et al., 1993; Metcalfe & Hales, 1994; Metcalfe,

1995; Arnauld et al., 1997). In the Yucatan Peninsula wet

conditions prevailed until 3000 BP and there is evidence

for an arid interval between � 1200 and 800 BP that

coincides with the collapse of the Mayans (Hodell

et al., 1995, 2001, 2005a; Curtis et al., 1996; Beach et al.,

2006). Furthermore, evidence from the study area

undertaken in pine-dominated forests revealed

intervals of aridity between � 4200 and 2500, 1200

and 850 and 500 and 200 cal years BP (Figueroa-Rangel

et al., 2008).

Coring and sediment sampling

A 96 cm sedimentary core of black organic material was

retrieved from a small forest hollow (approximately

11 m� 8 m diameter) in the cloud forest of the SMBR

at 1913503200N, 10411605600W (Fig. 1), using a Russian

corer (Glew et al., 2001). The core was extruded in the

field, wrapped, and returned to the Oxford Long-Term

Ecology laboratory for further analyses.

The core was sectioned in 1 cm3 subsamples for loss-

on-ignition (LOI) analysis to measure the contents of

Fig. 1 Map of the coring site in a cloud forest stand of the Sierra de Manantlan Biosphere Reserve, west-central Mexico.

C L O U D F O R E S T D Y N A M I C S I N M E X I C O 1691


carbonate and organic carbon in the sedimentary se-

quence (Dean, 1974).

Chronology

A chronology for the sedimentary sequence was estab-

lished by AMS radiocarbon dating from two labora-

tories (Poznan, Poland and East Kilbride, UK). Six

organic samples taken at regular intervals down

through the core were analysed and the results were

calibrated using the CALIB v5.02 and INTCAL04.14 pro-

grams (Reimer et al., 2004). The age–depth relationship

was modelled using linear interpolation (Bennett, 1994);

confidence intervals were reported using 1s range.

Fossil pollen, microfossil charcoal and geochemicalanalysis

A standard acetolysis method was used to extract

pollen (Bennett & Willis, 2001) from sedimentary sam-

ples 0.5 cm3 each. Sample processing included standard

sieving procedures with a maximum size fraction of

150 mm were undertaken. Tablets containing a known

quantity of Lycopodium spores were added to each

pollen samples in order to act as markers for the

estimation of pollen concentration (pollen grains

cm�3). To obtain a statistically significant sample size

at least 400 pollen grains was counted per sample

(Maher, 1972). The sequence was analysed every 2 cm

for a total of 48 samples. Pollen types were identified

using a pollen and spore reference collection of trees,

shrubs, herbs and terrestrial and epiphyte ferns col-

lected during the field season in the study area together

with the reference collection held in the Long-Term

Ecology Laboratory, Oxford University Centre for the

Environment.

Microfossil charcoal concentration of the sedimentary

sequence was determined using the point count method

(Clark, 1982). The same sampling interval was used as

for the pollen.

Geochemical analysis was undertaken at the same

sample resolution as for pollen and microfossil charcoal

analysis. A modified technique of the acid digestion

method (Bengtsson & Enell, 1986) was used whereby

soluble concentrations of different elements were deter-

mined using inductively coupled plasma mass spect-

ometer (ICP-MS) with a Perkin Elmer spectometer

(Perkin Elmer, Waltham, MA, USA) based in the Earth

Sciences Department of the University of Oxford.

Data handling

Pollen data were plotted and divided into zones by

optimal splitting and significant zones were determined

using a broken-stick model (Bennett, 1996). Rarefaction

analysis (Birks & Line, 1992) was applied to provide an

estimate of the palynological richness for each sample.

The rate-of-change analysis was undertaken to reveal

changes in the cloud forest assemblage over time (Ben-

nett & Humphry, 1995). The above-mentioned proce-

dures were undertaken using PSIMPOLL 4.25 and PSCOMB

1.03 software (Bennett, 2005). To detect significant dif-

ferences in the cloud forest assemblage and the envir-

onmental variables (geochemical elemental

concentrations, microfossil charcoal, pollen concentra-

tion, palynological richness, and rate-of-change) among

the zones determined by optimal splitting, a one-way

analysis of variance ANOVA was calculated using SPSS

v.16.0 [ SPSS, 2007; SPSS for Windows (version 16.0);

Science Inc., Chicago, IL, USA].

