Human impact on small-mammal diversity during the middle- to late-Holocene in Iberia: The case of El Mirador cave (Sierra de Atapuerca,Burgos,Spain)

Abstract

The human impact on the environment in the Holocene has usually been characterized on the basis of palaeobotanical records, but attempts to distinguish the anthropogenic impact from natural events in landscape evolution have been the subject of much debate in recent years. The aim of this paper is to analyse small-mammal diversity and the presence of synanthropic species, whose small size makes them more sensitive to any changes in their environment that may occur. This study has allowed us to characterize palaeoclimatic and palaeoenvironmental changes, recording small changes whether resulting from a human influence or otherwise. Our object of study is El Mirador cave, which has a sequence with a well-documented human occupation extending from 7200 to 3000 cal. BP. The study has led us to differentiate two phases. In one phase, we can see small changes in diversity related to climatic oscillations from ca. 7200 to 6800 cal. BP, while in the second phase, lasting from ca. 6800 to 3000 cal. BP, the changes in diversity and in the assemblage of synanthropic species are associated with human economic strategies. Moreover, we distinguish which kinds of economic activity (crop and livestock farming) have influenced these changes, because some small-mammal species are influenced, positively or negatively, by environmental changes based on crop farming and animal husbandry. All this information is contrasted with other archaeological proxies, such as the large-mammal and palaeobotanical assemblages from El Mirador cave. Furthermore, this integrative analysis has made it possible to identify the existence of altered environments more generally throughout the Iberian Peninsula from ca. 6000 cal. BP. It additionally confirms the theory of low human occupation intensity in the northern Meseta and in high mountainous areas during the early Neolithic.

Keywords

anthropogenic impact Bronze Age diversity Neolithic paleoclimate palaeoenvironment small mammals

Introduction

The climate during the Holocene was warm and wet with some arid episodes, but with many regional differences of which we know their reach across Europe (Aranbarri et al., 2014; Bond et al., 1997; Davis et al., 2003; Jalut et al., 2009; Kalis et al., 2003; Mayewski et al., 2004; Mercuri et al., 2011). All these climatic characteristics contributed to modifying the landscape, but so did the human use of the territory for economic purposes (Heinz et al., 2004; Morales-Molino et al., 2011; Pérez-Díaz et al., 2015; Tarroso et al., 2014). In fact, human disturbances have been considered the major agent of vegetation change in the Iberian Peninsula for at least the last 7500 years (Pérez-Obiol et al., 2011).

El Mirador is situated in the northwest of the Iberian Peninsula where the climate is typically Mediterranean, whereas in the northern areas variability is primarily in tune with central European climatic oscillations (Rivas-Martínez et al., 2011). In this area, the palaeoecological studies have registered the influence of anthropogenic activity on natural vegetation for ca. 6000 years (Iriarte, 2009; Tarroso et al., 2014). This influence has continuously increased over several millennia of human occupation of these environments, with the resulting fire and grazing pressure (López-Merino et al., 2012; Morales-Molino et al., 2011; Santos et al., 2000).

In this study, we have included the small mammals’ samples and the environmental (habitat weighting) and climatic (mutual ecogeographic range (MER)) conditions exposed in Bañuls-Cardona et al. (in preparation), to analyse the relationship between natural (environmental and climatic) and anthropic influences on the changes in small mammals’ diversity. The activities associated with an economy based on agriculture and livestock farming are known to contribute to modifying and homogenizing the landscape, influencing the ethology of small mammals and resulting in the changes in biodiversity (Barnosky et al., 2011; Benton et al., 2003; Torres-Romero and Olalla-Tárraga, 2014). In El Mirador cave (northern Meseta of Iberia), various archaeobotanical and archaeological proxies have been analysed to try to ascertain the difference between the anthropic and the natural origin of the landscape changes that took place during the Holocene (Cabanes et al., 2009; Euba et al., 2016; Expósito and Burjachs, 2016; Martín et al., 2014, 2016a, 2016b; Rodríguez et al., 2016).

Site

El Mirador cave is situated in the south of the Sierra de Atapuerca (Burgos, Spain). The site is located at an altitude of 1033 m a.s.l. (Figure 1). It was in 1999 that work was started on it, with the excavation of an area of 6 m² in the central part of the cave, on the basis of which the stratigraphic sequence was established. This is composed of a total of 26 layers displaying high lateral and vertical variability because of the sedimentary characteristics of the cave and the post-depositional processes that took place there, such as the collapse of blocks and anthropic spatial organization, as well as bioturbation (Figure 1). For this reason, it was decided that the naming and excavation of the site should be in assemblages, distinguishing between the characteristic facies of the anthropized units, mainly consisting of burned and unburned dung (Vergès et al., 2002, 2008). Most of these layers have been dated. There are a total of 17 radiocarbon dates for the sequence of El Mirador cave, which range from the latest Pleistocene to the Bronze Age (Angelucci et al., 2009; Vergès et al., 2002, 2016; Figure 2).

Figure 1.

(a) Geographical location of El Mirador cave and the sites mentioned in the discussion. 1. Peña Larga; 2. Padre Areso; 3. Puy Águila I; 4. Coto da Fenteria; 5. Arcucelos; 6. Basa de la Mora; 7. Tolla Collado de El Berrueco; 8. Rascafría; 9. Espinosa de Cerrato; 10. El Carrizal; 11. Sierra de Gádor; 12. Sierra de Baza; 13. Siles lake; 14. Cova de les Cendres; 15. Cova de l’Or; 16. Cova Colomera; 17. El Mirón; 18. Valdavara. (b) Stratigraphy of El Mirador cave (Angelucci et al., 2009). (c) Radiocarbon datings of studied layers. Uncal: mean of the radiocarbon dates. CalBP: 2σ range of the calibrated dates in cal BP.

