51 Gentili et al Ecol Complex 2015

Ecological Complexity

jo ur n al ho mep ag e: www .elsevier .c om /lo cate/ec o co m

Review

Potential warm-stage microrefugia for alpine plants: Feedback between geomorphological and biological processes

d R. a Gentili * , C. Baroni b c , a M. Caccianiga , S. Armiraglio , A. Ghiani , S. Citterio

b Dipartimento di Scienze dell’Ambiente e del Territorio, Universita` degli Studi di Milano Bicocca, Piazza della Scienza 1, I-20126 Milano, Dipartimento Italy di Scienze della Terra, Universita` di

c Pisa and CNR, Istituto di Geoscienze e Georisorse, Via S. Maria 53, I-56126 Pisa, Italy

d Dipartimento di Bioscienze Universita` degli Studi di Milano, Via Celoria 26, 20133 Milano, Italy Museo Civico di Scienze Naturali di Brescia, Via Ozanam 4, 25128 Brescia, Italy

Article history: During interglacial stages, microrefugia are sites that support locally favorable climates within larger areas

Received 21 July 2014 with unfavorable warmer climates. Despite recent theoretical representations of microrefugia, an

Received in revised form 11 October 2014 appropriate ecological characterization is still lacking, mostly for

Accepted 13 November 2014 warm periods. Across mountain/alpine

Available online areas, cold-adapted plant species could adopt different strategies to manage the effects of climate warming: (A) migration toward higher elevations and summits; (B) in situ resilience of communities and species

populations within microrefugia; and C) adaptation and evolution by genetic differentiation. This review

Keywords: Resilience

aims to distinguish and characterize from an ecological perspective glacial, nival, periglacial and composite

Mesorefugia landforms and deposits that may function as potential microrefugia during interglacial warm periods.

Periglacial refugia We conducted a literature screening related to the geomorphological processes and landforms

Evolutionary geomorphology associated with vegetation and plant communities in alpine/mountain environments of Europe. They

Marginal population include glacial deposits rock glaciers, debris-covered glaciers, composite cones and channels. In Alpine

Microclimate regions, geomorphologic niches that constantly maintain cold-air pooling and temperature inversions

are the main candidates for microrefugia. Within such microrefugia, microhabitat diversity modulates

the responses of plants to disturbances caused by geomorphologic processes and supports their aptitude

for surviving under extreme conditions on unstable surfaces in isolated patches. Currently, European

marginal mountain chains may be considered as examples of macrorefugia where relict boreo-alpine

species persist within peculiar geomorphological niches that act as microrefugia.

This review contributes to identifying potential warm-stage microrefugia areas across alpine and

mountain regions and determining certain landforms that play or may play such role under global-

change scenarios. The occurrence of warm-stage microrefugia within these locations may be of great

importance for the modeling of future distributions of species and assessing the risk of extinction for

alpine species. Microrefugia may have important implications in micro-evolutionary processes that

occur across alternating climatic phases.

ß 2014 Elsevier B.V. All rights reserved.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 88

2. Literature screening . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 89

3. Landforms working as warm-stage microrefugia . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 90

3.1. Mountain summits (and relict surfaces) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 90

3.1.1. Landform-vegetation unit . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 90

3.1.2. Climatic control . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 90

3.1.3. Microclimate features . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 90

3.1.4. Microrefugium function . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 90

* Corresponding author. Tel.: +39 02 64482700; fax: +39 02 64482996.

E-mail addresses: rodolfo.gentili@unimib.it (R. Gentili), baroni@dst.unipi.it (C. Baroni), marco.caccianiga@unimi.it (M. Caccianiga), botanica@comune.brescia.it

(S. Armiraglio), alessandra.ghiani@unimib.it (A. Ghiani), sandra.citterio@unimib.it (S. Citterio).

http://dx.doi.org/10.1016/j.ecocom.2014.11.006

1476-945X/ß 2014 Elsevier B.V. All rights reserved.

