This article was downloaded by: [UGR-BTCA Gral Universitaria]On: 21 November 2012, At: 00:53Publisher: Taylor & FrancisInforma Ltd Registered in England and Wales Registered Number: 1072954 Registered office: Mortimer House,37-41 Mortimer Street, London W1T 3JH, UK

Plant Biosystems - An International Journal Dealingwith all Aspects of Plant Biology: Official Journal of theSocieta Botanica ItalianaPublication details, including instructions for authors and subscription information:http://www.tandfonline.com/loi/tplb20

Vascular plant diversity and climate change in theupper zone of Sierra Nevada, SpainM. R Fernández Calzado a , J. Molero Mesa a , A. Merzouki a & M. Casares Porcel aa Faculty of Pharmacy, Department of Botany, University of Granada, Campus de Cartuja,18071, Granada, SpainAccepted author version posted online: 13 Jul 2012.Version of record first published: 17 Aug2012.

To cite this article: M. R Fernández Calzado, J. Molero Mesa, A. Merzouki & M. Casares Porcel (2012): Vascular plant diversityand climate change in the upper zone of Sierra Nevada, Spain, Plant Biosystems - An International Journal Dealing with allAspects of Plant Biology: Official Journal of the Societa Botanica Italiana, 146:4, 1044-1053

To link to this article: http://dx.doi.org/10.1080/11263504.2012.710273

PLEASE SCROLL DOWN FOR ARTICLE

Full terms and conditions of use: http://www.tandfonline.com/page/terms-and-conditions

This article may be used for research, teaching, and private study purposes. Any substantial or systematicreproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form toanyone is expressly forbidden.

The publisher does not give any warranty express or implied or make any representation that the contentswill be complete or accurate or up to date. The accuracy of any instructions, formulae, and drug doses shouldbe independently verified with primary sources. The publisher shall not be liable for any loss, actions, claims,proceedings, demand, or costs or damages whatsoever or howsoever caused arising directly or indirectly inconnection with or arising out of the use of this material.

Vascular plant diversity and climate change in the upper zone ofSierra Nevada, Spain

M. R. FERNANDEZ CALZADO, J. MOLERO MESA, A. MERZOUKI, &

M. CASARES PORCEL

Faculty of Pharmacy, Department of Botany, University of Granada, Campus de Cartuja, 18071, Granada, Spain

AbstractThis study examines the effects of altitudinal, temperature and aspect gradients on vascular plant species richness onmountain tops in Sierra Nevada (Spain) at different spatial scales (1 m2 quadrats, plot clusters of 4 m2, upper summit areadown to the 5-m contour line, entire summit down to the 10-m contour line). The methodology follows the GlobalObservation Research Initiative in Alpine Environments (GLORIA) programme. Floristic and soil temperature data of eightsummits sites in two neighbouring regions of the high part of Sierra Nevada (from 2668 m to 3327 m a.s.l.) were used in thisstudy. In total, 102 taxa were recorded (84 genera; 29 families). The species richness decreased, whereas the proportion ofendemic taxa increased with elevation. There were significant linear relationships between species richness and altitude andaverage soil temperature at each spatial scale. However, there was no significant relationship between species richness andaspect variables. Facing continued climate change, the high-altitude flora of Sierra Nevada is expected to be particularlyvulnerable and prone to warming-induced biodiversity losses due to the high proportion of endemic taxa, ranging from 23%at lower elevations up to 67% at higher ones.

Keywords: Altitude gradient, biodiversity, climate change, endemics plants, mountain, temperature

Introduction

Since the last century, the influence of climate change

on local-large scale biodiversity pattern has been

emphasized by several studies. Warming-induced

species migrations lead to latitudinal and altitudinal

shifts in species’ distribution ranges and may result in

species extinctions, especially in highly fragmented

ecosystems (Ozenda & Borel 1991; Grabherr et al.

1994; Hansen et al. 2001; Houghton et al. 2001;

Pearson & Dawson 2003; Araujo et al. 2005a,b;

Broennimann et al. 2006; Thuiller et al. 2006).

In this context, high mountain regions are of

particular interest as they usually harbour small-

scaled and fragmented ecosystems and, in some

regions, species with strongly restricted distribution

ranges (Nagy & Grabherr 2009). High mountain

areas appear to be very suitable places to study

the impacts of current climate change on natural

ecosystems. This is because they exhibit steep

ecological gradients and narrow ecotones dominated

by abiotic factors in relation to climate conditions,

and scarce anthropogenic disturbance compared to

lower altitudes (Theurillat 1995; Grabherr et al.

1994, 2001; Korner 1994, 2002; Pauli et al. 1996,

2004; Dullinger et al. 2007). Therefore, the long-

term monitoring programme GLORIA (Global

Observation Research Initiative in Alpine Environ-

ments: www.gloria.ac.at) was initiated at the turn of

the century.

The field work of GLORIA started in 2001 by

applying a common monitoring protocol in summit

areas of 18 European mountain regions with Sierra

Nevada among them. This protocol involved the

recording of the composition and cover of vascular

plant species and soil temperatures (Grabherr et al.

