Long-Term Records of Vegetation Dynamics As a Basis for Ecological Hypothesis Testing

Perspectives in Plant Ecology, Evolution and Systematics 15 (2013) 338–359

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Perspectives in Plant Ecology, Evolution and Systematics

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Review

Ecological palaeoecology in the neotropical Gran Sabana region:

Long-term records of vegetation dynamics as a basis for ecological hypothesis testing

a,∗ b c,d

Valentí Rull , Encarni Montoya , Sandra Nogué ,

e a,e

Teresa Vegas-Vilarrúbia , Elisabet Safont

Palynology & Paleoecology Lab, Botanic Institute of Barcelona (IBB-CSIC-ICUB), Pg. del Migdia s/n, 08038 Barcelona, Spain

Department of Environment, Earth & Ecosystems, Centre for Earth, Planetary, Space and Astronomical Research (CEPSAR), The Open University, Walton

Hall, Milton Keynes MK7 6AA, UK

Long-term Ecology Laboratory, Biodiversity Institute, Department of Zoology, University of Oxford, Tinbergen Building, South Parks Road, Oxford OX1 3PS, UK

Department of Biology, University of Bergen, N-5020, Bergen, Norway

Department of Ecology, University of Barcelona, Av. Diagonal 643, 08028 Barcelona, Spain

a r t i c l e i n f o a b s t r a c t

Article history: Long-term palaeoecological records are needed to test ecological hypotheses involving time, as short-

Received 18 March 2013

term observations are of insufﬁcient duration to capture natural variability. In this paper, we review the

Received in revised form 27 July 2013

published palaeoecological evidence for the neotropical Gran Sabana (GS) region, to record the vege-

Accepted 29 July 2013

tation dynamics and evaluate the potential effects of natural climatic and anthropogenic (notably ﬁre)

Available online 19 September 2013

drivers of change. The time period considered (last 13,000 years) covers major global climate changes

and the arrival of humans in the region. The speciﬁc points addressed are climate–vegetation equilib-

Keywords:

rium, reversibility of vegetation changes, the origin of extant biodiversity and endemism patterns and

Long-term ecology

biodiversity conservation in the face of global warming. Vegetation dynamics is reconstructed by pollen

Non-analogue communities

analysis and ﬁre incidence is deduced from microscopic charcoal records. Palaeoclimatic inferences are

Community stability

Climate–vegetation disequilibrium derived from global and regional records using independent physico-chemical evidence to avoid circular

Origin of biodiversity reasoning. After analyzing all the long-term records available from both GS uplands and highlands, we

Biodiversity conservation conclude that: (1) Upland vegetation (mostly treeless savannas and savanna–forest mosaics, with occa-

sional Mauritia palm swamps) is not in equilibrium with the dominant climates, but largely conditioned

by burning practices; (2) a hypothetical natural or “original” vegetation type for these uplands has not

been possible to identify due to continuous changes in both climate and human activities during the last

13,000 years; (3) at the time scale studied (millennial), the shift from forest to savanna is abrupt and

irreversible due to the existence of tipping points, no matter the cause (natural or anthropogenic); (4)

on the contrary, the shift from savanna to palm swamps is reversible at centennial time scales; (5) some

of the reconstructed past vegetation types have no modern analogues owing to the individual species

response to environmental shifts, leading to variations in community composition; (6) extant biodiver-

sity and endemism patterns are not the result of a long history of topographical isolation, as previously

proposed but, rather, the consequence of the action of climatic and palaeogeographic variations; (7) the

projected global warming will likely exacerbate the expansion of upland savannas by favouring positive

ﬁre-climate feedbacks; (8) in the highlands, extinction by habitat loss will likely affect biodiversity but

to a less extent that prognosticated by models based only on present-day climatic features; (9) future

highland communities will likely be different to present ones due to the prevalence of individual species

responses to global warming; and (10) conservation strategies at individual species level, rather than

at community level, are enriched by long-term palaeoecological studies analyzed here. None of these

∗

Corresponding author. Tel.: +34 93 2890611.

E-mail address: [email protected] (V. Rull).

V. Rull et al. / Perspectives in Plant Ecology, Evolution and Systematics 15 (2013) 338–359 339

Contents

Introduction ...... 339

Ecological palaeoecology and the Gran Sabana ...... 339

The origin of upland savannas ...... 339

The role of ﬁre...... 341

The origin of highland biodiversity and endemism ...... 341

Aims and temporal scope ...... 341

Study area...... 342

Geology, geomorphology and soils ...... 342

Climate ...... 342

Vegetation ...... 342

Human occupancy ...... 343

Methods...... 344

Sites and general procedures ...... 344

Pollen analysis ...... 344

Charcoal analysis ...... 344

Palaeoclimatology...... 344

Long-term patterns of vegetation change ...... 345

Forest–savanna dynamics ...... 345

Savanna–morichal dynamics ...... 346

Non-analogue communities ...... 347

Elevational migration ...... 348

Community stability through time ...... 349

Discussion...... 351

Climate–vegetation equilibrium ...... 351

Irreversibility and thresholds ...... 352

Origins of biodiversity ...... 354

Global warming and biodiversity conservation ...... 355

Conclusions ...... 356

Acknowledgements ...... 356

References ...... 357

Introduction Here, we study the Guayana uplands and highlands, a very distinct

and unique biogeographical region (Berry et al., 1995; Rull, 2007b,

2010a).

Ecological palaeoecology and the Gran Sabana

Long-term ecological studies are needed to record community The origin of upland savannas

dynamics over time and to understand properly the underlying

ecological processes and environmental drivers that come into The Venezuelan Gran Sabana (GS) region, in northern South

play, and to inform conservation practices (Birks, 1993, 2008, 2013; America (Fig. 1), offers excellent opportunities for ecological

Huntley, 1996; Jackson, 2001; Willis et al., 2007, 2010; Vegas- hypothesis testing using palaeoecological records of vegetation

Vilarrúbia et al., 2011; Rull, 2010c, 2012). This type of studies, change, in relation to environmental shifts and human disturbance.

in which ecological patterns and processes, rather than palaeoen- A number of hypotheses have been proposed that are difﬁcult to

vironmental reconstruction, are the target, constitute the core of test with typical neoecological evidence encompassing annual to

so-called ecological palaeoecology (Birks, 2008, 2013; Rull, 2010c, decadal time scales. First, it should be stressed that the GS uplands

2012; Seddon, 2012). In ecology, there is no universal deﬁnition have often been considered to hold anomalous vegetation – tree-

for “long-term”, as it depends on the life cycle of the organisms less savannas and forest–savanna mosaics (Fig. 2) – as its wet

involved and their response lags to external forcing (Rull and Vegas- climate would seem to be able to support dense rainforests sim-

Vilarrúbia, 2011). In the case of vegetation, the time interval needed ilar to those of its surroundings (Huber, 1995a,c). In other words,

to study ecological dynamics often transcends the usual neoecolog- the GS vegetation may be in disequilibrium with climate. This

ical observation time scales (weeks to decades, rarely centuries), belief is not shared by others who consider that open savannas or

thus making it necessary to use palaeoecological records (Jackson, savanna–forest mosaics occur naturally in the GS uplands (Fölster

2001). This is especially true for ecological topics such as commu- and Dezzeo, 1994; Huber, 2006). It is remarkable, however, that the

nity assembly and stability over time, successional trends under ﬂoristic composition of the GS savannas is very similar to that of

changing environmental conditions, biotic responses (e.g., indi- the northernmost Orinoco lowlands (Fig. 1), situated at an eleva-

vidual versus collective, time lags, magnitude) to environmental tion ca. 500–1000 m below, under warmer, drier and more seasonal

changes, equilibrium/non-equilibrium conditions between com- climates (Huber, 1986, 2006). This phenomenon has prompted

munities and the environment, or natural versus anthropogenic several hypotheses attempting to explain the alleged anomaly. Cli-

drivers of ecological change (Rull, 2012). In such cases, palaeoeco- matic hypotheses suggest that the GS savannas are relicts of the

logical records are able to provide decisive, otherwise unavailable, last glacial maximum (LGM), when the entire Neotropics was likely

evidence to test fundamental ecological hypotheses (Willis et al., drier and covered by extensive savannas and semi-desert vegeta-

2010; Rull, 2012). In the Neotropics, recent syntheses have empha- tion (Eden, 1974). This proposal has received little palaeoecological

sized the utility of palaeoecological data for a better understanding support from both regional and local levels (Bush et al., 2004;

of savanna and forest–savanna dynamics in the Amazon and Rull, 2007a). Edaphic hypotheses contend that GS soils are unable

Orinoco lowlands (Mayle and Whitney, 2012; Berrio et al., 2012). to support forests due to their high nutrient deﬁciency and low

340 V. Rull et al. / Perspectives in Plant Ecology, Evolution and Systematics 15 (2013) 338–359

Fig. 1. Location map. (A) Leaf area index (LAI) map of northern South America showing the rainforest (dark green/grey) and savanna (light green/grey) areas (based on

Terra MODIS data, downloaded from http://earthobservatory.nasa.gov). The study area is indicated by a yellow/grey box. CB – Cariaco basin, LV – Lake Valencia, NA –

northern Andes, R – Roraima savannas, OL – Orinoco lowlands. (B) The study area considered in this paper with the selected localities (large red dots). The tepui summits

are represented as green/grey areas. Ac – Acopán, Am – Amurí, Ap – Apakará, C – Chonita, Ch – Churí, E – Encantada, Er – Eruoda, M – Mapaurí, P – El Paují, T – Toronó, U –

Urué. (For interpretation of the references to colour in this ﬁgure legend, the reader is referred to the web version of the article.)

water retention capacity; hence, savannas would be the natural soil degradation, which ends in savanna expansion (Fölster and

vegetation under these conditions. So far, there has been no con- Dezzeo, 1994; Fölster et al., 2001; Dezzeo et al., 2004a; Dezzeo

clusive evidence to either support or refute this hypothesis. Finally, and Chacón, 2005). Palaeoecological evidence supports this view

anthropogenic hypotheses advocate man-made ﬁres as the main in some localities for the last millennium (Rull, 1999), but the idea

cause of the origin and maintenance of savanna. The supporters of of extensive rainforests as the natural vegetation for the GS uplands

this proposal implicitly assume that the GS was formerly forested is still far from being well established. Therefore, the question of the

and that the forests have been progressively reduced due to fre- savannas as either a natural or anomalous vegetation type in the GS

quent burning, favouring savanna expansion. Recent short-term remains open and may constitute an excellent case study to address

ecological studies show that the GS forests, once burnt, undergo a the long-standing ecological debate on climate-community equi-

degenerative and irreversible successional process coupled with librium dynamics (Davis, 1986). Naturalness is a time-dependent

V. Rull et al. / Perspectives in Plant Ecology, Evolution and Systematics 15 (2013) 338–359 341

Fig. 2. Typical Gran Sabana landscapes. (A) The Angasima (left) and Upuigma (centre) tepuis and part of the Chimantá massif (right) are shown in the background. The

uplands are covered by savannas, with gallery forests along the rivers (in the foreground). Monane forests are dominant on the tepuian slopes. (B) Treeless savannas in the

surroundings of S. Elena, with the Roraima and Kukenán tepuis in the background (right).