88 R. Gentili et al. / Ecological Complexity 21 (2015) 87–99

3.2. Debris-covered glaciers. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 90

3.2.1. Landform-vegetation unit . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 90

3.2.2. Climatic control . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 90

3.2.3. Microclimate feature . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 90

3.2.4. Microrefugium function . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 90

3.3. Moraine ridges and deglaciated forelands . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 92

3.3.1. Landform-vegetation unit . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 92

3.3.2. Climatic control . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 93

3.3.3. Microclimate features . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 93

3.3.4. Microrefugium function . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 93

3.4. Nivation niches/snow patches . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 93

3.4.1. Landform-vegetation unit . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 93

3.4.2. Climatic control . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 93

3.4.3. Microclimate features . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 93

3.4.4. Microrefugium . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 93

3.5. Rock glaciers . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 93

3.5.1. Landform-vegetation unit . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 93

3.5.2. Climatic control . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 93

3.5.3. Microclimate feature . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 93

3.5.4. Microrefugium function . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 93

3.6. Alpine composite debris cones (debris slopes/scree) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 94

3.6.1. Landform-vegetation unit . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 94

3.6.2. Climatic control . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 94

3.6.3. Microclimate feature . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 94

3.6.4. Microrefugium . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 94

3.7. Alpine corridors (composite channels/avalanche channels and tracks) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 94

3.7.1. Landform-vegetation unit . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 94

3.7.2. Climatic control . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 94

3.7.3. Microclimate features . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 94

3.7.4. Microrefugium . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 94

3.8. Ice caves . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 94

3.8.1. Landform-vegetation unit . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 94

3.8.2. Climatic control . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 94

3.8.3. Microclimate feature . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 94

3.8.4. Microrefugium function . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 94

3.9. Other landforms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 95

3.10. Primary topographic factors: elevation, aspect and slope. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 95

4. The feedback between geomorphological and biological processes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 95

5. Survival strategies for high-altitude species . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 96

6. Microrefugia in European marginal mountain chains . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 96

7. Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 97 Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 97 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 97

1. Introduction the ‘‘refuge hypothesis’’ was postulated for birds of the Amazon forest as a theory of ice-age speciation events based on climate

Global temperatures have increased over the last century ( IPCC,

change ( Haffer, 1969 ). Favarger and Robert (1966) considered that

2007 ), and in recent decades, the climate has become more

the Maritime Alps, South-Eastern Alps and Jura Mountains were

extreme in many regions of the world, with further changes

important migration areas (e.g., refugia) in which alpine taxa expected in the nature, extent and incidence of different weather concentrated during quaternary glaciations. Holder et al. (1999)

events, such as exceptional summer heat waves in certain

assumed a ‘‘glacial refugium hypothesis’’ for the Northern Hemi-

temperate regions or in mountain areas ( Abeli et al., 2012a;

sphere and proposed that during the Pleistocene, glacier Mastrandrea and Tavoni, 2013 ). An urgent challenge in conserva- expansion favored intraspecific diversity by isolating populations

tion biogeography is to determine how species will respond to such in ice-free refugia. Recently, the terms refugia/refugium were

climate changes. To avoid extinction, species may respond to

similarly applied to Neotropical forest regions and areas where

climate change by migrating to new areas and adapting through species survive during warm-stage interglacial periods ( Birks and

phenotypic plasticity and adaptive evolution to the new environ- Willis, 2008; Rull, 2009 ). Stewart et al. (2010) defined a refugium as

mental conditions ( Ghalambor et al., 2007 ).