2000; Pauli et al. 2003, 2004). The peculiarities of

the highest zone of Sierra Nevada (geographical

location, Mediterranean climate, high floristic biodi-

versity and endemism rate) and its being considered

as one of the most sensible and vulnerable zones to

climate change effects in Spain (Fernandez-Gonzalez

et al. 2005) motivated us to extend the number of

summit sites (Molero Mesa et al. 2009). Currently,

Correspondence: M. R. Fernandez Calzado, Department of Botany, Faculty of Pharmacy, University of Granada, Campus de Cartuja, 18071, Granada, Spain.

Tel: 0034 607 678 047. Fax: 0034 958 243 916. Email: rosafc@ugr.es

Plant Biosystems, Vol. 146, No. 4, December 2012, pp. 1044–1053

ISSN 1126-3504 print/ISSN 1724-5575 online ª 2012 Societa Botanica Italiana

http://dx.doi.org/10.1080/11263504.2012.710273

Dow

nloa

ded

by [

UG

R-B

TC

A G

ral U

nive

rsita

ria]

at 0

0:53

21

Nov

embe

r 20

12

Sierra Nevada has eight summit sites distributed over

two neighbouring regions within Sierra Nevada’s

upper zone.

The aim of this article was to analyse the effect of

altitude on vascular plant species richness at different

spatial scales by using data from standardized

GLORIA plots established on summit sites of

different elevations. In particular, we aim to deter-

mine if there are correlations between species

richness and distribution (endemic vs. more wide-

spread species) altitude and average soil temperature.

Possible implications of climate warming for biodi-

versity conservation are discussed.

Study area

The Sierra Nevada is part of the Baetic Cordillera of

southern Spain, and stretches over about 90 km in

the west-east direction (Figure 1). Its altitude

exceeds any other part of the Baetic Cordillera by

41100 m, with numerous summits above 3000 m

a.s.l., including the highest peak on the Iberian

Peninsula (Mulhacen, 3481 m).

Figure 1. Location of the Sierra Nevada mountain (Spain) and sampling summits.

Diversity and climate change in Sierra Nevada (Spain) 1045

Dow

nloa

ded

by [

UG

R-B

TC

A G

ral U

nive

rsita

ria]

at 0

0:53

21

Nov

embe

r 20

12

Eight summits, assembled in two neighbouring

regions (target regions) of the high part of Sierra

Nevada, were selected and permanently marked

(Figure 1), using criteria specified in the GLORIA

field manual (Pauli et al. 2004). The Sierra Nevada

west target region (coded ES-SNE) is situated in the

central-occidental zone of the range, with four

summit sites: Machos (MAC) 3327 m; Tosal Car-

tujo (TCA) 3150 m; Cupula (CUP) 2968 m and

Pulpitito (PUL) 2778 m. The second target region,

Sierra Nevada northeast (coded ES-SNN), is located

in the oriental part of the high Sierra Nevada, also

with four summit sites: Cuervo (CUE) 3144 m;

Diegisa (DIE) 2800 m; Miron (MIR) 2717 m and

Monte Rosa (MOR) 2668 m. Species data from the

ES-SNE sites were from 2001, and those from the

ES-SNN sites from 2004 to 2006.

All of the summits are exposed to the same local

climate, namely a Mediterranean bioclimate in its

pluviseasonal oceanic variant (Rivas-Martınez et al.

2007), with a pronounced summer drought at all

altitudes and with precipitation occurring almost

exclusively as snow during winter at altitudes above

2500 m. They also have similar siliceous bedrock

except for PUL, having a less acidic substrate. The

vegetation changes between the lower summits (i.e.

PUL or MOR) where dwarf shrub communities are

predominant in the landscape, and in the highest

summits such us MAC, TCA, CUE, where the

vegetation is composed of scattered psycroxerophytic

grasses and scree plants.

Materials and methods

Sampling design

The sampling design and the recording methods

follow the GLORIA field manual (Pauli et al. 2004).

Firstly, the survey area on each summit was defined

as a polygon with four corners, at each point of the

compass (N, S, E and W), and at an altitude

difference of 5 m form the highest summit point

(HSP) and a lower area extending from five vertical

metres below the summit to 10 vertical metres below

the summit. Intersection lines from the HSP to the

NE, SE, SW and NW directions resulted in eight

summit area sections (SASs; four upper and four

lower ones). Recording in each SAS included a

complete list of all vascular plants species, and

visually estimated percentage top cover of surface

types such as total vegetation cover (vascular plants),

solid rock, scree, etc.

Secondly, to evaluate the quantitative floristic

compositions at each aspect, four quadrat clusters

(3 m63 m resulting in nine 1-m2 quadrats) were

established at each cardinal direction (N, E, S, W).

The vegetation sampling (vascular plant species

and their percentage cover) was recorded in the

four corners-quadrats of each 3 m63 m quadrat

cluster.

Thirdly, data-loggers (StowAway TidbiT, Onset

Corporation, MA, USA) were installed at 10 cm

below the surface in each central quadrat in the

3 m63 m quadrat clusters, to measure the soil

temperature every hour. Temperature was recorded

from August 2001 to July 2008 in the ES-SNE target

region, and from October 2005 to March 2008 in the

ES-SNN target region.

Data analysis

The effect of aspect and altitude on species richness

at each spatial scale, i.e. (1 m2 and 4 m2 of one plot

cluster in the upper summit area (from the top down

to the 5-m level), and the entire summit area (from

the top to the 10-m level) was tested by Analysis of

Covariance (ANCOVA) with altitude as the covari-

ate. Linear regression was used to analyse the

relation between species richness, altitude and

average soil temperature. Both analyses were per-

formed using the statistical package SPSS.