Photos V. Rull.

and pervasive concept (Willis and Birks, 2006), but for the purpose diversity and endemism patterns, which are unparalleled in the

of this study we will consider as natural the ecological state of the Guayana region and elsewhere (Huber, 1995c). The origin of such

GS before human arrival. biotic patterns has been attributed to either long physical isola-

tion of the GS highlands, thus promoting allopatric speciation (Lost

World hypothesis) or recurrent connection–disconnection trends

The role of ﬁre

linked to Pleistocene glacial–interglacial cycles facilitating vicari-

ance and gene ﬂow alternation (Vertical Displacement hypothesis)

Another controversial issue is the potential consequences of

(Rull, 2004a,b,c). Preliminary palaeoecological evidence in support

the frequent burning that the GS upland communities undergo at

of the second option resulted in the proposal of a complex diversi-

present. In addition to the discussion about the former GS vege-

ﬁcation model for the origin of the high diversity and endemism of

tation, it seems evident that the savanna is currently maintained

the GS highlands (Rull, 2005a; Rull and Nogué, 2007; Nogué et al.,

and even expanded by these ﬁres (Rull, 2009b), thus preventing

2013). However, such long-term evidence comes from one single

an eventual forest recovery. As noted before, neoecological studies

site and needs further replication for a sound assessment. Second,

suggest that the GS forests have a low resilience to ﬁre practices,

the biota of these highlands has progressed without any direct

and their degradation process to savannas would be an irreversible

anthropogenic inﬂuence. Thus, natural drivers alone are respon-

threshold-crossing process triggering a positive feedback favouring

sible for the present features and their eventual past changes (Rull,

savanna expansion at the expense of forests (Rull, 1992; Vegas-

2007b, 2010a). However, despite the absence of direct human dis-

Vilarrúbia et al., 2011). Fölster and Dezzeo (1994) describe in detail

turbance, the GS highlands’ vegetation has been proposed to be

the stages of the degradative ecological sequence of GS forests after

at risk of suffering signiﬁcant diversity decline by habitat loss due

burning. This process begins with colonization by short-lived sec-

to global warming (Rull and Vegas-Vilarrúbia, 2006; Nogué et al.,

ondary forests that are progressively replaced by mixed fern-bush

2009a). The estimated biodiversity loss is based on modelling the

communities, shrubby savannas and, ﬁnally, treeless savannas. ◦

potential effect of a prognosticated increase of 2–4 C in average

According to these authors, the transition from secondary forests

temperatures (Solomon et al., 2007) and on the corresponding

to fern-bush communities would be a natural process, while the

upward migration of species, assuming that the present-day lapse

shift to savannas requires repeated burning. This process is cou-

rate and the response of species to warming will remain con-

pled with the corresponding soil degradation in terms of increasing

stant until the end of this century. Thus far, however, there has

nutrient and water stress. Therefore, this is a synergistic process in

been no empirical evidence conﬁrming this hypothesis. Palaeoe-

which anthropogenic and edaphic drivers interact. Palaeoecologi-

cology can help examining, for example, the response of the ﬂora

cal evidence is needed to assess whether these successional trends

and vegetation to eventual past climatic changes in terms of ele-

have been common through time and to evaluate the potential role

vational migration, individualistic vs. community-level responses

of changing climates as one more driver. Palaeoecological studies

and non-analogue communities, community constancy and equi-

from elsewhere have shown that species respond in an individ-

librium with climate, environmental drivers of high biodiversity

ualistic fashion to climate changes, thus determining changes in

and endemism, etc. The palaeoecological studies developed thus

community composition over time and the development of unusual

far on the GS highlands seem to point towards a relative con-

communities with no modern analogues (Williams and Jackson,

stancy in community composition during the last 6000 years and a

2007; Williams et al., 2007), a possibility that is still to be explored

prevalence of local over general patterns of vegetation change that

in the GS uplands. In addition to evident basic interest, knowing

determines a high spatial heterogeneity in community turnover,

the response of GS vegetation to climate shifts would have practi-

even at the top of the same massif (Rull, 2005b). It is also possi-

cal implications for prognosticating the potential effects of global

ble that differential site sensitivity could play a role, thus masking

warming on vegetation, soils and human activities, as well as their

potential environmental and ecological changes (Rull et al., 2011).

corresponding interactions.

An unequivocal answer to these questions has not been possible

yet.

The origin of highland biodiversity and endemism

The GS highlands, conformed by the summits of some of Aims and temporal scope

the peculiar Guayana table mountains, locally called tepuis, are

radically different in terms of ecological conditions and human The main aim of this paper is to use the published palaeoecolog-

impact. First, their vegetation is very characteristic showing unique ical studies developed in the GS uplands and highlands to test the

342 V. Rull et al. / Perspectives in Plant Ecology, Evolution and Systematics 15 (2013) 338–359

existing ecological hypotheses about their vegetation patterns and from diabases are lower in silica and richer in nutrients, thus being

the potential underlying processes. Speciﬁcally, we focus on four more capable of supporting dense forests. Shallow inceptisols are

main ecological topics: (1) potential equilibrium states between common in ﬂoodplains and on mountain slopes. Histosols derived

vegetation and climate, (2) the reversibility or irreversibility of veg- from the accumulation of organic matter are common on top of

etation changes and the occurrence of thresholds, (3) the origin of the tepuis, where they develop peat bogs and extensive peat mats

extant biodiversity and the potential drivers involved and (4) biodi- (Huber, 1995a; Zink and García, 2011).

versity conservation in the face of the ongoing global warming. The

possibility of suggesting new hypotheses more compatible with the Climate

long-term empirical evidence, to be tested with further studies, is

contemplated as well. The time interval considered encompasses Huber (1995a) classiﬁed the climates of the Venezuelan

the Lateglacial and the Holocene (the last ∼13,000 years), and Guayana into six major types, of which four are present in the

special emphasis is placed on the last few millennia, when the region under study. The submesothermic ombrophilous climate

present-day communities were shaped (Rull, 2005b; Montoya and occurs in the GS uplands (between 500 and 1200 m elev.) and is

◦

Rull, 2011). characterized by average temperatures between 18 and 24 C and

2000–3000 mm of total annual precipitation with a weak dry sea-

son (<60 mm/month) from December to March. In the southern GS,

Study area

the climate becomes submesothermic tropophilous, which is less

2 humid (1600–200 mm/year) and more seasonal, likely due to local

The GS is a region of approximately 18,000 km (of which

2 rain shadows. The GS highlands between 1500 and 2400 m eleva-

ca. 11,000 km is covered by savannas) located in southeastern

tion are under a mesothermic ombrophilous climate, with average

Venezuela between the Orinoco and Amazon basins (Huber and ◦

temperatures between 12 and 18 C and 2500–3500 mm of annual

Febres, 2000). It is part of a huge savanna island, known as the

2 precipitation, without a true dry season. Additional moisture is

Roraima savannas, with ∼68,000 km shared by Venezuela (16%),

supplied by the frequent occurrence of dense mists. Winds and

Brazil (63%) and Guyana (21%). These savannas lie within the

thunderstorms are frequent, mainly from March to November, the

dense and extensive Guayana and Amazon rainforests (Barbosa and

period of maximum precipitation. Submicrothermic ombrophilous

Campos, 2011) (Fig. 1). A general description of the main GS fea-

climates are typical on the highest tepuian summits, above 2400 m

tures is as follows, but it should be stressed that our results refer to

in elevation. There, the precipitation and mist regime are simi-

the southern sector of the uplands, usually below 1000 m elevation,

lar to the former, but the annual average temperature is lower,

as the northern part has several ecological differences and is still ◦

approximately 10 C or less. Freezing temperatures have not yet

under study. Concerning the highlands, our records come from dif-

been measured there and it has been proposed that the constantly

ferent tepui summits from the Chimantá massif, which is the better

high air moisture (Huber and García, 2011) may act as a buffer pre-

studied tepuian complex and has been considered representative

venting the air from reaching freezing point. It has been reported

of the so-called Eastern district, including all the table mountains ◦

that the general lapse rate for the whole region is −0.6 C/100 m

within and around the GS region (Huber, 1992a,b, 1995a).

elevation (Galán, 1992).

Geology, geomorphology and soils Vegetation

The GS lies on the Guayana Shield, which is characterized by The GS uplands are mostly covered by treeless savannas

an igneous-metamorphic basement formed during Archaean and (Fig. 2) dominated by grasses of the genera Axonopus and

Proterozoic times between 3.6 and 0.8 billion years ago (Mendoza, Trachypogon, accompanied by sedges such as Bulbostylis and

1977; Gibbs and Barron, 1993). The whole GS region is covered by Rhynchospora. Woody elements are rare in these savannas,

a thick sedimentary layer of Precambrian sandstone and quartzite and they are restricted to stunted plants that do not emerge

(the Roraima Group, formed between 1.4 and 2.3 billion years above the herb layer (Huber, 1995c). Most GS forests are con-

ago), spiked with intrusive rocks (mostly diabase but also gran- sidered to fall within the category of lower montane forests

ite) that penetrated this sedimentary cover during the Paleozoic because of their intermediate position between lowland and high-

and Mesozoic (Briceno˜ et al., 1990). Geomorphologically, the GS is land forests (Hernández, 1999). These forests are highly diverse

an undulated erosion surface developed on the Roraima sediments and their composition varies with elevation; common genera

that forms an altiplano slightly inclined to the south, ranging from include Virola (Myristicaceae), Protium (Burseraceae), Tabebuia

approximately 750 to 1450 m in elevation (Briceno˜ and Schubert, (Bignoniaceae), Ruizterania (Vochysiaceae), Licania (Chrysobal-

1990). This peneplain constitutes the basal level from which the anaceae), Clathrotropis (Fabaceae), Aspidosperma (Apocynaceae),

emblematic tepuis emerge, with characteristic ﬂat summits and Caraipa (Clusiaceae), Dimorphandra (Caesalpinaceae) and Byrson-

vertical cliffs (Fig. 2). These table mountains developed on the ima (Malpighiaceae) (Huber, 1986). See Hernández et al. (2012)

Roraima Group by differential erosion during the Cretaceous (145 for further details on the GS upland forests. Gallery forests are also

to 65 million years ago), after the splitting of the Gondwana common along rivers and on lake shores. The GS shrublands usually

supercontinent (Briceno˜ and Schubert, 1990). Huber (1995a) rec- occur between 800 and 1500 m elevation and are more frequent

ognized three main elevational levels on the Venezuelan Guayana, at the northern area than at the southern part (Huber, 1995b).

namely lowlands (0–500 m a.s.l.), uplands (500–1500 m) and high- They are also highly diverse, and their composition varies according

lands (1500–3000 m). Lowlands are absent in the GS, which is to soil type (rocky, sandy or ferruginous). The common elements

mainly characterized by uplands and several isolated highlands are Clusia (Clusiaceae), Humiria and Sacoglottis (Humiriaceae), Pera

(the tepuis). Soils developed on the Roraima Group are mostly (Euphorbiaceae), Emmotum (Icacinaceae), Matayba (Sapindaceae),

savanna oxisols, which are highly weathered and poor in nutrients Bonnetia (Bonnetiaceae), Phyllanthus (Euphorbiaceae), and Cyrillop-

(especially P, N and Ca), highly acidic (pH 4–5) and have very low sis (Ixonanthaceae) (Huber, 1995c). A special vegetation type called

cation exchange capacity. Fe accumulation is characteristic pro- morichales, dominated by the palm Mauritia ﬂexuosa L., develops

ducing a red upper layer with concretions and nodules. Toxic Al on wide alluvial plains associated with ﬂooded areas such as lake

accumulations are also frequent (Fölster, 1986). Soils originating shores and water courses (Fig. 3). The upper elevational boundary of

V. Rull et al. / Perspectives in Plant Ecology, Evolution and Systematics 15 (2013) 338–359 343

Fig. 3. Morichal communities from the Gran Sabana uplands dominated by Mauritia ﬂexuosa (Arecaceae). (A) Aerial view of a morichal along a water course near Wonkén.

