Rock hyrax middens: A palaeoenvironmental archive for southern African drylands

Quaternary Science Reviews 56 (2012) 107e125

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Rock hyrax middens: A palaeoenvironmental archive for southern African drylands Brian M. Chase a, b, *, Louis Scott c, Michael E. Meadows d, Graciela Gil-Romera e, Arnoud Boom f, Andrew S. Carr f, Paula J. Reimer g, Loïc Truc a, Verushka Valsecchi a, Lynne J. Quick d a

Institut des Sciences de l’Evolution de Montpellier, UMR 5554, Centre National de Recherche Scientifique/Université Montpellier 2, Bat. 22, CC061, Place Eugène Bataillon, 34095 Montpellier, cedex5, France Department of Archaeology, History, Culture and Religion, University of Bergen, Postbox 7805, 5020 Bergen, Norway c Department of Plant Sciences, University of the Free State, Bloemfontein 9300, South Africa d Department of Environmental and Geographical Science, University of Cape Town, Private Bag X3, Rondebosch 7701, South Africa e Pyrenean Institute of Ecology e CSIC, Campus de Aula Dei, Avda. Montañana 1005, 50159 Zaragoza, Spain f Department of Geography, University of Leicester, Leicester LE1 7RH, UK g School of Geography, Archaeology and Palaeoecology, Queen’s University Belfast, Belfast, BT7 1NN, Northern Ireland, UK b

a r t i c l e i n f o

a b s t r a c t

Article history: Received 27 June 2012 Received in revised form 26 August 2012 Accepted 28 August 2012 Available online 23 October 2012

Like many of the world’s subtropical regions, southern Africa is highly sensitive to changes in the earth’s climate system, but a dearth of reliable palaeoenvironmental records means that relatively little is known about how regional environments have been affected over centennial to multi-millennial timescales. To a large extent this sensitivity is a function of the position of these regions at the interface between temperate and tropical circulation systems. The resulting seasonality and irregularity of rainfall have limited the development of suitable archives, such as lakes and wetlands, for the preservation of palaeoenvironmental proxies. This paper reviews and evaluates the value of rock hyrax middens as novel palaeoenvironmental archives in southern Africa. Considered are (1) the contemporary taxonomy, distribution and ecology of hyraxes, (2) the mechanisms of hyrax midden development, their physical and chemical structure, rates of accumulation and age; and (3) the palaeoenvironmental proxies preserved within hyrax middens, including fossil pollen, stable isotopes and biomarkers. The interpretive constraints and opportunities offered by these various midden characteristics are assessed with a view to demonstrating the potential of these deposits, widespread as they are through arid and semi-arid southern Africa, in providing a more detailed and chronologically resolved view of late Quaternary palaeoenvironments across the subcontinent. Ó 2012 Elsevier Ltd. All rights reserved.

Keywords: Rock hyrax Midden Southern Africa Palaeoenvironment Pollen Stable isotopes d13C d15N Biomarkers

1. Introduction Southern Africa is a critical region for studying Southern Hemisphere climate and circulation dynamics. At the interface of the temperate and tropical moisture-bearing systems, the region is known to have experienced phases of significant environmental change driven by variations in hemisphere-scale atmospheric and oceanic circulation patterns. These large-scale changes in climate in

* Corresponding author. Institut des Sciences de l’Evolution de Montpellier, UMR 5554, Centre National de Recherche Scientifique/Université Montpellier 2, Bat. 22, CC061, Place Eugène Bataillon, 34095 Montpellier, cedex5, France. Tel.: þ33 04 67 14 49 03. E-mail address: [email protected] (B.M. Chase). 0277-3791/$ e see front matter Ó 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.quascirev.2012.08.018

the recent geological past have been conceptualised as taking place along three general axes: one extending northward from the Cape, where wet winter climates quickly grade to hyperarid conditions with rare summer rain; another extending eastward along the south coast where a progressive increases in summer rainfall create a year-round rainfall zone; and another that extends into the semiarid interior of the continent across the modern NEeSW rainfall gradient (Fig. 1) (cf. Chase and Meadows, 2007). Over glacialeinterglacial cycles, climatic and environmental changes along these axes have been linked to latitudinal migrations of the winter westerlies and the intensity and amount of precipitation related to the Inter-tropical Convergence Zone (ITCZ)/Congo Air Boundary (CAB) (Lancaster, 1979; Meadows and Baxter, 1999; Chase and Meadows, 2007). Proxies from these regions are therefore

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Fig. 1. Map of southern Africa showing seasonality of rainfall and sharp climatic gradients dictated by the zones of summer/tropical (red) and winter/temperate (blue) rainfall dominance. Winter rainfall is primarily a result of storm systems embedded in the westerlies. It has been postulated that these systems have expanded equatorward during glacial periods, increasing their influence eastward across the south coast and interior, as well as northward into the presently hyperarid regions of Namibia. Major atmospheric (white arrows) and oceanic (blue arrows) circulation systems and the austral summer positions of the Inter-tropical Convergence zone (ITCZ) and the Congo Air Boundary (CAB) are indicated. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

palaeoenvironments: the rock hyrax midden. Rock hyraxes (Procavia capensis) are herbivores that are common throughout southern Africa, and that have the particular habit of defecating in the same location over many generations (Scott,1990a). These locations, often sheltered in caves, become covered in faecal pellets and accumulations of dried urine. Contained in these deposits are a range of palaeoenvironmental proxies that are protected from mechanical disruption and the wetting and drying effects typical of semi-arid environments. They may be preserved perfectly in this manner for upwards of 50,000 years (Sections 3.2 and 3.3 of this paper). Research carried out so far has produced reliable high-resolution records that have provided detailed information regarding past climate and vegetation change in southern Africa. When coupled with high-precision chronologies, these proxies provide sub- to multi-decadal records of rapid environmental change spanning thousands of years (Chase et al., 2009, 2010, 2011; Quick et al., 2011). Although hyrax middens are generally only preserved in dryland environments, their occurrence across the subcontinent dove-tails with the presence of permanent lakes in more mesic regions, and they are now providing the potential for a more balanced coverage of palaeoenvironmental records across southern Africa. The aim of this paper is to review and evaluate the palaeoenvironmental significance of biogenic accumulations in hyrax middens. As such, we consider: (a) the contemporary taxonomy, distribution and ecology of the forming agents, (b) the mechanisms of hyrax midden development, their physical and chemical structure, rates of accumulation and age; and (c) the palaeoenvironmental proxies preserved within hyrax middens, including preserved pollen, stable isotopes and biomarkers. The interpretive constraints and opportunities offered by these various midden characteristics are assessed with a view to demonstrating the potential of these deposits to provide a more detailed and better resolved view of late Quaternary palaeoenvironments across the subcontinent. 2. Hyrax taxonomy, distribution, ecology and physiology 2.1. Taxonomy

likely to preserve important information on long-term low latitude and temperate circulation dynamics, elucidate questions regarding the region’s high levels of floral endemism and species richness (Goldblatt and Manning, 2002), and provide a context for interpreting southern Africa’s rich archaeological record. Despite southern Africa’s sensitivity to climate change, and its position relative to hemispheric and global circulation systems, the environmental history of the region remains largely unknown. This is principally due to the region’s topography and semi- to hyperarid climate, which are not conducive to the occurrence of lakes and wetlands that typically preserve long records of environmental change in temperate and tropical regions. In lieu of such traditional terrestrial palaeoenvironmental records, a variety of terrigenous proxies obtained from marine cores (Shi et al., 2000, 2001; Stuut et al., 2002; Dupont et al., 2006, 2007, 2011) and geomorphological records (Eitel et al., 2005; Srivastava et al., 2005; Chase and Thomas, 2007; Telfer and Thomas, 2007; Burrough et al., 2009; Stone et al., in press) have been analysed, but interpretations of their significance vary and have often been contradictory (Partridge et al., 1999; Lancaster, 2002; Thomas and Shaw, 2002; Scott et al., 2004; Chase and Meadows, 2007; Chase, 2009; Thomas and Burrough, 2012). In this context, that is a region with a rich and dynamic environmental and human history, as well as a dearth of reliable palaeoenvironmental information, we present a palaeoenvironmental archive that is ideally suited to the reconstruction of dryland

Hyraxes (Procaviidae) are the only members of the order Hyracoidea, of which there are three extant genera: Procavia (rock hyrax), Heterohyrax (bush hyrax, or yellow-spotted rock hyrax) and Dendrohyrax (tree hyrax). It was thought that both Procavia and Heterohyrax are monospecific (P. capensis and Heterohyrax brucei, with 17 and 25 subspecies respectively (Wilson and Reeder, 1993)), but DNA evidence suggests that Procavia may in fact include two distinct species (Prinsloo and Robinson, 1992). There are two identified species of Dendrohyrax: D. arboreus (southern tree hyrax) and D. dorsalis (western tree hyrax), the latter of which includes six subspecies (Wilson and Reeder, 1993) (Fig. 2). Considering that hyraxes are all furry, rabbit-sized animals, with small rounded ears and stubby tails, it is remarkable that their closest relatives are the Proboscidea (elephants) and Sirenia (sea cows) (Simpson, 1945; Kleinschmidt et al., 1986). Unlike their extant relatives, hyraxes are extremely adept climbers, an ability enhanced by the morphology and nature of their leathery footpads. Studies conducted by Adelman et al. (1975) suggest that this ability is, at least in part, linked to the occurrence of sweat glands in their footpads, which enable them to run up extraordinarily steep rock faces without slipping (Adelman et al., 1975). 2.2. Distribution The distribution of hyraxes spans most of Africa; with the western and southern tree hyraxes inhabiting the western and

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Fig. 2. A rock hyrax (Procavia capensis) standing sentry outside the communal shelter. Cederberg Mountains, South Africa.

eastern equatorial forests respectively, the yellow-spotted hyrax being found primarily in the drier regions of east and northeastern Africa, and the rock hyrax being found commonly, but not exclusively, over the greater portion of the subtropical drylands (Barry et al., 2008). In southern Africa, they are abundant from sea-level to more than 2500 m, and on Mount Kenya they are found at elevations as high as 5500 m (Haltenorth and Diller, 1977). While they are often associated with desert environments, commonly occurring even in regions with less than 100 mm mean annual precipitation, they also inhabit significantly moister forested parts of the subcontinent, where rainfall exceeds 1500 mm yr1 (Barry et al., 2008). This exceptional adaptability suggests that it is unlikely that past changes in climate would have had a significant effect on their distribution during the Quaternary (Fig. 3). 2.3. Ecology and physiology In terms of diet, Heterohyrax and Dendrohyrax are predominantly/exclusively browsers, choosing to eat shrubs, forbs, bushes

Procavia capensis Heterohyrax brucei Dendrohyrax arboreus Dendrohyrax dorsalis Fig. 3. Map of the observed distribution of hyrax species in southern Africa (data from IUCN, 2011).