Results

Chronology

Radiocarbon dating of the sedimentary sequence indi-

cates that sediment accumulation began about

1540 � 30 cal years BP and continues to present with

no evidence for a hiatus in the sequence (Table 1). The

age–depth model (Fig. 2) indicates that approximately

1 cm of sediment accumulated in the basin every 16

years resulting in a pollen, microfossil and geochemical

sampling interval of one sample every 32 years starting

approximately at 1300 cal years BP. Pollen preservation

Table 1 Radiocarbon calibrated dates calculated from CALIB v5.02 and INTCAL04.14 programs (Reimer et al., 2004) used to develop

the chronology for cloud forest in west-central, Mexico

Depth (cm) Laboratory code 14C age (BP) Calibrated age (cal years BP)(1s)

16 SUERC-5872 207 � 24 162 � 10

40 SUERC-5873 586 � 21 615 � 20

60 SUERC-5874 743 � 24 678 � 10

75 SUERC-5877 925 � 21 879 � 30

82 Poz-10750 1100 � 30 1040 � 10

96 Poz-4747 1635 � 35 1540 � 30



before this time was poor and did not allow preserva-

tion of a statistically significant sample size. The aver-

age content of organic material was � 18% while

carbonate content averaged � 0.02%.

This sequence therefore covers two important

historical episodes in Mexico, the pre- (before AD 1521

or � 465–436 cal years BP) and post-Hispanic (after AD

1521 or � 465–436 cal years BP) periods. These two

periods can be seen as contrasting epochs where human

occupation differed substantially in terms of natural

resource use and social interactions (Denevan, 1992;

Lentz, 2000). Pre-Hispanic (before AD 1521) includes

years before Spaniards conquered Mexico. Post-Hispa-

nic (after AD 1521) years enclose the Spanish conquest,

the Spanish Colony and recent times.

Cloud forest assemblage dynamics

The reconstructed cloud forest assemblage dynamics

from � 1300 cal years BP to present is displayed for all

pollen types, even those with scarce number of grains,

in order to portray the diversity of taxa through this

time (Fig. 3). Previous work on the modern pollen

signature has also indicated that, for the determination

of cloud forest, it is essential to include rare or very

infrequent taxa (B.L. Figueroa-Rangel, unpublished

data). Arboreal taxa indicative of cloud forest (Table 2)

are represented throughout the entire sequence

although with low abundances. However, as has been

previously demonstrated (Rzedowskii, 1996), epiphytic

fern spores such as Aspleniaceae, Hymenophyllaceae

and Polypodiaceae are good indicators of cloud forest

presence and their percentages are high at certain

intervals in the diagram (Fig. 3). According to the ANO-

VA results, pollen concentration and the rate-of-change

calculated through the chord distance are different

among the four zones while palynological richness is

similar (Table 3).

The four pollen zones determined by optimal split-

ting are named according to Mexican history; Pre-

Hispanic I, Pre-Hispanic II and Pre-Hispanic III repre-

sent years before AD 1521 and Post-Hispanic years after

AD 1521 (Fig. 3):

Pre-Hispanic I (� 1300–832 cal years BP)

In this zone arboreal taxa commonly found in present-

day cloud forest predominate. These include Pinus,

Quercus, Alnus, Magnolia, Carpinus and some which

are more abundant in the first half of the zone such as

Clethra, Lauraceae and Tilia (Fig. 3a). Although these

are taxa commonly found in present-day cloud forest

(Table 2), the sum including all cloud forest taxa

indicates low percentages when compare with the

following zone (Fig. 3b). Quercus and Pinus show simi-

lar percentages (from 20% to 30%) while Alnus displays

a high peak (� 15%) at the lowermost section of the

zone (Fig. 3a).

Ferns are evident through the presence of Adiantum,

Anogramma, Dryopteris, other Aspleniaceae, Poly-

podiaceae and Hymenophyllaceae. Low values for

Other Aspleniaceae (o10%) can be observed for this

zone. However, Polypodiaceae and Hymenophyllaceae

show their highest percentages (Fig. 3b). In terms of

herbaceous taxa, Poaceae and Asteraceae are predomi-

nant. The lowest pollen concentration occurred in this

zone with the minimum values around 1200 and 1100

cal years BP while the highest palynological richness is

observed in this zone (Fig. 4).

Pre-Hispanic II (� 832–620 cal years BP)

This zone is a flourishing stage for cloud forest as

revealed by the highest percentages in cloud forest taxa

(Fig. 3b) as well as the highest values in pollen concen-

tration (Fig. 4). Arboreal components with high percen-

tages in this zone are Quercus, Clethra, Meliosma,

Carpinus and Parathesis. Opposite to this pattern is Pinus

with the lowest percentages in the sequence (Fig. 3a).