Flora Iberica (Castroviejo et al. 1986–2009) and

regional floras (Molero Mesa & Perez-Raya 1987;

Molero Mesa et al. 1996) were used as references to

define the distribution and the altitudinal ranges of

species.

Soil temperature data (hourly time series from

October 2006 to September 2007) were used in this

analysis as mean annual temperature. This was the

first time period in which vegetation sampling was

done on all eight summits.

Results

Species richness and life forms

The total number of vascular plants species of all

eight summit sites (entire summit areas down to the

10-m contour line) was 102, belonging to 84 genera

(Table I). It was impossible to distinguish the species

in five genera (Cerastium, Rumex, Viola, Veronica and

Helictotrichon) across different summits on the ES-

SNN. The taxa are included within 29 families, the

most common being the typical Mediterranean

families such as Asteraceae (17 species), Poaceae

(15), Brassicaceae (11) and Caryophyllaceae (10).

The altitudinal distribution of the species found on

the eight GLORIA summits in Sierra Nevada range

from almost sea level to a maximum altitude of

around 3500 m a.s.l., but shows a pronounced peak

between 2500 and 3000 m (Figure 2). The total

vascular plant species richness on the study summits

decreased with increasing elevation, with the excep-

tion of MIR (2717 m) and CUP (2968 m), which

1046 M. R. Fernandez Calzado et al.

Dow

nloa

ded

by [

UG

R-B

TC

A G

ral U

nive

rsita

ria]

at 0

0:53

21

Nov

embe

r 20

12

Table I. List of vascular plant taxa on the eight GLORIA summits in Sierra Nevada.

Type taxon Taxon name Family Life form Distribution

subsp. Acinos alpinus subsp. meridionalis Lamiaceae Ch Eu-N

subsp. Aethionema saxatile subsp. marginatum Brassicaceae Ch Eu-N

S Agrostis nevadensis Poaceae He_g Ne

S Alyssum nevadense Brassicaceae He_ng Ne

subsp. Androsace vitaliana subsp. nevadensis Primulaceae Ch Ne

S Andryala agardhii Asteraceae He_ng Be

subsp. Anthyllis vulneraria subsp. pseudoarundana Fabaceae He_ng Ne

S Arenaria armerina Caryophyllaceae Ch Ib-N

S Arenaria grandiflora Caryophyllaceae He_ng Eu-N

S Arenaria pungens Caryophyllaceae Ch Be

subsp. Arenaria tetraquetra subsp. amabilis Caryophyllaceae Ch Ne

S Artemisia granatensis Asteraceae Ch Ne

subsp. Asperula aristata subsp. scabra Rubiaceae He_ng Eu-N

S Asplenium septentrionale Aspleniaceae He_ng Others

subsp. Astragalus nevadensis subsp.nevadensis Fabaceae Ch Be

S Avenella iberica Poaceae He_g Ib

S Biscutella glacialis Brassicaceae He_ng Ne

S Bromus tectorum Poaceae Te Others

subsp. Campanula rotundifolia subsp. hispanica Campanulaceae He_ng Eu

subsp. Carduus carlinoides subsp. hispanicus Asteraceae He_ng Ne

G Cerastium sp. Caryophyllaceae Te

S Cerastium ramosissimum Caryophyllaceae Te Others

S Chaenorhinum glareosum Scrophulariaceae He_ng Ne

S Cirsium gregarium Asteraceae He_ng Be

subsp. Coincya monensis subsp. nevadensis Brassicaceae He_ng Ne

S Crepis oporinoides Asteraceae Ch Be

subsp. Cystopteris fragilis subsp. fragilis Athyriaceae He_ng Others

S Cuscuta planiflora Convolvulaceae Te Others

S Dactylis juncinella Poaceae He_g Ne

subsp. Dianthus pungens subsp. brachyanthus Caryophyllaceae Ch Ib-N

subsp. Digitalis purpurea subsp. purpurea Scrophulariaceae He_ng Eu-N

subsp. Draba hispanica subsp. laderoi Brassicaceae Ch Ne

S Erigeron frigidus Asteraceae He_ng Ne

S Erigeron major Asteraceae He_ng Be

S Erodium cheilanthifolium Geraniaceae Ch Be

S Erophila verna Brassicaceae Te Others

S Erysimum nevadense Brassicaceae He_ng Be

S Eryngium glaciale Apiaceae He_ng Ib-N

S Euphorbia nevadensis Euphorbiaceae Ch Ib

S Euphrasia willkommii Scrophulariaceae Te Ib-N

S Festuca clementei Poaceae He_g Ne

S Festuca indigesta Poaceae He_g Ib-N

S Festuca pseudeskia Poaceae He_g Ne

S Galium nevadense Rubiaceae He_ng Ib-N

S Galium pyrenaicum Rubiaceae Ch Ib

S Galium rosellum Rubiaceae He_ng Be

S Genista versicolor Fabaceae Ch Be

G Helictotrichon sp. Poaceae He_g

S Herniaria boissieri Caryophyllaceae Ch Be

S Hieracium castellanum Asteraceae He_ng Eu

S Holcus caespitosus Poaceae He_g Ne

S Hormathophylla spinosa Brassicaceae Ch Eu-N

subsp. Iberis carnosa subsp. embergeri Brassicaceae He_ng Ne

subsp. Jasione crispa subsp. tristis Campanulaceae Ch Ne

subsp. Juniperus communis subsp. hemisphaerica Cupressaceae Ph Others

S Juniperus sabina Cupressaceae Ph Others

S Jurinea humilis Asteraceae He_ng Eu-N

S Koeleria crassipes subsp. nevandensis Poaceae He_g Ne

subsp. Lactuca perennis subsp. granatensis Asteraceae He_ng Be

S Leontodon boryi Asteraceae He_ng Be

S Lepidium stylatum Brassicaceae He_ng Ne

S Leucanthemopsis pectinata Asteraceae Ch Ne

(continued)