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and trees, while rock hyraxes will browse but prefer to eat grasses when they are available (Sale, 1965a; Hoeck, 1975). These dietary preferences between genera are borne out by stable carbon isotope studies, which clearly show enriched d13C values from bone collagen for Procavia relative to Heterohyrax (DeNiro and Epstein, 1978). As mixed feeders, rock hyraxes are particularly flexible regarding the environments they are able to inhabit. Sale (1965b) reports rock hyraxes eating an extraordinary range of plants, including grasses, twigs, bark, leaves and shoots of shrubs and trees, and even liverworts and lichen at higher altitude. A study in the Serengeti found that rock hyraxes consumed 79 species of plant, with high seasonal variability; spending most of their time grazing during the wet season (78%), when grasses are available, and only browsing significantly (57%) during the dry season or dry years (Hoeck, 1975). In captivity, hyraxes will eat a wide range of non-typical foods, including apples, carrots, biscuits, and have been observed to enjoy hotdogs and hard liquor (Rudnai, 1987). An early study, however, concluded that even when starved for a day and locked in a cage with a chicken they will not resort to carnivory (Bruce, 1790). In the wild, hyraxes do not take food into their shelters to eat (Sale, 1966a), but feed in the open, foraging within w60 m of their shelters (Sale, 1965a). This range is limited by the threat of predation, but the size and exploitation of this space is maximised by the use of sentinels, who alert the feeding animals with sharp barks when there is danger, allowing them time to escape to their shelters (Kotler et al., 1999). It has been suggested that part of the reason for their highly varied diet may be the need to obtain sufficient water, rather than palatability or nutrient content, and often the plant species consumed are those that contain the most water (Sale, 1965a, 1966a). Indeed, hyraxes are non-obligate drinkers, and drink very little in the wild, if at all. Even during extended droughts they appear to be able to get all of the water they need from succulent plants or latex-producing leaves (Sale, 1965a; Louw et al., 1972). Moisture that is consumed is used very efficiently, with urine volumes ranging from 5 ml/kg0.82/24 h (Meltzer, 1976) to 65 ml/ kg0.82/24 h (Rübsamen et al., 1979). This low urine volume is associated with high solute loads, which are normally between 1940 and 2340 mOsm/kg in hydrated animals (Maloiy and Sale, 1976), but can be as high as 3200 mOsm/kg when the animals are dehydrated (Rübsamen et al., 1979, 1982). Analyses of the urine show these solutes are composed mainly of calcium carbonate, presumably as the result of highly efficient calcium absorption, although the advantage gained by this is unclear (Leon and Belonje, 1979). The hyrax can also reduce its faecal water content, from 70 to 75% when water is freely available to around 55% when water availability is restricted, but this ability is not as well developed as other desert animals such as camels (43%) (Maloiy, 1972; Rübsamen et al., 1982). Evaporative water loss in hyraxes is low relative to the predicted value for a eutherian mammal its size, which is related to the animals’ low metabolic rates (20% below average based on body weight (Bartholomew and Rainy, 1971)). Interestingly, hyraxes can tolerate shifts in body temperature of as much as 7e8  C (Bartholomew and Rainy, 1971). The range of ambient temperatures that can thus be tolerated without invoking heating or cooling mechanisms e which helps hyraxes conserve energy in extreme environments e is in fact significantly extended in water deprived animals (Rübsamen et al., 1982). When drought stressed, hyraxes’ body temperatures decrease, oxygen consumption declines by some 20% and evaporative water loss is reduced. When temperatures are above 35  C, water deprived hyraxes become hyperthermic, which can result in a reduction in evaporative water loss of as much as 50% (Rübsamen and Kettembeil, 1980).

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Hyrax behaviour also plays a role in energy conservation. As gregarious animals, living in colonies of 25e40 individuals (Kingdon, 1971), hyraxes habitually huddle together in rock shelters and crevices at night to stay warm (Sale, 1970). In the morning, the animals bask in the sun to raise their body temperatures to functional levels, and just before retreating into their shelters at night they soak up the last heat of the day to maximise the potential afforded by environmental conditions (Brown and Downs, 2006). The primary restriction on rock hyrax distribution is in fact not dictated by climate or vegetation, but rather the availability of shelter, most often in the form of rock outcrops or talus slopes. Indeed, shelter is so critical to these animals that their fur contains long sensory vibrissae much like cats’ whiskers, which aid them in hiding in and exploring shelters (Maloiy and Eley, 1992). While hyraxes will take shelter in almost any available hole if threatened, they will generally only inhabit durable geological features that provide a network of suitable crevices. Well-worn paths often connect the various entrances to the shelters, and while there are clear spatial preferences for basking and common latrines (Sale, 1960), any internal differentiation of shelter use is unknown (Sale, 1966b). In terms of shelter choice at the landscape scale, there appear to be few fixed rules. In general, the entrance to the shelters must restrict access to dominant predators and it has been noted that a degree of protection from prevailing winds is favoured (Sale, 1966b). Shelters are more likely to be found on cliffs and slopes that provide ample, secure basking opportunities and it might be expected that the distance between shelter and available food would be an important factor. In many cases, the shelters themselves, particularly in the case of kopijes (small rocky hills), provide favourable environmental conditions for water storage and vegetation growth relative to the surrounding landscape. While these criteria generally apply, we have observed that at least in hyperarid landscapes hyraxes congregate in higher concentrations near water courses with denser vegetation.

3. Rock hyrax middens As previously noted, hyraxes are known to use communal latrines (Sale, 1960; Louw et al., 1972). These sites are often found in sheltered locations, where the threat of predation is reduced, and can be identified by accumulations of faecal pellets and a brown tar-like substance known as hyraceum, which together in their various admixtures are referred to as middens. Hyraceum, is a urinary product, which is composed of organic elements, soluble salts and carbonates (Leon and Belonje, 1979). When protected from rain, it may accumulate in deposits in excess of a metre thick and several meters across.

At poorly protected sites in sufficiently arid regions (or even in the open in hyperarid regions) hyrax urine leaves a white precipitate on the rocks. These deposits, which are primarily composed of calcium carbonate (Leon and Belonje, 1979), can reach significant thicknesses (several tens of centimetres) depending on the nature of the shelter and the regional climate history and geology. Thicker formations tend to occur in shallow shelters that during more arid periods, presumably provided sufficient shelter from rainfall for substantial midden accumulations, but under wetter conditions no longer provide adequate protection, resulting in the removal of the more soluble components of the midden (Fig. 4). Varying degrees of protection result in varying degrees of midden preservation. Small overhangs, vertical fractures in cap rocks, and groundwater flow along weakness in the shelter’s architecture may lead to midden degradation if rainfall exceeds a certain amount and/or intensity. The thickest middens occur at sites composed of granites or horizontally bedded quartzites with between w30 and 480 mm of annual rainfall (Fig. 5). In more humid environments (>800 mm mean annual rainfall), there is little to no evidence of hyraceum accumulation, and middens typically resemble piles of compost, as the masticated plant material in the pellets rapidly decomposes into soil. Taken further, the simple presence and timing of development of middens at a site, depending on the site’s architecture, may sometimes indicate patterns of climate change. At the Namibian sites of Okonjambo and Vrede, for instance, basal ages as early as 7 ka have been obtained from the middens (Gil-Romera et al., 2006, 2007), but the great majority of midden material preserved at these sites dates to the late Holocene arid period described at the better protected Spitzkoppe and Austerlitz sites. All of these sites postdate the humid phase identified at w8 ka (Chase et al., 2009, 2010). Hyraceum shows hygroscopic properties and it is likely that periods of increased precipitation or elevated ambient humidity will destroy existing middens, while more arid periods allow their development/preservation. Thus, the existence or persistence of middens in a region generally means that precipitation has not increased beyond the threshold for development dictated by the structure of a given site. To the authors’ knowledge, hyraceum-rich middens do not form in coastal situations, despite the presence of hyraxes, and it is hypothesised that the ambient humidity of the air and the occurrence of coastal fogs preclude midden development. 3.1. Comparisons with fossilised herbivore middens from other regions Studies of other herbivore midden remains have been very effective in palaeoenvironmental studies in dryland regions on

Fig. 4. Hyrax middens from the De Rif site in the Cederberg Mountains of South Africa (a), and near Purros in the northern Namib Desert (b). While a large overhang above the De Rif midden has resulted in excellent preservation, the Purros midden is exposed to the elements, and despite the hyperarid climate, significant degradation has occurred, leaving only the less soluble carbonate skeleton.