(B) Morichal communities around Laguna Encantada. (Photos V. Rull).

the morichales is approximately 1000 m (Rull, 1998); hence, they Human occupancy

are restricted to the southernmost part of the GS. Another pecu-

liar vegetation type that grows on peaty soils and is interspersed The GS region is presently the homeland of the Pemón indige-

with treeless savannas is the broad-leaved meadows dominated by nous group, of the Carib-speaking family. Today, they are sedentary,

Stegolepis (Rapateaceae), with Xyris and Abolboda (Xyridaceae), sev- living in small villages, usually in open savannas. Although the GS

eral Cyperaceae, Nietneria (Nartheciaceae) and conspicuous tubular population density is relatively low, the indigenous settlements

rosettes of Brocchinia (Bromeliaceae). These meadows are simi- have experienced an expansion since the arrival of modern-day

lar in physiognomy and composition to some communities from European missions, and today more than 17,000 people live in GS

the tepui summits (see below), and they have been interpreted as (Medina et al., 2004). The date of arrival of the Pemón people at GS

relicts of glacial vegetation, assuming that during the Pleistocene is still unknown. Based mainly on historical documents, it has been

cold episodes, the tepuian meadows (or at least some of their com- postulated that this culture settled in GS approximately 300 years

ponents) reached the GS uplands after the downward migration of ago, coming from Guyana to the east (Thomas, 1982; Colson, 1985),

vegetation (Huber, 1995c). or approximately 500–600 years ago, migrating from Brazil, to the

The GS highlands are part of the so-called Pantepui phytogeo- south (Huber, 1995a). Recent palaeoecological studies suggest that

graphical province, which is characterized by unique biodiversity human groups with landscape management practices similar to

and endemism patterns, encompassing all the tepui summits above the Pemón people would have been present in the GS since at least

1500 m elevation (Huber, 1994b; Berry et al., 1995). For the pur- 2000 years ago (Montoya and Rull, 2011; Montoya et al., 2011c).

pose of the present paper, the Pantepui and Guayana Highlands Fire is a key component of the Pemón culture and they use it

(GH) are interchangeable, although their corresponding deﬁni- every day to burn savannas and the adjacent forests (Kingsbury,

tions are based on different criteria (biotic and physiographic, 2001). With time, the cumulative effect of these ﬁres becomes evi-

respectively) and may have slight differences. The vegetation is dent in vast burnt areas that display different successional stages

characterized by a mosaic of bare rock, pioneer vegetation, tepuian of re-colonization by savannas. In addition to the slow and con-

forests, herbaceous formations and shrublands (Huber, 1995c). Pio- tinuous savanna expansion due to the edge effect of ﬁres on the

neer communities are composed mainly of algae (Stigonema) and forest–savanna ecotone, accidental uncontrolled ﬁres burning huge

lichens (Cladonia, Cladina, Siphula) growing directly on rocks. The forest areas have also been observed on occasion (Fölster, 1986).

forests are mostly situated along rivers and are dominated by The reasons for the extent and frequency of these ﬁres include

Bonnetia roraimae Oliv. (Fig. 4), accompanied by Schefﬂera (Arali- activities such as cooking, hunting, ﬁre prevention, communication

aceae), Spathelia (Rutaceae), Stenopadus (Asteraceae) and Malanea and magic, among others (Rodríguez, 2007). Surprisingly, land-use

(Rubiaceae). The forests on the diabase intrusions are similar, practices such as extensive agriculture or cattle raising, typical of

but they are dominated by Stenopadus and Spathelia instead of other cultures strongly linked to ﬁre, are not characteristic of the

Bonnetia. Among the herbaceous communities, grasslands and Pemón culture (Rodríguez, 2004a). The large number of ﬁres today

meadows are more important. Grasslands are restricted to ﬂooded in the GS uplands (∼10,000 each year; Huber, 1995d) are essen-

plains on the centre of the massif and are characterized by tially human-made, which has resulted in a debate related to the

grasses (Cortaderia, Aulonemia), and sedges (Cladium, Rhycocla- sustainability of the present landscape and the possible factors that

dium, Rhyncospora). The meadows are broad-leaved communities led to its development (Rodríguez, 2004b; Dezzeo et al., 2004b;

dominated by Stegolepis ligulata Maguire (Rapateaceae) (Fig. 4), Rull, 2009a). It is estimated that most of the GS areas are burned

which is endemic to the Chimantá, accompanied by Xyris, Ever- every 1–3 years (Hernández and Fölster, 1994).

ardia and Lagenocarpus (Cyperaceae), Lindmania and Brocchinia In contrast, the GS highlands remain virtually pristine (Rull,

(Bromeliaceae), Heliamphora (Sarraceniaceae), and Syngonanthus 2007b, 2010a). The Pemón people do not visit the tepui summits,

(Eriocaulaceae). Shrubs occur as small clusters or as isolated as they consider the tepuis the home of gods or the remains of

individuals. Shrublands are the more developed and diverse com- their tree of life, and are thus sacred lands forbidden to humans

munities of the Chimantá. The paramoid shrublands (Fig. 5) are (Gorzula and Huber, 1992). In addition, the tepui summits are

exclusive to this massif and are dominated by species of Chiman- remote and nearly inaccessible, as only a few can be reached by foot

taea (Asteraceae), a genus endemic to the Chimantá and other after several days of walking and climbing. Since the ﬁrst known

neighbouring tepuis. The herbaceous stratum is dominated by the expedition in 1884, most visits have been for scientiﬁc reasons, as

bambusoid Myriocladus (Poaceae) and several Xyridaceae, Cyper- attempts to ﬁnd any economic proﬁt have failed. No exploitable

aceae and Eriocaulaceae, as well as Lindmannia, Everardia and mineral resources have been found, the soils are unsuitable for

Heliamphora. agriculture, and there are no grasslands suitable for cattle raising

344 V. Rull et al. / Perspectives in Plant Ecology, Evolution and Systematics 15 (2013) 338–359

Fig. 4. Tepuian plants. (A) Stegolepis ligulata (Rapateaceae) from the Apakará summit. (B) Bonnetia roraimae (Theaceae) from the Eruoda summit.

Photos V. Rull.

(Gorzula and Huber, 1992). Scientiﬁc expeditions ceased in recent Palynological interpretations of past records largely rely on the

decades due to ofﬁcial protection, but tourism increased. How- use of modern analogues, that is, present-day pollen and spore

ever, tourism is restricted to sporadic activities, and there is no sedimentation in relation to vegetation patterns. In the case of non-

permanent establishment or structure on top of the tepuis. Since analogue communities, individual autoecological features of the

1962, several conservation measures have been implemented to species involved are considered (Marchant et al., 2002). Modern

protect the tepuis, including the creation of national parks, natural pollen analogue studies are available for both GS uplands and high-

monuments, and biosphere reserves (Huber, 1995d). lands, and although not extensive, they have proved to be suitable

for vegetation reconstruction (Rull, 1991). In the uplands, certain

Methods key palynological parameters were found to be useful for differen-

tiating four main vegetation types: treeless savannas, morichales,

mixed forests and gallery forests. In the highlands, modern pollen

Sites and general procedures

studies allow the differentiation of forests, shrublands and mead-

ows (Rull, 1999, 2005b).

The locations used in this study are from the southernmost

part of the GS uplands and the Chimantá massif, being repre-

sentative of the highlands, which are the best-studied areas Charcoal analysis

palaeoecologically. Upland localities include one lake (Chonita)

and four bogs (Mapaurí, Urué, Encantada and El Paují), whereas Microscopic charcoal particles are traditionally used in palaeoe-

the highland sites contain six bogs (Eruoda, Toronó, Churí, Acopán, cology as proxies for ﬁre frequency and intensity (Whitlock et al.,

Amurí and Apakará) on the Chimantá massif (Fig. 1). The original 2010). As in pollen analysis, modern analogue studies are needed

palynological results have been previously published by Rull to calibrate properly particle records against ﬁre incidence (Dufﬁn

(1991, 1992, 1999, 2007a, 2009a), Rull et al. (2011), Montoya et al. et al., 2008). In the GS region, some of these studies are available

(2009, 2011a,b,c) and Nogué et al. (2009b). Here, we analyze these showing that smaller charcoal particles are proxies for regional

data in a synthetic fashion. Vegetation dynamics is inferred from ﬁres, whereas larger ones better relate to local burning events, with

␮

pollen analysis while microcharcoal is used as a proxy for ﬁre the boundary at 100–150 m (Rull, 1999, 2009a; Leal, 2010). Total

−3 −1

incidence (Birks and Birks, 1980). The inferred vegetation changes charcoal concentration (particles cm or particles g ) or inﬂux

−2 −1

through time are then compared with known global and regional (particles cm year ) are used here as indicators of general ﬁre

palaeoclimatic trends to assess the corresponding biotic responses incidence.

to these environmental shifts. Palaeoclimatology

Pollen analysis

Palaeoclimatic trends are derived from independent evidence to

Pollen analysis has been a preferred tool for vegetation avoid circular reasoning when addressing the vegetation response

reconstruction since about a century ago (Birks & Birks, 1980). to environmental shifts. Long-term temperature trends are derived

Fig. 5. Paramoid shrublands from Apakará-tepui (Chimantá massif) dominated by Chimantaea mirabilis Maguire, Steyerm. & Wurdack (Asteraceae). (A) General view. The

term “paramoid” refers to the physiognomic similarity of these shrublands with the Andean páramo biome, situated above the treeline and dominated by species of another

Asteraceae (Espeletia). (B) Closer view of Ch. mirabilis.

Photos V. Rull.

V. Rull et al. / Perspectives in Plant Ecology, Evolution and Systematics 15 (2013) 338–359 345

Fig. 6. Lateglacial and Holocene vegetation changes recorded in the GS uplands compared with the climatic trends the oxygen isotope records from Greenland ice cores

(GISP2) and the titanium record from Cariaco marine cores (ODP-1002). The main climatic trends are highlighted by grey bands: YD – Younger Dryas, EHW – Early Holocene

Warming, HTM – Holocene Thermal Maximum, ENSO–Increased ENSO variability, MWP – Medieval Warm Period, LIA – Little Ice Age (Haug et al., 2001). Raw data downloaded

from the World Data Center for Paleoclimatology at http://www.ncdc.noaa.gov/paleo. Vegetation changes are represented as summary pollen diagrams grouped according to

−3 −2 −1

the main GS vegetation types. Charcoal concentration (particles cm ) or inﬂux (particles cm y ) are also indicated as proxies for ﬁre incidence. Bs – Bonyunia shrublands,

Mf – “Moraceae forests”, Mch – Morichales.

Raw data from Rull (1999, 2007a, 2009a), Montoya and Rull (2011) and Montoya et al. (2009, 2011a,b,c).

from global palaeotemperature reconstructions from Greenland ice However, a dramatic increase in the smaller charcoal fraction, as a

cores (GISP2), whereas regional (northern South America) palaeo- proxy for regional ﬁres, during the replacement of Mapaurí forests

precipitation trends are derived from the Cariaco record (Haug by savannas suggested that ﬁre would have played a signiﬁcant role

et al., 2001) (Fig. 6). in the landscape shift. The lack of evidence for human presence in

the GS during the early Holocene hinders attributing these ﬁres to

Long-term patterns of vegetation change human activities, and the question remains open.

The “Moraceae rainforests” were recorded at the El Paují,

Forest–savanna dynamics Encantada and Chonita sites. It should be stated that forests

dominated by species of this family have not been described in

Four main types of forests have been identiﬁed in the fos- the GS (Hernández, 1999), but their pollen record is common in

sil pollen records from the GS uplands since the Lateglacial the region, especially during the Holocene (Rull, 1991). A similar

to the present: (1) cloud forests dominated by Catostemma situation was found in other neotropical rainforests of the Amazon

(Bombacaceae) with Acalypha (Euphorbiaceae), Melastomataceae basin, where this pollen is largely dominant in the modern forest

and Ericaceae; (2) rainforests dominated by Urticales (mostly assemblages, but Moraceae species, although present, are not

Moraceae) with Alchornea (Euphorbiaceae); (3) semi-deciduous among the major forest elements (Gosling et al., 2009). Therefore,

forests dominated by Fabaceae; and (4) and open secondary forests the name “Moraceae rainforests” refers only to palynological traits.

of Caraipa (Clusiaceae), Sloanea (Elaeocarpaceae), Pagamea (Rubia- These rainforests dominate the El Paují area during most of the

ceae), ferns and grasses. Holocene (between approximately 8300 and 2700 cal yr BP), with

The Catostemma forests were documented in Mapaurí (Fig. 1), a maximum in the 7700–5000 cal yr BP interval (Montoya et al.,

at a 950 m elevation, around the Pleistocene–Holocene boundary 2011b), when the pollen percentage of forest trees was at or above

(11,700 cal y BP). At present, these mesothermic forests, domi- 40% of the pollen sum, the boundary for in situ dense rainforest

nated by Catostemma durifolius W.S. Alverson, grow above 1400 m occurrence according to the available modern analogue studies

elevation in the montane belt of the adjacent tepuian slopes from Guayana and Amazonia (Rull, 1999; Gosling et al., 2009). This

