Climate and landscape during Heinrich Event 3 in south-western Europe: the small-vertebrate...

Climate and landscape during Heinrich Event 3 insouth-western Europe: the small-vertebrate associationfrom Galls Carboners cave (Mont-ral, Tarragona,north-eastern Iberia)

JUAN MANUEL LOPEZ-GARCIA,1* HUGUES-ALEXANDRE BLAIN,2,3 MARIA BENNASAR,2,3 JOSEP ANTONI ALCOVER,4

SANDRA BANULS-CARDONA,1 MONICA FERNANDEZ-GARCIA,3 MARTA FONTANALS,3,2 PATRICIA MARTIN,2,3

JUAN IGNACIO MORALES,2,3 LAURA MUNOZ,5 MIREIA PEDRO6 and JOSEP MARIA VERGES2,31Sezione di Scienze Preistoriche e Antropologiche, Dipartamento di Studi Umanistici, Universita degli Studi di Ferrara, Ferrara,Italy

2IPHES, Institut Catala de Paleoecologia Humana i Evolucio� Social, Tarragona, Spain3Area de Prehistoria, Universitat Rovira i Virgili (URV), Tarragona, Spain4Institut Mediterrani d’Estudis Avancats, CSIC-UIB, Esporles, Mallorca, Spain5Area de Historia Contemporanea, Departamento de Historia, Facultad de Filosofıa y Letras, Universidad de Extremadura,Caceres, Spain

6SERP, Seminari d’Estudis i Recerques Prehistoriques, Departament de Prehistoria, Historia Antiga i Arqueologia, Universitat deBarcelona, Barcelona, Spain

Received 24 September 2013; Revised 6 December 2013; Accepted 9 December 2013

ABSTRACT: Heinrich Event 3 (H3) is well documented in the North Atlantic Ocean as a cooling event thatoccurred ca. 31 000 years ago. Deep-sea cores around the Iberian Peninsula coastline have been analysed tocharacterize the H3 event, but there are no data on the terrestrial response to this event. Here we present for thefirst time an analysis of terrestrial proxies for characterizing the H3 event, using the small-vertebrate assemblage(comprising small mammals, squamates and amphibians) from the Galls Carboners cave, an archaeo-palae-ontological deposit located in the Prades mountain range in the north-eastern Iberian Peninsula. This assemblageshows the H3 event to be characterized in north-eastern Iberia by harsher and drier terrestrial conditions thantoday. Our results were compared with the small-vertebrate assemblage data recovered from present-day Strixaluco pellets available from this site, as well as with the general H3 event fluctuations and with other sites wherethe previous Heinrich events (H5 and H4) and subsequent Late Glacial Maximum have been detected in theMediterranean and Atlantic regions of the Iberian Peninsula. Terrestrial proxies seem to follow the same climaticpattern as detected in the deep-sea cores at NorthGRIP and the Iberian margins.Copyright # 2014 John Wiley & Sons, Ltd.

KEYWORDS: biodiversity; herpetofauna; Iberian Peninsula; palaeoclimate; palaeoenvironment; small mammals.

Introduction

A decrease in the values of d18O, peaks in magneticsusceptibility, an increase in the proportions of the foramini-fer Neogloboquadrina pachyderma and the appearance ofice-rafted debris (IRD) are what define the last six HeinrichEvents (H6 to H1) (Cayre et al., 1999). Like the two previousones (H5 and H4), Heinrich Event 3 (H3) is characterized bya pattern divided into three phases: (1) the first features areduction in the marine surface temperature, as indicated bya rise in the percentages of N. pachyderma – this phase isassociated with the first arrival of IRD during HE3, and iscontemporaneous with relatively high percentages of Euro-Siberian trees, such as deciduous Quercus and Ericaceaeshrubs, as well as with the end of a temperate and humidterrestrial phase; (2) the middle phase is characterized bymaximum input of IRD, maximum levels of N. pachydermaand the optimal development of steppe vegetation, thusreflecting synchronous terrestrial and oceanic cooling; and (3)the ceiling of H3 is characterized by a fall in the values ofIRD, magnetic susceptibility and d18O, as well as a decline inthe percentages of the cold species N. pachyderma. Thesecharacteristics are further associated with an increase in theproportions of Euro-Siberian trees and Ericaceae, reflecting anew temperate and humid period at average terrestrial

latitudes and North Atlantic Ocean latitudes (Sanchez-Go~niet al., 2000).Here we present for the first time a characterization of the

environment and climate of the H3 event based on the small-vertebrate assemblage of the Galls Carboners cave. Ourresults are compared with current climatic data for the zone(Ninyerola et al., 2003) and data from present-day Strix alucopellets obtained from this site, as well as with the general H3event fluctuations, to see whether the phases detected bySanchez-Go~ni et al. (2000) and Cacho et al. (2006) can beobserved in the data from the Galls Carboners cave. They arealso compared with data from other sites where the previousHeinrich events (H5 and H4) and the subsequent Late GlacialMaximum (LGM) have been detected in the Mediterraneanand Atlantic regions of the Iberian Peninsula, to observewhether the terrestrial proxies follow the same patterns as theclimatic and environmental conditions detected by the deep-sea cores at the Iberian margins.

Site description

The Galls Carboners Cave, or Gall Carboner cave (the namegiven to Strix aluco in the region), opens onto the cliff onthe north-eastern slope of the Motllats, at 965m a.s.l., on thewestern margin of the Brugent river valley (Fig. 1). TheMotllats is a plateau located in the Prades mountain range,and is composed of dolomite, dolomitic breccias, sands and

�Correspondence: J. M. Lo�pez-Garcıa, as aboveE-mail: [email protected]

Copyright # 2014 John Wiley & Sons, Ltd.