Figure 2.

Most representative species of El Mirador cave. From left to right: 1. Crocidura russula, right mandible (lingual and posterior view) and right m2 (occlusal view); 2. Apodemus sylvaticus, right m1 (occlusal view); 3. Microtus arvalis, right m1 (occlusal view); 4. Microtus agrestis, left m1 (occlusal view); 5. Microtus (Terricola) duodecimcostatus, right m1 (occlusal view). Scale bars = 1 mm.

The Pleistocene deposit is composed of 14 m of metric and decimetric limestone blocks with no sedimentary matrix in between. It is the result of the collapsed roof (MIR51/4 and MIR51/1) and contains two intercalated layers: MIR51/3, a shallow, archaeologically sterile layer composed of wind-borne sediment, and MIR51/2, with the same sedimentary characteristics but with evidence of human activity: remains of a hearth, and lithic and faunal materials (Vergès et al., 2016). The 6-m-thick Holocene sedimentary layers rest directly on top of MIR51. Four metres are attributed to Neolithic occupations (layers MIR24–MIR6) occurring between the last third of the sixth millennium and the first half of the fourth millennium cal BC (Vergès et al., 2008), while the remaining 2 m are from the Middle Bronze Age (MIR4 and MIR3A), between the second and fourth quarters of the second millennium cal. BC (Vergès et al., 2002). These Holocene layers were essentially formed as a result of the use of the cave as a livestock pen. The activities related to animal husbandry left sedimentary layers of dung, which was piled together and burned at regular intervals to reduce its volume and to eliminate parasites (Angelucci et al., 2009). These burned layers alternate with partially burned and unburned layers of dung and nodules of ash from burned dung. An artefact record related to domestic occupations is often present in these layers. This kind of deposit is known as a fumier (Brochier, 1988; Vergès et al., 2016).

Archaeological remains are abundant in this site, and many specific studies are available in the literature. These include analyses of ceramic and lithic artefacts (Vergès et al., 2002, 2008, 2016), archaeobotanical studies (Cabanes et al., 2009; Euba et al., 2016; Expósito and Burjachs, 2016; Rodríguez et al., 2016), studies of human remains (Cáceres et al., 2007; Ceperuelo et al., 2015; Lozano et al., 2015) and of large mammals (Martín et al., 2009, 2014, 2016a, 2016b), and also preliminary studies of small-mammal remains (Bañuls-Cardona et al., 2013; López-García, 2008).

Material and methods

Small mammals

The small mammals analysed in this study belong to 14 Holocene layers (MIR24, MIR23, MIR22, MIR21, MIR19, MIR18, MIR17, MIR16, MIR11, MIR10, MIR9, MIR6, MIR5 and MIR4). These small mammals were identified using the methods of systematic palaeontology from Bañuls-Cardona et al. (in preparation). We used mandibles and isolated teeth to identify insectivores (Cuenca-Bescós et al., 2008; López-García, 2008; Reumer, 1984); for chiropters, mandibles, isolated teeth and humeri (Bruijn and Rumke, 1974; Menu and Popelard, 1987; Sevilla, 1988); for Arvicolinae, the first lower molars (Cuenca-Bescós et al., 2008; López-García, 2008; Van der Meulen, 1973); while the identification of Apodemus sylvaticus and Eliomys quercinus was based on isolated teeth (Cuenca-Bescós et al., 2008; Damms, 1981; López-García, 2008; Pasquier, 1974).

In this manuscript, we describe the sample of small mammals that is the subject of this study; we start from the premise that all ecosystems are described in terms of the number of individuals of each species represented (Margalef, 1972). The first method that we apply in this basic analysis of biodiversity is Chao-1 (Colwell and Coddington, 1994). This method consists of a simple estimator of the richness in an assemblage.

S_{C h a o 1} = S_{o b s} + \frac{F_{1}^{2}}{2 F_{2}}

$S_{o b s}$ is the number of species in the sample, $F_{1}$ is the number of observed species represented by a single individual and $F_{2}$ is the number of observed species represented by two individuals.

Measurement of species diversity is based on the Simpson index, which emphasizes dominance as opposed to richness in assessing the development and evolution of an ecosystem (Magurran, 2004).

D = \sum^{​} (\frac{n_{i [n_{i} - 1]}}{N [N - 1]})

$n_{i}$ is the number of individuals in the i species and N is the total number of individuals.

We further analyse the percentage of synanthropic species, that is, species that are adapted to conditions created or modified by human activities (Mistrot, 2000). The synanthropization of indigenous small mammals was considered to be a recent phenomenon in European mammals. However, the recent studies show that is readily observable during the late Neolithic in southeastern Europe, and perhaps before (Cucchi et al., 2011). Within our assemblage, there are four: Crocidura russula, Microtus arvalis, Microtus (Terricola) duodecimcostatus and E. quercinus (Table 2). C. russula favours human-inhabited areas because its winter survival depends on heat and nutritive resources generated by human activities (Tarjuelo Mostajo et al., 2010). M. arvalis prefers landscapes with high percentage of arable land and low habitat diversity (Burel et al., 2004; Fischer et al., 2011). M.(T) duodecimcostatus selects open environments, often in human-inhabited areas. It is common in growing areas and pastures and fallow land, as long as there is sufficient grass cover and easy excavability (Campos Marcos et al., 2003). Finally, E. quercinus can live in many terrestrial and arboreal habitats and also be found close to rural homes, on roofs or on stone walls between cultures and is a semi-commensal species (Pokines, 1998).