(Alverson, 1994; Hernández, 1999). The Catostemma forests com- forest maximum coincided with the Holocene Thermal Maximum

pletely disappeared from Mapaurí in the early Holocene (Fig. 6) (HTM) that was characterized by increased precipitation at a

when they were replaced by treeless savannas, which dominated regional level due to the latitudinal migration of the Intertropical

throughout the entire Holocene (Rull, 2007a, 2009a). This vegeta- Convergence Zone (ITCZ) (Haug et al., 2001). During this phase,

tion turnover was used to propose a warming trend linked to the charcoal values were intermediate, suggesting continuous but

global Early Holocene Warming (EHW). Similar temperature trends low-level human disturbance. This, together with the consistent

were inferred by Bush et al. (2004) in the Amazon basin, a few hun- occurrence of Cecropia (Moraceae), a typical secondary colonizer

dred kilometres south of the GS. A decrease in P/E was dismissed, of burnt rainforest areas (Marchant et al., 2002), in moderate

as regional moisture proxies from the Cariaco record suggested values suggested the occurrence of shifting agriculture practices

a trend to wetter climates during the EHW (Haug et al., 2001). based on the clearing of small forest spots (conucos). This type

346 V. Rull et al. / Perspectives in Plant Ecology, Evolution and Systematics 15 (2013) 338–359

of forest exploitation is currently common in the region and the results provide some support to the above-mentioned hypothe-

adjacent Amazon areas. The “Moraceae rainforests” of El Paují sis of Fölster and Dezzeo (1994), according to which the transition

experienced a remarkable decline between ca. 5000 and 2700 cal from secondary forests to fern-bush communities would be a nat-

yr BP leading to savanna expansion. The regional decrease in ural process while the shift to savannas requires repeated burning.

precipitation experienced since ca. 5400 cal yr BP (Haug et al., Treeless savannas were fully established in the site by 680 cal

2001), together with the increase in El Paují charcoal record points yr BP and persisted even after a signiﬁcant decline of ﬁres. The

towards a synergistic coupling between climatic dryness, which establishment of treeless savannas occurred under a signiﬁcant

contributed to enhanced vegetation ﬂammability, and an increase intensiﬁcation of burning practices, enough to cause forest retreat

in the frequency and/or intensity of anthropogenic burning prac- in spite of a regional increase in precipitation occurring during the

tices (Montoya et al., 2011b). The “Moraceae rainforests” at the so-called Medieval Warm Period (MWP) (Haug et al., 2001).

Encantada site were also widespread between 7500 and 2500 cal In the Colombian Orinoco lowlands, the Lateglacial and

yr BP (Montoya et al., 2009). In this case, the lower percentages Holocene forest–savanna dynamics are believed to have been con-

of pollen from forest trees indicated that forests were not in situ trolled mostly by the centennial- to millennial-scale migration

but close to the site, likely around the Encantada lake as gallery of the ITCZ, which would have mastered variability in precipita-

forests. A decline in the abundance of these forests was recorded tion patterns thus creating the complex pattern of gallery forests

between about 4000 and 2500 cal yr BP, coinciding with a phase of and savannas observed currently. For example, open savannas

regional precipitation decrease, likely due to increased El Nino-like˜ would have been more widespread during the LGM, likely due

conditions (Haug et al., 2001). Between 2500 and 1200 cal yr BP, to drier conditions, whereas during the Holocene the incom-

these forests were signiﬁcantly reduced for the beneﬁt of treeless ing of wetter climates would have led to forest expansion. It

savannas, thus determining the establishment of open savanna has been proposed that human disturbance would have affected

landscapes. Neither charcoal nor moisture indicators experienced the forest–savanna ecotone dynamics since the early Holocene

any signiﬁcant change during this interval; hence, the attribution (Behling and Hooghiemstra, 1998, 1999, 2000, 2001; Berrio et al.,

of this vegetation shift to either climatic or human causes would 2012). In the lowland savannas of southern Amazonia (Bolivia and

be speculative, so far. The situation at Chonita lake is very similar Brazil), this dynamic seems to have also been affected by both cli-

to that at Encantada, but the record encompasses only the last mate and humans at different time scales. Indeed, regional-scale

∼

3600 years and the rainforests were replaced by morichales; forest–savanna shifts are likely climate-driven, whereas local/ﬁner

therefore, this sequence will be described in the following section. spatial scale shifts may well have been human-driven (Mayle, 2004;

Semi-deciduous forests dominated by Fabaceae genera (Cen- Mayle and Whitney, 2012; Mayle et al., 2000, 2007). The climate

trolobium and others) were only recorded at El Paují between ca. during the LGM was assumed to be too cold and too dry for tropical

2700 and 1400 cal yr BP (Montoya et al., 2011b). These forests rainforests, and the region was covered by treeless grasslands. At

established after a transitional phase (ca. 5000–2700 cal yr BP), are the onset of the Holocene, warmer and wetter climatic conditions

characterized by rainforest clearing and savanna expansion. These would have led to major ﬂooding, thus favouring changing patterns

forests replaced the former rainforests, which experienced a signif- of wetland savannas and ﬂoodplain forests. At present, most of

icant reduction. Open savannas were also greatly reduced during these sites are covered by a forest–savanna mosaic and seasonally

this phase. Both charcoal and moisture indicators also experienced dry tropical forests. Humans have also affected vegetation dynam-

signiﬁcant declines, which were interpreted in terms of drier cli- ics, but the extent to which they did so remains unknown (Mayle

mates and low or absent human disturbance. Centrolobium is a and Whitney, 2012). Major vegetation changes have been asso-

genus of deciduous trees typical of the dry seasonal semideciduous ciated with late-Holocene ﬁres ignited by humans (Urrego et al.,

forests of lowland Amazonia (Toniato and de Oliveira-Filho, 2004; 2013), coinciding with the situation reported by the GS uplands

Ortuno˜ et al., 2011). Centrolobium species are able to regenerate (Montoya and Rull, 2011).

from the roots (Hayashi and Appezzato-da-Glória, 2009), becoming

one of the more important invaders of the earlier phases of sec- Savanna–morichal dynamics

ondary forest regeneration after the abandonment of intense land

use and/or after ﬁre (Gould et al., 2002; Park et al., 2005; Bertoncini The morichales currently growing on some of the study sites

and Rodrigues, 2008). Therefore, the most likely interpretation (Chonita, Encantada, Urué) were established during the last ∼2000

at El Paují is the rapid invasion of the site by Centrolobium- years (Montoya and Rull, 2011). The absence of these communities

dominated semi-deciduous forests after the sudden cessation of in Mapaurí and El Paují is due to unknown causes. The morichales

ﬁres at approximately 2700 cal yr BP (Montoya et al., 2011b). These are restricted to the southern GS region, as they have an upper

forests disappeared and were replaced by open savannas at approx- limit at approximately 1000 m elevation (Rull, 1998) that prevents

imately 1400 cal yr BP, coinciding with a signiﬁcant increase in them from reaching the northernmost areas and the tepui sum-

charcoal suggesting that forest burning could have been decisive. mits. However both Mapaurí (950 m) and El Paují (940 m) are at

The synergistic action of drier climates, likely favouring vegeta- similar elevations to the other localities; hence, the absence of

tion ﬂammability, and ﬁres could have lead to positive feedbacks morichales could be related to dispersal and/or biogeographical

between them thus magnifying savanna expansion. features (Montoya and Rull, 2011). In the GS, the morichales com-

Open secondary forests with Caraipa, Sloanea, Pagamea, ferns monly occur as gallery forest stands on ﬂooded soils along water

and grasses were documented at Urué between >1500 and ca. courses and lake shores within open grasslands and are thus typical

1200 cal yr BP, likely as a result of the burning of a former rain- elements of the savanna landscape.

forest community on the site (Rull, 1999). Charcoal values were In the Chonita lake sediments, the occurrence of morichal com-

oscillating during this time, showing a local maximum at approxi- munities was recorded from ca. 2200 cal yr BP to the present

mately 1400 cal yr BP. After a charcoal minimum (ca. 1300 cal yr BP), (Montoya et al., 2011c) (Fig. 6). During the former phase studied

the vegetation shifted to a mixed community of ferns (Sticherus) (ca. 3600–2200 cal yr BP), the region around the lake was cov-

and bushes (Ilex) that persisted until approximately 1050 cal yr BP. ered by a mosaic of treeless savannas and Moraceae gallery forests.

This period was characterized by continuous and intensive burn- This occurred during the already mentioned precipitation minima

ing resulting in the establishment of savannas at approximately linked to increased ENSO activity. The incoming of morichal com-

900 cal yr BP, after a transitional phase of ca. 100 years. These munities at 2200 cal yr BP was sudden and coeval with a signiﬁcant

V. Rull et al. / Perspectives in Plant Ecology, Evolution and Systematics 15 (2013) 338–359 347

Fig. 7. Contrasting consequences of ﬁres on Gran Sabana forests and morichales. (A) Morichal community in the vicinity of S. Elena, showing that ﬁres affect only the

herbaceous layer. (B) Aerial view of a gallery forest near Wonkén, showing the retreat experienced by this community under recurrent burning. The isolated “trees” inside

the burnt patches are Mauritia palms.

Photos V. Rull.

increase of ﬁres, which would have caused the observed rainfor- region (Meneses et al., 2012), with human activities as relevant

est retreat. The persistence of Mauritia and its communities under drivers of change. The establishment of morichales in the Orinoco

frequent fires may be explained by the difficulty of fires reach- lowlands began earlier (∼4000 cal yr BP) than in the GS (∼2000 cal

ing ﬂooded areas or by selective burning (Vegas-Vilarrúbia et al., yr BP), and their expansion is attributed to human cultivation

2011), given that Mauritia provides abundant and varied services (Berrio et al., 2012). Unfortunately, no charcoal analyses exist for

to the indigenous communities (Henderson et al., 1995; Gomez- most of these records. In the Roraima region, Mauritia communities

Beloz, 2002; Heckenberger and Neves, 2009). Savanna ﬁres used have been present during the last 1500 cal yr BP and their expansion

to be short-lived and superﬁcial affecting only herbaceous plants is explained in terms of wetter climates and human disturbance

among the Mauritia palms, which remain unaltered, whereas forest (Meneses et al., 2012).

ﬁres effectively reduce the forested areas (Fig. 7). The prevalence of

ﬁres, rather than climatic shifts, as drivers for morichal expansion Non-analogue communities

at the expense of forests is supported by the continuous increase of

these palm communities, even in the presence of signiﬁcant pre- The more striking record of past GS communities with no

cipitation increases and decreases during the MWP and the Little modern analogues is from the Lateglacial and involves upland

Ice Age (LIA), respectively. The establishment of morichales around shrublands. At present, four main types of upland shrublands have

the Encantada site was a more gradual process that took place via been distinguished depending on soil features: (1) shrublands on

a transitional phase between approximately 2500 and 1200 cal yr sandstone outcrops, (2) shrublands growing on isolated patches of

BP (Montoya et al., 2009). No evident signals of moisture or local sandy soils, (3) shrublands on ferruginous soils and 4) shrublands

burning shifts were recorded during this interval. However, a sud- developing on peaty soils (Huber, 1994a, 1995b). A different type of

den increase in Mauritia at ca. 1200 cal yr BP followed a similarly shrubland was documented in the Chonita lake sediments during

abrupt increase of ﬁre incidence shortly after, during a phase of the Lateglacial (ca. 12,700–11,700 cal yr BP) (Montoya et al., 2011a),

drier climates prior to the MWP, indicated the establishment of coinciding with the warming trend at the end of the Younger Dryas

morichal communities around the bog. As in the case of Chonita, (YD) (Rull et al., 2010; Stansell et al., 2010). This shrubland commu-

the persistence of these morichales under subsequent wetter and nity, characterized mainly by Bonyunia (Loganiaceae) shared some

drier conditions supports the hypotheses of increased and selective similarities with the present-day shrublands on ferruginous, rocky

burning. and sandy soils, but they did not belong to any of these types or

In Urué, the morichales were already in place at the beginning others known so far (Fig. 8). This shrubland developed under drier

of the studied interval (>1500 cal yr BP). In this case, the morichales climates and it persisted for ca. 1000 years, until the onset of the

were not preceded by treeless savannas but by fern-bush com- first fires documented in the GS that are among the older fires doc-

munities resulting from the secondary colonization of burnt areas umented in the Neotropics (Montoya et al., 2011a) (Fig. 1). The shift