Diversity and climate change in Sierra Nevada (Spain) 1047

Dow

nloa

ded

by [

UG

R-B

TC

A G

ral U

nive

rsita

ria]

at 0

0:53

21

Nov

embe

r 20

12

showed slightly higher numbers of species than the

lowest sites.

The life form spectrum over all sites revealed the

predominant role of hemicryptophytes (52 taxa: 13

graminoid and 39 non graminoid) and chamaephytes

(36 taxa) (Table I). Hemicryptophytes grow in

number with increasing altitude reaching 55.6% in

MAC, whereas chamaephytes have similar percen-

tages on the eight summits. The number of taxa

belonging to the phanerophytes declines along the

elevation gradient, becoming absent on the three

highest summits, while therophytes occurr on all the

summits, except at the highest one, with percentages

ranging between 1.9% and 20%.

Biogeographic elements and endemism

Out of the total number of vascular plant species

(except for the five unidentified ones), 35% are

endemic to Sierra Nevada (Ne), 16% to the Baetic

range of southern Spain (Be), 9% are restricted to

the Iberian Peninsula (Ib) and 7% are present in the

Iberian Peninsula and in North Africa (Ib-N), 5%

are more widely distributed in Europe (Eu) and 9%

in Europe as well as in North Africa (Eu-N). The

remaining taxa (Others, 17%) have an even wider

distribution (compare Table I).

The proportion of taxa from each of the seven

biogeographic elements on a summit varied with

Table I. (Continued).

Type taxon Taxon name Family Life form Distribution

S Linaria nevadensis Scrophulariaceae He_ng Ne

S Logfia arvensis Asteraceae Te Eu

subsp. Lotus corniculatus subsp. glacialis Fabaceae Ch Ne

S Luzula hispanica Juncaceae He_ng Ib

S Myosotis minutiflora Borraginaceae Te Others

S Nevadensia purpurea Brassicaceae He_ng Ne

S Plantago nivalis Plantaginaceae He_ng Ne

S Plantago holosteum Plantaginaceae Ch Eu

subsp. Nepeta amethystina subsp. laciniata Lamiaceae Ch Ne

S Paronychia polygonifolia Caryophyllaceae Ch Others

S Pimpinella procumbens Apiaceae He_ng Ne

S Poa ligulata Poaceae He_g Ib-N

subsp. Poa minor subsp. nevadensis Poaceae He_g Ne

S Poa nemoralis Poaceae He_g Eu

S Prunus prostrata Rosaceae Ch Others

S Polygonum aviculare Polygonaceae Te Others

S Potentilla reuteri Rosaceae He_ng Be

S Rhamnus pumila Rhamnaceae Ch Eu-N

S Ranunculus demissus Ranunculaceae He_ng Others

S Reseda complicata Resedaceae Ch Ne

G Rumex sp. Polygonaceae Te

S Saxifraga granulata Saxifragaceace He_ng Others

S Saxifraga nevadensis Saxifragaceace Ch Ne

S Scutellaria javalambrensis Lamiaceae He_ng Ib

S Sedum amplexicaule Crassulaceae Ch Others

S Sedum dasyphyllum Crassulaceae Ch Eu-N

S Sempervivum minutum Crassulaceae Ch Be

S Senecio boissieri Asteraceae Ch Ib

S Senecio nebrodensis Asteraceae He_ng Ib

subsp. Senecio pyrenaicus subsp. granatensis Asteraceae Ch Be

S Sideritis glacialis Lamiaceae Ch Ne

S Silene boryi Caryophyllaceae He_ng Ib

S Solidago virgaurea Asteraceae He_ng Others

S Teucrium aureum subsp. angustifolium Lamiaceae Ch Ib

S Thymus serpylloides Lamiaceae Ch Ne

S Trisetum glaciale Poaceae He_g Ne

S Urtica dioica Urticaceae Ch Others

G Veronica sp. Scrophulariaceae Te

G Viola sp. Violaceae Te

S Viola crassiuscula Violaceae He_ng Ne

Notes: Type of taxon: S¼ species; G¼ genus; subsp.¼ subspecies. Life form: Ph¼ phanerophytes, Ch¼ chamaephytes, He_g¼ graminoid

hemicryptophytes, He_ng¼non graminoid hemicryptophytes, Ge¼ geophytes, Te¼ therophytes. Distribution: Ne¼Nevadense (restricted

to Sierra Nevada); Be¼Baetican; Ib¼ Iberian; Ib-N¼ Iberian-North African; Eu¼European; Eu-N¼European-North African;

Others¼more widely distributed.