JOURNAL OF QUATERNARY SCIENCE (2014) 29(2) 130–140 ISSN 0267-8179. DOI: 10.1002/jqs.2687

limestones attributed to the Lias (Jurassic). It ranges around1000m a.s.l., reaching a peak of 1075.8m a.s.l (Puig Pelat).This Jurassic series is built on dolomite clays of the Keuper(Triassic), located at around 750m a.s.l., which form the baseof this relief.The abruptness of the relief, the significant hydrological

differences between the plateau, which tends to be arid, andthe north-eastern slope, which is shady and features severalsprings, and the closeness of the river (which is situated at astraight-line distance of roughly 2 km) produce a mosaic ofdifferent environments, reflected in the distribution of theplant communities. At present the plateau hosts semi-openwoodland made up of holm oak (Quercus ilex ssp. rotundifo-lia) and Scots pine (Pinus sylvestris), together with shrubs,common juniper (Juniperus communis) and common box(Buxus sempervirens). The slope of the Motllats is covered byclosed woodland consisting of holm oak together with Scotspine in the higher parts and Aleppo pine (Pinus halepensis) inthe lower parts. The undergrowth is fairly thick, consistingmainly of boxwood, laurustinus (Viburnum tinus), Mediterra-

nean buckthorn (Rhamnus alaternus) and strawberry tree(Arbutus unedo), among other shrubs. Cultivated farmlanddominates the plain where the Keuper clays are located,while between this area and the river Brugent are scrubformations, bordered by well-developed riparian woodland.Access to the cave is through a triangular entrance facing

north, which is 3.75m high by 3m wide and located 5.5mabove the foot of the cliff. The cave runs a distance of some60m. It is divided into two clearly differentiated sectors. Thefirst covers roughly 25m, and is between 4 and 5m in height.The rest of the cave is reached via a crawl. To put the recordinto context, it was decided to divide it into zones, sectorsand sub-sectors on the basis of the existence of significantchanges in size, features and the direction of the conduits(Fig. 2). It was from sub-sector I-1-c that the small vertebrateswere recovered (Fig. 2). Stratigraphically, sub-sector I-1-cshows a strong level of mixed sediment at the top (Fig. 2).This unit has been identified as layer 100, which coversarchaeological levels 105–108 and attaches to levels 101–104. Levels 101 and 103 correspond to two limestone crusts

Figure 1. Above: location of the sites mentioned in text in the Iberian Peninsula, including the Galls Carboners cave. Below: schematic topographiccross-section showing Galls Carboners within the Prades mountain range.

Copyright # 2014 John Wiley & Sons, Ltd. J. Quaternary Sci., Vol. 29(2) 130–140 (2014)

CLIMATE AND LANDSCAPE DURING H3 IN SW EUROPE 131

formed by carbonate precipitation due to surface water flow.Level 102 lies between these two levels and presents anirregular base, forming irregular bodies. It consists of highlyorganic sediment, which contains numerous charcoal re-mains. These sediments were probably also swept along bythe action of water, filling up the depression in the surface oflevel 103 and then level 101, which incorporated charcoalremains from level 102. Below level 103, level 104 iscomposed of organic brown sediment. These four levels areretained as a testimonial, adhering to the wall of the cave.Levels 105–108, from the small vertebrates derive, display a

very similar composition, and are separated from the previouslevels by a thin stalagmitic plate. There is a series of clayey–muddy yellow levels with a sporadic presence of small clastsemerging from the cave wall. In fact, these levels seem to bethe product of the same sedimentary dynamics, differing onlyin slight changes in colour and in the relative percentages ofclay and slit. 14C accelerator mass spectrometry (AMS) datinghas been performed on the humerus of a yellow-billed chough(Pyrrhocorax graculus) from level 107, showing an age of 31170–31 380 cal a BP (Beta-317 704) (Table 1).

Materials and methods

Small-vertebrate sorting and the palaeontologicalstudy

The small-vertebrate fossil remains used for this study consistmainly of disarticulated bone fragments and isolated teethcollected by water-screening. About 500 kg of sediment was

water-sieved using superimposed 1.5- and 0.5-mm meshscreens. The present-day small-vertebrate remains used forthis study consist of disarticulated remains from Strix aluco(tawny owl) pellets recovered from the entrance to the cave.The fossils and modern material was processed, sorted andclassified at the Institut de Paleoeoclogia Humana y Evolucio�Social (IPHES, Tarragona, Spain). The fossil assemblageincludes 399 identified specimens, corresponding to a mini-mum of 122 individuals, representing at least 16 taxa(Table 2; Fig. 3). The modern assemblage includes 2067identified specimens, corresponding to a minimum of 209individuals, representing at least 25 taxa (Table 2). Bothkinds of fragment were identified following the palaeonto-logical criteria given by Sevilla (1988), Cuenca-Besco�s et al.(2008) and Lo�pez-Garcıa (2011) for small mammals, andBailon (1999), Sanchız (1984), Sanchız et al. (2002), Bar-ahona and Barbadillo (1997), Blain (2009) and Szyndlar(1984) for the herpetofauna. The specific attribution of this

Figure 2. (A) Plan showing the location of the different sectors of Galls Carboners, indicating sector I-1-c and sector I-1-b. (B) Plan of sector I-1-c.(C) Section a–a0 of sector I-1-c.

Table 1. Radiocarbon date from Galls Carboners archaeologicallevel 107.

Archaeologicreference sample

CGC’10-107-Bone(Pyrrhocorax graculus)

Laboratory reference Beta-317 704Conventional age (14C a BP) 26 940�130Calibrated age 2s (95% probablity)

(cal a BP)31 380–31 170

(29 430–29 220 BC)


132 JOURNAL OF QUATERNARY SCIENCE

material rests principally on the best diagnostic elements:humerus, ilium, scapula and sacrum for anurans; skullelements for lizards; vertebrae for snakes; mandible, maxillaand isolated teeth for bats and shrews; isolated teeth andhumerus for Talpidae; first lower molars for Arvicolinae; andisolated teeth for Apodemus sylvaticus and Eliomys querci-nus. Moreover, the fossils were grouped using the minimum-number-of-individuals (MNI) method, by which we deter-mined the sample (i.e. from each level) by counting the bestdiagnostic elements, taking into account, whenever possible,laterality and sex (for anurans).