(Rull, 1999). Once established, the morichales persisted until today to treeless savannas occurred exactly at the YD/Holocene boundary

but their abundance decreased twice in favour of savanna expan- and was abrupt, thus suggesting a threshold-crossing replacement.

sion, during the MWP (ca. 950–800 cal yr BP; AD 1000–1150) and This vegetation switch was irreversible, as the described non-

the LIA (ca. 500–100 cal yr BP; AD 1450–1850), respectively. The analogue shrubland community did not reappear again during the

MWP savanna expansion also occurred in Encantada, coinciding Holocene and is still absent (Montoya et al., 2011b). The Fabaceae-

with a regional precipitation increase, which could seem contra- dominated semi-deciduous forests recorded in El Paují between ca.

dictory. However, a coeval conspicuous charcoal peak suggests 2700 and 1400 cal yr BP (Fig. 6) may be also considered past com-

that increased burning activities could have been more decisive munities with no modern analogues as they do not occur at present

for Mauritia retreat and savanna expansion. In this case, selec- in the GS uplands. Similar but not identical forest communities

tive burning favouring Mauritia persistence was not observed. The are presently common in the so called “dry diagonal” of Season-

LIA savanna–morichal shift also coincided with the same trend ally Dry Tropical Forests (SDTF) extending from southwestern to

in Encantada but this time during a drier climatic oscillation, northwestern Brazil (Bullock et al., 1995).

which likely favoured vegetation ﬂammability leading to a positive Other examples include mid-Holocene shrublands recorded in

climate-ﬁre feedback. peat bogs from the highlands. As it occurs today, these Holocene

Similar trends in savanna–morichal dynamics have been doc- communities were dominated by Chimantaea (Asteraceae), a genus

umented in the Colombian Orinoco lowlands (Berrio et al., 2000, endemic to the Chimantá massif and a few more nearby tepuis, but

2002a,b) and are beginning to be evident in the Brazilian Roraima they show a different taxonomic composition. For example, today’s

348 V. Rull et al. / Perspectives in Plant Ecology, Evolution and Systematics 15 (2013) 338–359

A) Chonita (uplands) established just after the HTM, suggests climatic stress (dryness

and/or lower temperatures) that may have prevented the growth of

a number of species currently present in these communities. After

Axis

the ENSO intensiﬁcation occurred between ca. 3800 and 2800 cal y

5.0

BP, characterized by precipitation minima, the impoverished Chi-

mantaea shrublands were replaced by Stegolepis meadows, which

Peat persisted until the warm and wet MWP oscillation, when the

present-day Chimantaea–Stegolepis shrubby meadows established.

The whole picture suggests that taxa from the Chimantaea shrub-

2.5 lands responded individualistically to climatic forcings and that

these communities, although persistent, experienced signiﬁcant

changes in taxonomic composition through time. Chonita

YD Elevational migration

-2.5 Rock 2.5

Upward and downward migration shifts have also been

Axis 1

Sand recorded in both GS uplands and highlands. In the uplands, the

Fe more conspicuous case involves Catostemma (Bombacaceae). As

noted before, this genus is represented in the study area by C.

durifolius, a tree that dominates the cloud forests from the tepuian

-2.5 slopes above 1400 m elevation, together with Pouteria (Sapotaceae)

and Calyptranthes (Myrtaceae) (Hernández, 1999). The high domi-

nance of Catostemma pollen in the Mapaurí bog (950 m elevation)

B) Churí (highlands)

before the Pleistocene/Holocene boundary suggested that, by that

time, the lower distribution boundary of Catostemma was at least s

ACEAE

450 m below the present (Fig. 9). Similar results were obtained by

Chimantaea Xyris ERICACEAEStegolepi POACEAECyrillaCYPERACEAESAPOTBrocchiniaIle Bush et al. (2004) in a nearby area from northern Brazil, where

LIA Podocarpus, another montane element, was approximately 1000 m Chim sh + Steg

1 MWP below its present lower boundary by the LGM, when the average

◦

other temperatures were estimated to be ca. 5–6 C lower than today in

2 Stegolepis the neotropical lowlands (Farrera et al., 1999; Bush et al., 2001).

meadows

The general warming trend occurring since the LGM to the early

3 Holocene would have been responsible for the upward migration

ENSO

of Podocarpus and Catostemma until their present-day elevational

4 settings, which would explain their total disappearance from the

Chimantaea

shrublands lowlands by the early Holocene.

cal y BP (x1000)

5 In the highlands, the more relevant cases are those of Myrica

(Myricaceae) and Stegolepis (Rapateaceae), both in the Chimantá

massif. Myrica rotundata Steyerm. & Maguire is the only species

HTM of this genus (and of the family) reported for the ﬂora of the

Venezuelan Guayana, according to which these evergreen shrubs

020 02040 0 020 020 0 0 0 0 0 050 % or small trees occur in mixed Bonnetia forests between 1900 and

2200 m (Miller, 2001). This species was not found in a locality

shrublands meadows

at the Apakará summit situated around the uppermost distribu-

Fig. 8. Examples of past communities with no modern analogues in the GS uplands tion boundary of M. rotundata. The vegetation was dominated by

and highlands. (A) Correspondence analysis biplot of taxa (black dots) from present

paramoid shrublands of Chimantaea humilis Maguire, Steyerm. &

day GS shrublands growing on peaty (Peat), rocky (Rock), sandy (Sand) and ferrugi-

Wurdack (Fig. 5), herbaceous stands with Stegolepis (Rapateaceae),

nous (Fe) soils compared with those living on the same site during the Younger Dryas

and gallery forests. Sandstone outcrops were colonized by a vari-

(Chonita YD), which disappeared in the Holocene (Fig. 6). Redrawn from Montoya

et al. (2011a). (B) Simpliﬁed pollen diagram showing the Holocene shifts in the com- ety of shrubs. However, the vegetation was completely different

ponents of Chimantaea shrublands (black) and Stegolepis meadows (grey). Acronyms between ca. 8000 and 5300 cal yr BP, with Myrica the main ligneous

for climatic trends and events as in Fig. 6.

element, followed by Ilex (Aquifoliaceae) and Cyrilla. Chimantaea

Redrawn from Rull (2004a).

and grasses were less abundant than today and Cyperaceae were

remarkably scarcer (Rull et al., 2011). This phase was coeval with

Chimantaea humilis Maguire, Steyerm. & Wurdack shrublands on the warm and wet HTM, suggesting that the upper distribu-

top of the Churí-tepui (Chimantá massif) would be classiﬁed as tion limit of Myrica was displaced upward at that time (Fig. 9).

shrubby meadows due to the prevalence of herbaceous taxa such The incoming of cooler and drier climates after the HTM may

as Brocchinia (Bromeliaceae) and Stegolepis (Rapateaceae) (Huber, have caused the downward migration of Myrica to its present-

1992b). However, the Churí Chimantaea shrublands were radically day setting. This example also shows that upward and downward

different between approximately 5400 and 3500 cal yr BP (Fig. 8). migrations did not involve the whole community but some of their

Indeed, they were remarkably less diverse, and Brocchinia and Ste- components, thus reinforcing the view that biotic responses to cli-

golepis were absent (Rull, 2004a,b), which suggest the presence of matic forcing are mostly individualistic at the species level.

a low-diversity and almost pure Chimantaea shrubland with a poor Stegolepis ligulata (Rapateaceae) is endemic to the Chimantá

herbaceous layer. The absence of independent proxies for tem- massif and the absolute dominant of its meadows until approx-

perature and moisture precludes interpretation in climatic terms. imately 2300 m, where they have their uppermost distribution

However, the fact that the impoverished Chimantaea communities boundary. The species may occur slightly above this boundary but

V. Rull et al. / Perspectives in Plant Ecology, Evolution and Systematics 15 (2013) 338–359 349

Catostemma Myrica Stegolepis phases of blanket mire formation (Zink, 2011) (Fig. 11). The site is

(lower: 1400 m) (upper: 2200 m) (upper: 2300 m)

on one of these vegetation patches and holds a bog dominated by

Brocchinia (Bromeliaceae) and Orectanthe (Xyridaceae). Bonnetia

LIA

forests and Chimantaea shrublands grew in the vicinity, whereas

1 MWP Stegolepis-dominated meadows were absent as the site is located

400–500 m above their upper distribution boundary. The same

vegetation type, with only minor and irrelevant differences, occu-

pied the locality from ca. 4300 cal years BP onward (Nogué et al.,

2009b). The alternation of post-HTM wet and dry regional climatic

3 oscillations (ENSO intensiﬁcation, MWP, LIA) did not affect the

ENSO

vegetation trends. Charcoal particles below 100 ␮m were present

in small amounts, with a peak at approximately 3900 cal yr BP.

The small size and the common grass cell morphology of most of

these particles, together with the absence of changes in the local

5 vegetation, led to the conclusion that charcoal was transported by

winds from the GS uplands. This mid-late Holocene record lies on

6 a thin layer of older Lateglacial-early Holocene (12,700–8500 cal

yr BP) peat that overlies the basal rock, indicating that peat

accumulation was interrupted between approximately 8500 and

cal y BP (x1000) 7

4300 cal yr BP. This interval falls within the HTM, as recorded at

the Apakará summit (Rull et al., 2011) and it corresponds to the

0 10 20 30 %

8 HTM period of maximum rainfall in northern South America (Haug et al.,

0 10 20 % 2001). In environments prone to peat formation, as for example

CHURÍ

the Guayana Highlands, it is commonly assumed that interrup-

9 APAKARÁ (2250 m)

(2170 m) tions in peat accumulation are due to insufﬁcient organic matter

production and/or oxidation under arid climates (Schubert and

10 Fritz, 1985; Schubert et al., 1986; Zink, 2011). In the case of Eruoda,

however, this view is in conﬂict with palaeoclimatic interpreta-

tions and the abundant evidence for early-mid Holocene peats on

11 EHW

top of the tepuis (Schubert and Fritz, 1985; Schubert et al., 1986;

Rull, 1991, 1996, 2005b,c). Alternatively, it has been proposed that

older peat layers would have been progressively washed out by

0 10 20 30 40%

subsurﬁcial water currents ﬂowing along the rock-peat contact

MAPAURÍ (Rull, 1991; Rull et al., 1988). These waters ultimately ﬂow out of

(950 m)

the tepuis and originate the GS rivers, most of which are typically

blackwater rivers (Fig. 11) due to their high organic matter content

Fig. 9. Pollen diagram of taxa which appearance (Stegolepis) and disappearance

in the form of humic substances. It is likely that a high proportion

(Catostemma and Myrica) suggest elevational migration. Arrows indicate the direc-

of this organic matter comes from peat washing on top of the

tion of migration (upward or downward). The elevation of each locality and the

upper distribution limit for each parent plant is also indicated. Acronyms for climatic tepuis, as it is known that vegetation inﬂuences the type of humic

trends and events as in Fig. 6.

material released to rivers (Vegas-Vilarrúbia et al., 1988). Another

Raw data from Rull (2004a, 2007a, 2009a) and Rull et al. (2011).

possibility is peat sliding, a phenomenon that has been observed

in some tepuian blanket peats (Zink et al., 2011). During excep-

only in small and scattered stands (Huber, 1992b). The Churí local- tionally rainy phases, the combination of water oversaturation of

ity analyzed above lies near the Stegolepis upper limit and, as stated peat by heavy rainfall, fragmentation by small creeks and shear

before, its vegetation is dominated by Chimantaea shrublands with failure at the rock-peat contact by subsurﬁcial waters led to peat

the massive presence of Stegolepis (Huber, 1992b). It has also been detachment and removal (Zink, 2011; Zink and García, 2011). Such

shown that this was not the case before 3500 cal yr BP, when Ste- peat fragments sediment at lower elevations causing apparent

golepis was very scarce or absent (Fig. 9) and the shrubland was age inconsistencies in their sediments, a feature also observed on

remarkably less diverse, likely due to cooler and drier climates fol- some tepuis (Zink et al., 2011). In summary, peat removal may also

lowing the HTM. The absence of Stegolepis was restricted to this occur during phases of exacerbated precipitation, which would

post-HTM phase (ca. 5400–3500 cal years BP) and was present both explain the absence of peat at Eruoda during the HTM maximum.