1048 M. R. Fernandez Calzado et al.

Dow

nloa

ded

by [

UG

R-B

TC

A G

ral U

nive

rsita

ria]

at 0

0:53

21

Nov

embe

r 20

12

altitude (Figure 3). The pattern of restricted Sierra

Nevada taxa is striking because these increase almost

perfectly along the elevation gradient, whereas the

other biogeographic elements show a more indiffer-

ent pattern.

Altitude, aspect and temperatures

Species richness on the study summits decreases

with increasing elevation, varying from 39 on the

lowest summit (MOR 2668 m) to 18 on the highest

one (MAC 3327 m, Table II). If we consider our

two target regions separately (ES-SNN, ES-SNE),

species richness shows a pronounced peak at middle

altitudes: between 2700 and 2800 m for the first one,

and 2900 and 3000 m for the second one.

There was a significant linear relationship between

species richness and altitude at each spatial scale

(Table III, Figure 4). A decrease of 1.2 species with

every 100 m rise in altitude was calculated for the

1-m2 level (R-squared¼ 0.449, Figure 4a), two

species at the 4-m2 level (R-squared¼ 0.514, Figure

4b), 2.6 species for the upper summit area level

(R-squared¼ 0.484, Figure 4c) and 3.2 species for

the entire summit area level (R-squared¼ 0.450,

Figure 4d). There was no significant relationship

between species richness and the four aspects of the

summits (Table III).

Species richness also correlated with average soil

temperature (2006–2007) at each spatial scale

(Table III). With one degree increase in average soil

temperature, species richness rises, on average, by

1.4 species at the 1-m2 level (R-squared¼ 0.395), 2.1

at the 4-m2 level (R-squared¼ 0.406), 3.1 at the

upper summit area (R-squared¼ 0.467, Figure 5),

and 3.7 at the entire summit area level (R-

squared¼ 0.411).

Discussion

Species richness and endemic taxa

The species numbers found on the sampling

summits in Sierra Nevada fitted well into the overall

altitudinal distribution pattern of the species (com-

pare Figure 2).

Species richness decreased with the increase in

altitude at different spatial scales and, thus, confirms

Figure 2. Vascular plant species richness on each of the eight

summits (triangles) and the overall vertical distribution of all

species found on the summits (horizontal bars).

Figure 3. Biogeographic distribution of taxa on each summit. Ne¼Nevadense; Be¼Baetic range; Ib¼ Iberian peninsula; Ib-N¼ Iberian

peninsula and North Africa; Eu¼Europe; Eu-N¼Europe and North Africa; Others¼more widely distributed.

Diversity and climate change in Sierra Nevada (Spain) 1049

Dow

nloa

ded

by [

UG

R-B

TC

A G

ral U

nive

rsita

ria]

at 0

0:53

21

Nov

embe

r 20

12

Table II. Summary of the features of the eight GLORIA summits in Sierra Nevada.

MOR MIR PUL DIE CUP CUE TCA MAC

Altitude (m a.s.l.) 2668 2717 2778 2800 2968 3144 3150 3327

Species richness per summit 39 65 47 48 52 25 40 18

Percentage top cover vascular plants per summit 31.25 15.37 18.7 19.87 17.5 4.89 15 4.9

Number of Sierra Nevada endemics 12 17 11 19 25 12 22 12

Percentage of Sierra Nevada endemics 31.58 26.98 23.4 42.22 48.08 48 55 66.67

Table III. Results of the One-Way ANCOVA and linear regressions for different measures of species richness against three independent

variables: aspect, altitude, and average soil temperature (2006–2007).

1 m2 plots

Four 1 m2 plots

combined

Upper summit area

(down to 5 m line)

Entire summit area

(down to 10 m line)

Species richness F P F P F P F P

ANCOVA

Aspect 0.208 0.890 0.128 0.942 0.837 0.485 1.169 0.340

Altitude 22.482 50.001 29.015 50.001 27.711 50.001 24.916 50.001

Linear regressions

Altitude 24.415 50.001 31.785 50.001 28.169 50.001 24.503 50.001

Average soil temperature 19.565 50.001 20.529 50.001 26.235 50.001 20.918 50.001

Figure 4. Changes in species richness with increasing altitude at the four aspects and at different spatial levels for eight summits in Sierra

Nevada. (a) Species richness 1 m quadrats; (b) Species richness 4 6 1 m quadrats; (c) Species richness – 5 m SAS; (d) Species richness –

10 m SAS. Full circle¼North, empty circle¼South, Full triangle¼East, empty triangle¼West.

1050 M. R. Fernandez Calzado et al.

Dow

nloa

ded

by [

UG

R-B

TC

A G

ral U

nive

rsita

ria]

at 0

0:53

21

Nov

embe

r 20

12

a common pattern in high-mountain regions (Korner

2002; Nagy & Grabherr 2009) as this was also

reported form GLORIA regions in the Alps (Pauli

et al. 2003; Erschbamer et al. 2010), Carpathians

(Coldea & pop 2004), Pyrenees (Villar & benito

alonso 2003), Apennines (Stanisci et al. 2005), Crete

(Kazakis et al. 2007), Australian Alps (Pickering

et al. 2008), and from sites in the tropical Andes

(Halloy et al. 2010). The decrease in Sierra Nevada,

however, was not uniform, since the second-lowest

showed the highest number of species. This may

indicate an ecotonal situation, where the vertical

distributions of oromediterranean species overlap

with those of cryoromediterranean species; a similar

increase in species richness in the Alpine-nival

ecotone was reported in the central Alps (Gottfried

et al. 1998).