Palaeodiversity reconstruction

Species evenness is fundamental for assessing the homogenei-ty of an environment (Magurran and McGill, 2011). Evennessis a diversity index that is used to quantify how equal thevarious communities are numerically. The evenness of acommunity can be represented by Simpson’s index of diversi-ty, which is also equivalent to the probability of interspeciesencounters (Simpson, 1949; Blois et al., 2010; Lo�pez-Garcıa

et al., 2013b), i.e. Simpson’s index of diversity¼ 1–S(pi2),

where pi is the proportion of individuals in the ith species.The evenness index is constrained between zero and 1. Thelower the variation in species between communities, thehigher the value of the evenness index. The index will beclose to zero if there is a single dominant species. To avoidthe statistical problems of high sample-size dependence, wehave standardized the absolute values by dividing by totalsample abundances, expressed as percentages of MNI. Thisstandardization allows taxon evenness to be compared insamples of different size. This index of evenness was calculat-ed using the Paleontological Statistics Program (PAST) (Ham-mer et al., 2001).

Palaeoenvironmental reconstruction

To reconstruct the palaeoenvironment at Galls Carboners, weuse the method of habitat weightings (see Evans et al., 1981;Andrews, 2006), distributing each small-vertebrate taxon inthe habitat(s) where it can be found at present in the IberianPeninsula. Habitats are divided into five types (in accordance

Table 2. Representation of the number of identified specimens (NISP), the minimum number of individuals (MNI) and the percentage of the MNI(%) for the small vertebrates from the Galls Carboners H3 event levels and present-day Strix aluco pellets, and the small-vertebrate distribution byhabitat and by chorotype.

Taxon

Carboners Heinrich Event 3 Pellets Strix aluco Chorotypes Habitat

NISP MNI % NISP MNI % C1 C2 C3 C4 OD OH Wo R Wa

Amphibians and squamate reptilesAlytes obstetricans 1 1 0.82 224 21 10.05 x 0.6 0.2 0.2Pelodytes punctatus 0 0 0 1 1 0.48 x 0.5 0.2 0.1 0.2Bufo calamita 9 3 2.46 0 0 0.00 x 0.65 0.25 0.1cf. Rana temporaria 1 1 0.82 0 0 0.00 x 0.4 0.4 0.2cf. Pelophylax perezi 0 0 0 8 2 0.96 x 1cf. Tarentola mauritanica 0 0 0 1 1 0.48 x 1cf. Psammodromus sp. 0 0 0 79 5 2.39 – – – – – – – – –cf. Podarcis sp. 216 34 27.87 0 0 0.00 – – – – – – – – –Lacertidae indet. 18 6 4.92 0 0 0.00 – – – – – – – – –Anguis fragilis 0 0 0 20 1 0.48 x 0.25 0.75Coronella girondica 0 0 0 504 5 2.39 x 0.25 0.25 0.25 0.25Malpolon monspessulanus 0 0 0 15 1 0.48 x 0.5 0.35 0.15cf. Rhinechis scalaris 0 0 0 2 1 0.48 x 0.4 0.45 0.15Vipera latastei 0 0 0 180 2 0.96 x 0.38 0.25 0.38Ophidia indet. 0 0 0 709 0 0.00 – – – – – – – – –

Small mammalsCrocidura russula 16 8 6.56 39 20 9.57 x 0.5 0.5Suncus etruscus 0 0 0 6 4 1.91 x 0.75 0.25Sorex minutus 2 1 0.82 14 9 4.31 x 0.5 0.5Rhinolophus gr. euryale-mehelyi 9 4 3.28 0 0 0.00 x 0.75 0.25Myotis gr. myotis-blythii 1 1 0.82 0 0 0.00 x 0.75 0.25Myotis sp. 8 4 3.28 1 1 0.48 x 0.75 0.25Plecotus gr. auritus-austriacus 8 4 3.28 0 0 0.00 x 0.25 0.25 0.5Pipistrellus pipistrellus 1 1 0.82 1 1 0.48 x 0.5 0.5Chionomys nivalis 19 9 7.3 0 0 0.00 x 1Microtus arvalis 5 3 2.46 0 0 0.00 x 0.5 0.5Microtus (Iberomys) cabrerae 0 0 0 13 7 3.35 x 0.5 0.5Microtus (Terricola) duodecimcostatus 0 0 0 4 2 0.96 x 0.5 0.5Arvicola sapidus 0 0 0 1 1 0.48 x 1Apodemus sylvaticus 18 9 7.38 238 119 56.94 x 1Mus spretus 0 0 0 2 1 0.48 x 0.5 0.25 0.25Rattus rattus 0 0 0 1 1 0.48 x 1Eliomys quercinus 67 33 27.05 2 1 0.48 x 0.5 0.5Glis glis 0 0 0 1 1 0.48 x 1Sciurus vulgaris 0 0 0 1 1 0.48 x 1Total 122 100 2067 209 100 4.78 4 13.3 5.28 2.7

OD, open dry; OH, open humid; Wo, woodland/woodland-edge; Ro, rocky; Wa, water; C1, chorotype 1; C2, chorotype 2; C3, chorotype 3; C4,chorotype 4. An ‘x’ represents the relationship between chorotypes and taxa. The rows of dashes indicate that these taxa could not be classified tochorotype and habitat level.