before and after, suggesting that it migrated downwards after the The other localities exhibiting community constancy (Acopán,

HTM and that its reappearance at approximately 3500 cal yr BP was Amurí and Toronó) lie at intermediate levels within the tepuian

due to subsequent upward migration fostered by more favourable meadows dominated by Stegolepis (Rapateaceae). These meadows

climatic conditions. have remained present and constant in composition over the whole

recorded period, which goes back to ca. 6500 cal yr BP in Amurí

Community stability through time (Fig. 12). The only exceptions have been short phases of Bonnetia

(Bonnetiaceae) increases interpreted as small expansions of gallery

Several palaeoecological records from the highlands display a forests dominated by this tree. However, the asynchronous char-

remarkable constancy in taxonomic composition over time. In the acter of such expansions and the lack of chronological correlation

Eruoda summit, the constancy extends back to the middle Holocene with known climatic shifts pointed to local community reorganiza-

(Fig. 10). The studied site was situated on the highest summits of tions, rather than expressions of general environmental shifts (Rull,

the Chimantá massif (2630 m elevation), which are characterized 2005b).

by mostly bare rock and small vegetation patches on rock cavities It has been argued that the high levels of moisture on top of the

that are prone to water and peat accumulation, similar to the initial tepuis, i.e. high precipitation, no dry season, frequent mists and

350 V. Rull et al. / Perspectives in Plant Ecology, Evolution and Systematics 15 (2013) 338–359

0 100%

ACEAE AT a a s OM a a AE -t ALACEAE AT a inmanni YGALACEAE ALMAE irola x APILIONACEAE ARALIACEAEBonnetiaP PodocarpusV CaseariaChimantaeaCyrilla ERICACEAEGUTTIFERAEIle MELASTMyricaMYRTACEAEMYRSINACEAEOCHNACEAEHypericumURTICALESWe HedyosmumBrochiniDroserERIOCAULACEAEHeliamphorLILIACEAEPOACEAEPOL SANTXyris ASTERACEAEEUPHORBIACEAELEGUMINOSAERUBIACEAELABILENTIBULARIACEAE (others)P ClethrOther dicotTREESHERBS & SHRUBSOTHERS 30 0.1 LIA 40 0.5

1.0 MWP 50 1.5 60 2.0

70 2.5

80 3.0

90 3.5 ENSO

100 Ch

Depth (cm) 110 MID-LATE HOLOCENE MID-LATE

120 cal y BP (x1000)

130 4.0

140

150

160

170 4.3 8.5 SG LgH 12.7

Trees & shrubs Herbs Others 0 100%

Fig. 10. Pollen diagram from Eruoda tepui summit (Chimantá massif). LgH – Lateglacial/Early Holocene, SG – sedimentary gap, Ch – charcoal peak.

Redrawn from Nogué et al. (2009b).

elevated air relative humidity (Galán, 1992), would have acted as a lie at extreme topmost environments (Eruoda) or close to relevant

buffer for climatic changes thus providing relatively stable environ- vegetation ecotones (Churí and Apakará); therefore, upward and

mental conditions for the biota, favouring community constancy. downward biotic displacements are more easily recorded than at

However, this scenario cannot be generalized as signiﬁcant veg- other localities situated inside the Stegolepis-dominated meadows,

etation changes have been observed in some summits, such as where stronger displacements are required to record eventual veg-

Churí and Apakará. The difference of these localities is that they etation changes. This phenomenon has been called site sensitivity,

Fig. 11. (A) Aerial view of the topmost Chimantá highlands showing the dominant bare rock (brown/dark grey) surface with vegetation patches (green/light grey) on small

depressions and hollows. (B) Aerial view of a typical blackwater river near Wonkén surrounded by gallery forest. (For interpretation of the references to colour in this ﬁgure

legend, the reader is referred to the web version of the article.)

Photos V. Rull.

V. Rull et al. / Perspectives in Plant Ecology, Evolution and Systematics 15 (2013) 338–359 351

Fig. 12. Holocene vegetation changes on different tepui summits of the Chimantá massif following the same rules as in Fig. 6. Bf – Bonnetia forests.

Raw data from Rull (1991, 1996, 2005b).

which seems to be at the maximum at the ecotones (Fægri et al., forests, a background grass pollen signal has been present in the GS

1989), intermediate at the highermost summits, and low within diagrams almost continually, suggesting the permanent presence

the Stegolepis meadows (Rull, 2005b; Rull et al., 2011). Therefore, of grasslands that would have existed as isolated patches or in the

community constancy is a function of the interplay between site form of a forest–savanna mosaic.

sensitivity and the intensity of climatic shifts. The case of the GS uplands landscape, subject to long-standing

human disturbance, cannot be addressed using simple and deter-

Discussion ministic climate–vegetation equilibrium/disequilibrium models.

Rather, the vegetation features of this region would be more prop-

Climate–vegetation equilibrium erly understood under a patch dynamics model that considers

that the coupling of spatial heterogeneity, climate change and dis-

All the Lateglacial and Holocene forest types documented in the turbance patterns led to a non-equilibrium dynamic common in

GS uplands were eventually replaced by savannas coinciding with most mosaic landscapes (Pickett and White, 1985; Pickett and

signiﬁcant increases in ﬁre incidence. It is noteworthy that these Cadenasso, 1995). In this model, ecosystems are open systems

vegetation shifts occurred under both drier and wetter climates, without a deﬁnite stable state, and they are regulated by both

suggesting that the resulting savannas were not in equilibrium internal and external factors (including human disturbance) that

with climate and that repeated and intense burning has been the determine a persisting non-equilibrium dynamics. Turner et al.

main environmental driver of vegetation change. In support of this (2001) deﬁned several potential states under patch dynamics, from

view, experiments conducted in the lowland Orinoco savannas steady state or equilibrium (A) to an unstable state leading to sys-

have documented forest encroachment into savanna upon long- tem bifurcation or crash (F) (Fig. 13). In the case of the GS, the ﬁre

term ﬁre suppression (San José and Farinas,˜ 1991), a phenomenon frequency is high (low disturbance interval) and of low to medium

that seems to be common across the Neotropics (Hoffmann et al., extent, which places the vegetation dynamics within the unsta-

2012). However, the short-term nature of these studies means they ble zone. The frequency of large uncontrolled ﬁres is unknown but

only documented the initial successional stages of the eventual re- there are records of at least two of them during the past century

colonization, preventing the identiﬁcation of the types of forests (Fölster, 1986). These large ﬁres also determine unstable dynamics

that would ﬁnally be established and their similarities and dif- (Fig. 13), as forest recovery has not occurred and the burnt terrains

ferences from the “original” forests. According to Hoffmann et al. are still covered by treeless savannas with characteristic charred

(2012), climate alone may prevent the establishment of forests in trunks (Fölster, 1986; Huber and Schubert, 1989). In addition to

drier savannas. However, in mesic savannas that are under rela- the low resilience of forests, their recovery is hindered by further

tively wet climates, as is the case for the GS uplands, the persistence small, recurrent savanna ﬁres, showing a close interaction between

of savanna vegetation is more linked to ﬁre than to climatic and/or these ﬁre regimes. Palaeoecological records support that instability

edaphic factors, although positive ﬁre-climate feedbacks may be dynamics were maintained during most of the Holocene due to the

also relevant. It should be noted that, aside from the occurrence of coupling action of several forcings (Rull, 1992).

352 V. Rull et al. / Perspectives in Plant Ecology, Evolution and Systematics 15 (2013) 338–359

prep.). Hopefully, this analysis will provide evidence to test the stable, E

low stable,

equilibrium/disequilibrium hypotheses for the top of the tepuis. variance very high A variance equilibrium, B

steady state C

stable, Irreversibility and thresholds high variance

stable, The preceding palaeoecological records show a general pat-

low variance

tern of change from rainforest to savanna favoured either by ﬁres

or drier climates (or their coupling, depending on the case), and

huge

exceptional a further eventual establishment of morichales after ﬁre inten-

fires

siﬁcation, independently of climatic conditions. A hypothetical

daily unstable: rainforest recovery has not been documented in any of the case fires system bifurcation or crash F

disturbance/recovery interval

studies analyzed; therefore, the savanna and morichal expan-

disturbance/landscape extent sion seems to be deﬁnitely irreversible at the time scale studied

(Fig. 15). Fire pressure, especially the maintained recurrence of

Fig. 13. Equilibrium states deﬁned by Turner et al. (2001) under patch dynamics. ﬁres, seems to be decisive in preventing forest recovery, overriding

Grey ellipses show the two cases discussed for the GS, within the unstable zone.

the effects of climate. In other words, the occurrence of widespread

treeless savannas spiked with morichales is not the natural con-

In the highlands, the issue of climate–vegetation equilibrium is sequence of the dominant climatic features. This does not mean,

difﬁcult to elucidate with the available palaeoecological data. It is however, that the GS uplands should have been completely cov-

known that direct human impact has been negligible in the past, as ered by rainforests, as grassland communities would have been

at present (Gorzula and Huber, 1992; Huber, 1995d; Rull, 2007b, existed in the form of spots or mosaics. The conclusion is that

2010a). In addition, ﬁre (whether natural or human-induced) the savanna expansion documented during the Holocene, espe-

has not been a relevant ecological factor on top of the tepuis cially during the last two millennia, has been caused mainly by

(Rull, 2005b, Nogué et al., 2009b). Therefore, the hypothetical recurrent burning. Similar results have been obtained in African

climate–vegetation offsets may have been due primarily to sig- savannas using palaeoecological records, where forest–savanna

niﬁcant time lags in biotic responses to environmental shifts. mosaics have dominated during most of the Holocene and savan-

Unfortunately, the lack of independent evidence for climatic nas have expanded in the last 1800 years due to human-made ﬁres,

changes prevents the clariﬁcation of this point. The low resilience even under climates favourable for forest establishment (Breman

of tepuian vegetation under low-level human disturbance would et al., 2012).

support the existence of some disequilibrium in the short term. The abruptness observed in some forest–savanna turnovers

For example, Gorzula and Huber (1992) noted that local vegetation supports that, although high ﬁre pressure has been relatively con-

did not recover >20 years after its disturbance by low-intensity stant over certain periods, the biotic response has been sudden. This

camping activities for botanical research. Moreover, the summit suddenness suggests the existence of tipping points that, once sur-

of mount Roraima, one of the few tepuis open to public (although passed, lead to the sudden and irreversible expansion of savannas

controlled) visits, shows evident signs of vegetation degradation, and morichales. However, palaeoecological evidence is still insuf-

including the presence of invader plants (Safont et al., in prep.), ﬁcient to identify such potential thresholds. Neoecological studies

that seems to be irreversible. However, these observations are have provided some hypotheses related to edaphic features, such as

insufﬁcient for a deﬁnite conclusion and should be complemented the reaching of critical points of water retention capacity, nutrient

with long-term records. Thus far, clear evidence of recent ﬁres content or Al-Fe toxicity (Fölster et al., 2001; Dezzeo and Chacón,

has been documented on a few tepuian summits, all of them 2005). A possible way of testing these proposals with palaeoeco-

likely ignited in the uplands and climbing to the summits through logical evidence would be to compare past records on sediments

the slopes. An example is the Uei-tepui (Fig. 14), which is now derived from either sandstone or diabase, as they hold contrasting

under study. Preliminary radiocarbon dating suggests that Uei soil properties and the communities they support would have

ﬁres were relatively recent (the last few centuries) and extensive responded in a different way to ﬁre and climatic pressure. Another

in most of the summit area, affecting former forests. A peat potential threshold, as suggested for the African savannas, is the

sequence covering the last ∼6000 cal yr BP is currently being accumulation of enough grassy mass to carry ﬁre during forest

analyzed to unravel palaeoecological trends (Safont et al., in retreat thus causing positive feedbacks between vegetation and ﬁre

Fig. 14. Tepuian ﬁres. (A) View of the Chimantá massif from the E showing a recently burnt slope with (reddish brown/dark grey) with ﬁre nearly reaching the summit. (B)

View of the top of the Uei-tepui showing scattered burnt trees within a Stegolepis meadow, the result of a historical ﬁre that started in the uplands. (For interpretation of the

references to colour in this ﬁgure legend, the reader is referred to the web version of the article.)