Chorotypes

This palaeoclimatic reconstruction is completed by classifying the taxa in accordance with the chorotypes established by Sans-Fuentes and Ventura (2000), Real et al. (2003) and López-García et al. (2010b). A chorotype can be defined as a group of species whose distributions in space overlap more than expected at random. Chorotype 1 (CH-1) refers to species with Euro-Siberian requirements; this implies a mean summer temperature lower than 20°C, a mean annual temperature (MAT) that should be between 10°C and 12°C and a mean annual precipitation (MAP) higher than 800 mm. Chorotype 2 (CH-2) refers to Euro-Siberian species that nonetheless tolerate Mediterranean conditions, with a MAP greater than 600 mm. Chorotype 3 (CH-3) denotes generalist species, and finally Chorotype 4 (CH-4) denotes species with strictly Mediterranean requirements (Table 3).

Results

Small mammals

We have identified 1666 remains (number of identified specimens (NISP)), with a minimum number of individuals (MNI) of 888 pertaining to nine small-mammal taxa: two insectivore, two chiropter and five rodent species (Table 1).

Table 1.

Distribution of the small-mammal remains of El Mirador cave by layers.

Taxa	MIR4	MIR5	MIR6	MIR9	MIR10	MIR11	MIR16	MIR17	MIR18	MIR19	MIR21	MIR22	MIR23	MIR24
Crocidura russula	19	6	0	17	0	1	2	16	21	6	0	1	0	8
Sorex coronatus-araneus	6	4	1	5	1	1	0	9	21	4	0	0	0	3
Myotis myotis-blythii	0	0	0	2	1	0	0	0	3	0	0	0	0	4
Miniopterus schreibersii	0	0	0	2	0	0	0	0	1	1	0	2	0	2
Microtus arvalis	21	20	3	3	1	1	2	18	16	9	1	2	0	22
Microtus agrestis	14	37	3	13	2	0	2	34	26	22	1	0	3	15
Microtus (Terricola) duodecimcostatus	17	14	2	1	3	5	2	18	21	11	2	2	4	24
Apodemus sylvaticus	18	8	2	9	6	8	4	32	73	58	4	5	2	56
Eliomys quercinus	1	0	0	1	0	1	1	1	3	6	1	0	1	0
Total MNI	96	89	11	53	14	17	13	128	185	117	9	12	10	134
Total NISP	280	193	17	77	19	19	14	230	376	154	17	15	15	240

MNI: minimum number of individuals; NISP: number of identified specimens.

The preliminary taphonomic study of the small mammals presents slight signs of digestion on the remains. These slight alterations were examined and it can be surmised that the main animal responsible for the accumulation in the cave was a category 1 predator, a nocturnal bird of prey such as the barn owl (Tyto alba) or the long-eared owl (Asio otus), both species are present in semi-open forests, with the nearby presence of large clear areas that display an opportunistic trophic pattern and produce slight modifications of the bones it ingests (Andrews, 2006). The small mammals form an assemblage of great taxonomic variety, indicating that it was the work of an opportunistic hunter.

Systematic palaeontology allowed nine different species to be identified: C. russula, Sorex gr. coronatus-araneus, Myotis myotis-blythii, Miniopterus schreibersii, M. arvalis, Microtus agrestis, M.(T) duodecimcostatus, A. sylvaticus and E. quercinus (Figure 2). The most abundant species in the sequence of El Mirador is A. sylvaticus (Table 3).

The Chao-1 analysis of diversity indicates that the highest number of species is in MIR18 and MIR9, with nine species each, whereas the lowest number of species is registered in MIR23, with four species. The Simpson index indicates that the greatest diversity is in MIR11 (0.68), MIR19 (0.70) and MIR23 (0.70), whereas the lowest diversity is recorded in MIR4 (0.82) and MIR17 (0.81). Moreover, the lowest percentage of synanthropic species is detected in MIR19 (27.4%) and MIR10 (28.6%), while the highest percentage is registered in MIR4 (60.4%) and MIR16 (53.8%) (Table 2).

Table 2.

Richness and diversity index and percentage representation of synanthropic species (Crocidura russula, Microtus arvalis, Microtus (Terricola) duodecimcostatus and Eliomys quercinus) obtained from small-mammal remains of El Mirador cave by layers.

Layers	MIR4	MIR5	MIR6	MIR9	MIR10	MIR11	MIR16	MIR17	MIR18	MIR19	MIR21	MIR22	MIR23	MIR24
Chao-1	7	6	5	9	6	6	6	7	9	8	5	5	4	8
Simpson_1-D	0.82	0.74	0.78	0.79	0.73	0.68	0.80	0.81	0.78	0.70	0.72	0.74	0.70	0.75
Synanthropic	60.42	44.94	45.45	41.51	28.57	47.06	53.85	41.41	32.97	27.35	44.44	41.67	50.00	40.30

Climate

From the base to the top, the climatic analysis of the Holocene sequence yields the following results. MIR24 displays mild, humid conditions. By the MER method, we observe that the MAT is 0.1°C lower than nowadays, while the MAP is 252 mm higher than nowadays in the Burgos area (Table 4). The chorotype analysis indicates that 45% of species are generalist (CH-3) (Table 3).

Table 3.

Percentage of open and woodland areas and chorotypes represented in the studied layers of El Mirador cave.