with Cuenca-Besco�s et al., 2005; Blain et al., 2008a; Lo�pez-Garcıa et al., 2010a). These types are detailed as follows(Table 2): open dry, meadows under seasonal climate change;open humid, evergreen meadows with dense pastures andsuitable topsoil; woodland, mature forest, including wood-land margins and forest patches, with moderate ground cover;water, areas along streams, lakes and ponds; and rocky, areaswith a suitable rocky or stony substratum. The Chorotypes 1and 2 (C1 & C2) and Chorotype 3 (C3) data were obtainedfrom the percentage representation of the MNI by classifyingour taxa according to chorotypes established by Sans-Fuentesand Ventura (2000) and Lo�pez-Garcıa et al. (2010b). Thesechorotypes are detailed as follows (Table 2): chorotype 1includes species with mid-European requirements, with meansummer temperatures lower than 20 ˚C, mean annual temper-atures (MAT) between 10 and 12 ˚C and mean annualprecipitation (MAP) higher than 800mm; chorotype 2 in-cludes mid-European species tolerant of Mediterranean con-ditions, with a broader distribution in Catalonia than those ofchorotype 1, with MAP higher than 600mm; chorotype 3includes strictly Mediterranean species, with a distributionrange that covers lower altitudes than the Pyrenees and pre-Pyrenees mountain range; and chorotype 4 includes specieswithout very strict requirements, and with a broad distributionin Catalonia.

Palaeoclimatic reconstruction

Climatically, the Iberian Peninsula may be considered aminicontinent due to its large latitudinal range (between

36˚N and 44˚N), its geographical position between Atlantic(temperate-cool) and African–Mediterranean (temperate-warm or subtropical) influences, and its complex topography.The Iberian Peninsula is one of the most mountainous areasin Europe and these mountains play a major role in thecharacterization of its climatic diversity. As a result, thetaxonomic composition of an assemblage allows us toevaluate the climatic conditions that prevailed at a givenlocation. To assess the palaeoclimatic data for the GallsCarboners cave, we evaluate the current distribution of all thetaxa found there, permitting us to calculate the potentialpalaeoclimatic conditions at the site [mutual climatic rangemethod (MCR), in accordance with Blain et al., 2009]. Onthe basis of the distribution of the extant Iberian fauna, wesimply identify the geographical region where all the speciespresent in a given stratigraphical level currently live. Becauseour sources for the distribution of the small-vertebrate taxa(Pleguezuelos et al., 2004; Palomo and Gisbert, 2005) arebased on a 10�10-km UTM network, the climatic data areresolved to 10� 10-km UTM squares. Several climatic factorsare estimated: MAT, mean temperature of the coldest month(MTC), mean temperature of the warmest month (MTW) andMAP, using various climatic maps of Spain (Font-Tullot,2000) and data provided by the network of Catalonianmeteorological research stations over a period of 30 years.From this variably sized region we can estimate the climaticparameters and compare them with the modern climatic dataobtained from Ninyerola et al. (2003). For the area aroundthe Galls Carboners cave these current data show an MAT of11.5 ˚C, an MTC of 4.5 ˚C, an MTW of 19.5 ˚C and an MAPof 750mm (Ninyerola et al., 2003).

Results and discussion

The age of the H3 deposits from Galls Carbonerscave

As noted above, we have a single AMS radiocarbon datefrom the critical level within the case deposits of 31 170–31 380 cal a BP (Beta-317 704) (Table 1). In the absence offurther absolute dating control, we use several other sourcesof sedimentological and biostratigraphic data to provideindependent chronological control on the age of thesedeposits. First, archaeological levels 105–108 have the samesedimentological characteristics (a series of clayey–muddyyellow deposits with occasional small clasts derived locallyfrom the cave wall), which suggests synchronous depositionof this 0.5-m-thick unit that is sealed by a stalagmitic plate(Fig. 1). Second, the small-vertebrate fossil material recovered(discussed in detail below) also corroborates the hypothesisthat this unit was deposited during a cold period (wehypothesize, H3). In particular, we note the presence of thesnow vole (Chionomys nivalis), the common vole (Microtusarvalis) and the common frog (Rana temporaria), which arespecies that today live in north-eastern Iberia in the Pyreneanregion (Sans-Fuentes and Ventura, 2000; Lo�pez-Garcıaet al., 2010b). It is notable that these species remains are notobserved in present-day samples of Strix aluco pellets(Table 2). Furthermore, previous studies show that althoughthe snow vole first appeared in the Iberian Peninsula duringthe Late Pleistocene, it became abundant after ca. 35 ka,towards the end of Marine Isotope Stage (MIS) 3 and duringMIS2 (Lo�pez-Garcıa, 2011). The abundant presence of snowvole teeth (n¼ 19, Table 1) suggests strongly that the depositis younger than 35 ka. Therefore, the rapidity of depositionof archaeological levels 105–108, which are sealed by astalagmitic plate, and the abundant remains of the snow vole

Figure 3. Some small vertebrates from Galls Carboners. (A) First leftlower molar (m1) of Microtus arvalis (occlusal view); (B) right m1 ofChionomys nivalis (occlusal view); (C) right m1 of Apodemussylvaticus (occlusal view); (D) right scapula of Bufo calamita (dorsalview); (E) male right humerus of cf. Rana temporaria (ventral andmedial views); (F) left maxilla of cf. Podarcis sp. (lateral view). Scalebars¼1mm.



and other cold-tolerant remains, provides confidence in thesingle AMS 14C age determination from this unit, placing it atthe broad time interval of H3.

Remarks on the small-vertebrate taphonomy

The number of remains recovered from each of the levels islow, especially from levels 105 and 106, so the results of thistaphonomic study of potential predators should be taken withcaution. The alterations caused by digestion found in theincisors and femurs from all the studied levels indicate thatthe accumulation of small mammals is associated withpredation.According to the categories of alteration in incisors and

femurs proposed by Andrews (1990) and Fernandez-Jalvo andAndrews (1992), the predator responsible for the accumula-tion in levels 106–108 seems to be a predator capable of‘intermediate’ modification, such as the tawny owl (Strixaluco) or the Eurasian eagle-owl (Bubo bubo) (Table 3).The alterations produced by these two predators are very

similar, although there are small differences, such as thedegree of digestion and the size of the prey consumed. Theprey consumed by B. bubo are usually larger (from rabbits tosmall deer) than those consumed by S. aluco. To distinguishthe predator, a taphonomic review of the alterations pro-duced in the leporids and ovicaprines from Galls Carbonerswas undertaken. These remains showed no physical modifi-cation (fractures or digestion) that suggested consumption byB. bubo. Thus, we think the probable accumulator of thesmall-mammal remains from levels 106–108 is the tawny owl(S. aluco).By contrast, the remains from level 105 show few tapho-

nomic alterations, indicating that the accumulator could wellbe a predator with only a slight capacity for modification,such as a barn owl (Tyto alba) (Table 3).