Excepting Plantago with a peak around 678 � 10

cal years BP, the rest of the herbaceous taxa are scarce

in this zone (Fig. 3b). Other Aspleniaceae, Adiantum and

Anogramma are ferns showing highest percentages

along the sequence (Fig. 3b). Palynological richness is

fairly constant except for a decrease around 640 cal

years BP immediately followed by an increase in the

uppermost section of this zone (Fig. 4). The chord

distance curve, expressing the amount of change in

the cloud forest assemblage, is considerably higher for

Fig. 2 Age-depth model based on radiocarbon dates using

linear interpolation. The age is measured as calibrated years

before present (cal years BP).



(a)

(b)



this zone suggesting a rapid change starting around

678 � 10 cal years BP and dropping in the following

zone (Fig. 4).

Pre-Hispanic III (� 620–480 cal years BP)

This is also a predominant cloud forest stage. Pinus

percentages rise in this zone coincident with a decline in

Quercus and Alnus (Fig. 3a). Main arboreal components

also include Clethra, Cleyera, Dendropanax, Fraxinus,

Hedyosmum, Ilex, Magnolia, Carpinus, Parathesis and Tilia

with very low percentages (Fig. 3a). Herbaceous taxa

such as Zea sp. and the families Chenopodiaceae,

Asteraceae and Poaceae are scarce or even absent

(Fig. 3b). Ferns present in this zone are Adiantum, Other

Aspleniaceae, Polypodiaceae and Hymenophyllaceae.

The highest drop in palynological richness can be ob-

served in this zone while chord distance decreases

reaching low values as well (Fig. 4).

Post-Hispanic (� 480 cal years BP to present)

Some cloud forest taxa decrease in this zone, in parti-

cular Quercus and Carpinus. At the same time, Pinus

performs the highest percentages of the sequence,

reaching 50% in some depths (Fig. 3a). Contrarily others

(e.g. Fraxinus and Tilia) increase only in this zone. In

general, the sum of all cloud forest taxa (ferns included)

decrease to the lowest percentages in the sequence

(Fig. 3b). The maximum number of rare pollen types

(e.g. Dalea, Polygonum, Apiaceae, Juncaceae and Lilia-

ceae) is present in this zone, although they are not

displayed graphically. The herbaceous element is pre-

sent with Crotalaria, Chenopodiacaeae, Asteraceae and

Poacaeae although all with low percentages (Fig. 3b).

Two peaks reaching 30% in Other Aspleniaceae are

apparent in the first section of the zone while Poly-

podiaceae reaches high values during the last 150 years.

There is a peak in pollen concentration around 162 � 10

cal years BP; chord distance is constant but low along

this zone (Fig. 4).

Environmental dynamics

Results from the geochemical and microfossil charcoal

analysis suggest that the environment surrounding the

cloud forest has been changing over the last 1300 years

in tandem with the pollen fluctuations (Figs. 3–5).

Burning has occurred irregularly over those years.

Although there are nonsignificant differences for char-

coal concentration among the zones (Table 3), the

Table 2 Present-day taxa representative of cloud forest in the

Sierra de Manantlan, Biosphere Reserve, west-central Mexico

Arboreal taxa (species) Non-Arboreal taxa (families)

Abies religiosa Araceae

Alnus jorullensis Apiaceae

Carpinus tropicalis Asclepiadaceae

Cinnamomum pachypodum Aspleniaceae

Citharexylum mocinnii Asteraceae

Clethra vicentina Begoniaceae

Cleyera integrifolia Bromeliaceae

Clusia salvinii Convolvulaceae

Conostegia volcanalis Cyperaceae

Cornus disciflora Dennstaedtiaceae

Dendropanax arboreus Euphorbiaceae

Fraxinus uhdei Fabaceae

Fuchsia arborescens Hymenophyllaceae

Garrya laurifolia Melastomataceae

Hedyosmum mexicanum Ophioglossaceae

Ilex brandegeana Orchidaceae

Inga vera subsp. eriocarpa Piperaceae

Juglans major Poaceae

Lippia umbellata Polypodiaceae

Magnolia iltisiana Rubiaceae

Matudaea trinervia Solanaceae

Meliosma dentata Thelypteridaceae

Oreopanax echinops

Ostrya virginiana

Parathesis villosa

Perrottetia longistylis

Persea hintonii

Pinus douglasiana

Prunus cortapico

Quercus candicans

Quercus salicifolia

Rhamnus hintonii

Rondeletia manantlanensis

Sebastiana hintonii

Styrax argenteus

Symplococarpon purpusii

Symplocos citrea

Tilia americana var. mexicana

Triumfetta barbosa

Vaccinium stenophyllum

Xylosma flexuosum

Zinowiewia concinna

Source: Cuevas-Guzman et al. (2004).