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Fig. 5. Map of the optimal climatic envelope for hyrax midden preservation, showing areas with precipitation during the wettest month below 90 mm (purple), mean annual precipitation below 480 mm (orange), and the overlapping range where the best preserved middens have been found (red). (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

several continents. In the southwestern United States pack rat middens have provided an unprecedented record of environmental changes over the last 40,000 years (King and van Devender, 1977; Betancourt and Davis, 1984; Anderson et al., 2000). As a result of this work, the vegetation dynamics of this area are some of the best understood for any of the world’s drylands at this timescale, and the critical data provided have dramatically helped define the range of regional climate variability. This work has also lead to important perspectives on ecological theory (Betancourt et al., 1990), which have impacted on management strategies (Betancourt et al., 1991, 1993) by allowing a distinction to be made between anthropogenic environmental impacts and natural processes. More recently, midden studies have also been undertaken in Australia (Pearson, 1999; Pearson and Dodson, 1993; McCarthy et al., 1996; Pearson and Betancourt, 2002) and South America (Betancourt et al., 2000; Holmgren et al., 2001; Latorre et al., 2003; Maldonado et al., 2005; Latorre et al., 2006; Holmgren et al., 2008; Díaz et al., 2012; Gayo et al., 2012). This work has highlighted a fundamental difference between middens from these regions and hyrax middens. American and Australian middens are essentially nests composed of sticks and other macrobotanical remains. These middens often have no clear stratigraphy, and researchers have thus adopted the methodology of processing them as single samples that provide a palaeoenvironmental snapshot (Spaulding et al., 1990). Hyrax middens, on the other hand, are primarily urino-fecal deposits, and are deposited progressively as a series of layers. This diachroneity is one of the fundamental advantages of hyrax middens over nest middens, which are only secondarily preserved as the animals urinate in their shelters. Examinations of the internal and external structure of the middens suggest flow/deposition dynamics similar to speleothems (cave deposits, e.g. stalactites), with the fresh urine flowing across the surface of the midden, then drying and crystallising, preserving the stratigraphic integrity of the midden (Fig. 6). The general

morphology of middens is often characterised by (1) lobate forms, (2) undulating weathering features on exposed midden faces, and (3) in some cases the formation of thin (1e3mm in diameter) stalactites on the underside of some middens. As a result, questions over the potential for post-depositional remobilisation of hyraceum may be raised. Our detailed examination of over 150 middens, however, has confirmed the visible stratigraphic integrity of the middens, and while some surficial alteration of exposed surfaces can occur, consistently coherent age-depth models, and the nearly

Fig. 6. A 2 cm section of a hyrax midden, showing fine laminae at the 30e100 mm scale.

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vertical exposed external faces of the middens indicate that, once dry, hyraceum is not prone to significant remobilisation. In any case, with careful field sampling and subsequent laboratory subsampling it is a routine matter to avoid middens, or sections of middens, that have been subjected to post-depositional alteration.

3.2. Midden structure, accumulation rates and age Hyrax midden structures and accumulation rates can vary considerably based on the relative proportion of their two primary components, pellets and hyraceum, which is determined by the architecture of the site itself. Depending on the shape and irregularities of the floor of the site in question, pellets are likely to either accumulate (in concave structures) or roll away (in convex or inclined structures). Whereas hyrax urine will deposit only a very thin film of hyraceum after evaporation, pellets are usually 0.5e 1 cm in diameter, and thereby accumulate much more quickly, with deep piles accumulating perhaps within just a few years, or even months. Compared to this, we have observed that middens composed primarily of hyraceum accumulate much more slowly; generally between 200 and 500 years/cm (Fig. 7). The rate of hyraceum accumulation depends on the morphology of the midden, the architecture of the site, as well as presumably the size of the hyrax colony, and as such net rates can be highly variable, ranging from 20 years/cm to more than 2000 years/cm. The proportion of pellets also affects midden stratigraphic integrity. Layers of pellets create/preserve substantial pore-spaces, which are e or can be e subsequently filled with hyraceum. It may thus be very difficult to determine the correct age of any given sample from such amalgamated material, and attention to this is important when selecting middens for analysis. Middens that are composed more completely or entirely of hyraceum better preserve the stratigraphic integrity, and exhibit coherent structures of fine laminae (10e100 mm laminations), with each perhaps relating to the periodic excretions that lead to the formation of the middens (Fig. 6).

3.3. Midden ages Radiocarbon ages from hyraceum are not subject to reservoir effects or the inclusion of new carbon (Kaufman and Broecker, 1965; Grimm et al., 2009). This is primarily a function of middens being isolated systems, and that through respiration the hyraceum is brought into equilibrium with atmospheric 14C at the time of deposition. Published data show that hyrax middens can be of considerable antiquity (Scott et al., 2004), and middens from the Jaagvlakte site in the Cederberg Mountains of South Africa are as old as 48,174e50,000 cal yr BP (UBA-16715) and beyond (>50,000 cal yr BP; UBA-19294) (unpublished data). It has also been commonly observed that many middens are no longer actively accumulating. Often this is controlled by the shelters in which they are found, with accumulation ceasing when the middens grow to such an extent that the hyraxes can no longer physically enter the shelters. Until recently, field sampling was limited to the collection of middens that were most accessible and easiest to sample. In many cases this meant that the individual sampled middens were relatively thin (<5 cm) with aggregate records subsequently constructed from fragments of as many as 25 separate middens (Scott and Woodborne, 2007a, b). With recent developments in sampling tools and techniques, we are now able to sample larger, more stratigraphically coherent middens, which better represent the full period of accumulation at a given site. It is interesting to note that most sampled middens post-date the early Holocene (w11 cal kBP), and even fewer pre-date the Last Glacial Maximum (w24 cal kBP) (Fig. 8). Although the geological architecture of most sites indicates that middens may be expected to be 105e106 years old, most are in fact significantly younger. Considering that at most midden localities, hyraxes have likely been present for a long time (see Section 2), the question arises as to where have all the older middens gone? Periodic deterioration/ destruction must occur, but age data from those middens with better-resolved chronologies do not indicate significant hiatuses or periods during which the midden eroded. Thus this question remains unresolved.

Number of middens comprising material of age specified

50 45 40 35 30 25 20 15 10 5 0 0

Fig. 7. Age models for sections taken from opposite sides of the De Rif hyrax midden (Chase et al., 2011; Quick et al., 2011). The models clearly indicate a marked increase in accumulation rate corresponding with a layer of pellets in the central portion of the midden, and consistent (42e65 yr/mm) accumulation rates for the upper and lower portions of the midden composed of hyraceum.

10000

20000 30000 Age (cal yr BP)

40000

50000

Fig. 8. Plot of midden material age (500 year bins) from 78 radiocarbon dated middens, including both published and unpublished data. The age of the material has been estimated by linear interpolation between radiocarbon ages. The practice of dating near-surface and near-basal material, and the amount of material included in each sample (generally equivalent to w50e250 years of accumulation) results in an underestimate here of both the number of middens dating to the present day (although modern middens do appear to be a relative rarity) and the antiquity of the oldest material composing each midden.

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3.4. Chemical composition of hyrax middens The very nature of hyrax middens implies that they comprise a mixture of materials, which include animal metabolic products, undigested food, and any allochtonous material blown into the middens or deposited via feet or fur. In terms of organic matter (OM), the existence of such potentially distinct sources (i.e. extraneous OM and animal metabolites) implies that a range of information concerning inter alia: animal diet, animal behaviour, metabolic responses to environmental stress, changing behaviour, as well the wider palaeoecological setting of the site may all be preserved within hyraceum. As such, detailed characterisations of the OM within middens have been attempted and are ongoing. Hyraceum essentially comprises a mix of organic compounds, soluble salts, calcium carbonate and the mineral sylvite (Leon and Belonje, 1979; Scott, 1994). More recent data from Raman Spectroscopy and Fourier Transform Infrared (FTIR) Spectroscopy demonstrate the presence of a number of CaCO3 polymorphs, the abundance of sylvite (KCl) and an organic component (Prinsloo, 2007). The organic components within hyraceum have been investigated using pyrolysis-GC/MS (py-GC/MS) and GC/MS analysis of solvent-extractable lipids (Carr et al., 2010). Py-GC/MS is commonly applied to elucidate macromolecular organic matter structure and composition. Py-GC/MS measurements on samples from two sites, Spitzkoppe, Namibia (SPZ) and Truitjes Kraal (TK), Western Cape Province, South Africa produced remarkably similar suites of pyrolysis products (Fig. 9), despite their contrasting environmental settings. The pyrolysis products were dominated by aromatic compounds; notably the nitrogenous compounds benzonitrile and benzamide. Pyrolysis in the presence of a methylating agent tetramethylammonium hydroxide (TMAH) implied that benzamide is

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a monomer of a larger polymeric structure, the major organic component of the hyraceum OM (Carr et al., 2010). This is further supported by the ubiquity of benzamide within solvent extracts (see below) and it is probable that it is derived from hippuric or benzoic acid, which are common metabolites in ruminants (Bristow et al., 1992). Given its abundance, the metabolite (or metabolite product) benzamide is likely the major source of organic nitrogen and carbon measured in bulk stable isotope analyses (Chase et al., 2009, 2011; Carr et al., 2010), and can therefore provide insights into animal diet and its isotopic signature (see Section 4.2). Interestingly, common plant-derived pyrolysis products, such as lignin were not detected using py-GC/MS, although low molecular weight polysaccharide pyrolysis products (e.g. acetyl furan, furaldehyde, dimethyl furan) were found in trace amounts. That such plant-derived compounds might be identified with this technique following more detailed analytical pyrolysis protocols is implied by new FTIR analyses of the organic fraction, which support the basic pyrolysis-based interpretation of SPZ and TK midden chemical compositions (Fig. 10). The SPZ FTIR spectra following carbonate removal contains a broad absorption band at w3300 cm1 as well as sharper absorptions from w1600 to 1700, 1400, 1130, 770 and 690 cm1. Multiplets between 1560 and 1640 cm1 have been reported as being due to NeH bending in primary amines (Williams and Fleming, 1989; Brittain, 2009), while a signal at w1650 cm1 is representative of C]O stretches of the amide band. The spectra thus bear a strong resemblance to benzamide (Kniseley et al., 1962; Brittain, 2009). FTIR spectra from the TK midden, which is rich in faecal material, shows some resemblance to that of cellulose, with strong broad bands at 3400 cm1 and 1050 cm1, and some weaker broad bands at 1730 and1670 cm1. Overall, the FTIR spectra and previous studies reveal a complex mixture of salts and organic compounds, with the latter

Fig. 9. Pyrograms for the Truitjes Kraal (top) and Spitzkoppe (bottom) middens, showing the total ion current (TIC) with no sample pre-treatment. Compounds mentioned in the text are labelled as diamonds (styrene), circles (benzonitrile) and stars (benzamide).