Both the tawny owl (S. aluco) implicated in levels 106–108and the barn owl (T. alba) identified in level 105 areopportunistic nocturnal predators. The barn owl can be foundin various habitats, being very common in rocky areasand open and semi-open forests below 1000m. a.s.l.(Mikkola, 1983; Konig et al., 1999). The tawny owl preferssemi-open forests, usually comprising hardwood and decid-uous trees, and mixed with clearings. It is also common inriparian forests, open landscapes and forests near rocky areaswith scattered trees and shrubs. The owl is a stronglyterritorial and sedentary raptor, which explains its persistenceon the Motllats during the formation of levels 108–106 aswell as today. The tawny owl does not use the abandonednests of other birds, but nests in rocky soil, in rock crevices orin tree holes (Mikkola, 1983; Konig et al., 1999).These two nocturnal predators are distributed over similar

environments, suggesting a mosaic landscape in the Pradesmountains consisting of semi-forest areas, riparian forests oropen areas near forests and large rocks. As the preferredhabitat of the two predators is very similar, it is possible toobserve significant changes in the landscape through thepredator during the formation of the successive levels of GallsCarboners. The predators identified had no preferentialcriteria in selecting the taxa they consumed. Palaeoecologicalinterpretations based on the relative abundances of small-mammal taxa thus similarly show the habitat in which preywere hunted and consumed by predators.Amphibians and squamate reptiles are rather scarce (with

the exception of small lacertids) in the fossil assemblage(Table 2). This may be explained first by the physicalcharacteristics of the entrance to the cave, which today has asignificant step (more than 3m high) and which may wellhave prevented toads and snakes from entering the cave bythemselves (though not lizards, which are well represented).It is also probable that this scarcity resulted from the dietchoice of the predators, which are nevertheless known tooccasionally include some frogs and lizards in their diet (seeMikkola, 1983).

Small-vertebrate assemblage from the GallsCarboners cave

The archaeological levels in which the small-vertebrateremains were found have the same composition and wereformed in a similarly short period. In the interpretation of ourdata, they will be treated as the same sedimentary unit.The small vertebrates from Galls Carboners comprise at

least 16 taxa: three amphibians, two squamates, two insecti-vores, five bats and four rodents (Table 2; Fig. 3).The small-mammal fossil assemblage at the Galls Carbon-

ers cave is characterized by the abundance of Eliomysquercinus. Although mid-European taxa, such as Chionomysnivalis, Microtus arvalis or Sorex minutus, are better repre-sented than Mediterranean taxa, such as Crocidura russula orRhinolophus gr. euryale-mehelyi, the representation of thetwo groups is reasonably equal. In quantitative terms, Eliomysquercinus together with Chinomys nivalis and Crocidurarussula are the best-represented species in Galls Carboners,accounting for more than 40% of the total fossil sample.Among the fossil material analysed here, E. quercinusrepresents 27.05%, C. nivalis 7.38% and C. russula 6.56% ofthe total fossil sample (Table 2). The presence of E. quercinusis common in Late Pleistocene sites, but such abundance isnot frequent (see, for example, Cuenca-Besco�s et al., 2008;Lo�pez-Garcıa, 2011; Lo�pez-Garcıa et al., 2010a, 2012a), be-cause during these generally cold periods dominant species,such as M. arvalis or M. agrestis, normally associated with

Table 3. Percentages of small-mammal elements from Galls Carbon-ers showing different degrees of digestion. Where it is not possible todetermine the degree of digestion due to the location of the fractures,the remains are considered invalid.

Femur Incisor

Degree of digestion n % n %

Level 105Absent 4 100 11 78.6Light 0 0 3 21.4

Level 106Absent 0 0 6 37.5Light 1 50 5 31.3Moderate 1 50 1 6.3Heavy 0 0 2 12.5Extreme 0 0 1 6.3Invalid 0 0 1 6.3

Level 107Absent 10 76.9 15 46.9Light 3 23.1 14 43.8Moderate 0 0 1 3.1Heavy 0 0 1 3.1Invalid 0 0 1 3.1

Level 108Absent 28 75.7 25 54.3Light 9 24.3 15 32.6Moderate 0 0 1 2.2Invalid 0 0 5 10.9

Total 56 108



open environments, tend to replace E. quercinus. Today,however, E. quercinus is very abundant throughout Spain. Itis a generalist species, but its greatest abundance is currentlyreported to be in woodland-edge/woodland and rocky hab-itats (Palomo and Gisbert, 2005). The snow vole (Chionomysnivalis) appeared in the Iberian Peninsula during the LatePleistocene. Its first record is from Camino Cave, dated to74.5 ka (Laplana et al., 2013). During the Late Pleistocene itwas widely distributed in Iberia (Lo�pez-Garcıa, 2011). C.nivalis is adapted to rocky accumulations and nowadays is arelict species found only in the main mountain ranges of theIberian Peninsula (Palomo and Gisbert, 2005). Crocidurarussula is common in Late Pleistocene sites, but suchabundance is rare in Late Pleistocene cave localities (Lo�pez-Garcıa, 2011). It is today a generalist species with Mediterra-nean requirements (Palomo and Gisbert, 2005).When comparing the small-mammal fossil assemblage with