‘‘a region or regions that a species inhabits during the period of a glacial/

In addition to such mechanisms, there has been an increasing interglacial cycle that represents the species’ maximum contraction in

acknowledgment of the role of refugium areas in facilitating the geographical range.’’

long-term survival of species and populations throughout several Rull et al. (1988) introduced the term ‘‘microrefugium,’’ which

climatic oscillations, which contributes to the preservation of

was theoretically centered on a biogeographic perspective ( Rull,

biological diversity from extinction. Historically, the notion of

2009 ) as a ‘‘small area with local favorable environmental features, in

ecologic refugium/refugia was referred to as areas of survival for which small populations can survive outside their main distribution

species during quaternary glacial phases with unfavorable climate area (the macrorefugium), protected from the unfavorable regional

conditions. For instance, Battandier (1894) introduced the impor- environmental conditions.’’ From its name, macrorefugium can be

tance of Mediterranean glacial refugia in North Africa. Subsequently, determined as ‘‘a large scale refugia that may form from a contracting

R. Gentili et al. / Ecological Complexity 21 (2015) 87–99 89

main (continuous) range,’’ and it can be further distinguished from biogeographical roles and ecological characterizations is still various terms (cryptic refugia and microrefugia) and synonyms lacking ( Rull, 2009; Mee and Moore, 2014 ), especially for mountain

(interglacial refugia, periglacial refugia and northern refugias) regions where future climatic scenarios are predicted to produce

( Holderegger and Thiel-Egenter, 2009; Rull, 2010; Dahlberg, 2013 ).

significant effects ( Thuiller et al., 2005; Thuiller, 2007 ) and for

In addition, Olson et al. (2012) defined mesorefugia as ‘‘large areas which microrefugia could play an important role for the survival of

that contain nested clusters of microrefugia with similar species alpine plants. Even if mountain regions appear to be especially

assemblages that have functioned as a refugium over millennia.’’ well-suited to providing potential microrefugia, their number,

However, the occurrence of micro- and macrorefugia for some

characteristics, location and spatial extent remain cryptic, both regions and climatic periods (e.g. northern Europe) is still debated for paleoecological analyses ( Rull, 2009; Holderegger and Thiel-

( Tzedakis et al., 2013; Rull, 2014 ). Egenter, 2009 ) and current analyses ( Keppel et al., 2012 ). It has been widely accepted that during the Pleistocene,

According to the recent works of Dobrowski (2011) and Ashcroft

numerous arctic and alpine species migrated in deglaciated areas et al. (2012) , the most suitable level to which microrefugia can be

or tolerated glacial conditions within nunatak refugia ( Schneeweiss identified is based on microclimatic and microtopographic and Schoenswetter, 2011 ). Despite the debate regarding ecological characterizations of landscapes and by using species distribution

refugia for animal and plant species during glacial periods having models ( Keppel et al., 2012; Keppel and Wardell-Johnson, 2012;

reached a climax across literature works, warm-stage refugia have Patsiou et al., 2014 ). However, most of the predictive models for

still been poorly considered ( Stewart et al., 2010 ). the potential distribution of species in alpine environments and all

During interglacial warm periods, forest and cold-adapted of the refugial hypotheses rarely consider the role of geomorpho-

species endured through an upward migration to mountain refugia logical processes acting in mountain areas as potential forces ( Bush, 2002 ) or persisted in other refugial areas ( Bhagwat and capable of creating local microhabitat conditions for hosting Willis, 2008 ) or within microrefugia ( Rull, 2009 ). In interglacial

species during adverse climatic conditions and geomorphological

stages, microrefugia are sites supporting locally favorable cold/ processes. For this reason, in this review, going over such a mere

fresh climates interspersed in larger areas with unfavorable warm technical approach, we present a literature screening on the climate, and they allow populations of species to persist outside of mountain landforms or geomorphological features that have been

their main distributions ( Stewart et al., 2010; Dobrowski, 2011 ).

predicted or inferred to function as current or future (micro- The terminology ‘‘microrefugia’’ as defined by Rull (2009) will be )refugia. The specific goals of this work are to a) characterize

used throughout the manuscript. geomorphological processes and related landforms of alpine life

Gottfried et al. (2012) observed a significantly higher abun- zones in European mountains and depict their function in creating

dance of thermophilic species in the mountain summits of Europe ecological heterogeneity and acting as potential microrefugia; and

over the last decade. In addition, recent projections of high

b) evaluate the role of such landforms in certain marginal, low

mountain species habitat shifts that result from temperature mountain chains of Europe that host relict alpine flora and, even

increases indicate that there will be a decline of cold habitats and now, function as microrefugia.