Photos V. Rull.

V. Rull et al. / Perspectives in Plant Ecology, Evolution and Systematics 15 (2013) 338–359 353

(chronosequences). This author defended the idea that the

gb reversibility

morichal is the ﬁrst step of a regenerative succession that even-

tually ends with the recovery of rainforests after an intermediate

stage of mixed forests with Mauritia. The use of chronosequences

to reconstruct ecological successions, however, has been widely

discouraged in light of palaeoecological evidence (Johnson and

Miyanishi, 2008). Furthermore, the assumed community trends

proposed by González (1987) have not been observed in any of

SV the studied GS sequences. The second option (hysteresis) seems

ba to be common in the palaeoecological record (e.g., Bradley et al.,

A ge

2003; Maslin, 2004; Williams et al., 2011) but no information is

hysteresis available from the GS uplands. Based on neoecological studies,

Hoffmann et al. (2012) argue that the return from savanna to for-

est is also a threshold-crossing process, and they propose that two

of these tipping points are the “ﬁre-resistant threshold” (ﬂamma-

bility reduction by bark accumulation) and the “ﬁre-suppression

threshold” (grass exclusion by dense forest canopies). According

to these authors, if critical boundaries for these traits are crossed,

moisture moisture

then switching from savanna to forest would be possible. In the

SV GS uplands, as in the Orinoco lowlands, several ﬁre-resistant trees

occur, such as Byrsonima crassifolia (L.) Kunth (Malpighiaceae);

B ge

however, they are not relevant components of the GS rainforests

gb irreversibility but are species that grow as isolated trees interspersed within the

RF savanna landscape (Huber, 1986, 2006). The discovery of species

with similar characteristics in the GS forests with potential for

good pollen representation in the sediments would be welcome.

MR However, as mentioned before, grasses seem to have always been

present in the GS, at least since the early Holocene, which has likely

si sb

hindered progress towards the second threshold. These would con-

moisture

stitute possible future directions of palaeoecological research.

SV MR

sb In the case of GS morichales, both ﬁres and climate are involved

C in their establishment and further dynamics. The main role of

ﬁre seems to be the removal of rainforests and their replace-

fire

ment by savannas, while wet climates promoting soil ﬂooding

Fig. 15. Hypothetical and observed possibilities of community change in the Gran are needed for Mauritia growth. Further shifts in ﬁre incidence

Sabana uplands as related to ﬁre and moisture trends. (A) Reversibility: ﬁre and/or and available moisture, acting either alone or synergistically, may

increased dryness determines the replacement of forests by savannas, and fur-

be responsible for the ensuing changes in morichal density. In

ther ﬁre cessation and/or moisture increase causes forest recovery through the

this case, the switching between open savannas and morichales

same intermediate states (shrubby savannas, fern-bush communities and secondary

seems to be reversible. High-resolution palaeoecological studies of

forests). (B) Hysteresis: the same as the former but the return from savanna to for-

est proceeds via different intermediate communities. (C) Irreversibility (supported savanna–morichal transitions and vice versa are also needed to test

by palaeoecological evidence): after the replacement of forests by savannas, ﬁre

the hypotheses on the eventual reversible nature of the process and

increases lead to the development of morichales instead of the former forests, which

the existence or not of tipping points, as well as the potential role

do not recover again. The savanna–morichal switching seems to be reversible. Com-

of selective burning.

munities: RF – rainforests, SV – savannas, MR – morichales; thresholds (arrows): gb

– grassy biomass, ba – bark accumulation in trees, ge – grass exclusion, si – soil In the GS highlands, the synergistic coupling between site sensi-

impoverishment; sb – selective burning. tivity and intensity of climatic shifts has determined the existence

of thresholds for vegetation change (Table 1). In the ecotones,

even climatic changes of lower intensity have led to elevational

able to prevent forest recovery by suppressing seedling recruitment vegetation shifts. Temperature is the main control for the eleva-

(Breman et al., 2012). In the GS, this threshold would be applicable tional distribution of vegetation in the Guayana mountains (Huber,

to intermediate stages of the forest–savanna replacement, whereas 1995c); hence, changes in this parameter are expected to have been

tipping points bounded to soil deterioration seem more plausible the main drivers for these elevational shifts. In the highest sum-

once the savannas have been established. Some recent simulations mits, being under extreme climates, the thresholds would be linked

also suggest that non-equilibrium systems appear when disturb- to precipitation excess that may have determined the dramatic

ance is continuous over long time periods and exceeds 50% of the shifts from peat accumulation, together with community con-

landscape extent (Turner et al., 2001). stancy, to peat removal by sliding under huge precipitation. Given

Whether GS forests would be able to recover after a long the present-day rainfall amounts on the Chimantá (Galán, 1992)

period of ﬁre suppression is difﬁcult to ascertain with the avail- and the fact that peat is currently accumulating on their rock cav-

able palaeoecological evidence, as ﬁre has been present almost ities, the tipping point for this to occur should be above 3600 mm

continually during the time interval studied. The continuous occur- of total annual precipitation. Within the Stegolepis meadows, nei-

rence of savannas during some phases with reduced ﬁre incidence ther lower nor higher intensity climatic changes have modiﬁed

would be informative but total ﬁre suppression would be a better the community composition during the time interval studied. A

way to envisage the problem. An eventual forest recovery would comparison among the different records from the tepuian summits

theoretically proceed in two main modes: reversibility or hystere- may provide estimates for this temperature threshold. The eleva-

sis (Fig. 15). A reversible trend was proposed by González (1987) tional difference between Churí (2250 m) and the other localities

based on the spatial arrangement of present-day communities is between 100 m (Amurí) and 300 m (Acopán) which, using the

354 V. Rull et al. / Perspectives in Plant Ecology, Evolution and Systematics 15 (2013) 338–359

Table 1

Threshold-crossing processes at the GS highlands as a function of site sensitivity (rows) and the intensity of environmental changes.

Lower intensity Higher intensity Threshold Example

◦

Ecotones Vegetation change Vegetation change <0.6 C Churí

Rocky summits Community constancy Denudation >3600 mm Eruoda

◦

Stegolepis meadows Community constancy Community constancy 0.6–1.8 C Acopán Amurí Toronó

◦

present-day lapse rate of −0.6 C/100 m elevation (Galán, 1992),

◦ ◦

represents a difference of 0.6–1.8 C (average 1.2 C) in tempera- GLACIAL

ture. Therefore, a downward shift of at least this magnitude would

isolation

be needed for Stegolepis to disappear from the summits of Acopán,

Amurí and Toronó, as it occurred in Churí during the post-HTM migration

1100m

cooling (5400–3500 cal yr BP). Similar calculations for the Apakará migration H

are hindered by the lack of Myrica records at other elevations. coalescence

Origins of biodiversity U

The biodiversity and endemism patterns of the Guayana High-

lands (GH) are striking. Although systematic exploration is far

from complete (Huber, 1995b), almost 2500 vascular plant species

(belonging to 630 genera and approximately 160 families) have

vicariance U

been described, of which 62% are endemic to the Guayana region,

42% are endemic to the Pantepui province, and approximately

25% are endemic to a single tepui (Berry and Riina, 2005). Local

endemism can reach 60% in some tepuis, which is comparable to

most oceanic islands (Rull, 2009c). To explain these biotic features,

Maguire (1970) suggested a long history of isolation starting in the hibridation

? adaption

Late Cretaceous, when the disconnection of tepui summits began. ?

This is the so-called lost world (LW) hypothesis (Rull, 2004a), which

U H

is similar to the “plateau theory” proposed by Chapman (1931)

and Tate (1938) for the bird fauna. The LW hypothesis requires the

complete isolation of the summits, but less than 20% of the tepuis

are actually isolated topographically, and most of the summits are

“connected” to the surrounding lowlands by extensive river valleys,

ridges, and eroded cliffs, which could have acted as migrational INTERGLACIAL

pathways (Huber, 1988). The suggested forcing mechanism for

isolation

such migration was the alternation of glacial and interglacial phases

during the Quaternary (Steyermark and Dunsterville, 1980; Huber,

isolation

1988). This is the so-called vertical migration (VM) hypothesis (Rull, 1100m

isolation H

2004a), similar to the “cool climate theory” of Chapman (1931) H

migration

and Tate (1938). Until recently, both the LW and VM hypotheses

were based on present-day biogeographical studies. About a decade

ago, however, palaeoecological evidence in support of the second

hypothesis was found at the Churí summit (Rull, 2004a,b). Detailed

and comprehensive discussions on this topic are provided by Rull

(2004c, 2005a, 2010a). U

The elevational migrations documented in this paper, linked to vicariance

global and quasi-global climatic shifts, reinforce the VM hypoth- extinction U

esis and, consequently, the signiﬁcant role of Pleistocene climatic

changes as diversiﬁcation drivers in the GS highlands. In addition,

this evidence, together with the record of changes in community

composition, strengthens the view that elevational shifts have not

involved entire communities but rather individual species. These H gene flow

vicariance

ﬁndings match the diversiﬁcation model proposed by Rull (2005a), extinction

vicariance

according to which, glacial phases were characterized by down- extinction

ward displacement of the tepuian ﬂora and dispersal through the U H

uplands, thus promoting hybridization and gene ﬂow. During inter-

glacial periods the species migrated upward leading to vicariance

and possibly extinction by habitat loss on top of the tepui summits

(Fig. 16). This model was an adaptation of the dispersal-vicariance

Fig. 16. Diversiﬁcation model for the tepuian summits under recurrent Quaternary

model, as proposed for the Amazon basin (Bush, 1994), to the GH.

glacial–interglacial cycles.

From a neotropical perspective, these proposals radically differ

Redrawn from Rull (2005a).

from the “refuge theory”, which proposed that allopatric speciation

V. Rull et al. / Perspectives in Plant Ecology, Evolution and Systematics 15 (2013) 338–359 355

occurred during arid glacial phases due to rainforest fragmentation facilitate its burning thus generating a positive ﬁre-vegetation

into refugia, whereas gene ﬂow took place during humid inter- feedback, and exacerbating savanna expansion at the expense of

glacials when rainforests expanded and coalesced again (Prance, forests. In addition to the upland forests, those from the tepui slopes

1982; Whitmore and Prance, 1987). After its initial proposal (Haffer, and even their top vegetation would be at risk of being removed by

1969), the refuge hypothesis was very popular, almost paradig- burning, a situation that is already occurring today in some tepuis

matic, for a few decades; however, further palaeoecological evi- (Fig. 14). Within this context, it is expected that the tipping points

dence seriously challenged this view (Bush and De Oliveira, 2006). for the forest–savanna transition would be reached sooner, while

The signiﬁcance of Pleistocene climatic changes for biotic diver- those for the forest recovery would be even further delayed, per-

siﬁcation is only part of the story, as recent meta-analyses on haps resulting in enhanced irreversibility. The potential effect of

dated DNA phylogenies have shown that neotropical speciation global warming on the morichales is still unknown due to the lack

has been a continuous process since at least the early Miocene of detailed successional studies, as mentioned above. However, as

(Rull, 2008; Hoorn et al., 2010; Turchetto-Zolet et al., 2012). these palm communities are largely dependent on the occurrence

Furthermore, the available evidence shows that neotropical diver- of high moisture availability and ﬂooding, it is possible that their

siﬁcation is not a single-time/single-cause issue but, rather, a area would also be reduced. It is also uncertain how global warm-

complex process involving different environmental drivers acting ing may affect human populations and, thus, ﬁre incidence, but the

alone and/or synergistically at different time scales (Rull, 2011a,b). predicted climate change does not seem to be critical for human

Among these drivers, Plio-Pleistocene climatic changes, marine life. Therefore, it is possible that ﬁre practices remain similar to

incursions (Miocene), the Andean uplift (Miocene) and correspond- the trend observed for the last 2000 years. Under these conditions,

ing changes in drainage patterns, and the closure of the Panama savanna expansion and forest shrinking may progress indeﬁnitely.

isthmus (Pliocene) have been highlighted. Unfortunately, phyloge- From a strictly conservationist perspective, ﬁres must be drasti-

netic DNA studies on taxa from the Guayana highlands are very cally reduced or suppressed if the rainforests of the uplands and

scarce due to non-scientiﬁc constraints (Rull and Vegas-Vilarrúbia, the tepuian slopes are to be preserved (Dezzeo et al., 2004b). How-

2008; Rull et al., 2008). However, some data are available to illus- ever, such as goal seems to be in conﬂict with the traditional use and

trate the diversiﬁcation process. For example, the genus Stegolepis management of ﬁre by the Pemón culture (Rodríguez, 2007, 2009)

has more than 30 species, of which more than 20 are endemic and multidisciplinary initiatives have been launched to address

to single tepuis each (Berry, 2004). Contrarily to the expecta- the dilemma, including palaeoecological surveys (Rodríguez et al.,

tions of the LW hypothesis, the genus originated in the Miocene 2009; Bilbao et al., 2010). The debate between scientiﬁc and indige-

between 6 and 12 million years ago, and its species originated nous traditional knowledge in nature conservation is widespread

during the Plio-Pleistocene (Givnish et al., 2000). Similar trends and a solution is not straightforward (e.g., Nepstad et al., 2006;

were observed in several Bromeliaceae genera, such as Navia and Schmidt and Peterson, 2009; Painter et al., 2011; Rutte, 2011).