the modern Strix aluco pellets, the modern material ischaracterized by the abundance of Apodemus sylvaticus.Mediterranean taxa, such as Crocidura russula, Microtus(Iberomys) cabrerae or Suncus etruscus, are dominant,although species associated with mid-European requirementsand tolerant of Mediterranean conditions, such as Sorexminutus, are also well represented. In quantitative terms,Apodemus sylvaticus is the best-represented species in theStrix aluco pellets, accounting for more than 50% of the totalsample (Table 2). Like E. quercinus in the fossil record ofGalls Carboners, A. sylvaticus is a generalist species currentlyreported to inhabit woodland-edge/woodland habitats (Pal-omo and Gisbert, 2005).Regarding amphibians and squamates, the fossil assem-

blage is very poor and characterized by a low diversity.When compared with the modern sample, it is surprising thatthere is no snake represented in the fossil sample. Thepresence of Bufo calamita in the fossil sample is alsonotable, as today predators usually avoid consuming toads.The probable presence of Rana temporaria, represented by amale right humerus in level 105, may be related to the colderclimate during H3. During the cold periods of the Pleistocenethis frog appears in localities situated at lower altitudes orslightly to the south of its current distribution in northernSpain (Blain et al., 2008b; Blain, 2009). In this respect, if thepresence of Rana temporaria is confirmed in Galls Carboners,this may constitute its southernmost record in Catalonia andin the Iberian Peninsula.

Changes in biodiversity

Simpson’s evenness index shows that, although the numberof species is lower in the fossil assemblage (n¼ 16) than inthe present-day Strix aluco pellets (n¼24), the evenness ishigher during H3 (1–D¼0.8267) than today (1–D¼ 0.6517).This phenomenon is explained by the fact that although thereis a larger number of species recovered from the modernpellets, there is one species that dominates (Apodemussylvaticus; 56.94%) the others, whereas in the fossil materialthere are fewer species, but these are more evenly repre-sented (Eliomys quercinus, 27.05%, cf. Podarcis sp., 27.87%)(Table 2). Climate has been considered the overriding factorinfluencing changes in diversity (e.g. Blois et al., 2010;Lo�pez-Garcıa et al., 2013b, among others). As has recentlybeen argued for the latest Pleistocene (LGM and H1) of theIberian Peninsula by Lo�pez-Garcıa et al. (2013b), small-vertebrate communities are highly even during relatively coldand humid periods. It thus seems consistent that speciesdiversity was greater during H3 than currently in the GallsCarboners cave.

Palaeoenvironmental and palaeoclimaticreconstruction

The resulting intersection for the Galls Carboners cave,located in the central–north Iberian mountain ranges, suggeststhat MAT during H3 was lower than at present (–3.72 ˚C) andMAP was higher than at present (þ437mm). MTC was lowerthan the current mean (–3.77 ˚C), as was MTW (–2.2 ˚C)(Tables 4 and 5). These data suggest harsher and more humidclimatic conditions for the H3 event in northeastern Iberiathan at present. The data are well supported by the presenceof taxa such as Microtus arvalis, Chionomys nivalis andcf. Rana temporaria at the Galls Carboners cave, whichcurrently live in mountain areas where MAT is lower than11˚C and MAP higher than 700–800mm (Sans-Fuentes andVentura, 2000; Lo�pez-Garcıa et al., 2010b; Rivera et al.,2011), and by the presence of Pyrrhocorax graculus, a birdbelonging to the crow family that currently breeds at above900–1000m in the Iberian Peninsula. According to the data

Table 4. Relationships between temperature and precipitation.

Event n Mean Max. Min. SD

Galls Carboners H3 eventMAT (˚C) 37 7.78 10 4 1.8MTW (˚C) 37 17.03 22 14 2MTC(˚C) 37 0.73 4 –1 1.3MAP (mm) 37 1162 2000 700 337

Present-day Strix aluco pelletsMAT (˚C) 27 11.74 15 8 1.9MTW (˚C) 27 19.81 23 16 2.1MTC (˚C) 27 3.3 6 0 1.8MAP(mm) 27 868.5 1250 600 187

MAT, mean annual temperature; MTC, mean temperature of coldestmonth; MTW, mean temperature of warmest month; MAP, meanannual precipitation; n, number of intersection points; Max., maxi-mum of values obtained; Min., minimum of values obtained; Mean,mean of values obtained; SD, standard deviation of values obtained.

Table 5. Average difference between the current mean temperatureand precipitation over 30 years (data from Font-Tullot, 2000) and thedata obtained for small vertebrates.

Event and siteDMAT(˚C)

DMTC(˚C)

DMTW(˚C)

DMAP(mm)

LGM eventValdavara1 (VLU) –0.5 –3.7 1.4 90Portalon P1 –2.3 –0.1 0.9 378Arbreda C –4.6 –4.3 –4.2 309Arbreda D –4.6 –4.3 –4.2 309Arbreda E –4.6 –4.3 –4.2 309MTV-Chimeneas –3.7 –1.1 –7.2 712H3 eventGalls Carboners –3.72 –3.77 –2.2 437H4 eventCanyars –5.19 –4.5 –6.08 98.6N20b –1.1 –2.1 –0.3 465H5 eventXaragalls C4 –5.4 –2.75 –2 296Romanı E –5.7 –5.5 –7.11 148Gegant III –5.3 –5.3 –1.7 350

MAT, mean annual temperature; MTW, mean temperature of warm-est month; MTC, mean temperature of coldest month; MAP, meanannual precipitation.