Impacts of environmental and, in particular, of

climate change on biodiversity are expected to

strongly affect restricted endemic species that dwell

at high altitudes. In Sierra Nevada, such specialised

endemic species are the principal component of the

prevailing vegetation of the uppermost life zone (i.e.

especially the cryoromediterranean zone). The high-

altitude flora of Sierra Nevada appears to be

particularly vulnerable to climate warming, with a

high risk of warming-induced species loss.

In a European context, the proportions of local

endemics taxa of 27–67% (27–48% in ES-SNN,

(23–67% in ES-SNE) found on the Sierra Nevada

summits (Table II, Figure 3) are certainly out-

standing compared to other central to southern

European GLORIA sites, such as the NE-Car-

pathians, Rumanian Alps (7% Coldea & Pop

2004), NE-Alps, Austria (2–10%, Pauli et al.

2003), central Apennines, Italy (18–24%, Stanisci

et al. 2005) and Lefka Ori/Crete, Greece (31–36%,

Kazakis et al. 2007). Although the high degree of

endemism in Sierra Nevada has long been recog-

nized (Quezel 1953; Rivas Goday & Mayor Lopez

1966; Molero Mesa et al. 1996), our study presents

an almost continuous elevational increase of the

endemism ratio, documented through a standardised

sampling design.

The isolated geographic position of Sierra Nevada

with an outstandingly high elevation, protruding over

much lower surroundings, are suggested to be the

primary reasons for this high percentage of local

endemic taxa (compare Blanca et al. 1998; Gimenez

et al. 2004; Penas et al. 2005; Perez-Garcıa et al.

2007). Other factors specific to mountain environ-

ments that cause habitat separation, such as un-

common soil and geological conditions, or ‘stressful’

habitats such as low-temperature conditions, can

also be associated with the presence of endemic

plants (Kruckeberg & Rabinowitz 1985; Medail &

Verlaque 1997).

Biodiversity conservation and climate change

Climate projections using GCM models indicate a

rather uniform temperature increase on the Iberian

Peninsula during the twenty-first century. The

average projection is an increase of 0.48C/decade in

winter and of 0.78C/decade in summer, for the least

favourable scenario (A2 of the IPCC), and of 0.48Cand 0.68C/decade, respectively, for the most favour-

able scenario (B2 of the IPCC) (Fernandez-Gonzalez

et al. 2005). A general warming and associated

earlier snow-melt, combined with an expected

precipitation decrease (Mariotti et al. 2008), will

have a strong impact on the species composition of

high-mountain vegetation (Guisan et al. 1995). The

narrower the altitudinal distribution and the geogra-

phical range, the more severe is the potential

vulnerability to climate warming (Ohlemuller et al.

2008; Dirnbock et al. 2011). In Mediterranean

climates, where precipitation is widely absent during

the growing season, forecasted climatic changes are

expected to generally increase environmental severity

in high-mountain habitats, and are likely to lead to

serious biodiversity losses. In this context, species

present on the summits, such as Erigeron frigidus,

Nevadensia purpurea or Trisetum glaciale, with an area

of distribution situated at the highest altitudes of the

Sierra Nevada, will have serious difficulties to survive

if the trend continues. A similar critical situation can

be anticipated for other S-European high mountains

and for the High Atlas or for the fragmented low-

temperature areas of Iran’s mountains, where the

rate of endemism increases very sharply with altitude

(Noroozi et al. 2011). Continued observation and

more detailed studies in Sierra Nevada and new

Figure 5. Changes in species richness in relation to average soil

temperature at the four aspects for eight summits in Sierra

Nevada. Full circle¼MAC, empty circle¼TCA, Full triangle¼CUE, empty triangle¼CUP, Full square¼DIE, empty square¼PUL, Star¼MIR, Diamond¼MOR.

Diversity and climate change in Sierra Nevada (Spain) 1051

Dow

nloa

ded

by [

UG

R-B

TC

A G

ral U

nive

rsita

ria]

at 0

0:53

21

Nov

embe

r 20

12

monitoring in other mountains in Mediterranean-

type climates are required for a thorough assessment

of the rate and magnitude of expected species

declines.

Acknowledgements

This research was supported by GLORIA-EUROPE

(2001–2003; No. EVK2-CT-2000-00056) and by

the National Parks Network (Red de Parques

Nacionales) of the Spanish Ministry of the Environ-

ment, Project 2/2003.

References

Araujo MB, Pearson RG, Thuiller W, Erhard M. 2005a.

Validation of species–climate impact models under climate

change. Glob Change Biol 11: 1504–1513.

Araujo MB, Whittaker RJ, Ladle RJ, Erhard M. 2005b. Reducing

uncertainty in projections of extinction risk from climate

change. Glob Ecol Biogeogr 14: 529–538.

Blanca G, Cueto M, Martınez-Lirola MJ, Molero Mesa J. 1998.

Threatened vascular flora of Sierra Nevada (Southern Spain).

Biol Conserv 85: 269–285.

Broennimann O, Thuiller W, Hughes G, Midgley GF, Alkemalde

JMR, Guisan A. 2006. Do geographic distribution, niche

property and life form explain plants’ vulnerability to global

change? Glob Change Biol 12: 1079–1093.