Layers	Habitat weighting		Chorotypes
	Open	Woodland	CH1	CH2	CH3	CH4
MIR4	40.6	59.4	36.5	6.3	19.8	37.5
MIR5	45.5	54.5	64.0	4.5	9.0	22.5
MIR6	44.2	55.9	54.5	9.1	18.2	18.2
MIR9	41.6	58.5	30.2	9.4	22.6	37.7
MIR10	28.6	71.4	21.4	7.1	50.0	21.4
MIR11	26.5	73.5	5.9	5.9	52.9	35.3
MIR16	34.6	65.4	30.8	0.0	38.5	30.8
MIR17	37.5	62.4	40.6	7.0	25.8	26.6
MIR18	30.2	69.7	22.7	11.4	42.7	23.2
MIR19	25.2	74.8	26.5	3.4	54.7	15.4
MIR21	27.8	72.2	22.2	0.0	55.6	22.2
MIR22	29.2	70.8	16.7	0.0	58.3	25.0
MIR23	40	60.0	30.0	0.0	30.0	40.0
MIR24	29.1	70.9	27.6	2.2	44.8	25.4

The temperatures recorded in MIR23-22 are the highest in the entire sequence. In these layers, the MAT exceeds the current level by 1°C (Table 4). The principal chorotype in MIR23 is chorotype 4, that is, Mediterranean species (40%), and in MIR22 it is chorotype 3 (58%) (Table 3). In contrast, the MAP of these layers is the lowest in the entire sequence. The MAP in MIR23 is 148 mm higher than nowadays, while in the case of MIR22 the MAP is 608 mm, only 14 mm higher than nowadays (Table 4). In these layers, the end of the African Humid Period can be identified (Bañuls-Cardona et al., in preparation).

Table 4.

Relation of temperatures and precipitation obtained using the MER (mutual ecogeographic range) method.

Layers	MAT					MTC					MTW					MAP
	Max.	Min.	Mean	SD	Δ	Max.	Min.	Mean	SD	Δ	Max.	Min.	Mean	SD	Δ	Max.	Min.	Mean	SD	Δ
MIR4	13	5	9.94	1.52	0.16	5	0	2.54	1.17	0.06	22	15	18.53	1.41	0.18	1500	500	794	221	−200
MIR5	13	5	10.03	1.57	0.07	7	0	2.65	1.25	−0.05	23	15	18.60	1.44	0.10	2500	500	846	284	−252
MIR6	13	5	9.97	1.55	0.13	7	0	2.64	1.20	−0.04	22	15	18.49	1.36	0.21	2000	500	867	277	−273
MIR9	13	5	9.94	1.52	0.16	5	0	2.54	1.17	0.06	22	15	18.53	1.41	0.18	1500	500	794	221	−200
MIR10	13	5	9.97	1.55	0.13	7	0	2.64	1.20	−0.04	22	15	18.49	1.36	0.21	2000	500	867	277	−273
MIR11	13	5	9.62	1.81	0.48	5	0	2.46	1.24	0.14	23	15	18.70	1.33	0.00	2000	500	792	238	−198
MIR16	13	5	10.17	1.47	−0.07	5	0	2.62	1.01	−0.02	23	15	18.97	1.51	−0.27	1500	400	715	230	−121
MIR17	13	5	9.94	1.52	0.16	5	0	2.54	1.17	0.06	22	15	18.53	1.41	0.18	1500	500	794	221	−200
MIR18	13	5	9.94	1.52	0.16	5	0	2.54	1.17	0.06	22	15	18.53	1.41	0.18	1500	500	794	221	−200
MIR19	13	5	9.94	1.52	0.16	5	0	2.54	1.17	0.06	22	15	18.53	1.41	0.18	1500	500	794	221	−200
MIR21	13	5	10.07	1.56	0.03	5	0	2.57	1.12	0.03	23	15	19.05	1.44	−0.35	1500	400	740	249	−146
MIR22	15	5	10.83	1.53	−0.73	7	0	2.96	1.14	−0.36	25	15	20.17	1.51	−1.47	2500	300	608	233	−14
MIR23	15	5	11.02	2.07	−0.92	9	0	3.37	1.77	−0.77	25	15	19.79	1.83	−1.09	1500	400	742	233	−148
MIR24	13	5	10.03	1.57	0.07	7	0	2.65	1.25	−0.05	23	15	18.60	1.44	0.10	2500	500	846	284	−252

MAT: mean annual temperature; MTC: mean temperature of the coldest month; MTW: mean temperature of the warmest month; MAP: mean annual precipitation; n: number of 10 × 10 km UTM squares forming the intersection obtained for micromammals; mean ± SD: mean and standard deviation of the values obtained; min.: minimum of the values obtained; max.: maximum of the values obtained: Δ: difference between the current mean for Burgos weather station over 30 years and that obtained for the small mammals.

The MER method reveals that the MAT in MIR21 is equal to the current levels, but the MAP is 146 mm higher than nowadays. In MIR19, MIR18 and MIR17, the palaeoclimatic analysis shows an increase in precipitation, with the MAP 54 mm higher with respect to MIR21; the temperatures were lower, and we have registered a decrease of 0.5°C in the mean temperature of the coldest months (MTC). The most highly represented chorotype from MIR21 to MIR18 is chorotype 3, whereas in MIR17 species with Euro-Siberian requirements (CH-1) are most abundant. After this slight cooling, in MIR16 temperatures are again similar to nowadays; the MAT is 0.1°C higher than today, and a significant decrease in rainfall of 79 mm is observed with respect to MIR17.

In MIR11, slightly cooler conditions are detected (from ca. 6300 to 5940 cal. BP). The MER shows the MAT (9.6°C) to be the lowest in the Holocene sequence of El Mirador cave, 0.5°C lower than nowadays, mainly because of the low MTC (2.4°C). The climatic data obtained on the basis of the small mammals suggest an increase in MAP in MIR11 (792 mm) with respect to the pluviometric data for MIR16 (715 mm). The chorotype data indicate generalist species to be most abundant in this layer (53%). In MIR10, a significant increase in the rainfall (75 mm) and temperatures (0.4°C) is observed with respect to MIR11, while the principal chorotype is chorotype 3, that is, generalist species (CH-3).