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processes within an ecosystem can be better resolved, resulting in a fuller and more reliable understanding of palaeoenvironmental dynamics.

100

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Hyrax middens contain well-preserved micro plant material including pollen, which is sealed in middens by hyraceum, protecting it from microbial activity and decay. The earliest study of fossil pollen from a hyrax midden was undertaken by Pons and Quézel (1958) in the Hoggar Massif of Algeria, whereas the first palynological analyses of southern African middens were undertaken during the late 1980s (Scott and Bousman, 1990; Scott, 1990a, b; Bousman and Scott, 1994), and demonstrated that hyrax middens are very useful as pollen and microfossil traps (Scott and Bousman, 1990; Scott, 1990a).

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Wave number (cm-1)

Fig. 10. Fourier Transform Infrared (FTIR) spectra for hyraceum samples from Namibia (Spitzkoppe) and the Western Cape (Truitjes Kraal). The sprectra are essentially indicative of the major types of bond within a sample, from which compositional information may be inferred. The Spitzkoppe sample (blue) produces spectra that are comparable to those of benzamide, while the Truitjes Kraal spectra (red) show some commonalities with cellulose (see Section 3.4). (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

incorporating aromatics, polysaccharides, amines, amides and other carbonyl-containing compounds. There are also clear similarities with the spectrum of benzamide, particularly at Spitzkoppe, which is consistent with the pyrolysis data.

4. Palaeoenvironmental proxies Part of the extraordinary potential of hyrax middens as palaeoenvironmental archives is the large range of proxies that are contained within them. In the past, when their diachronic nature was less evident, they were viewed as the poor relation to the better studied pack rat middens. While pack rat middens are rich in identifiable macrofossils, which can be directly dated and provide high taxonomic resolution, hyrax middens are poor in macroremains. Those that are found are almost exclusively masticated material that has been incorporated into the deposits as faecal pellets. While some studies have analysed these midden components (Fall, 1990; Fall et al., 1990), our recent work suggests that this approach does not maximise the full potential of hyrax middens as palaeoenvironmental archives. Hyrax middens contain a suite of proxies that have the potential to provide clear insights into past climate and vegetation change. Working within the context of the middens’ stratigraphy (Fig. 6), and building on robust chronologies indicating predictable and consistent accumulation rates (Fig. 7), sampling methodologies are now more akin to those applied to speleothems rather than to pack rat middens. Whereas the early focus was on small (<1 kg), accessible middens and in some cases in-situ sub-sampling, it is now standard practice to collect larger (10e70 kg) segments of the best-developed middens. The segments are then split and polished in a controlled environment, and subsamples for radiocarbon dating and proxy analysis. That multiple proxies can be analysed from the same subsample allows for direct comparability, and much more reliable insights into the interrelationships between the systems being studied. This is valuable when comparing proxies that reflect vegetation change (e.g. pollen) and those that are primarily influenced by climate (e.g. d15N), as the relative roles of climatic forcing versus vegetation dynamics related to competitive

4.1.1. Taphonomy, preservation and concentrations Middens are excellent traps for pollen derived from the local and regional surroundings either via the alimentary channel of the animals (excreted in pellets) or via deposition on the middens. The airborne pollen rain is incorporated by (1) collecting on the surface of the midden, (2) being brought in on the fur of the hyraxes, or (3) being ingested as dust on dietary items such as plant leaves or drinking water (Scott and Bousman, 1990; Scott, 1990a). The dietary component may also represent the ingestion of flowers, which may result in the occasional over-representation of pollen of certain plant species in the pellet fraction of certain middens (see Section 4.1.2). A clear benefit of midden pollen spectra over wetland pollen spectra is that they may more clearly reflect terrestrial vegetation, without the high proportions of hydrophilic elements found in wetland sequences, which is particularly problematic in some dryland pollen records (Horowitz, 1992). Furthermore, as the pollen found in hyraceum is not exclusively wind-transported, usually under-represented entomophilous plants are more clearly represented (Fig. 11). Preservation of pollen sealed in hyraceum is usually very good, but the degradation of pollen grains has been occasionally observed in loose pellets or middens semi-exposed to the elements, such as in dolerite shelters in the central grassland region of South Africa, where some Asteraceae pollen have apparently lost their ektexine (L. Scott, unpublished observation). Compared to other available palaeoarchives in the region, such as fluvial sediments or paleosols, and to more widely used pollen records from peat bog and lakes, middens contain high fossil pollen concentrations; usually between 1 and 2  105 pollen grains per gram of sample. Pollen concentrations are high even in poorly productive ecosystems such as the Namib Desert margins (Gil-Romera et al., 2007). Concentrations increase markedly when analysing pollen contents from pellets, reaching 5e30  105 pollen grains/gram of sample. 4.1.2. Interpretation of pollen data There are some potential drawbacks for the palynological analysis of middens, however, as the diverse taphonomic vectors can complicate interpretations if they are not adequately considered and controlled for. Pollen spectra from pellets e reflecting the animal’s needs or preferences on a particular day e may contrast strongly with pollen spectra preserved in hyraceum, and which thought to be primarily brought to the midden via the fur of the hyraxes (which is collected as it moves through the vegetation around its shelter) and the wind. The degree to which dietary biases affect pollen spectra in pellets is a subject that is not fully understood. While Scott and Cooremans (1992) have shown that at the biome scale, fresh pellets reflect vegetation of the region from

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Fig. 11. Pollen percentages in the Pakhuis Pass hyrax middens (Scott and Woodborne, 2007a).

which they were collected, including the seasonal variations within vegetation types, most published studies also indicate significant differences both between modern pellets, and between modern pellets and surface sediment samples from the same site (e.g. Hubbard and Sampson, 1993; Gil-Romera et al., 2007). A number of options might explain this, but it is assumed that as any given pellet represents what was eaten in the last day(s), there will be substantial inter-seasonal and inter-annual variation in the pollen preserved. It is relatively straightforward to control for variation based on taphonomic vectors, as while the airborne pollen rain and the pollen brought in on the animals are compatible e relating to regional and local environments respectively e the influence of the ingested pollen is largely restricted to faecal pellets, which are easily identifiable in the middens. For most studies, pellets are avoided in sub-sampling, but at some sites middens are pelletrich, leaving few sampling alternatives. Palaeoenvironmental interpretations of pollen data from such middens, and the potential influence of dietary preferences, must therefore be carefully considered. In most fossil pollen archives, wind-pollinated plants may dominate the natural pollen rain. Pollen production, however, is likely to have a less significant influence on the pollen that hyraxes

ingest, and considering the wide variety of plants that they may eat, it may be possible to control for the taxon over-representation resulting from a production bias while still attaining a reasonable representation of the local vegetation (Scott and Cooremans, 1992; Scott, 1994; Carrión et al., 1999). A study from the Lower Omo Basin of Ethiopia collected several dozen pellets from different areas around the study site, aggregated them into a single sample, and compared them to the local vegetation (Gil-Romera et al., 2010). The percentage vegetation cover at the landscape level was estimated using remote sensing and classification techniques using structure and floral composition criteria. The results obtained indicate that the pollen proportions in hyrax pellets were closer to the current vegetation cover than the pollen spectra found in surface sediment samples, wherein Poaceae were overrepresented in comparison to tree and shrub taxa (Fig. 12). Although studies of seasonal variation remain to be done, the representation of the tree and shrub taxa in the pellets implies that despite probable differences due to dietary biases, hyrax pellets are useful pollen traps for both insect and wind-pollinated taxa. Structured studies to clarify the relative influence of regional (aeolian) and local (fur) signals in the pollen preserved in hyraceum remain to be completed. At least in some cases, aeolian inputs

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Land cover % 7%

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Combretaceae Capparaceae Anacardiaceae Mimosoideae Euphorbiaceae Poaceae Other herbs

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Fig. 12. Pie diagrams showing the vegetation composition cover (in percentages) at Dewachaga, Ethiopia (top), the pollen abundance of the surface samples (left) and the hyrax pellets (right) (Gil-Romera et al., 2010).

proxy for water availability in the environment (Chase et al., 2009, 2010, 2011).