flora by the end of twenty-first century ( Thuiller et al., 2005; Pauli

et al., 2012; Dullinger et al., 2012 ). However, future extinction

2. Literature screening

rates could be overestimated if microrefugia are not considered in

models ( Mosblech et al., 2011 ). We focused on literature data related to the geomorphological

In mountain areas, climate is a key limiting factor for plant life, processes and landforms associated with vegetation and plant and it is directly related to topography, which determines specific communities in alpine/mountain environments. Even if mountains

microhabitat conditions ( Harris, 2008; Gentili et al., 2013 ). For with an alpine zone occur at all latitudes from the wet tropics to

instance, different slopes and aspects modulate the effects of polar regions ( Grabherr et al., 2010 ), in this paper, we refer to the

temperature and water balance for plant species (topo-climate). alpine life zone of Europe in which both vegetation patterns and

According to Abbott (2008) and Crawford (2008) topographic geomorphologic processes have been deeply studied. In particular,

heterogeneity may favor the survival of several arctic and alpine we considered the mountain chains of Europe that host alpine

species that are able to occupy a range of habitats, which may vary habitats and flora and are included in the ‘‘alpine floristic system’’

in temperature, soil-moisture content and wind exposure. For

( Aeschimann et al., 2004) , which comprises the Alps in sensu stricto

these reasons, topographic locations that constantly maintain and alpine marginal chains. Alpine marginal chains include the

cold-air pooling and temperature inversions can be predicted as

Pyrenees, Central Massif, Jura, Vosgi, Black Forest Mountains,

the main candidates for warm-stage microrefugia. From this

Apennines (northern and central), Carpathians, Dinaric Alps,

perspective, Mosblech et al. (2011) indicated that local topo-

Corsica and Balcan mountains. In this study, some northern or

graphic shelter effects can increase the probability of a species eastern Europe mountain chains were considered as well as north

surviving in a microrefugium. American.

We reviewed the literature from the Web of Knowledge they called ‘‘cryptic refugia’’) with micro-environmentally

Birks and Willis (2008) specified certain microrefugia (that

database (Thomson Reuters) through a search of the online favorable conditions, such as north-facing slopes, steep cliffs, database using several combinations of the following queries: sea-cliffs and cool ravines. During the current phase of climate landforms/geomorphological processes*, vegetation or plant com-

warming, they noted that (micro-)refugia within alpine areas can munity*, plants*, flora*, refugia*, and Alps/Alpine*. Distinct

be niches where alpine species might be able to grow below the searches were performed for the main geomorphologic processes

altitudinal forest limit (e.g., warm-stage microrefugia). According of alpine environments in relation to vegetation*/plant communi-

to Grabherr et al. (1995) , more than one-third of the alpine/nival ty*, which included alpine corridor*, debris flow*, debris-covered

flora is restricted to azonal habitats, especially rocks, debris

glacier*, glacial deposit*, mountain summit/peak*, nivation niche*,

slopes and snowbeds that represent nonstandard habitats created rock/debris fall* rock glacier*, snow avalanche*, and composite/

by disturbances. Such landscape locations may have climatic

debris/talus cone*.

environmental patterns that are constantly dissimilar from

Certain gray literature data (i.e., journal that is not cataloged in

regional patterns ( Dobrowski, 2011 ). the Web of Knowledge and Scopus databases or is not shown after

Despite such recent characterizations and theoretical repre- a search) were extrapolated from reference lists of papers collected

sentations of microrefugia, an appropriate representation of their through the search and then included. The gray literature data

90 R. Gentili et al. / Ecological Complexity 21 (2015) 87–99

often included articles related to marginal local mountain chains Such processes can induce differentiated environments with ( Table 1 ).

marked seasonality, even if rigid temperatures in winter are We organized the collected literature data based on the main mitigated by thermal inversion ( Berry, 1992 ).