In MIR9, we detect a dry event. This shows a decrease in MAP from 867 mm in MIR10 to 794 mm in MIR9. As regards temperatures, however, we do not observe major changes. The chorotype data indicate that species with Mediterranean requirements (CH-4) are most abundant (38%).

After this dry event, in MIR6 and MIR5 we observe a significant increase in rainfall (73 mm more than in MIR9). The temperature remains similar to MIR9, but chorotype 1 is most abundant (55% and 64% in MIR6 and MIR5, respectively).

Finally, in MIR4 we do not observe changes in temperature with respect to MIR6 and MIR5, but the MAP recorded is 52 mm higher, while chorotype 4 is the most important (Bañuls-Cardona et al., in preparation).

Environment

Woodland is the most representative kind of habitat in El Mirador, but with some changes along the sequence. The highest percentages of woodland are registered in MIR19 (75%) and MIR11 (74%), while the lowest percentages are registered in MIR5 (54%) and MIR6 (56%). The other habitat that is well represented is the ‘open humid’ habitat, indicating evergreen meadowland with pastures and dense topsoil. It is in MIR23 and MIR6 that the highest percentages of open humid habitat are identified (40% and 32.4%, respectively), whereas MIR24 and MIR22 are the layers with the lowest values (16.8% and 12.5%, respectively). The ‘open dry’ habitat is the least represented habitat in El Mirador, and in MIR23 it is not registered at all. The maximum value for this type of habitat is recorded in MIR9 and MIR4 (20.8%), while the minimum values are registered in MIR11 (5.9%) and MIR10 (5.4%) (Bañuls-Cardona et al., in preparation).

Discussion

In the Iberian Peninsula, palaeobotanical studies document the first human landscape modifications around 6000 cal. BP. However, some palaeoenvironmental changes that were probably not the result of the human impact are also recorded; these could have been in response to the arid climate event that occurred at 8200 cal. BP. The clear intensification of farming activities in the landscape started to appear later (Iriarte, 2009; Martínez-Cortizas et al., 2009). We used a range of multiproxy analyses (pollen, charcoal, sedimentology, geochemistry and chironomids) from different parts of the Iberian Peninsula to characterize the main features of the landscape evolution during the Holocene (Badal et al., 1994, 2012; Carrión, 2002; Carrión et al., 2004; Iriarte, 2009; Martínez-Cortizas et al., 2009; Pérez-Sanz et al., 2013).

In the north of Iberia, the first human impact has been registered around 4000–3000 cal. BP. According to this chronology, the lowest values of forest coverage were in Peña Larga (Cripán, Álava) and Padre Areso (Bigüézal, Navarra). A special case was Puy Aguila I (Bárdenas Reales, Navarra), where the human influence was produced when the site was inhabited (Iriarte, 2009). Among the earliest evidence of significant landscape transformation by humans in northwestern Iberia was the Coto da Fenteira (Redondela, Pontevedra). In this site, two layers have been found (dated to 4690 and 3735 cal. BP) evidencing episodes of forest fire use, a technique that caused serious soil erosion. However, this erosion increases around 3000 cal. BP, with a significant decline in arboreal pollen, as occurs at Arcucelos (Orense) from 3040 cal. BP (Martínez-Cortizas et al., 2009). A multiproxy analysis (pollen, sedimentology, geochemistry, chironomids and charcoal) from the high-mountain glacier-lake of Basa de la Mora (Huesca) in northeastern Iberia reveals probably the first evidence of forest management, indicating negligible anthropogenic pressure until ca 1150 cal. BP (Pérez-Sanz et al., 2013).

Pollen analysis of sites situated on the northern Meseta has revealed an intense human impact on the environment, but only in very recent times (which ones). In the Tolla Collado de El Berrueco (Sierra de Guadarrama, Madrid), dated to 1830 cal. BP, very intense human action was detected by a regression of Pinus forest and an increase in anthropophilic species of pollen (Ruiz-Zapata et al., 2009a). In Rascafría (Valle del Lozoya, Madrid), increased soil erosion is detected from 920 ± 50 BP, because of increased grazing throughout the year (Ruiz-Zapata et al., 2009b). Human activity also appears in the Espinosa de Cerrato sequence (Palencia), where a change in the ratio between Pinus and Quercus pollens from 1400 cal. BP has been detected, and in El Carrizal lake (Cuéllar, Segovia) the presence of weed and Cerealia taxa from 2650 cal. BP is a sign of human activity (García-Antón et al., 2011).

In the southeastern part of the Iberian Peninsula, the intensity and timing of the human impact on vegetation vary from one part to another. In the Sierra de Gádor (Almeria), after 3940 cal. BP a frequent alternation in the dominance of Pinus and evergreen Quercus at the expense of deciduous Quercus is observed. This change is preceded by an increase in microcharcoal particles at 4200 cal. BP, suggesting an increase in fire use. In the Sierra de Baza (Granada), the replacement of mesophytic by more xeric Mediterranean vegetation around 3800 cal. BP is preceded by greater fire activity at 4100 cal. BP. However, deforestation expanded over the next two millennia, with anthropogenic disturbance (agriculture, mining and pastoralism) reaching its maximum after 2560 cal. BP (Carrión et al., 2010). In Siles lake (Jaén), high grazing pressure is registered from 2400 cal. BP; this may well have promoted local increases in the proportion of grasses, because extensive pastures are natural above the tree line (Carrión, 2002).