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4.2. Stable isotopes Over the last 10 years there has been increasing emphasis on the application of stable isotope analyses to midden sequences. Initially this focussed on the use of bulk 13C data, with an emphasis on identifying changes in the relative abundance of C3/C4/CAM vegetation and associated palaeoecological/palaeoenvironmental inferences (e.g. Scott and Vogel, 2000). This is useful in climatic transition zones, such as the Western Cape Province of South Africa, where modern rainfall seasonality has a strong impact on C3/C4 grass distributions (Scott and Vogel, 2000; Meadows et al., 2010). d13C records can also be used in some ecoregions, such as the dry savannah at Spitzkoppe in Namibia, as an indicator of the reliability of grass cover. As hyraxes will preferentially graze (grasses are C4 in the region), more depleted d13C values from hyrax middens have been interpreted as evidence that the animals were forced to obtain a greater proportion of their diet from trees and shrubs, which are less susceptible to extended periods of drought (Chase et al., 2009) (Fig. 13). However, these data do not necessarily provide a direct and unambiguous indicator of past arid/humid shifts. As such, other studies have focussed on the use of d15N data as a potential

-20

δ13C (‰ VPDB)

appear to be negligible as some middens that have accumulated in vertical cracks e precluding the incorporation of pellets and direct contact with the animals e have been found to be devoid of pollen. If aeolian pollen does represent a small percentage of the pollen preserved in hyraceum then it might be inferred that hyraceum pollen assemblages reflect primarily local vegetation cover from within the animals’ primary feeding range. Pollen analyses in fossil hyrax middens thus provide a unique opportunity to study long-term vegetation dynamics in subhumid to hyperarid biodiversity-relevant areas, such as the Cape Floristic Region (Quick et al., 2011) and the Namib Desert (Scott et al., 2004), which are otherwise lacking other suitable palaeoenvironmental archives. Work is ongoing to improve sampling technique, with a focus on continuous, high-resolution (1e2 mm samples) sampling of larger middens. Preliminary unpublished results are extremely promising, and our expectation is to be able to produce the most detailed vegetation histories obtained thus far from southern Africa.

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Fig. 13. d15N and d13C values from hyrax middens from Spitzkoppe, Namibia. The d15N record has been interpreted as indicating a long-term aridification in the region, a finding supported by a range of regional proxies (Chase et al., 2009, Fig. 14). The d13C record is believed to reflect the vegetative response to these changes in climate, with grasses (more enriched d13C values) becoming less abundant as rainfall diminished/ became less regular and only deeper-rooted trees could access groundwater resources (Chase et al., 2009).

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temporal variations need to be adequately controlled for if reliable

d15N-climate correlations are to be identified. If we accept that plant d15N is determined by soil d15N, and the link with climate, while identified, has been imperfectly explored, it remains to determine to what extent variations in plant d15N account for the variations identified in animal tissue and/or excrement. Murphy and Bowman (2006, 2009) investigated variations in grass and kangaroo bone d15N from across Australia and demonstrated a remarkably consistent relationship between plant and bone d15N signals. Moisture availability, through its influence on the isotopic signature of plants/diet, was inferred as the primary control on animal d15N, with metabolism having no clear effect (Fig. 14). It is interesting to note that Ambrose and DeNiro’s (Ambrose and DeNiro, 1986a) findings are not inconsistent with these results, as drought-tolerant species can inhabit more arid regions with less regular rainfall (higher, wider d15N range) while water-dependent animals will be more restricted to well-watered areas (lower, smaller d15N range). To extend the findings of Murphy and Bowman (2006, 2009) to the study of excrement and hyrax middens, one can consider the studies of (1) Codron and Codron (2009), which concluded that faecal d15N correspond to changes in plant d15N, and (2) Sponheimer et al. (2003), which found that, while preferential urinary excretion of isotopically light nitrogen may occur under conditions of disequilibrium, an unstressed animal at “steady state” will have equivalent dietary and excreta d15N. Since faecal and animal d15N track plant d15N, and under normal conditions total excreta d15N is equivalent to dietary (plant) d15N, it follows that urinary d15N, while perhaps more negative relative to dietary d15N (Sponheimer et al., 2003), will reflect trends in plant d15N and water availability. Hyrax middens thus provide an optimal archive for the study of d15N as a proxy for long-term environmental change. The

Bone Grass 16

Bone Grass

11

δ15N (‰)

4.2.1. d15N of hyrax middens as an indicator of past hydrologic change In palaeoclimatology, the variables for which reconstructions are most often sought are humidity and temperature. Unfortunately, direct, or even reliable, proxies for these are rarely available, and it is necessary to make several inferential steps in order to interpret their past variability. Recent work on hyrax middens has shown that d15N records from middens may provide a clearer, more direct estimation of water availability than previously possible in southern Africa (Chase et al., 2009, 2011). It has long been understood that the 15N abundance in animal tissues is influenced by diet, climate and/or physiology (Heaton et al., 1986; Ambrose and DeNiro, 1986a; Ambrose, 1991). In terms of diet, a clear distinction exists between d15N values in carnivores and herbivores, with enrichment in 15N occurring up trophic levels (Schoeninger and DeNiro, 1984). Among herbivores, a link between increased d15N values in animal tissues and aridity was identified very early (Schoeninger and DeNiro, 1984; Heaton et al., 1986), but it was thought to be predominantly a function of the animals’ metabolism. Ambrose and DeNiro (1986a, b), based in part on the apparent lack of relationship between 15N/14N ratios in plants and the amount of rainfall (Heaton et al., 1986), developed a model to account for the enrichment of 15N in animal tissues based on physiological mechanisms of water conservation and nitrogen isotope mass balance. In this model, under arid conditions drought-tolerant herbivores concentrate their urine and excrete more 15N-depleted urea, leaving the body enriched in 15N. Conversely, water-dependent species that do not concentrate their urine were observed to have smaller d15N ranges and lower mean values in their tissues (Ambrose and DeNiro, 1986a). This predicted differentiation between drought-tolerant and water-dependent species, however, only found partial support in South Africa (Sealy et al., 1987). This study suggested that animals in arid regions are likely to eat lower protein diets (%N decreases with increasing aridity (Aranibar et al., 2004)), and that the additional protein produced by symbiotic bacteria in the animals’ digestive tracts would essentially result in a shift in trophic level and an enrichment of 15N in the animals’ tissues. Similarly, Codron and Codron (2009) found no significant difference in faecal d15N between drought-tolerant and water-dependent herbivores, but did identify a significant correlation between %N and d15N. In contrast to the initial findings of Heaton et al. (1986), subsequent studies of soils and plants across aridity gradients, indicate a clear negative correlation between 15N and rainfall (Handley et al., 1999; Schwarcz et al., 1999; Aranibar et al., 2004; Swap et al., 2004). As this was the original impetus for the construction of the mass balance model and its corollaries, these models, and their implications for interpreting d15N records in plant and animals tissues, should be reconsidered. Although a strong relationship has been established between soil and plant d15N, the link with rainfall is sometimes considered to be less robust (e.g. Codron and Codron, 2009). One of the primary difficulties in determining the relationship between precipitation and d15N values in soils, plants, animal tissues and excrement is the means by which precipitation is determined. It has been noted by Handley et al. (1999) that d15N in soils and plants may change substantially across a landscape as a function of variations in soil moisture. Since soil moisture varies as a result of subtle changes in topography, aspect and soil type, particularly in drylands where sparse vegetation and poorly-formed soils exacerbate the heterogeneity of the biogeochemical landscape (Schade and Hobbie, 2005), the common practice of using rainfall records from the nearest gauge and/or interpolated from regional stations will inevitably weaken the significance of any correlation. Soil moisture and d15N also vary significantly over short, sub-seasonal timescales (Handley et al., 1999) and, combined, these fine-scale spatio-

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Fig. 14. d15N of kangaroo bone collagen (orange) and grass foliage (green) collected throughout Australia plotted against mean annual precipitation (Murphy and Bowman, 2006). (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

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effects of contemporary ecosystem variability are mitigated by the spatial and temporal averaging intrinsic in hyraxes’ wide dietary preferences, restricted range (see Section 2.3), the probable contribution of multiple individuals to a single d15N sample, and the relatively long periods of time incorporated into each sample. In these archives, microtopographic variations in soil moisture (and thus d15N) are accounted for by the feeding habits of the hyrax, and it is expected that the spatio-temporal averaging will allow for the reliable identification of long-term changes in water availability as reflected in variations in midden d15N. Over long timescales (102e103 yr), this expectation is borne out, and the potential of hyrax middens as diachronic palaeoclimatic records has been supported by strong similarities between variations in d15N records and a range of palaeoenvironmental proxies reflecting changes in precipitation (Chase et al., 2009) (Fig. 15).

wetter

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4.2.2.2. Water-use efficiency (WUE). In addition to the above mentioned controls on the d13C in hyrax middens, in certain cases it has been possible to identify clear changes in plant water-use efficiency as determined by water availability and temperature (Ehleringer and Cooper, 1988; Pate, 2001). This raises the possibility that d13C records from hyrax middens in C3 ecosystems may provide an independent proxy for past hydrologic conditions that may be compared with d15N and fossil pollen records. The De Rif hyrax midden (Chase et al., 2011; Quick et al., 2011) provides a case study to illustrate this (Fig. 16). The site is located within the Mountain

δD n-C29 alkane (‰ VSMOW)

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4.2.2. d13C of hyrax middens as an indicator of vegetation change and plant water-use efficiency 4.2.2.1. Vegetation and diet. Variations in the d13C values of plants, and thus hyrax middens, are generally considered to be determined by: (1) the plant’s photosynthetic pathway (C4, C3 or CAM) (Smith, 1972), (2) leaf-level responses to water availability (Ehleringer and Cooper, 1988; Pate, 2001), (3) long-term variations in atmospheric CO2 (Polley et al., 1993; Richards and Hedges, 2003; Hedges et al., 2004) and/or d13CO2 (Arens et al., 2000; Hedges et al., 2006), and (4) the canopy effect, which causes a depletion in 13C abundance (van der Merwe and Medina, 1989; Cerling et al., 2004). Of these, the first two provide the potential to use hyrax middens to reconstruct past vegetation and climate respectively, whereas the third introduces a non-climatic control that needs to be considered over 103e105 yr timescales. In the sparse vegetation characterising dryland environments, the canopy effect is unlikely to have any significant effect.