Fig. 3 (a) Pollen diagram of cloud forest trees and shrubs in west-central Mexico. Ages are calibrated years BP. Divisions are delineated

by zones according to the optimal splitting option available in PSIMPOLL 4.25. (b) Pollen diagram of cloud forest herbs and ferns in west-

central Mexico. The sum of all cloud forest taxa contributing to the total pollen sum is also displayed. Ages are calibrated years BP.

Divisions are delineated by zones according to the optimal splitting option available in PSIMPOLL 4.25.



greatest peak occurred in the Pre-Hispanic II and Post-

Hispanic zones coinciding with small decreases in the

sum of cloud forest taxa (Fig. 3b). Two high peaks are

centred at 678 � 10 cal years BP and a third one around

100 cal years BP while low values occurred indistinctly

in the four zones (Fig. 4). The ANOVA results show

statistically significant differences in some of the geo-

chemical elements (Table 3); an influx of some of these

elements (Fe, Cr, Co, Mg, K, Mn, Ba, Pb, U and Zn) can

be observed in the Pre-Hispanic I zone (� 1300–832 cal

years BP) with the highest values of the sequence

occurring in this zone. The following two zones are

represented by low values except for a distinct peak

around 500 cal years BP for all the elements. The Post-

Hispanic zone (� 480 cal years BP to present) experi-

ences a rise in some of the geochemical elements such

as Co, Mg, Mn, Ba and Pb (Fig. 5).

Discussion

What have been the long-term dynamics of the cloud forestin this biosphere reserve?

According to the zonation by optimal splitting, four

distinctive zones can be discriminated along the last

1300 years of forest dynamics in the present cloud forest

of the SMBR. These zones are particularly defined by

the alternate dominance of canopy arboreal elements

namely by Pinus, Quercus, Tilia, Carpinus, Fraxinus,

Magnolia, Clethra, Cleyera and Ilex. These taxa are com-

mon to most of the cloud forest studied in Mexico

(Alcantara & Luna, 2001; Cartujano et al., 2002;

Sanchez-Rodrıguez et al., 2003; Mejıa-Rodrıguez

et al., 2004). Their attainment of large heights and

diameters has enabled them to thrive in the upper

Table 3 Confidence intervals and ANOVA significant values (in bold) among the four zones delineated according to optimal

splitting (Bennett, 1996) for some of the most important vegetation and environmental variables in the sedimentary sequence

recovered in cloud forest of west-central Mexico

Variables

Zones

SignificancePre-I Pre-II Pre-III Post

Pollen concentration (# grains/cc) 6217.41 � 2432.9 52324.45 � 14564.7 69992.07 � 41705.0 39301.06 � 10763.5 0.000

Palynological richness E(T240) 17.76 � 1.4 16.73 � 0.9 14.90 � 6.0 15.90 � 1.1 0.093

Charcoal concentration (cm2/cm3) 1.01 � 04 1.84 � 0.9 0.84 � 1.6 1.93 � 0.8 0.272