mountain landforms that can be found along slopes according to

the main mountain/alpine landforms and deposits above or

3.1.4. Microrefugium function

(sometime) across treeline ( Fig. 1 ): (a) mountain summits above In mountain areas, climate warming is projected to shift

trimlines (including relict surfaces); (b) glacial landforms and

species’ ranges to higher elevations, even if the alpine plants react

deposits, such as glacial forelands, moraines, and debris-covered individualistically to climate change ( Grabherr et al., 2010 ). glaciers; (c) nival landforms and deposits, such as nivation niches/ Currently, the local diversity of the majority of boreal and snow patches; (d) periglacial landforms and deposits, such as rock temperate mountain peaks is increasing because of rising

glaciers; (e) composite landforms (polygenic), such as alpine

temperatures ( Klanderud and Birks, 2003; Pauli et al., 2007 ). composite cones, alpine corridors (composite channels/avalanche Even if some species have been found as relicts on summits of

channels) and tracksu`; (f) other landforms (ice caves, roches

marginal alpine chains ( Table 1 ), the role of mountain peaks as

moutonne´es, etc.). The main topographic features were also

microrefugia is undefined and debated, especially for the considered, such as elevation, slope and aspect. middle-long period if the increasing trend continues ( Pauli et We then characterized each landform according to its vegeta- al., 2012 ). According to Dobrowski (2011) , mountain peaks are

tion features (landform-vegetation units; see Baroni et al., 2007 ),

expected to play a limited role as microrefugia because they climatic controls, microclimate features of active landforms and show the strongest similarity to the free-air environment and

microrefugium functions. exhibit the smallest diurnal temperature variance with respect

We did not consider wetlands and peat bogs that have already to bottom valleys and valley slopes. However, Randin et al. been considered as refugia and where only highly specialized plant (2009) projected species distribution models and indicated species and communities occur. that local scale models can predict persistent alpine species habitats toward higher elevations, where the aspect and local

3. Landforms working as warm-stage microrefugia topographic conditions may locally preserve favorable micro-

habitats.

3.1. Mountain summits (and relict surfaces)

3.2. Debris-covered glaciers

3.1.1. Landform-vegetation unit

Mountain summits consist of highest elevations of mountain

3.2.1. Landform-vegetation unit

chains above the trimlines and sharp ridges (Are´te´s). They include Debris-covered glaciers (or black glaciers) are glaciers whose

the top levels of mountains and relict surfaces that were not ablation area is mainly covered by a continuous layer of affected by Pleistocene glacial action and include peaks, crests and supraglacial debris ( Fig. 1 b). Vegetation cover is mainly discontin-

crowns affected by frost action mainly under periglacial conditions uous and patchy with a species assemblage that may be similar to

( Fig. 1 a). In alpine areas, generally deglaciated terrains along sharp that of alpine and subalpine glacier forelands, with the latter

ridges and on horns extend downward to the highest portions of enriching high-altitude species such as Androsace alpina ( Caccia-

accumulation basins as glacial basins reduce their size ( Baroni and niga et al., 2011 ). Orombelli, 1996 ). The acceleration of glacier contractions ( Haeberli

et al., 1999 ) has been increasingly furnishing new and wider

3.2.2. Climatic control

portions of the highest accumulation basins, which are suitable for As a general rule, debris-covered glaciers follow the course of

refugia during warm periods (e.g., the Careser Glacier, Carturan et glacier retreats and advances under a regional/continental climatic

al., 2013 ). regime. Under the present climatic conditions, debris-covered Erosional processes, (both periglacial, glacial or gravity-based) glaciers exhibit a far less negative mass balance, which may even

of mountain summits are mainly controlled by the type, structure be positive in certain circumstance, than white glaciers ( Fickert et

and mass strength of the rock and geometry of the slope

al., 2007; Diolaiuti and Smiraglia, 2010 ), so they may show a long

( Cruden and Hu, 1999 ). On summits, floristic and vegetation

persistence within warm climatic periods.