Castroviejo S, Laınz M, Lopez Gonzalez G, Montserrat T, Munoz

Garmendia F, Paiva J, et al. editors. 1986–2009. Flora Iberica.

Plantas vasculares de la Penınsula Iberica e Islas Baleares. Vols.

I-VIII, X, XIII-XV, XVIII y XXI. Madrid: Real Jardın

Botanico de Madrid, Consejo Superior de Investigaciones

Cientıficas.

Coldea G, Pop A. 2004. Floristic diversity in relation to

geomorphological and climatic factors in the subalpine-alpine

belt of the Rodna Mountains (the Romanian Carpathians).

Pirineos 158: 61–72.

Dirnbock T, Essl F, Rabitsch W. 2011. Disproportional risk for

habitat loss of high-altitude endemic species under climate

change. Glob Change Biol 17: 990–996.

Dullinger S, Kleinbauer I, Pauli H, Gottfried M, Booker R, Nagy

L, et al. 2007. Weak and variable relationships between

environmental severity and small-scale co-occurrence in alpine

plant communities. J Ecol 95: 1284–1295.

Erschbamer B, Mallaun M, Unterluggauer P, Abdaladze O,

Akhalkatsi M, Nakhutsrishvili G. 2010. Plant diversity along

altitudinal gradients in the Central Alps (South Tyrol, Italy)

and in the Central Greater Caucasus (Kazbegi region,

Georgia). Tuexenia 30: 11–29.

Fernandez-Gonzalez F, Loidi J, Moreno Sainz JC. 2005.

Impactos sobre la biodiversidad vegetal, 5. Evaluacion

preliminar de los impactos en Espana por efecto del cambio

climatico. MMA. Secretarıa General Tecnica. Madrid:

Centro de Publicaciones.

Gimenez E, Melendo M, Valle F, Gomez-Mercado F, Cano E.

2004. Endemic flora biodiversity in the south of the Iberian

Peninsula: Altitudinal distribution, life forms and dispersal

modes. Biodiver Conserv 13: 2641–2660.

Gottfried M, Pauli H, Grabherr G. 1998. Prediction of vegetation

patterns at the limits of plant life: a new view of the alpine-nival

ecotone. Arctic Alp Res 30: 207–221.

Grabherr G, Gottfried M, Pauli H. 1994. Climate effects on

mountain plants. Nature 369: 448–448.

Grabherr G, Gottfried M, Pauli H. 2000. GLORIA: A global

observation research initiative in Alpine environments. Mt Res

Dev 20: 190–191.

Grabherr G, Gottfried M, Pauli H. 2001. Long-term monitoring

of mountain peaks in the Alps. In: Burga CA, Kratochwil A,

editors. Biomonitoring: General and applied aspects on

regional and global scales. Tasks for Vegetation Science. Vol.

35. Dordrecht (the Netherlands): Kluwer Academic Publish-

ers. pp. 153–177.

Guisan A, Tessier L, Holten JI, Haeverli W, Baumgartner M.

1995. Understanding the impact of climate changing on

mountain ecosystems: an overview. In: Guisan A, et al.,

editors. Potential ecological impacts of climate change in the

Alps and Fennoscandian mountains, Ed. Conserv. Jard. Bot.

Geneve.

Halloy S, Yager K, Garcıa C, Beck S, Carilla J, Tupayachi A, et al.

2010. South America: Climate monitoring and Adaptation

Integrated across regions and disciplines. In: Settele J, et al.

editors. Atlas of biodiversity risk. Sofia: Pensoft Publishers. pp.

90–95.

Hansen A, Neilson RP, Dale VH, Flather CH, Iverson LR, Currie

DJ, et al. 2001. Global change in forests: Responses of species,

communities, and biomes. BioScience 51: 765–779.

Houghton JT, Ding Y, Griggs DJ, Nouger M, Van der Linden PJ,

Dai X, et al. 2001. Climate change 2001: The scientific basis.

Intergovernmental panel on climate change, Working group I.

New York: Cambridge University Press.

Kazakis G, Ghosh D, Vogiatzakis IN, Papanastasis VP. 2007.

Vascular plant diversity and climate change in the alpine zone of

the Lefka Ori, Crete. Biodiver Conserv 16: 1603–1615.

Korner C. 1994. Impact of atmospheric changes on high mountain

vegetation. In: Beniston M, editor. Mountain environments in

changing climates. London: Routledge. pp. 155–166.

Korner C. 2002. Mountain biodiversity, its causes and function:

An overview. In: Korner C, Spehn E, editors. Mountain

biodiversity – A global assessment. London, New York:

Parthenon. pp. 3–20.

Kruckeberg AR, Rabinowitz D. 1985. Biological aspects of

endemism in higher plants. Ann Rev Ecol Syst 16: 447–479.

Mariotti A, Zeng N, Yoon J-H, Artale V, Navarra A, Alpert P,

et al. 2008. Mediterranean water cycle changes: Transition to

drier 21st century conditions in observations and CMIP3

simulations. Environ Res Lett 3: 044001 (8pp).

Medail F, Verlaque R. 1997. Ecological characteristics and rarity

of endemic plants from southeast France and Corsica:

Implications for biodiversity conservation. Biologic Conserv

80: 269–281.

Molero Mesa J, Perez Raya F. 1987. La Flora de Sierra Nevada.

Avance sobre el catalogo florıstico nevadense. Ed. Universidad

de Granada, Spain.