The debate about anthropogenic versus climatic determinism has been particularly intense with regard to the Mediterranean area (Carrión et al., 2004). During the earliest Neolithic, Mediterranean woodland was dominated by Quercus while the presence of secondary plant formations was insignificant in Cova de l’Or (Beniarrés, Alicante) and Cova de les Cendres (Teulada-Moraira, Alicante). However, around 5000 cal. BP, a reduction in Quercus is observed in favour of more open formations, and the sedimentology reveals one of the wettest periods in the Neolithic, so these changes may be related to the economic activities of human groups. As has been documented for most of the Iberian Peninsula, this reduction increases at Cova de les Cendres from the Bronze Age on, because of the intensification of farming activities (Badal et al., 1994, 2012).

However, the climatic and the human impact on small-mammal diversity are indiscriminately mentioned as causes of rapid oscillations in the environment during the Holocene, yet efforts to disentangle the specific causes of this process are complicated (Jalut et al., 2009; Jiménez-Moreno et al., 2013; Mercuri et al., 2011). At the beginning of the Holocene, the most frequently cited explanations for patterns of elevational diversity relate to gradients in single factors, such as rainfall, temperature, productivity, competition, resource abundance, habitat complexity or habitat diversity, but the current theory recognizes climatic factors as a principal influence on trends in diversity (Lomolino, 2001; McCain, 2004). In the mid-Neolithic and Bronze Age, in contrast, the richness and diversity of species have been associated with the human impact (Carrión et al., 2010; López-García et al., 2013).

Because of their size, small mammals are more sensitive to minor variations in climate and environment than larger ones, and these changes affect their ethology (López-García et al., 2013). It is for these reasons that we use small mammals in this study. Some small-mammal species have a capacity for adaptation to these new conditions, enabling them to modify their climatic and environmental requirements (McKinney, 1997). This ability allows them to maintain populations in their area of current distribution despite changing environmental conditions, as well as to colonize other areas (Arribas et al., 2012; Bellard et al., 2012), as in the case of synanthropic species, which have adapted to conditions created or modified by human activities (Mistrot, 2000).

Climate influence

The small-mammal studies of levels MIR24–MIR19 of El Mirador establish that the changes in the environment and in the degree of diversity were related to climatic conditions. The palaeoclimatic analysis shows the temperatures to have hovered around 10°C (Table 4). Species belonging to chorotype 3 (species with generalist climatic requirements) are the most abundant (Table 3), and A. sylvaticus is the most representative species in these layers. However, MIR23 is an exception to this. In this layer, we have identified the end of the African Humid Period, with higher temperatures than nowadays (Table 4) (Bañuls-Cardona et al., in preparation). Chorotype 4 is the most representative chorotype, and the most abundant species is M.(T) duodecimcostatus, a species with Mediterranean climatic requirements (Table 3).

According to some authors, moreover, the decline in diversity may have been a direct effect of the general transition from a cooler to a warmer climate and the corresponding habitat change (Blois et al., 2010). In contrast, in MIR23 the rise in diversity was related to an increase in temperature (1°C) and an increase in open environment (11%) (Figure 3). The simultaneous availability of water and high temperatures is the best explanation for the variation in species richness (Real et al., 2003). In MIR19, the same Simpson index is recorded (0.70), associated with a minor decrease in temperature (0.3°C) and a decrease in open environment, which is at its lowest level in the sequence of El Mirador (25%).

Figure 3.

Comparisons between various proxies used throughout El Mirador cave sequence. From left to right: habitat interpretation for El Mirador cave based on the habitat weighting method. Mean annual precipitation (MAP) and mean annual temperature (MAT) of the El Mirador cave sequence. Representation of the chorotypes: CH-1 (chorotype 1), CH-2 (chorotype 2), CH-3 (chorotype 3) and CH-4 (chorotype 4). Diversity study with Simpson index. Finally, representation of synanthropic species (Crocidura russula, Microtus arvalis, Microtus (Terricola) duodecimcostatus and Eliomys quercinus) for each layer. Phase 1: climatic influence (changes associated with climatic influence); Phase 2: human impact (changes associated with human impact).

Human impact

From as early as ca. 6000 cal. BP, some archaeobotanical studies have detected the first evidence of a human impact on the landscape in the Iberian Peninsula (Badal et al., 1994; Fletcher and Sánchez-Goñi, 2008; Iriarte, 2009; Martínez-Cortizas et al., 2009; Zazo et al., 2008). However, this trend increases after ca. 5000 cal. BP, with a drastic reduction in the forest in Europe in general (Carrión et al., 2010; Heinz et al., 2004; Hernández-Beloqui et al., 2015; Kalis et al., 2003; Leira and Santos, 2002; López-Merino et al., 2012; Tarroso et al., 2014).

Farming practices have been documented in El Mirador cave by studies based on pollen, charcoal, seeds and phytoliths (Cabanes et al., 2009; Euba et al., 2016; Expósito and Burjachs, 2016; Rodríguez et al., 2016). These studies have confirmed the forest degradation, which is most likely because of intensified human activity. For example, pollen analyses clearly show higher values of anthropogenic signatures related to human activities, especially during the Bronze Age period (MIR4) (Expósito et al., in preparation). Zooarchaeological studies confirm the development of herding practices throughout the sequence. These were based on goat and sheep breeding. Moreover, the ‘fumier’ sequence and an abundance of ovicaprine foetal and neonatal remain suggest the use of the cave for livestock penning and, especially, as a breeding cave (Angelucci et al., 2009; Martín et al., 2016b; Vergès et al., 2016).