obtained by Cayre et al. (1999), Andersen et al. (2006) andCacho et al. (2006) for the NorthGRIP and Alboran Seamarine surveys, the fluctuation detected in the Galls Carbon-ers cave by means of small-vertebrate analyses may correlatewith the first phase of the H3 event, characterized by thefirst reduction in the marine surface temperature, asindicated by a rise in percentages of N. pachyderma, thefirst arrival of IRD, the relatively high percentages of Euro-Siberian trees, such as deciduous Quercus and Ericaceae, aswell as the end of the previous temperate and humidterrestrial phase. By contrast, the intersection calculatedon the basis of the Strix aluco pellet material inside theGalls Carboners cave (Table 4) suggests MAT, MAP, MTCand MTW similar to the present day in the area(MATpellets¼ 11.74� 1.9 ˚C; MATat present¼11.5 ˚C, MAPpellets¼858.5�187mm; MAPat present¼750mm, MTCpellets¼3.3�1.8 ˚C; MTCat present¼ 4.5 ˚C, MTWpellets¼ 19.81� 2.1 ˚C;MTWat present¼ 19.5 ˚C, current data from Ninyerola et al.,2003). These data support the conclusion that the method usedfor palaeoclimatic reconstruction on the basis of the small-vertebrate assemblage is valid for the fossils from Galls Carbon-ers cave.The small-vertebrate fossil assemblage from Galls Carboners

cave indicates a woodland environment (50%) (Fig. 4), giventhe presence of Eliomys quercinus, Apodemus sylvaticus andbats in general. It further suggests a landscape alternatingbetween woodland and rocky-dry meadows. Species associatedwith ‘open dry’ and ‘rocky’ habitats represent 45% of the totalassociation (Fig. 4), mainly composed of Bufo calamita,Crocidura russula, Microtus arvalis and Chionomys nivalis.These data are also supported by the presence of Pyrrhocoraxgraculus, a species associated with rocky and open areas inhigh mountain regions. There is also a low percentagerepresentation of species associated with open humid meadows(4%) and water streams (1%) (Fig. 4), suggesting the existenceof stable watercourses near the site, with riverbanks with loosesoils favourable for digging species, such as Alytes obstetricans

and Sorex minutus. This trend towards increasing aridity isobserved in marine surveys (NorthGRIP and the Alboran Sea)in the first phase of the H3 event (Cayre et al., 1999; Andersenet al., 2006; Cacho et al., 2006). In comparison, the present-day data obtained from the small-vertebrate assemblage fromStrix aluco pellets show a woodland environment to bepredominant (74%) (Fig. 4), mainly indicated by the predomi-nance of Apodemus sylvaticus. There is also a low percentagerepresentation of species associated with open humid meadows(12%), open dry meadows (8%), rocky areas (2%) and waterstreams (4%) (Fig. 4). The data obtained from small-vertebratepellets are consistent with the landscape currently representedin the Prades mountain range in the immediate vicinity of thecave, where the predominant vegetation is oak forest, asclerophyll forest dominated by oaks in the tree layer, but withabundant shrubs and lianas. By contrast, there is little herba-ceous vegetation, due to the permanent shadow generated bythe upper vegetation layers (Domingo and Borau, 1998).Finally, the small-vertebrate fossil assemblage from Galls

Carboners cave is dominated by taxa associated with mid-European requirements (chorotypes 1 and 2; 55%), but with ahigh percentage representation of taxa with Mediterraneanrequirements (chorotype 3; 45%) (Fig. 4). According to Sommerand Nadachowski (2006), the co-occurrence of temperate andcold-adapted species is the normal dynamic detected in southEuropean peninsulas, such as the Iberian Peninsula, whichfunctioned as refugia for species in cold periods, here duringthe H3 event. By contrast, the current small-vertebrate assem-blage from Strix aluco pellets shows the dominant taxa to bespecies with Mediterranean requirements (chorotype 3; 57%),though with a relatively high representation of mid-Europeantaxa tolerant of Mediterranean conditions (chorotype 2; 43%)(Fig. 4). These results are consistent, taking into account thelocation of the cave at 965m a.s.l. and the current MAP ofabout 750mm (Ninyerola et al., 2003). Such conditions aresuitable for species such as Alytes obstetricans, Pelodytespunctatus, Anguis fragilis, Sorex minutus and Glis glis, whichneed an MAP higher than 600mm (Sans-Fuentes andVentura, 2000; Lo�pez-Garcıa et al., 2010b).

Comparison with previous (H5 and H4) andsubsequent (LGM) cold climatic events

There are no others sites in the Iberian Peninsula where theH3 event has been detected based on small-vertebrateassemblages. However, we compared the H3 event detectedin the Galls Carboners cave with the previous H4 and H5events documented by small-vertebrate assemblages in: Covadel Gegant level III (Sitges, Barcelona), Abric Romanı level E(Capellades, Barcelona) and the Xaragalls cave level C4(Vimbodı-Poblet, Tarragona) in the case of the H5 event; andCueva del Conde level N20b (Santo Adriano, Asturias) andthe Canyars site (Gava, Barcelona) in the case of the H4event. We also compared it with the subsequent LGMdetected in the Iberian Peninsula using small-vertebrateassemblages in Maltravieso-Chimeneas level A (Caceres,Extemadura), l’Arbreda cave levels E–C (Serinya, Girona), ElPortalo�n level P1 (Sierra de Atapuerca, Burgos) and theValdavara-1 cave lower unit (Becerrea, Lugo) (Fig. 1) (Lo�pez-Garcıa and Cuenca-Besco�s, 2010; Ba~nuls-Cardona et al.,2012; Burjachs et al., 2012; Lo�pez-Garcıa et al., 2010a,2011a,b; 2012b,c, 2013a,b). In general, all these sitesassociated with cold climatic fluctuations are characterizedby MAT, MTC and MTW that are lower than at present, andMAP that is higher than at present (Table 5; Fig. 5). However,at those sites located in the Atlantic climatic domain, such asCueva del Conde, El Portalo�n and Valdavara-1, MAT, MTC,

Figure 4. Small-vertebrate association by habitats and chorotypes.Above: data from H3 event levels; below: data from modern Strixaluco pellets. Data have been taken from the percentage of theminimum number of individuals.