Chord distance (cm�1) 0.87 � 0.21 3.51 � 0.81 2.53 � 2.92 1.26 � 0.22 0.000

Geochemical elements

g kg�1

Mg 4.02 � 1.1 0.78 � 0.1 1.04 � 0.9 1.73 � 0.6 0.000

Al 21.52 � 6.2 18.37 � 4.1 16.78 � 14.1 20.77 � 4.0 0.626

Fe 13.56 � 3.2 4.04 � 1.1 3.82 � 3.4 8.54 � 2.0 0.000

Ca 1.21 � 0.4 1.14 � 0.2 0.71 � 0.7 1.19 � 0.2 0.270

P 0.77 � 0.4 0.77 � 0.1 0.58 � 0.5 0.89 � 0.2 0.527

mg kg�1

Na 51.84 � 23.8 41.84 � 37.2 25.26 � 30.0 43.44 � 13.7 0.820

K 340.18 � 83.4 75.50 � 28.1 10.3.09 � 45.7 41.20 � 43.3 0.000

V 95.08 � 22.7 76.93 � 15.9 45.54 � 41.7 45.14 � 10.7 0.000

Cr 12.53 � 3.0 6.34 � 1.2 3.80 � 3.5 5.07 � 1.1 0.000

Mn 140.65 � 37.9 32.89 � 6.3 33.80 � 22.4 85.71 � 25.8 0.000

Co 8.61 � 2.2 1.82 � 0.4 2.37 � 1.8 4.39 � 1.1 0.000

Cu 32.98 � 8.3 22.97 � 4.3 22.22 � 17.3 25.20 � 5.3 0.081

Sr 7.44 � 1.8 10.26 � 2.0 7.28 � 6.3 11.14 � 2.1 0.047

Cd 0.06 � 0.1 0.10 � 0.0 0.06 � 0.1 0.09 � 0.0 0.032

Ba 97.19 � 23.9 52.18 � 8.7 45.72 � 37.3 85.71 � 19.0 0.000

La 9.97 � 2.5 8.41 � 1.3 7.65 � 6.0 10.53 � 2.0 0.203

Ce 23.22 � 6.3 18.66 � 3.2 18.28 � 14.9 22.95 � 4.5 0.307

Nd 15.40 � 4.0 12.84 � 2.2 13.18 � 11.3 16.62 � 3.1 0.223

Pb 3.97 � 1.1 2.30 � 0.4 2.41 � 2.1 4.54 � 1.0 0.000

Th 1.73 � 0.5 1.14 � 0.2 1.07 � 0.9 2.01 � 0.8 0.075

U 0.36 � 0.1 0.24 � 0.1 0.24 � 0.2 0.31 � 0.1 0.042

Zn 117.88 � 29.1 62.01 � 11.8 52.95 � 41.5 70.88 � 12.6 0.000

ANOVA, analysis of variance.

Bold values signify Po0.05.



stratum. However, it is known from present-day studies

that cloud forest is much more diverse than this, usually

containing up to 100 different arboreal species (Cuevas-

Guzman et al., 2004).

Some of these arboreal elements, indicative of current

cloud forest in the SMBR (Table 2), are present in the

pollen sequence but the majority have low pollen

percentages or are absent from the record. This is most

likely a result of the pollination biology of the cloud

forest taxa which are mostly dispersed by animals,

mainly by insects and birds (Barbosa et al., 2006; Souba-

dra & Davidar, 2006; Deliso, 2008). In tropical forests

seventy percent of Nearctic forest taxa (e.g. Pinus, Alnus,

Quercus) are anemophilous while most of the Neotro-

pical taxa are entomophilous giving the possibility for

underrepresentation of pollen from Neotropical origin

and consequently overrepresentation of Nearctic pollen

(Bush, 2002). In view of the insufficient arboreal pollen

representing cloud forest, ferns are therefore regarded

as the main indicators for this community (Figueroa-

Rangel et al., 2008; B.L. Figueroa-Rangel, unpublished

data). Epiphytes embody the most diverse group (more

than 30% of all species) in the cloud forests of Mexico,

displaying a great endemism (Rzedowskii, 1996). In this

study Aspleniaceae, a family which includes a high

number of epiphytic species, presents percentages si-

milar to the most abundant trees (Pinus and Quercus)

while Polypodiaceae, considered the second most di-

verse family (47 genera) in cloud forest of Mexico

(Rzedowskii, 1996), shows abundances similar to that

of Carpinus, Tilia and Alnus. However, the rest of the

ferns, recognized to the genus level (Adiantum, Ano-

gramma, Botrichium, Cheilanthes, Dryopteris and Pteri-

dium), show limited numbers.

There has been change in the composition of the

cloud forest a number of times during the last 13

centuries as evidenced by the different taxa dominating

the pollen sum along the sequence. The rate-of-change,

calculated through the chord distance, expressed that

the main changes in the cloud forest assemblage

Fig. 4 Pollen concentration, palynological richness, chord distance and charcoal concentration for the cloud forest of west-central,

Mexico. Divisions are delineated by zones according to the optimal splitting option available in PSIMPOLL 4.25 undertaken on pollen data.



(a)

(b)

Fig. 5 Geochemical concentration for some elements in a cloud forest of west-central, Mexico. Divisions are delineated by zones

according to the optimal splitting option available in PSIMPOLL 4.25 undertaken on pollen data. Concentrations are expressed in mg kg�1

except Fe and Mg, which are in g kg�1.



occurred during the time (Pre-Hispanic II � 832–620

cal years BP) when the cloud forest flourished the most.

During this period pollen concentration was also higher

than in the rest of the zones, moreover the sum of all

cloud forest taxa reached high percentages in this zone

summing up to 70% in some depths. Two of the most

important taxa whose changes in abundance varied

along the sequence were Pinus and Quercus, one ex-

panded at the same time the other contracted.