patterns are a function of the elevation level, latitudinal range and

habitat availability ( Kazakis et al., 2007 ). In temperate mountains 3.2.3. Microclimate feature

(e.g., European Alps), the limit of higher plant life lies at

Variations in debris thickness influence the debris surface

approximately 3000–4000 m, where only specialized plants

temperature because of debris thermal conductivity and low

(cushion) or those with nival aptitudes are currently able to

albedo. The temperature pattern of supraglacial debris is survive under harsh conditions; these plants include Leucanthe- characterized by a high daily excursion with radiative heating mopsis alpina and Ranunculus galcialis ( Ko¨rner, 2003; Grabherr during the daytime and cooling by sensible heat transfer during the

et al., 2010 ).

night ( Brock et al., 2010 ).

3.1.2. Climatic control 3.2.4. Microrefugium function

Weathering erosional processes of mountain summits (peri-

Debris-covered glaciers can provide habitat with favorable glacial or because of gravity) are mainly controlled by relationships microclimatic conditions for numerous plant species wherever the

among the climate, type, structure and mass strength of the rock, glacier surface is sufficiently stable ( Table 1 ). High-altitude taxa

geometry of the slope, and biota ( Cruden and Hu, 1999 ).

have been found below their altitudinal limits on such glaciers because of the cooler subsurface soil temperatures ( Fickert et al.,

3.1.3. Microclimate features 2007 ). Moreover, shrubs and trees are able to germinate and grow

In mountain summits, thermal conditions have periglacial

across their surface once they become stable and thick enough

characteristics and may vary according to aspect. Summits may ( Pelfini et al., 2012 ). Debris-covered glaciers may act as a dispersal

benefit from favorable climatic conditions during the summer agent for alpine species; this role could have important implica-

season because of direct solar radiation (heating) and reflection of tions during glacial periods and particularly during warm periods

rock outcrops by the local availability of melt water from snow. of the Holocene ( Caccianiga et al., 2011 ).

R. Gentili et al. / Ecological Complexity 21 (2015) 87–99 91 Table 1

Landforms functioning or predicted to function as (micro-)refugia during warm periods.

Landforms Microrefugia Function Species Area Reference

Mountain summits Alpine species found in marginal/ Current

Leucanthemopsis alpina, N-Apennines Abeli et al. (2012a,b);

deglaciated/low elevation chain function

Senecio incanus Alessandrini et al. (2003)

Species predicted to persist after Predicted

Androsace alpina Tyrolean Alps Grabherr et al. (2010)

a projected warming effects of function

+5 K

Alpine species found in marginal/ Current function Androsace vandelli, Potentilla Pyrenees Go´mez et al. (2003)

deglaciated/low elevation chain nivalis

Debris-covered glaciers Alpine species found below the Deducted/predicted

Artemisia glacialis, Carex Western Alps Caccianiga et al. (2011)

tree line function

curvula, Ranunculus glacialis,

Saxifraga bryoides, etc.

Moraine ridges and Alpine species found in marginal/ Current function Juncus jacquinii N-Apennines Gentili et al. (2006)

deglaciated forelands deglaciated/low elevation chain

Alpine species found in marginal/ Current function Viola comollia Prealps Credaro and Pirola (1977)

deglaciated/low elevation chain

High Alpine-nival species found Current function Androsace alpina, Ranunculus Prealps Caccianiga and Andreis

in marginal/almost deglaciated/ glacialis, Saxifraga (2004)

low elevation chain oppositifolia

Nivation niches/snow Climatic niches for alpine species Inferred/predicted

‘‘Snowbed plants and Swedish Scandes Kullman (2010)

patches

function

bryophites’’ (species not

declared)

Alpine species found in marginal/ Current function Salix herbacea, Silene suecica N-Apennines Abeli et al. (2012a,b);

deglaciated/low elevation chain Alessandrini et al. (2003)

Alpine species found in marginal/ Current

Cerastium cerastioides N-Apennines Alessandrini et al. (2003)

deglaciated/low elevation chain

function

Alpine species found in marginal/ Current function Poa minor, Salix retusa, Dinaric Alps Surina and Surina (2010)

deglaciated/low elevation chain Soldanella alpina, Veronica

alpina, etc.