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Fig. 15. Comparison of d15N data from hyrax middens from Spitzkoppe (a; Chase et al., 2009) and Austerlitz (b; Chase et al., 2010) in the Namib Desert with records for upwelling intensity from marine sediment core ODP1084B off the coast of Namibia (c; Farmer et al., 2005), a dD from marine sediment core GeoB6518-1 reflecting rainfall variations in the Congo Basin (d; Schefuß et al., 2005), d13C (e) and greyscale (f) records from Cold Air Cave, South Africa indicating changes in vegetation and rainfall respectively (Lee-Thorp et al., 2001; Holmgren et al., 2003), and sea-surface temperature estimates from MD972572 (g; Sonzogni et al., 1998). Shaded areas indicate the mid- late Holocene transition (MLHT) and the Younger Dryas (YD). Taken together, these records indicate a broadly uniform climatic signal across the southern tropics during the Holocene (cf. Chase et al., 2010).

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Fig. 16. d15N and d13C values from a hyrax midden from De Rif, in the Cederberg Mountains of South Africa. The d15N and d13C records have been interpreted as indicating variations in water availability and water-use efficiency respectively; findings that are supported by a range of regional proxies (Chase et al., 2011, Fig. 17 of this paper).

B.M. Chase et al. / Quaternary Science Reviews 56 (2012) 107e125

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Fynbos ecosystem of the Cederberg Mountains of South Africa (an ecosystem that consists primarily of shrubs, C3 grasses/reeds, very few trees and persists under an exceptionally wide range of climatic conditions (Cowling,1983; Meadows and Sugden,1991)). While d13C variability related to photosynthetic pathways does not need to be considered in an exclusively C3 ecosystem, atmospheric CO2 has changed significantly in the past (Indermühle et al., 1999; Monnin et al., 2001), and its potential influence on the midden d13C record through carbon isotope discrimination (e.g. Farquhar and Sharkey, 1982; Farquhar and Richards, 1984) needs to be considered in records such as De Rif, which span the last glacialeinterglacial transition. The experimental work of Polley et al. (1993) identifies a strong negative relationship between changes in plant d13C and CO2 at CO2 concentrations between 160 and 350 mmol mol1. Predictions of d13C variability over the course of midden deposition based on these data would, however, be in excess of 10&; far more than the 2.3& recorded in the De Rif midden (Fig. 16). This discrepancy supports the possibility that plants are able to adapt to changing atmospheric CO2 concentrations, and thus maintain consistent carbon isotope discrimination (Ehleringer and Cerling, 1995). Combined with the poor correspondence between atmospheric CO2 trends since the Last Glacial Maximum (Indermühle et al., 1999; Monnin et al., 2001) and the De Rif record, this suggests that other factors are the primary determinants of the midden d13C values; a conclusion supported by comparison of the De Rif record with other regional and global records of longterm climate change, with the strong similarities between the records indicating that regional sea-surface temperatures (Farmer et al., 2005), and ultimately perturbations in the North Atlantic are strong determinants of regional climates (Chase et al., 2011) (Fig. 17). Indeed, some studies have now shown that atmospheric CO2 variations do not have a significant effect on plant d13C, and rather it is atmospheric d13CO2 and other environmental factors that primarily control plant d13C fluctuations (Arens et al., 2000; Hedges et al., 2006). Chase et al. (2011) showed that even after correction was applied for variations in atmospheric d13CO2 the De Rif d13C record still exhibits a strong correlation with both the d15N record, and other proxy records, indicating that climatic parameters, and not changes in CO2 or d13CO2, are responsible for the variability evident in the record (Fig. 18). In summary, our investigations thus far suggest that bulk 15N and 13C stable isotope analyses are effective and mutually supportive data sources within hyrax middens. In each of the recently published records in which these analyses have been applied (Chase et al., 2009, 2010, 2011) we see a strong, coherent relationship between the two isotope records. The 15N records appear to be a reliable proxy for moisture availability in the site locale, while interpretations of 13C are rather site/ecosystem dependent. While in much of southern Africa, particularly the savanna biome, d13C can be seen as indicative of the proportion/ abundance/consumption of C4 grasses relative to woody shrubs, in the winter rainfall Fynbos Biome of the Cederberg Mountains the 13 C record can be interpreted in terms of WUE and water availability in the environment. This interpretation is supported by the close correlation of 13C and 15N in the De Rif midden record (Chase et al., 2011). The high temporal resolution afforded through the application of bulk isotope analyses, which only require a few mg of material is a key advantage over previous studies and other proxy data source (e.g. pollen). Further geochemical analyses (Section 3.4) conducted on midden material thus far suggest that the bulk isotope signal is primarily measuring C and N derived from animal-metabolised compounds (e.g. Benzamide and alike). Unlike lake and wetland environments we therefore have some confidence that the

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Age (1,000 years BP) Fig. 17. Comparison of d15N (a) and d13C (b) records from the De Rif hyrax midden from the Cederberg Mountains of southwestern Africa (Chase et al., 2011) with sea-surface temperature estimates from marine sediment core ODP1084B off the coast of Namibia (c; Farmer et al., 2005), the d18O record from Greenland’s GRIP ice core (d; Dansgaard et al., 1993), Antarctic temperatures as reconstructed from dD variations at Dome C (e; Jouzel et al., 2007). Taken together, these records indicate a broadly uniform climatic signal across the southern tropics during the Holocene (cf. Chase et al., 2010). Shaded areas indicate the Younger Dryas (YD) Antarctic Cold Reversal (ACR) and Heinrich Stadial 1 (HS1).

measured signal is dominated by a single (metabolised) source. To some extent this assumption finds support in our preliminary lipid biomarker and compound specific stable isotope analyses (Section 4.3). 4.3. Lipid biomarkers Biomarkers are molecules with preservation potential that have a specific biological origin. A range of solvent-extractable lipids derived from both plant and animal sources have been isolated from hyraceum (Table 1). Sources of plant-derived lipids identified in middens include (1) leaf waxes (homologous suites of n-alkanes and n-alcohols), (2) terpenoids such as b-Sitosterol derived from plant cell membranes and (3) aromatic plant-derived biomarkers including cadalene (a likely degradation product of plant-derived sesquiterpenoids (Peters, 2005)) and a-curcumene. As they cannot be biosynthesised by animals they must be ingested by the hyraxes and pass through the digestive system and/or (given the wide distribution of leaf wax lipids within the atmosphere) be derived from wind-blown or fur-trapped inputs.

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De Rif Schmitt et al., 2012 Smith et al., 1999

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Fig. 18. d13C data from the De Rif hyrax midden, both in its raw form and once variations in d13CO2 (Smith et al., 1999; Schmitt et al., 2012) have been corrected for.

4.3.1. Plant biomarker records Plant-derived biomarkers have been consistently identified within lipid extracts from all middens studied thus far, and offer the potential to consider palaeo-diets and palaeoecology in more detail. Studies of plant biomarkers in Quaternary contexts, particularly compound specific stable isotope analyses (e.g. n-alkane d13C and n-alkane dD) use plant leaf waxes (usually long-chain nalkanes), which are widely distributed in the atmosphere or lacustrine systems, relatively resistant to post-depositional degradation, and are easily isolated in solvent extractions (Kawamura et al., 2003; Rommerskirchen et al., 2003; Castañeda et al., 2009a, b; Tierney et al., 2010; Sinninghe-Damsté et al., 2011). Table 1 Major compounds identified within lipid extracts from the Truitjes Kraal midden. Compound

Likely source(s)

Benzamide a-Curcumene Dimethyl naphthalene a-Calacorene Cadalene C16eC33 alkanes (C27eC31 dominant)

Animal metabolism Plants Plants Plants Plants C27eC33 ¼ higher plant leaf waxes Shorter chain lengths from various potential sources (including bacterial)a C24eC28 ¼ higher plant leaf waxes Animal metabolite Animal metabolite Degraded animal metabolite Fungal Plants Plants

C16eC28 alkanol 5-b-Cholestanol 5-b-Cholest-5-enol Cholestanol Ergostanol Sitosterol a-Amyrin

a Shorter chain length n-alkanes may not be plant-derived, but thus far have be found in concentrations at least two-three orders of magnitude lower than the longchain leaf wax lipids.