Molero Mesa J, Perez Raya F, Gonzalez-Tejero MR. 1996.

Catalogo y analisis florıstico de la flora orofila de Sierra

Nevada. In: Chacon Montero J, Rosua Campos JL, editors.

Sierra Nevada. Vol. 2. Madrid, Spain: Conservacion y

desarrollo sostenible. pp. 271–276.

Molero Mesa J, Fernandez Calzado MR, Merzouki A, Casares

Porcel M, Gonzalez-Tejero Garcıa MR. 2009. Escenarios

fitocenologicos de observacion para el seguimiento del cambio

climatico en Sierra Nevada. In: Ramırez L, Asensio B, editors.

Proyectos de investigacion en parques nacionales: 2005–2008.

Espana: Organismo Autonomo Parques Nacionales. pp. 73–

96.

Nagy L, Grabherr G. 2009. Biology of Alpine habitats. Oxford:

Oxford University Press.

Noroozi J, Pauli H, Grabherr G, Breckle SW. 2011. The subnival–

nival vascular plant species of Iran: A unique high-mountain

flora and its threat from climate warming. Biodiver Conserv

20: 1319–1338.

1052 M. R. Fernandez Calzado et al.

Dow

nloa

ded

by [

UG

R-B

TC

A G

ral U

nive

rsita

ria]

at 0

0:53

21

Nov

embe

r 20

12

Ohlemuller R, Anderson BJ, Araujo MB, Butchart SMH, Kudrna

O, Ridgely RS, Thomas CD. 2008. The coincidence of

climatic and species rarity: High risk to small-range species

from climate change. Biol Lett 4: 568–572.

Ozenda P, Borel JL. 1991. Les consequences ecologiques

possibles des changements climatiques dans l’Arc alpin.

Rapport Futuralp. No 1. Grenoble: ICALPE.

Pauli H, Gottfried M, Grabherr G. 1996. Effects of climate change

on mountain ecosystems – Upward shifting of alpine plants.

World Resource Rev 8: 382–390.

Pauli H, Gottfried M, Dirnbock T, Dullinger S, Grabherr G.

2003. Assessing the long-term dynamics of endemic plants at

summit habitats. In: Nagy L, Grabher G, Korner C,

Thompson DBA, editors. Alpine biodiversity in Europe – A

Europe-wide assessment of biological richness and change.

Ecological Studies. Berlin, Springer: Springer. pp. 195–207.

Pauli H, Gottfried M, Hohenwallner D, Reiter K, Grabherr G.

2004. The GLORIA field manual a multi-summit approach.

Luxembourg: European Communities. Available: www.gloria.

ac.at. Accessed Jul 2012 20.

Pearson RG, Dawson TP. 2003. Predicting the impacts of

climate change on the distribution of species: Are biocli-

mate envelope models useful? Global Ecol Biogeogr 12:

361–371.

Penas J, Perez-Garcıa F, Mota JF. 2005. Patterns of endemic

plants and biogeography of the Baetic high mountains (south

Spain). Acta Bot. Gallica 152: 347–360.

Perez-Garcıa FJ, Cueto M, Penas J, Martınez-Hernandez F,

Medina-Cazorla JM, Garrido-Becerra JA, et al. 2007. Selection

of an endemic flora reserve network and its biogeographical

significance in the Baetic range (Southern Spain). Acta Bot

Gallica 154: 545–571.

Pickering CM, Hill W, Green K. 2008. Vascular plant diversity

and climate change in the alpine zone of the Snowy Mountains,

Australia. Biodiver Conserv 17: 1627–1644.

Quezel P. 1953. Contribution a l’etude phytosociologique et

geobotanique de la Sierra Nevada. Mem Soc Brot 9: 5–77.

Rivas Goday S, Mayor Lopez M. 1966. Aspectos de la vegetacion

y flora orophila del Reino de Granada. Anal Real Acad Farm

31: 345–400.

Rivas-Martınez S. 2007. Mapa de series, geoseries y geopermaseries

de vegetacion de Espana (Memoria del mapa de vegetacion

potencial de Espana. Parte I). Itinera Geobotanica 17: 1–436.

Stanisci A, Pelino G, Blasi C. 2005. Vascular plant diversity and

climate change in the alpine belt of the central Apennines

(Italy). Biodivers Conserv 14: 1301–1318.

Theurillat JP. 1995. Climate change and the alpine flora some

perspectives. In: Guisan A, Holten JI, Spichiger R, Tessier L,

editors. Potential ecological impacts of climate change in the

Alps and Fennoscandian mountains. Geneve: Conserv Jard

Bot. pp. 121–127.

Thuiller W, Broennimann O, Hughes G, Alkemalde JMR,

Midgley GF, Corsi F. 2006. Vulnerability of African mammals

to anthropogenic climate change under conservative land

transformation assumptions. Global Change Biol 12: 424–440.

Villar L, Benito Alonso J-L. 2003. La flora alpina de europa y el

cambio climatico: El caso del pirineo central (Proyecto

GLORIA-Europe). VII Congreso Nacional de la Asociacion

Espanola de Ecologıa Terrestre. Barcelona: Edita AEET. pp.

92–105.

Diversity and climate change in Sierra Nevada (Spain) 1053

Dow

nloa

ded

by [

UG

R-B

TC

A G

ral U

nive

rsita

ria]

at 0

0:53

21

Nov

embe

r 20

12