Of particular significance is a decline in the abun-

dance of Quercus at approximately 615 cal years BP

during the Pre-Hispanic III zone. This genus is one of

the canopy dominants in most cloud forests in Mexico

with high densities and basal areas (Sanchez-Rodrıguez

et al., 2003; Mejıa-Rodrıguez et al., 2004) and high

numbers of species (� 32 species for the study area)

even exceeding very diverse herbaceous families

(Alcantara & Luna, 2001). The Quercus decline could

therefore be an indication of a cloud forest decline from

the end of the Pre-Hispanic III to present.

Tilia became an important component of the cloud

forest from approximately 670 cal years BP and Fraxinus

from approximately 200 years ago. There is also an

important shift in dominance with Cleyera, Fraxinus, Ilex

and Tilia dominating in the Post-Hispanic zone (� 480

cal years BP to present) while others such as Carpinus,

Clethra and Meliosma, predominate in the Pre-Hispanic

II zone (� 832–620 cal years BP).

Differences in life-intervals for canopy dominants

have been reported in tropical forests (Bush & Colin-

vaux, 1994), with some trees needing a century or less to

become mature while others needing up to three cen-

turies. In addition, cloud forest taxa need particular

microhabitat conditions to survive (Hietz & Briones,

1998), so a temporal division of the resources is prob-

ably taking place through temporal niche partitioning.

It is suggested that this is playing an important role in

the alternating occurrence of the taxa; as a result there is

a heterogeneous canopy composition although with

low abundances per taxa across the 13 centuries that

this sequence represents.

In summary, it is difficult to identify a specific con-

stant cloud forest assemblage along the sequence. The

spatial heterogeneity reported for high-altitude forests

in this region (Olvera Vargas et al., 2006), in concert with

high beta diversity (Vazquez-Garcıa & Givnish, 1998), is

a manifestation of the high temporal variability in

species composition for these forests. This diverse as-

semblage has therefore remained remarkably resilient

during the last 1300 years as it is evidenced by the

nonsignificant differences in palynological richness

among the four zones, but its components are highly

dynamic as portrayed by the high differences in chord

distance among the zones (averages from 0.87 to

3.51 cm�1 and standard errors from 0.21 to 2.92 cm�1).

The different taxa seem to follow different trends ac-

cording to the zone, a tendency common to many

biological communities (Lovejoy, 2006) with each taxon

displaying an individualistic response. Therefore the

cloud forest taxa, particularly the arboreal component,

appear and disappear from the cloud forest assemblage

along the last 1300 years. The higher values for chord

distance in the Pre-Hispanic II zone (� 832–620 cal

years BP) is expressing that larger change in the cloud

forest assemblage was taking place during this interval

in time.

How have past human disturbances and climate changeaffected its composition?

Cloud forest conservation is critical as this forest shel-

ters arboreal dominants of different phytogeographical

affinities, as well as herbs and ferns with particular

requirements for their establishment. Results from this

study indicate that even though the cloud forest block

has remained remarkably resilient during the last 1300

years, the composition of the cloud forest has changed

possibly as individual species react to climate change or

to human disturbances, but to what extent are these

factors influencing its composition?

Climate change

Previous studies on the climate of Mexico reconstructed

from various fossil proxies has revealed that over the

past 1300 cal years BP broad-scale climate changes have

occurred in both temperature and precipitation (O’Hara

& Metcalfe, 1997; Metcalfe et al., 2000; Almeida-Lenero

et al., 2005). These changes were widespread and de-

tected in records from Bolson de Mapimi in Durango

and Coahuila (northern Mexico), Lake Zacapu in Mi-

choacan, lakes Zempoala, Quila and Texcoco in central

Mexico, the northern Yucatan Peninsula and the Pacific

Guatemalan coastline. The dry period (� 1200–832 cal

years BP) reported for the present research project coin-

cides with the period when drier conditions have been

reported for Mexico (AD 800–1000) (Metcalfe et al., 2000;

Hodell et al., 2001; Haug et al., 2003) and elsewhere (Chu

et al., 2002; Russell & Johnson, 2005; Neff et al., 2006).

For central Mexico an analogous dry period has been

also reported (Metcalfe & Hales, 1994; Metcalfe, 1995;

Arnauld et al., 1997; O’Hara & Metcalfe, 1997; Almeida-

Lenero et al., 2005; Ludlow-Wiechers et al., 2005; Met-

calfe et al., 2007). A general pattern that has emerged

from these regions is that during the past 1300 years,

there have been two intervals of widespread aridity

between 1200 and 850 and � 500 and 200 cal years BP

(Haug et al., 2003; Neff et al., 2006), probably driven by



changes in latitudinal migration of the intertropical

convergence zone (ITCZ).