MTW and MAP are more similar to today’s in comparisonwith sites under the Mediterranean climatic influence(Table 5; Fig. 5).In general, studies of the sea core (Alboran Sea, marine

core MD95-2043) from the Iberian margin show the HeinrichEvents, including the H3 event, to have been characterizedby low sea-surface temperatures (SSTs), with values 7–10 ˚Clower than at present and climates on land drier than today,whereas the LGM was characterized by somewhat humidconditions in the Mediterranean region that further distinguishit from the Heinrich Events (Cacho et al., 1999; Sanchez-Go~ni et al., 2002; Sanchez-Go~ni and d’Errico, 2005; Sierroet al., 2005; Fletcher and Sanchez-Go~ni, 2008). Despite thesegeneral data, there are differences both between the variousHeinrich Events as well as the LGM and within them.According to Cacho et al. (1999) and Sierro et al. (2005), theH3 event is the least cold in comparison with the H4 and H5events and shows similar fluctuations to the LGM. Excludingthe sites under the Atlantic climatic influence (Cueva delConde, El Portalo�n and Valdavara-1), the data obtainedwith small-vertebrate studies for the H3 event, the H4 andH5 events, and the LGM (Lo�pez-Garcıa and Cuenca-Besco�s, 2010; Ba~nuls-Cardona et al., 2012; Burjachset al., 2012; Lo�pez-Garcıa et al., 2010a, 2011a,b, 2012a,b, 2013a,b) seem to follow the same pattern as the previouslyestablished sea-core studies in the NorthGRIP and at theIberian margin (Alboran Sea, marine core MD95-2043)(Fig. 5). These small-vertebrate studies show that the fluctua-

tions in MAT, MTC, MTW and MAP for the H5–H3 eventsand the LGM follow the same pattern as the curve extrapolat-ed for the Alboran Sea (Cacho et al., 2006) (Fig. 5), withminimum MAT values in the H5 event in Cova del Gegantlevel III, Abric Romanı level E and Xaragalls level C4(MAT¼ –5.7 to –5.4 ˚C, in relation to present) and in the H4event at Canyars (MAT¼ –5.19 ˚C, in relation to present)(Lo�pez-Garcıa and Cuenca-Besco�s, 2010; Burjachs et al.,2012; Lo�pez-Garcıa et al., 2012a,b, 2013a) (Table 5). As hasbeen pointed out by Cacho et al. (1999) and Sierro et al.(2005), however, small-vertebrate studies show less harshvalues for the H3 event and the LGM than the H4 and H5events, with MAT¼ –3.75 ˚C (in relation to present) for theH3 event detected in the Galls Carboners cave and MAT¼–4.6 to –3.7 ˚C (in relation to present) for the LGM detectedin Maltravieso-Chimeneas level A and l’Arbreda cave levels Eand D (Lo�pez-Garcıa and Cuenca-Besco�s, 2010; Ba~nuls-Cardona et al., 2012) (Table 5).

Conclusions

The data derived from the small vertebrates recovered fromthe Galls Carboners cave add significantly to our knowledgeof the H3 event in the Iberian Peninsula. The small-vertebrateassemblage reveals that the H3 event was characterized innorth-eastern Iberia by cool climatic conditions, with alandscape alternating between woodland and dry meadow-land. This assemblage is dominated by mid-European taxa

Figure 5. Approximate correlation between the average (D) mean annual temperature (MAT), mean temperature of coldest month (MTC), meantemperature of warmest month (MTW) and mean annual precipitation (MAP) obtained with small-vertebrate assemblages of the studied sites and theNorthGRIP isotope oxygen curve and the Alboran sea surface temperatures. H, Heinrich Events, LGM, Late Glacial Maximum; G, Gegant level III;AR, Abric Romanı; X, Xaragalls level C4; C, Cueva del Conde level N20b; Arb, l’Arbreda cave; TC, Canyars; GC, Galls Carboners; MTV-CH,Maltavieso-Chimeneas; P, El Portalo�n level P1; Val, Valdavara 1 lower unit.



together with a high percentage representation of Mediterra-nean taxa, a co-occurrence that represents the normaldynamic detected in south European peninsulas, whichfunctioned as refuges for species during cold periods.Secondly, direct comparison of the data obtained from the

small-vertebrate association from Galls Carboners with thoseobtained from present-day Strix aluco pellets recovered insidethe cave shows that the climate during the H3 event wascooler and drier than today in the north-eastern IberianPeninsula.Finally, comparison with other small-vertebrate studies

from sites in the Iberian Peninsula where the previous H5 andH4 events and the subsequent LGM have been detectedsuggests that the H3 event was warmer than the H4 and H5events, and shows similar fluctuations to the LGM, aspreviously indicated by studies undertaken for the Iberianmargin and NorthGRIP cores.

Acknowledgements. We thank Dr Rosa Huguet, Dr Palmira Saladie,Dr Andreu Olle, Amelia Bargallo�, Ivan Lozano and Maria Soto for theiraid in transporting the Galls Carboners cave sediments, and Dr AndreuOlle and Amelia Bargallo� for their aid during the excavationcampaigns. We also thank the editor (Professot Antony Long) andthe reviewers (Professor John R. Stewart and Anonymous) for theircomments that improved the final version of this manuscript. J.M.L.-G.is a beneficiary of a Beatriu de Pino�s postdoctoral fellowship (2011 BP-A00272) from the Generalitat de Catalunya, a grant cofunded by theEuropean Union through the Marie Curie Actions of the 7th Frame-work Program for RþD. J.I.M. was supported by a predoctoral grant(FI) from AGAUR (Generalitat de Catalunya) cofunded by theEuropean Social Fund. This paper is part of projects CGL2012-38358 and SGR2009-324.

Abbreviations. AMS, accelerator mass spectrometry; H3, HeinrichEvent 3; LGM, Last Glacial Maximum; MAP, mean annual precipita-tion; MAT, mean annual temperature; MIS, Marine Isotope Stage;MNI, minimum-number-of-individuals; MTC, mean temperature of thecoldest month; MTW, mean temperature of the warmest month.

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Climate and landscape during Heinrich Event 3 in south-western Europe: the small-vertebrate...

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