MIR18–MIR16 (7000–6300 cal. BP)

The small-mammal studies of El Mirador cave provide the first, minor evidence of a human impact on diversity in MIR18 (ca. 7000–6800 cal. BP). From MIR19 to MIR17, the MER analysis indicates the same temperatures and the same level of precipitation, but we have registered a progressive increase in an open environment type (Figure 3). Nevertheless, we observe a higher level of richness (nine species) and a significant decrease in diversity in MIR18 (Table 2), probably related to the increased volume of herds and/or the higher intensity of the occupation of the cave because of its use as a sheepfold (a large number of remains, large number of perinatal individuals) (Table 5) (Martín et al., 2016b).

Table 5.

General composition of the faunal assemblage in the studied layers of El Mirador cave and ovicaprine perinatal data, considering NR (number of remains) and MNI (minimum number of individuals). Percentages were calculated taking into account the sum of NR and MNI for all El Mirador layers.

Layers	NR	%NR	MNI	%MNI	Perinatals
					NR	%NR	MNI	%MNI
MIR4	560	6.10	24	6.74	18	2.09	5	4.76
MIR5	19	0.21	8	2.25	2	0.23	2	1.90
MIR6	62	0.68	9	2.53	4	0.47	3	2.86
MIR9	161	1.75	10	2.81	24	2.79	4	3.81
MIR10	107	1.16	10	2.81	17	1.98	3	2.86
MIR11	1364	14.85	24	6.74	23	2.67	4	3.81
MIR16	1386	15.09	30	8.43	183	21.28	12	11.43
MIR17	79	0.86	8	2.25	18	2.09	2	1.90
MIR18	762	8.30	28	7.87	138	16.05	13	12.38
MIR19	740	0.81	27	7.58	44	5.12	6	5.71
MIR21	630	6.86	24	6.74	61	7.09	8	7.62
MIR22	110	1.20	7	1.97	10	1.16	2	1.90
MIR23	130	0.14	10	2.81	13	1.51	3	2.86
MIR24	80	0.87	7	1.97	21	2.44	3	2.86

However, in MIR17, although no climatic variations are observed with respect to MIR19 (Table 4), we see a change in the predominant chorotype (Table 3). In MIR17, M. agrestis, a Euro-Siberian species (with 26% of the total of the assemblage), was more abundant than A. sylvaticus, a generalist species that was predominant from MIR24 to MIR18 (Table 1). The increase in the open environment (from 30% in MIR18 to 38% in MIR17) (Figure 3) and the abundance of M. agrestis and microtines in general (54%) could indicate an increase in cultivated lands to the detriment of herding practices, as indicated by the low percentage of large mammals (Table 5) (Martín, 2015). However, it remained a minor increase at this point, because agricultural intensification would have favoured the dominance of other species such as M. arvalis or C. russula (Burel et al., 2004).

In MIR16 (ca. 6600–6300 cal. BP), an increased number of synanthropic small mammals is registered (53.8%) (Table 2), as well as the highest percentage of large-mammal remains (8.43% of MNI), especially perinatal remains (11.43% MNI; Table 5; Martín et al., 2016b). These data could indicate a more intense occupation of the cave in this period. The intense occupation had effects on the diversity and richness of small mammals (Cam et al., 2000). In this layer, the diversity continued to be low (0.80; Table 2). The data from El Mirón cave (Cantabria) reveal a higher diversity than in El Mirador for the same period (López-García et al., 2013). In El Mirón, M. schreibersii has been found, indicating that the cave was probably not occupied, because in general these bats do not cohabit with humans (Cuenca-Bescós et al., 2008).

Moreover, the MER indicates a small increase in temperature (0.3°C) with respect to the previous layers (MIR19–MIR17), and the most abundant species is once again A. sylvaticus. This increase in temperature (Table 4) produces a reduction in the species that eat herbaceous plants throughout the year, such as species belonging to the genus Microtus. In contrast, omnivorous species such as A. sylvaticus and E. quercinus remain practically constant (Soriguer et al., 2003).

MIR11–MIR10 (6.200–6.000 cal. BP)

In MIR11, the MER method allows a minor cold event to be identified (Bañuls-Cardona et al., in preparation), and these climatic conditions would be expected to be associated with a lower percentage of diversity (Figure 3). However, we register the greatest level of diversity (0.68; Table 2), and there is also an increase in thermo-Mediterranean species such as C. russula and M.(T) duodecimcostatus, especially the latter, which increased 14% with respect to MIR16, in which the climatic conditions were milder. These results could be related to a change in herding strategies at this point in El Mirador. The importance of goats and sheeps decreases while the presence of equids, whose origin is likely to be wild, is more important in this layer (Martín et al., 2016a). This change in livestock management may, in part, be influenced by the low temperatures shown by the small-mammal study (Bañuls-Cardona et al., in preparation). Furthermore, archaeobotanical studies of El Mirador indicate that there are no cereals in this layer (Rodríguez et al., 2016). All these factors could have caused the increased presence of M.(T) duodecimcostatus. This species requires areas free from rapid and frequent changes to build the underground galleries that provide it with refuge and food storage, which explains its scarcity in fields (Tarjuelo Mostajo et al., 2010).

In contrast to MIR11, the changes seen in MIR10 could be associated with a lower intensity of herding activities, as indicated by the large mammals’ remains (2.8% MNI). The index of synanthropic species is lower and the diversity decreases 18.5% with respect to MIR11 (Table 2). Moreover, the presence of synanthropic species such as M.(T) duodecimcostatus has decreased, and C. russula has disappeared, in spite of the thermal recovery (from 9.6°C to 10°C) (Figure 3).