Results from the geochemical records in this study

provide evidence for significant change occurring

around the basin over the past 1300 years, often tempo-

rally coinciding with the climate changes suggested

from other records. For example, in the Pre-Hispanic I

zone (� 1200–832 cal years BP) high values of geochem-

ical elements are detected. The excess of some geochem-

ical elements (i.e. Co, Mg, Mn, Ba and Pb) in the

sediment for that particular period could be related to

the scarcity of water in the soil, which hindered leach-

ing processes. A similar high concentration of some

geochemical elements has been related to climate fac-

tors, particularly to droughts, in other studies from

tropical (Brncic et al., 2007) and temperate regions

(Tipping et al., 2003). In contrast, during intervals of

increased humidity (� 832–550 cal years BP), assumed

by the increase in cloud forest taxa that rely on foggi-

ness to survive, lower values of inorganic geochemical

element (Fig. 5) are detected in this study coincident

with the interval of greatest turnover in the cloud forest.

So what is the cloud forest response to these intervals

of increased aridity? During the dry interval there is a

decline in pollen concentration and the sum of all cloud

forest taxa is also reduced, in particular some canopy

dominant decrease percentages such as Clethra, Tilia,

Cleyera, Fraxinus, Ilex and Meliosma. There is also an

increase in open ground taxa such as Poaceae as well as

in ferns Dryopteris, Hymenophyllaceae and Polypodia-

ceae. The increase in Poaceae is possibly related to open

canopies where the incidence of sunlight into the forest

is associated to an increase in aridity (Markgraf, 1993).

Hymenophyllaceae family is recognized for its high

tolerance to desiccation (Proctor, 2003), while Poly-

podiaceae family fluctuates enormously according to

saturation deficit (Benzing, 1998) with some species

reported as desiccation-resistant ferns (Muslin &

Homann, 1992; Andrade & Nobel, 1997; Proctor, 2003).

In contrast, during intervals of increased humidity (i.e.

� 832–620 cal years BP) there is evidence for increased

change in the cloud forest assemblage given by the

higher chord distance in that zone. An increase in

humidity probably provided the best conditions for

the reproduction of cloud forest taxa.

Human disturbances

Archaeological evidence suggests that there has been

human activity in the SMBR region over the past 1300

years. Archaeological remains from this region date

back to ca. AD 1200 suggesting human occupation before

the Spanish Conquest (AD 1521). In addition, archae-

ological excavations in Autlan (� 25 km from the coring

site), one of the localities closest to the SMBR (Fig. 1),

have revealed that by AD 1525 the area was an urban

population reliant upon intensive agriculture and irri-

gation (Kelly, 1945).

So what impact did these people have on the cloud

forest? There is certainly no evidence, in the pollen

record, of widespread clearance of the cloud forest but

it is highly likely that they would have carried out

small-scale agriculture, clearance through burning and

logging.

Similarities in the cloud forest assemblage as well as

in environmental dynamics between the Pre-Hispanic I

and the Post-Hispanic zones are obvious. The decline of

cloud forest and the consequent dominance of Pinus are

particularly similar between the two zones. Some of the

geochemical elements such as Mn, Ba and Pb, also reach

their highest values in these two zones. These coinci-

dences therefore seem to indicate that the changes are

the result of climate change events rather than to a

higher human disturbance.

However, human disturbance and climate change are

intricately linked in this part of the world and it is

possible that some changes occurring during these two

intervals are also indicative of human activity (Metcalfe

et al., 2000; Williams, 2003). It is possible that the

extraction of timber taxa such as Pinus and Quercus

has dictated some changes in the cloud forest assem-

blage. The decline of Quercus in the cloud forest of the

SMBR from �615 cal years BP to present may be related

to human influences such as logging, which resulted in

the simultaneous increase in Pinus. Similarly the expan-

sion of Pinus in southern Mexico in recent times has

been widely attributed to the influence of human activ-

ity, in particular to the extraction of Quercus trees

(Ramırez-Marcial et al., 2001).

Burning is constant through the whole sequence and

again it is possibly linked to the forest clearance and the

slash-and-burn system of agriculture. Agriculture in

Mexico is mainly developed through the slash and burn

system (Ellingson et al., 2000; Castellanos et al., 2001;

Ochoa-Gaona, 2001; Negreros-Castillo et al., 2003). This

consists of clearing the land followed by burning. This

land is cultivated and then left fallow for a certain

period of time before cultivating again (Pascual, 2005).