The concentration of leaf wax-derived n-alkanes varies significantly between middens. For instance, n-alkane concentrations in the Cederberg middens from Truitjies Kraal and De Rif (unpublished data) are up to 28 times higher than those extracted from the Spitzkoppe site in Namibia (Carr et al., 2010). These differences are, however, commensurate with the markedly higher bulk organic matter contents in the Cederberg middens and the presence of other plant-derived molecules in the Truitjies Kraal midden (see Section 3.4). As with pollen, it is probable that the n-alkanes are derived from a combination of atmospheric deposition and contact with the animals as they move about the landscape. Although this provides less direct insights into the details of local environments than the bulk stable isotope analyses, lipids sampled from hyraceum may be more representative of regional scale vegetation change. Systematic studies of leaf wax distributions in modern plants and soils in regions surrounding important midden records are currently being conducted, and will serve as the basis for more detailed palaeoenvironmental reconstructions using this approach. This is motivated by numerous studies that have suggested that the distribution of leaf wax lipids is sensitive to source vegetation and/ or environmental conditions (e.g. Eglinton et al., 2002; Schwark et al., 2002; Rommerskirchen et al., 2003; Zhang et al., 2006; Vogts et al., 2009). Environmental interpretations of such trends are, however, somewhat conflicting (for example see discussion in Castañeda et al., 2009a), although a number of studies in southern Africa imply a distinction in the lipid distributions obtained from C4 grasses, which have been associated with increased prominence of longer carbon chain lengths (e.g. more C31 and C33 n-alkanes) and significantly more enriched n-alkane d13C, compared to C3 vegetation types (Rommerskirchen et al., 2003; Vogts et al., 2009). Studies on hyrax middens from distinct ecological communities show that the n-alkane distributions from the C3 vegetationdominated fynbos communities of the Cederberg (Truitjes Kraal) differ from Namibian C4 grass-rich savannas (Spitzkoppe) with the dominant homologue (Cmax) tending to the C29 n-alkane in the Cederberg (Fig. 19). In the case of the Spitzkoppe midden, the C29/C31 n-alkane ratios (C31/[C29 þ C31]) show an downwards trend during the mid Holocene indicating a shift to shorter chain lengths (i.e. increased significance of C29 at the expense of C31). This may e by at least one interpretation of C29/C31 n-alkane ratios (Rommerskirchen et al., 2003; Vogts et al., 2009) e indicate an increased prominence of woody plants relative to C4 grasses, which would (1) accurately reflect the response of the regional vegetation in this xeric savannah to drier conditions (Walker et al., 1981), and (2) correspond with a progressive enrichment in the bulk d15N and depletion in the bulk d13C records that has been interpreted as reflecting increasing aridity across the Holocene (Chase et al., 2009; Carr et al., 2010) (Fig. 20). A limited number of compound specific d13C analyses were reported by Carr et al. (2010). The n-alkanes were in sufficient concentration in all cases to produce very reproducible n-alkane d13C data (standard deviations mostly better than 0.5&). The most depleted d13C n-alkanes values are found in the C29 and C31 homologues, as anticipated for plant leaf waxes (e.g. Collister et al., 1994). In the Namibian savannas it was possible to use such data to estimate the relative proportions of C3 and C4 vegetation. In the Cederberg Mountains, despite an absence of C4 vegetation, the nalkane d13C was interpreted as potentially inconsistent with pure C3 vegetation end-member d13C values (approximately 35&; Castañeda et al., 2009a). A small contribution from CAM plants, which exhibit highly variable d13C ranges depending on the particular CAM mechanism used (Collister et al., 1994; Rundel et al., 1999; Bi et al., 2005), may account for this slight enrichment (Chase

B.M. Chase et al. / Quaternary Science Reviews 56 (2012) 107e125

1.0

a

121

b

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0.8 0.6 0.4 0.2

14

16

18

20 22 24 26 Carbon chain length

28

30

32

21

23

25 27 29 Carbon chain length

31

33

Fig. 19. n-Alkanol (a) and n-alkane (b) homologue distributions (presented normalised to the most abundant homologue) for the Truitjes Kraal hyrax midden. Both distributions are characteristic of leaf waxes in that they are dominated by high molecular weight homologues C29 and C26 for the alkanes and alkanols (respectively) and characteristic odd over even (alkane) and even over odd (alkanol) chain length preferences (Carr et al., 2010).

et al., 2011). The end-member n-alkane d13C values are, however, poorly defined for this region and ongoing analyses using modern plant material are refining the end-member values for southern African C3, CAM and C4 vegetation. Recent measurements (Carr et al., 2011) from De Rif produce comparable values to the Truitjes Kraal midden (Carr et al., 2010), although here they reach values as low as 33&. The data were obtained from material sub-sampled at a coarser temporal resolution than the bulk d13C samples, but the n-alkane values produce broadly similar trends, lending support to the original interpretation (Chase et al., 2011) that the bulk data essentially record isotopic variability in the surrounds of the midden site. Compound specific dD analysis of the same n-alkanes offers further scope to consider palaeo-hydrological conditions. It has been argued that dD variation provides insights into evapotranspiration and soil evaporation-induced fractionation, and can therefore provide further insights into palaeoenvironmental conditions (e.g. Tierney et al., 2008). These measurements can be effectively coupled with d13C measurements on the same n-alkanes

a

δ15N (‰)

9.0 9.5 10.0

b

-19.00 -19.50

c

0.9

-20.00

δ13C (‰)

10.5

C31/(C31+C29)

0.85 -20.50 0.8 0.75 0.7 0

2000 4000 6000 8000 10000 12000 Approximate age (cal yr BP)

Fig. 20. The bulk d15N (a), d13C (b) and normalised C31 index (C31/(C31 þ C29)) (c) records from hyrax midden SPZ-3 (Spitzkoppe, Namibia) plotted stratigraphically (Carr et al., 2010). Further details of this midden and its chronology are provided in Chase et al. (2009).

and in combination promise additional insights into palaeohydrologicaleecological interaction. 4.3.2. Other proxies 4.3.2.1. Micro-charcoal. Fire is a global ecosystem process particularly relevant in African ecosystems, where this disturbance has partly shaped the current landscape and has had an evolutionary role on both flora and vegetation (Keeley et al., 2011). Thus, longterm reconstructions of fire dynamics are important in understanding current thresholds for vegetation resilience and to make reliable vegetation reconstructions of the African landscapes. Sedimentary charcoal series have long been used as an excellent proxy of long-term fire history (Clark, 1989; Tinner et al., 1999; Higuera et al., 2010; Whitlock et al., 2010). Charcoal isolation from hyrax middens has provided insights into the fire history of some of the most fire-prone environments southern African fynbos (Quick et al., 2011) and East African savannas (Gil-Romera et al., 2011). Given the volatile nature of charcoal particles, the main input of these into the midden is via wind. For the most part these particles are unlikely to be incorporated through the animals’ diet although hyraxes grazing and browsing in a previously burnt area may add some charcoal particles into the midden through the pellets. Thus, as happens with sedimentary charcoal, lighter charred particles non-locally produced may reach the midden as transported by wind, while the local fires may leave a weaker signal as larger particles are transported over shorter distances. The very few fossil hyrax middens studies which have considered charcoal as a proxy, have analysed particles larger than 75mm. This has been tested in different basins and been found to be an acceptable threshold to discriminate local from regional charcoal inputs (Tinner and Hu, 2003; Duffin, 2008). The fire history inferred from the charcoal fraction >75mm has helped to shed some light onto interpretations of vegetation dynamics interpretation and it may help in the multi-proxy approach to palaeoclimatological reconstructions. It is still necessary to design site-based calibration studies in order to obtain an accurate charcoal particle-fire occurrence relationship on hyrax middens, so the analyst would need to make fewer assumptions on the charcoal production and deposition. 4.3.2.2. Ancient DNA. Pilot studies undertaken to assess the potential for the preservation and study of ancient DNA (aDNA) have shown it is well preserved in hyrax middens (Murray et al., submitted for publication). Whereas hot, arid to semi-arid environments generally preclude the preservation of DNA e studies of which have generally been restricted to colder climates (Hofreiter et al., 2000, 2003; Kuch et al., 2002; Poinar et al., 2003) e the effect of dessication and/or the anoxic environments within the

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middens allows for the preservation of genetic material for thousands of years (Murray et al., submitted for publication). Using Second Generation high-throughput sequencing (HTS) and genetic barcoding techniques, samples of hyraceum can be genetically audited, with multiple species being identified from a single bulk sample (Taberlet et al., 2012). One clear advance that this represents is the improvement in taxonomic resolution that can be achieved compared to fossil pollen analysis, particularly as regards certain diverse families with low identification resolution such as Poaceae and Asteraceae. aDNA results are able to identify the dominant genera, if not individual species. This increased resolution has important implications for the improvement of quantitative reconstructions of palaeoenvironmental variables derived from niche-based models, and the potential to explore changes in rainfall seasonality through the identification of C3 and C4 grasses, whose ranges vary as a function of growing season temperatures (Ehleringer et al., 1997; Collatz et al., 1998). 4.3.2.3. Phytoliths. Phytoliths (plant-derived silica bodies) are abundant and well preserved in modern hyrax dung (Finné et al., 2010), and have been observed and counted in fossil sequences from the Namib Desert (B. Chase unpublished data). Given their potential in vegetation reconstruction, including the distinction between C3 and C4 grasses (Cordova; Cordova and Scott, 2010; Rossouw, 2009), they promise to add considerable insights in palaeoclimate reconstructions. Currently, detailed studies of fossil assemblages are awaiting the establishment of a regionally specific reference collection. This has been shown to be required, as studies from the Namib Desert (B. Chase, unpublished data) and the Makgadikgadi Basin (Burrough et al., 2012; Cordova et al., in press) have identified high percentages (as much as 80%) of “C3 grass” phytoliths in late Holocene samples. Considering the current distribution of C3 grasses in southern Africa, and the factors controlling their distribution (Ehleringer et al., 1997; Collatz et al., 1998), it is very likely that these findings reflect misidentifications based on the use of extra-regional reference collections. 5. Conclusions Hyrax middens are proving to be exceptionally rich palaeoenvironmental archives in southern African drylands. These biogenic accumulations contain a great diversity of proxies, including fossil pollen, stable isotopes, biomarkers, micro-charcoal, ancient DNA and phytoliths, thus readily enabling a multi-proxy approach to environmental reconstructions that, to date, had been impossible due to the absence of appropriate sedimentary basins in the region. A significant advantage over other archives, or regional reconstructions based on a range of archives (lakes, speleothems, etc.) is that a wide variety of proxies can be obtained from any given sample; removing uncertainties based on microclimates, or relative dating uncertainties. Recent developments in sampling techniques, the acquisition of detailed chronologies and the application of new palaeoenvironmental techniques have improved our knowledge of midden composition, structure, chronology and geographical and climatological constraints on their formation, allowing for substantially more robust palaeoenvironmental reconstructions. Acknowledgements Funding was received from the European Research Council (ERC) under the European Union’s Seventh Framework Programme (FP7/2007e2013)/ERC Starting Grant “HYRAX”, grant agreement no. 258657, and from the Leverhulme Trust grants F/08 773/C and F/ 00 212/AF. L. Scott is supported by the South African National