Alpine species found in marginal/ Current function Salix herbacea Dinaric Alps Redzic (2011)

deglaciated/low elevation chain

Alpine species found in marginal/ Current function Andreaea nivalis Tatra mountain Fudari and Kucˇera (2002)

deglaciated/low elevation chain

Rock glaciers Same plants growing in glacier Inferred/predicted

Androsace alpina, Poa laxa, Central Swiss Alps Burga et al. (2004)

forefields or in mountain function

Oxyria digyna, Saxifraga

summits

bryoides, etc.

Cold-demanding and snowbed Inferred/predicted

Polytrichastrum alpinum, Central Italian Alps Gobbi et al. (2014)

species

function

Saxifraga bryoides, Oxyria

digyna etc.

Alpine species found in marginal/ Current function Empetrum hermaphroditum, N-Apennines Tomaselli and Agostini

deglaciated/low elevation chain Juncus trifidus, Luzula alpino- (1990)

pilosa

Alpine composite Alpine species found below the Inferred/predicted

Leucanthemopsis alpina, Central Italian Alps Baroni et al. (2007)

debris cones tree line function

Oxyria digyna, Poa laxa

Climatic niches for alpine species Inferred/predicted

Cerastium uniflorum, French Alps Bodin (2010)

function

Cryptogramma crispa,

Soldanella alpina, etc.,

Alpine species found in marginal/ Current function Doronicum grandiflorum, Corsican mountains Gamisans (2003)

deglaciated/low elevation chain Oxyiria digyna

Alpine species found in marginal/ Current function Ranunculus glacialis Carpathian massif Ronikier (2010)

deglaciated/low elevation chain

Alpine species found in marginal/ Current function Poa alpina, Silene acaulis, C-Apennines Di Pietro et al. (2008)

deglaciated/low elevation chain Linaria alpina, etc.

Alpine species found in marginal/ Current function Carex foetida N-Apennines Tomaselli (1991)

deglaciated/low elevation chain

Alpine species found in marginal/ Current function Polygonum viviparum, Salix Dinaric Alps Redzˇic´ et al. (2011)

deglaciated/low elevation chain retusa, S. serpyllifolia,

Soldanella alpina

Alpine species found in marginal/ Current function Cryptogramma crispa, Luzula Pyrenees Go´mez et al. (2004)

deglaciated/low elevation chain alpino-pilosa, Oxyria digyna,

etc.

Alpine species found in marginal/ Current function Andreaea rupestris, Northern Bhoemia Ru˚zˇicˇka et al. (2012)

deglaciated/low elevation chain Cryptogramma crispa,

Gymnomitrion spp.,

Polytrichum alpinum, etc.

Alpine corridors Alpine species found below the Inferred/predicted

Cerastium uniflorum, Oxyria Central Italian Alps Gentili et al. (2010)

tree line function

digyna, Saxifraga oppositifolia,

Cardaminopsis alpina, etc.

Alpine species found below the Current function Campanula pulla, Arabis Austrian Alps Komposch et al. (2013)

tree line alpina, Linaria alpina

Ice caves Alpine species found below the Current function Rhytidiadelphus triquetrus, Northeastern Iowa Nekola (2013)

tree line Seligeria pusilla, etc.