Evidence from our record also indicates the first

appearance of maize during the dry interval (� 1200–

832 cal years BP). It is likely that people in that time

started maize cultivation in the highlands as a conse-

quence of the scarcity of water in the lowlands. During

the subsequent wet periods (� 832 cal years BP to

present) reported in this study, maize is nearly absent

in the pollen spectra. We therefore suggest that the main

changes in the cloud forest assemblage of the SMBR

over the past 1300 years possibly indicate some evi-



dence of human disturbances although these are small

scale and appear to be coupled with climate changes.

Implications of this record for predicting the impact offuture climate change and human use in the region

Results from this study corroborate the existence of a

dry period from 1200 to 800 cal years BP in mountain

forests of the region (B.L. Figueroa-Rangel, unpublished

data); in central Mexico (Metcalfe & Hales, 1994; Met-

calfe, 1995; Arnauld et al., 1997; O’Hara & Metcalfe,

1997; Almeida-Lenero et al., 2005; Ludlow-Wiechers

et al., 2005; Metcalfe et al., 2007); lowlands of the Yucatan

Peninsula (Hodell et al., 1995, 2001, 2005a, b) and the

Cariaco Basin in Venezuela (Haug et al., 2003). This

period is also an interval (1200–1000 cal years BP) when

global scale rapid climate change has been reported

(Metcalfe & Davies, 2007). The causes associated to this

phase of climate change have been attributed to solar

activity (Hodell et al., 2001; Haug et al., 2003), changes in

the latitudinal migration of the ITCZ (Metcalfe et al.,

2000; Hodell et al., 2005a, b; Berrio et al., 2006) and to the

ENSO variability (Metcalfe, 2006). During this time

interval the effect of climate change on human activities

has been observed, particularly for the Yucatan Penin-

sula (deMenocal, 2001).

The response of the cloud forest in this study to

previous intervals of climate change and human impact

reveals some interesting implications for the possible

impact of future climate change and human distur-

bances on this forest as follows: (i) during intervals of

aridity, cloud forest taxa tend to become reduced; (ii) in

contrast during intervals of increased humidity, the

cloud forest thrives (unsurprisingly) and there is also

a higher rate of change. We suggest that this is indica-

tive of a higher temporal competition for resources

among the cloud forest taxa during this more humid

interval due to greater availability of resources, parti-

cularly those linked to water; and (iii) The cloud forest

appears to be remarkably resilient to small-scale human

disturbances and burning, the main impact possibly

apparent through change in forest dominance. How-

ever, more extensive activity to include logging and

agriculture would be detrimental to the resilience of this

forest, due to a reduction in the overall taxonomic

richness and the expansion of cultural taxa.

Given the global climate change predictions for Neo-

tropical Mexico, where drier environments are ex-

pected, coupled with an intensified land use in the

search for water in the uplands of the region, it is

possible that the cloud forest will become species-poor,

its ecological memory for returning to a diverse assem-

blage in wetter conditions, lost and thus its overall

resilience greatly reduced.

Conservation strategies

At present the high beta diversity, few individuals per

species and the fragmented character of cloud forest

make it difficult to conceive the idea of a constant

assemblage over centuries. Results from our study

indicate, however, that while there may be no such

thing as a ‘constant’ assemblage of species in these

highly diverse forest, cloud forest ecosystems as a

whole have been remarkably resilient over time. The

composition of the cloud forest is constantly changing

through time and appears to be remarkably resilient to

climate change and small-scale human activities. In this

respect, it is therefore important to maintain diversity

within these forests, even if there are only a few

individuals per species and to avoid excessive logging

in these stands. Alternatively a selective extraction

scheme for timber species has to be designed depend-

ing on the composition of the canopy taxa and the

structure of the present-day vegetation in order to

maintain diversity so that long-term resilience of the

ecosystem may be retained. The present results fully

support the current protection scheme for cloud forests

in west-central Mexico where areas are kept in exclu-

sion zones, namely the core areas of the SMBR. In these

areas timber extraction, grazing and agricultural activ-

ities are excluded. Our results confirm that these are the

best conservation strategies for the long-term main-

tenance of the cloud forest dynamics.

Acknowledgements

We are greatly indebted to Martın Vazquez Lopez from theUniversity of Guadalajara for his valuable assistance duringthe fieldwork and to John Arden, from the Earth SciencesDepartment, University of Oxford for the ICP-MS analysis. Thefollowing institutions provided funds for the fieldwork: LinacreCollege, St Hugh’s College and The Vaughan Cornish Bequestfrom the University of Oxford. NERC Radiocarbon Laboratory atEast Kilbride, UK funded the radiocarbon dates by datingallocation no. 1048.1003. This research was supported by Con-acyt (Mexican National Council for Science and Technology) andPromep (SEP) through a Doctorate Scholarship to the firstauthor.

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