Brocchinia, where species originated between the Plio-Pleistocene In the GS highlands, the evidence for elevational migration,

boundary and the Miocene (∼13 million years ago) (Givnish et al., together with the observed changes in community composition

1997, 2011), much later than the late Cretaceous, as predicted over time documented in some localities vs the constancy recorded

by the LW hypothesis. In addition, DNA phylogenetic and phy- in others, also furnish useful tools to discuss biodiversity conser-

logeographic analyses carried out on toads (Atelopus) and frogs vation issues. The present state of knowledge has been compiled

(Tepuiphyla) from the GH documented a mostly Plio-Pleistocene by Vegas-Vilarrúbia et al. (2011) and will be summarized here.

origin for their species (Noonan and Gaucher, 2005; Salerno et al., In this case, the critical parameter is temperature that, accord-

◦

2012). The case of Atelopus is particularly interesting, as the ances- ing to IPCC estimates, will rise by 2–4 C in the Guayana region

tral Andean lineage migrated downward due to the late Pliocene by the end of this century (Solomon et al., 2007). Previous works

cooling and dispersed across the Amazon lowlands during the have estimated that this increase in temperature will cause dra-

early-middle Pleistocene (until ca. 1.5 million years ago). The extant matic reductions of plant biodiversity. Indeed, ∼1700 of the ∼2500

GH species diversiﬁed from this ancestor on top of the table moun- known vascular plant species would be at risk of total habitat loss,

tains between ca. 500,000 and 100,000 years ago, favoured by the including approximately 400 Pantepui endemics, whose extinc-

alternating glacial-interglacial cycles (Noonan and Gaucher, 2005), tion would be of global importance (Rull and Vegas-Vilarrúbia,

which strongly supports the dispersal-vicariance and VM hypothe- 2006; Nogué et al., 2009a; Safont et al., 2012). This problem led

ses (Rull, 2006). to the consideration of several conservation options, such as for

example seed banks, living plant collections or managed relocation

Global warming and biodiversity conservation (Safont et al., 2012). It has also been proposed that some popu-

lations would persist within fairly stable refugia or microrefugia

In the GS uplands, the lack of equilibrium between climate (sensu Rull, 2009d, 2010b). One of these potential refugia would be

and vegetation, as well as the reversibility or irreversibility of the Chimantá massif which, according to current estimates of area

the vegetation shifts caused by ﬁres, provides insight into conser- reduction by the end of this century, would represent nearly the

vation issues. The sociological, ethnological and political aspects half of the remaining Pantepui surface in a non-fragmented state

of the ﬁre practices by the indigenous people in these uplands (Vegas-Vilarrúbia et al., 2012). However, the quoted habitat-loss

have been much debated (Dezzeo et al., 2004b; Rodríguez, 2004b; estimations were based on species-area modelling and elevational

Sletto, 2008, 2009, 2010, 2011) and are beyond the scope of this range displacement analysis, and relied on several hypothetical

paper, which focuses on the ecological aspects of the problem. assumptions, for example, that all species will migrate upwards

According to the projections of the Intergovernmental Panel on as a result of the global warming, and all at similar rates, following

Climate Change (IPCC) for the end of this century, the total pre- the pace of warming. The ﬁrst assumption is not fully supported by

cipitation amounts in the region under study will decrease by up palaeoecological studies demonstrating that only sensitive species

to 10%, with low seasonal variations (Solomon et al., 2007). This, are able to migrate following climatic shifts, whereas others would

together with ﬁre, is a critical ecological parameter for the GS be able to accommodate to changes, likely due to their phenotypic

uplands. A reduction in total precipitation would have a straightfor- plasticity. In addition, the long-standing community constancy

ward effect because of the reduced available moisture, but it could observed in some tepuian localities during the last 6000 years

also indirectly increase the ﬂammability of the vegetation and would seem to challenge the possibility of migration in response to

356 V. Rull et al. / Perspectives in Plant Ecology, Evolution and Systematics 15 (2013) 338–359

climate shifts. However, palaeoecological records have also shown has occurred in both directions in the palaeoecological records.

that the climatic changes that occurred during this interval have Another relevant lesson is that a hypothetical “original” vegetation

not been intense enough to promote conspicuous biotic responses type for the GS uplands cannot be deﬁned because neither envi-

at low-sensitivity sites. The possibility of rapid genetic adapta- ronmental nor anthropogenic drivers have been constant through

tion in response to warming is still to be demonstrated but should time. It is also noteworthy that some past forest and shrubland

not been dismissed without positive evidence (Vegas-Vilarrúbia communities from both uplands and highlands have no modern

et al., 2011). Concerning rates, the examples of Podocarpus and analogues as they are different in composition than their present

Catostemma allow the estimation of natural upward migration counterparts, due to the prevalence of individualistic species-

velocity since the LGM in response to postglacial warming, which level response to environmental shifts. All these inferences would

resulted in ∼0.1 m elev./yr, up to 70 times less than required to have not been possible with solely neoecological observations as

follow the predicted 21st century warming trajectory of 3–7 m they use present-day spatial vegetation patterns to reconstruct

elev./yr. No information exists for the Pantepui species in this ecological succession in a space-for-time substitution reasoning

respect but upward migration rates of this magnitude, ranging from (chronosequences) and usually assume, explicitly or not, environ-

1 to 5 m elev./yr, have been documented on mountains elsewhere mental constancy.

in response to the ongoing global warming (Beckage et al., 2008; According to the evidence presented in this paper, includ-

Kelly and Goulden, 2008; Lenoir et al., 2008). ing palaeoecological records and DNA molecular phylogenies, the

In general, the occurrence of past communities with no present striking biodiversity and endemism of the GS highlands has not

analogues in either uplands or highlands as a result of individ- been the result of a long history of topographical isolation favouring

ualistic species’ response to environmental shifts, suggests that vicariance (Lost World hypothesis). Rather, the Pleistocene climatic

future communities shaped under the inﬂuence of global warming changes likely determined elevational migrations of highland biota

will also be different from present ones and highly unpredictable leading to an alternation between isolation (interglacials) and gene

(Hobbs et al., 2009). Therefore, the recent proposal of using a static ﬂow through the uplands (glacials), resulting in net biotic diversiﬁ-

community approach for biodiversity conservation (Rodríguez cation. It has been shown that tectonic and climatic pre-Pleistocene

et al., 2011) would be insufficient to address the problem. The events also exerted a significant influence on neotropical diversi-

above palaeoecological results suggest that an individual species ﬁcation and their potential direct or indirect contribution to GS

approach, with emphasis on sensitive and keystone species, would highlands should be considered, in light of molecular evidence

be necessary to predict potential changes in community composi- showing a pre-Pleistocene age for a number of extant plant and ani-

tion following global warming. mal species. Again, such conclusions would have been impossible to

obtain from only short-term evidence that, in this case, consists pri-

Conclusions marily of present-day biogeographical patterns, on which the Lost

World and similar hypotheses are based. Regarding global warming

In general, it can be concluded that long-term (i.e. palaeoe- and biodiversity conservation, if the IPCC projections are realistic,

cological) studies developed so far in the GS region have been the GS uplands would be under signiﬁcantly warmer and drier cli-

demonstrated to be useful to address unresolved ecological issues mates, which would favour forest retreat and savanna expansion

in aspects that neoecological evidence cannot cover due to its as a direct result of reduced available moisture, ampliﬁed by pos-

intrinsically insufﬁcient temporal scope. For this to be true, how- itive climate-ﬁre feedbacks. Mauritia swamp communities would

ever, palaeoecologists should look at their data with a more also be negatively affected by global warming as they need water-

ecological perspective, rather than pursuing solely palaeoclimatic saturated or ﬂooded soils to grow. In the highlands, the main threat

and palaeoenvironemntal reconstructions. In particular, this paper seems to be extinction by habitat loss due to the unavailability

illustrates the advantages of using long-term ecological data sets of higher environments to migrate following the global warming.

in speciﬁc aspects such as the study of climate–vegetation equilib- Extinction estimates based on climatic modelling are alarming and

rium, the reversibility of vegetation changes, the origin of extant palaeoecological evidence can provide clues for a more realistic

biodiversity patterns and the conservation of this biodiversity in forecast. In this sense, past evidence has shown that not all species

the face of global change. but only the more sensitive ones have migrated up and down fol-

Concerning the ﬁrst point, extant upland savannas seem not to lowing temperature shifts. It has been also shown that highland

be in equilibrium with present-day climates. Rainforests of several GS communities have remained fairly stable, especially on low-

types, shrublands, savannas and mosaic patterns have alternated sensitivity sites, since the mid-Holocene, in spite of the occurrence

during the Lateglacial and the Holocene in the studied localities of several climatic shifts. Therefore, extinction estimates should

owing to the action of either climate or ﬁres (or both). How- be reconsidered in light of these observations. The possibility of

ever, since ca. 2000 years ago, the consequences of ﬁre have future communities with no modern analogues as a result of the

overridden the effects of climate thus promoting and maintain- individual nature of species’ responses to global warming, as has

ing a general and continuous trend of savanna expansion. The occurred in the past, should also be seriously envisaged. This would

current GS landscape of treeless savannas spiked with Mauritia have important implications for conservation policies that priori-

palm swamps is not the natural consequence of the present-day tize species rather than of entire communities or landscapes, as

dominant climatic features. Regarding reversibility, an eventual conservation targets.

forest/shrubland recovery at the expense of savannas has not

been observed in the past; therefore, the switch from rainforest

Acknowledgements

to savanna is irreversible at the time scale studied (millennial).

The sudden character of the forest/shrubland-savanna replace-

This work was developed under the auspices of project ECO-

ment suggests the existence of tipping points leading to abrupt

PAST, funded by the Ministry of Science and Innovation of Spain

responses but these thresholds have not been identiﬁed, so far.

(grant CGL2009-07069/BOS). The authors acknowledge the thor-

Potential candidates have been linked to edaphic (water retention

ough and detailed reviews of two referees (William Gosling and

capacity, nutrient depletion, chemical toxicity) and vegetation (fuel

anonymous), which contributed to the improvement of the original

accumulation) features. On the contrary, the shift from savannas

manuscript. Hayley Keen contributed to the English improvement.

to morichales shows some degree of reversibility, as the change

V. Rull et al. / Perspectives in Plant Ecology, Evolution and Systematics 15 (2013) 338–359 357

◦

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