MIR9–MIR4 (5.900–3.000 cal. BP)

From MIR9 to MIR4, the small-mammal analysis reveals an increase in open environments. In this period, the MER results indicate a minor decrease in precipitation (Table 4), but this cannot justify the strong reduction in forest cover. This reduction is more likely to be related to the human impact on the landscape, as multidisciplinary studies have shown this amplified aridity to be because of the significant human impact and the resulting soil disturbance (Domínguez-Villar et al., 2012; Frigola et al., 2007; Pérez-Lambán et al., 2014).

Moreover, the palaeoclimatic analysis of the small mammals of El Mirador shows that the temperature remains stable from MIR9 to MIR4, although the chorotype analysis indicates important changes. Thermo-Mediterranean species are more abundant in MIR9 and MIR4, whereas in MIR6 and MIR5 species with Euro-Siberian requirements are more important (Table 3). However, the amount of large-mammals is lower, as in MIR10, and there is a decrease in the intensity of the occupation as a sheepfold ‘sensu stricto’, with a reduced herd or a limited number of shepherds (Martín, 2015). At the same time, however, the pollen remains indicate a significant increase in crops around the cave (Expósito et al., in preparation). The agricultural intensification causes a deterioration in habitat quality and a reduction in availability, leading to a homogenization of the landscape. This phenomenon affects diversity, favouring the dominance of a few species, in particular more generalist species as opposed to others whose needs are more stringent (Benton et al., 2003; Dunning et al., 1992).

The Simpson diversity index in MIR9 undergoes a decline with respect to MIR10, while we see an increase in the percentage of synanthropic species (13%), and these tendencies persist through to MIR4 (Table 2). In general, the most abundant species in the entire sequence had been A. sylvaticus but from MIR9 this trend changes. In MIR9, the most abundant species is C. russula, a generalist species in terms of habitat and food requirements (Table 1). Such a species would benefit from a reduction in landscape heterogeneity that reduces the presence of other species such as A. sylvaticus (Blanco, 1998; Tarjuelo Mostajo et al., 2010). In MIR6 and MIR5, the most abundant species is M. agrestis, whose presence has been shown to increase when grazing levels decrease (Wheeler, 2008). A comparison of the small-mammal diversity of MIR6 with that of a layer from El Mirón with the same chronology (layer 8.1) shows them to be equal (0.78) (López-García et al., 2013). This would indicate that, as observed in the palaeobotanical analysis, landscape anthropization was quite widespread throughout the Iberian Peninsula around 6000–5000 cal. BP (López-Merino et al., 2012; Morales-Molino et al., 2011). In the case of MIR5, small-mammal diversity can be compared with that of three different sites: Colomera cave (Lleida), El Mirón cave (Cantabria) and Valdavara-1 cave (Lugo). The diversity in El Mirón cave (Cantabria) and Valdavara-1 cave (Lugo) can be seen to be higher and in Colomera cave (Lleida) lower than in El Mirador. This analysis confirms the theory of low human occupation intensity in the northern Meseta (García-Antón et al., 2011; Ruiz-Zapata et al., 2009a) and in high mountainous areas, as proposed by various authors (Carrión et al., 2010; Tarroso et al., 2014). Finally, during the Bronze Age, cereal-growing and livestock farming are widely documented throughout Europe (Broothaerts et al., 2014; López-Sáez et al., 2001; Pérez-Díaz et al., 2015). In MIR4 of El Mirador, bovid remains with pathologies related to traction force have been detected (Martín, 2015), and the palaeobotanical records and small-mammal analysis indicate that cultivated fields were gaining ground over forest (Allué and Euba, 2008; Bañuls-Cardona et al., in preparation; Expósito et al., in preparation). As we have seen in MIR9, this intense agricultural system favours the dominance of the most generalist species, compared with other species with more stringent requirements (Arribas et al., 2012; Dunning et al., 1992). In MIR4, we see the greatest values in diversity in El Mirador (0.82) and also the highest index of synanthropic species (60.4%). The most representative species was M. arvalis, a synanthropic species that occurred in landscapes with a high percentage of arable land. Also, this species can cause significant economic losses during population outbreaks (Jacob and Tkadlec, 2010; Luque-Larena et al., 2013).

Conclusion

The small-mammal study of El Mirador has proved to be a useful tool to identifying the changes in diversity related to human activities during the middle- to late-Holocene of the northwest of the Iberian Peninsula. El Mirador is particularly valuable in this context because it has a sequence with a well-documented human occupation from 7200 to 3000 cal. BP. Two phases are identified by our studies of diversity and synanthropic species. In the first phase (7200–7000 cal. BP), small changes in diversity related to climatic oscillations have been established; while in the second phase (7000–3000 cal. BP), changes in diversity associated with the human impact have been detected. Moreover, from 5900 to 3700 cal. BP, the dominance of microtines and the evidence from other remains studied (large mammals, seeds, charcoal, pollen, phytoliths) indicate changes probably caused by intensive agricultural practices. In general, the most significant decline in biological richness in El Mirador cave was caused in the layers with the greatest human pressure derived from both agriculture and livestock. Further comparison with other proxies has allowed us to corroborate generalized human pressure on the landscape throughout the Iberian Peninsula from 6000 cal. BP on. Moreover, it has confirmed the theory of low human occupation intensity in the northern Meseta and in high mountainous areas.

Footnotes

Acknowledgements

The authors would like to thank the team of El Mirador cave for providing them with the material studied.

Funding

This paper is part of project 2014-SGR900 and CGL2015-65387-C3-1-P (MINECO/FEDER). S.B.-C. is a beneficiary of an Erasmus Mundus Doctorate scholarship.

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