92 R. Gentili et al. / Ecological Complexity 21 (2015) 87–99

Fig. 1. Main landforms in the alpine area. (a) Mountain summits and frontal moraines close to recent deglaciated areas (Presena, Central Alps, Italy). (b) Debris-covered glacier

in the Miage Glacier Basin (Western Alps, Italy); the local tree limit is at the boundary or sometimes above the debris-covered glacier. (c) Avalanche channel and snow

accumulation across treeline (Malga Caldea, Central Alps, Italy); box c1: the alpine C. uniflorum, which is generally a pioneer species in the upper alpine area close to glacial

bodies and can be found below the tree limit within avalanche channels. (d) Active and inactive rock glaciers (Eastern Alps, Val D’Ultimo, Italy); (e) Alpine composite debris

cones: different lines separate the different geomorphological unit originating from the different processes. (f) Alpine composite channels below to active glacier: high alpine

species such as Oxyria digyna (box f1) and Poa laxa can be found close to the treeline.

3.3. Moraine ridges and deglaciated forelands (or forefields) are valley-floor deposits that are exposed to erosion

after glacial retreat ( Fig. 1 a). They are subjected to paraglacial

3.3.1. Landform-vegetation unit modification by mass movements, frost sorting, wind and water Moraine consists of rock and soil material picked up and

transport, sediment storage (sandur), and they are also subjected

transported by glaciers and then deposited. Deglaciated forelands to vegetation colonization; in addition, glaciofluvial processes

R. Gentili et al. / Ecological Complexity 21 (2015) 87–99 93 contribute to sediment reworking ( Eichel et al., 2013 ). Areas with in relation to the snow duration and micro-morphologic and

thin debris deposits may uncover bedrock areas with roches

topographic characteristics, such as grain size, slope and aspect

muoutonne´es that produce peculiar vegetation mosaics ( Parolo

( Palacios et al., 2003 ).

et al., 2005 ). On moraines, depending on the surface age and stabilization, vegetation may consist of different plant

3.4.2. Climatic control

communities in a continuum of successional phases from pioneer The patterns of snow distribution in alpine terrain are a

communities growing on active/recent moraines (e.g., Saxifraga

consequence of interactions between climatic variables, such as

spp. and O. digyna), to alpine grasslands (often dominated by Poa radiation, precipitation and wind, and topographic variables,

alpina) on stabilized deposits and to subalpine discontinuous

primarily slope and aspect ( Keller et al., 2005 ).

shrubland (Salix spp.) and woodlands (Picea excelsa and Larix decidua) ( Birks, 1980; Matthews, 1992; Caccianiga et al., 2001; 3.4.3. Microclimate features

Caccianiga and Andreis, 2004 ).

Snow cover affects the air and soil temperatures (until the occurrence of snow melt) and various abiotic conditions, such as

3.3.2. Climatic control soil moisture and nutrients. With a complete disappearance of the

Moraines and deglaciated forelands follow the course of glacial snow cover, a greater amount of solar energy is absorbed by the soil

retreats and advances under a regional/global climatic regime. surface, which heats the ground and air ( Wipf and Rixen, 2010 ).

3.3.3. Microclimate features 3.4.4. Microrefugium

Distance from the glacier along with local differences in

In low mountains or in peripheral mountain chains, nivation

topographic features (e.g., height of the ridge crest) above the niches and long-lasting snow cover have been reported as the

glacier foreland primarily affect the microclimate of these

principal factors favoring the persistence of a scattered alpine belt

landforms and deposits ( Matthews, 1992 ). Secondary factors

at the highest peaks and/or survival of high mountain species

may include the sedimentary and textural characteristics of the within small microsites ( Stanisci et al., 2005; Grabherr et al., 2010;

glacial deposits and water availability, such as from glacial

Abeli et al., 2012a ; Table 1 ).

melting.

3.5. Rock glaciers

3.3.4. Microrefugium function

Until recently, glacial deposits and foreland and moraine

3.5.1. Landform-vegetation unit

ridges have been reported as performing the role of glacial

Rock glaciers are tongue-shaped bodies made of coarse debris

refugia and/or microrefugia for plant and animal species during that may develop after a glacier retreat and under permafrost

cold periods ( Lutz et al., 2000; Bhagwat and Willis, 2008;

conditions ( Fig. 1 d). Active and inactive rock glaciers consist of a

Kaltenrieder et al., 2009 ). In particular, several paleoenviron-