Research Foundation, Pretoria (GUN 2053236). We would also like to thank Matthew Britton and Ian Newton for assistance in collecting and analyzing the material, and Claudio Latorre and an anonymous reviewer for provide constructive comments that have helped to improve this paper. This paper is ISEM contribution 2012-131. References Adelman, S., Taylor, C.R., Heglund, N.C., 1975. Sweating on palms and paws: what is its function? American Journal of Physiology 229, 1400e1402. Ambrose, S.H., 1991. Effects of diet, climate and physiology on nitrogen isotope abundances in terrestrial foodwebs. Journal of Archaeological Science 18, 293e317. Ambrose, S.H., DeNiro, M.J., 1986a. The isotopic ecology of East African mammals. Oecologia 69, 395e406. Ambrose, S.H., DeNiro, M.J., 1986b. Reconstruction of African human diet using bone collagen carbon and nitrogen isotope ratios. Nature 319, 321e324. Anderson, R.S., Betancourt, J.L., Mead, J.I., Hevly, R.H., Adam, D.P., 2000. Middle- and late-Wisconsin paleobotanic and paleoclimatic records from the southern Colorado Plateau, USA. Palaeogeography, Palaeoclimatology, Palaeoecology 155, 31e57. Aranibar, J.N., Otter, L., Macko, S.A., Feral, C.J.W., Epstein, H.E., Dowty, P.R., Eckardt, F., Shugart, H.H., Swap, R.J., 2004. Nitrogen cycling in the soil-plant system along a precipitation gradient in the Kalahari sands. Global Change Biology 10, 359e373. Arens, N.C., Jahren, A.H., Amundson, R., 2000. Can C3 plants faithfully record the carbon isotopic composition of atmospheric carbon dioxide? Paleobiology 26, 137e164. Barry, R., Bloomer, P., Hoeck, H., Shoshani, H., 2008. IUCN 2011. IUCN Red List of Threatened Species. Bartholomew, G.A., Rainy, M., 1971. Regulation of body temperature in the rock hyrax, Heterohyrax brucei. Journal of Mammalogy 52, 81e95. Betancourt, J.L., Davis, O.K., 1984. Packrat middens from Canyon de Chelly, northeastern Arizona: paleoecological and archaeological implications. Quaternary Research 21, 56e64. Betancourt, J.L., Latorre, C., Rech, J.A., Quade, J., Rylander, K.A., 2000. A 22,000-year record of monsoonal precipitation from Northern Chile’s Atacama Desert. Science 289, 1542e1546. Betancourt, J.L., Pierson, E.A., Aasen Rylander, K., Fairchild-Parks, J.A., Dean, J.S., 1993. Influence of history and climate on New Mexico Pinyon-juniper Woodlands. Managing Pinyon-Juniper for Sustainability and Social Needs. Department of Agriculture, Forest General Technical Reports, Santa Fe, pp. 42e62. Betancourt, J.L., Schuster, W.S., Mitton, J.B., Anderson, R.S., 1991. Fossil and genetic history of a pinyon pine (Pinus edulis) isolate. Ecology 72, 1685e1697. Betancourt, J.L., van Devender, T.R., Martin, P.S., 1990. Packrat Middens: The Last 40,000 Years of Biotic Change. University of Arizona Press, Tucson. Bi, X., Sheng, G., Liu, X., Li, C., Fu, J., 2005. Molecular and carbon and hydrogen isotopic composition of n-alkanes in plant leaf waxes. Organic Geochemistry 36, 1405e1417. Bousman, B., Scott, L., 1994. Climate or overgrazing: the palynological evidence for vegetation change in the eastern Karoo. South African Journal of Science 90, 575e578. Bristow, A.W., Whitehead, D.C., Cockburn, J.E., 1992. Nitrogenous constituents in the urine of cattle, sheep and goats. Journal of the Science of Food and Agriculture 59, 387e394. Brittain, H.G., 2009. Vibrational Spectroscopic studies of Cocrystals and salts. 1. The benzamide-benzoic acid system. Crystal Growth and Design 9, 2492e2499. Brown, K.J., Downs, C.T., 2006. Seasonal patterns in body temperature of free-living rock hyrax (Procavia capensis). Comparative Biochemistry and Physiology e Part A: Molecular & Integrative Physiology 143, 42e49. Bruce, J., 1790. Travels to Discover the Source of the Nile. Burrough, S.L., Breman, E., Dodd, C., 2012. Can phytoliths provide an insight into past vegetation of the Middle Kalahari palaeolakes during the late Quaternary? Journal of Arid Environments 82, 156e164. Burrough, S.L., Thomas, D.S.G., Singarayer, J.S., 2009. Late Quaternary hydrological dynamics in the Middle Kalahari: forcing and feedbacks. Earth-Science Reviews 96, 313e326. Carr, A.S., Boom, A., Chase, B.M., 2010. The potential of plant biomarker evidence derived from rock hyrax middens as an indicator of palaeoenvironmental change. Palaeogeography, Palaeoclimatology, Palaeoecology 285, 321e330. Carr, A.S., Fisher, K., Boom, A., Chase, B.M., Meadows, M.E., Reimer, P.J., 2011. Late Quaternary Palaeohydrology and Palaeoecology of Southern Africa Revealed by Lipid Biomarker Analysis of Rock Hyrax Middens. XVIII INQUA-Congress, Bern, Switzerland. Carrión, J.S., Scott, L., Vogel, J.C., 1999. Twentieth century changes in montane vegetation in the eastern Free State, South Africa, derived from palynology of hyrax dung middens. Journal of Quaternary Science 14, 1e16. Castañeda, I.S., Mulitza, S., Schefuß, E., Lopes dos Santos, R.A., Sinninghe Damsté,, J.S., Schouten, S., 2009a. Wet phases in the Sahara/Sahel region and human migration patterns in North Africa. Proceedings of the National Academy of Sciences 106, 20159e20163.

B.M. Chase et al. / Quaternary Science Reviews 56 (2012) 107e125 Castañeda, I.S., Werne, J.P., Johnson, T.C., Filley, T.R., 2009b. Late Quaternary vegetation history of southeast Africa: the molecular isotopic record from Lake Malawi. Palaeogeography, Palaeoclimatology, Palaeoecology 275, 100e112. Cerling, T.E., Hart, J.A., Hart, T.B., 2004. Stable isotope ecology in the Ituri forest. Oecologia 138, 5e12. Chase, B., 2009. Evaluating the use of dune sediments as a proxy for palaeo-aridity: a southern African case study. Earth-Science Reviews 93, 31e45. Chase, B.M., Meadows, M.E., 2007. Late Quaternary dynamics of southern Africa’s winter rainfall zone. Earth-Science Reviews 84, 103e138. Chase, B.M., Thomas, D.S.G., 2007. Multiphase late Quaternary aeolian sediment accumulation in western South Africa: timing and relationship to palaeoclimatic changes inferred from the marine record. Quaternary International 166, 29e41. Chase, B.M., Meadows, M.E., Carr, A.S., Reimer, P.J., 2010. Evidence for progressive Holocene aridification in southern Africa recorded in Namibian hyrax middens: implications for African Monsoon dynamics and the “African humid period”. Quaternary Research 74, 36e45. Chase, B.M., Meadows, M.E., Scott, L., Thomas, D.S.G., Marais, E., Sealy, J., Reimer, P.J., 2009. A record of rapid Holocene climate change preserved in hyrax middens from southwestern Africa. Geology 37, 703e706. Chase, B.M., Quick, L.J., Meadows, M.E., Scott, L., Thomas, D.S.G., Reimer, P.J., 2011. Late glacial interhemispheric climate dynamics revealed in South African hyrax middens. Geology 39, 19e22. Clark, J.S., 1989. Ecological disturbance as a renewal process: theory and application to fire history. Oikos 56, 17e30. Codron, D., Codron, J., 2009. Reliability of d13C and d15N in faeces for reconstructing savanna herbivore diet. Mammalian Biology e Zeitschrift Fur Saugetierkunde 74, 36e48. Collatz, G.J., Berry, J.A., Clark, J.S., 1998. Effects of climate and atmospheric CO2 partial pressure on the global distribution of C4 grasses: present, past, and future. Oecologia 114, 441e454. Collister, J.W., Rieley, G., Stern, B., Eglinton, G., Fry, B., 1994. Compound-specific d13C analyses of leaf lipids from plants with differing carbon dioxide metabolisms. Organic Geochemistry 21, 619e627. Cordova, C.E., C3 Poaceae and Restionaceae phytoliths as potential proxies for reconstructing winter rainfall in South Africa. Quaternary International. Cordova, C.E., Scott, L., 2010. The potential of Poaceae, Cyperaceae, and Restionaceae phytoliths to reflect past environmental conditions in South Africa. In: Runge, J. (Ed.), Palaeoecology of Africa. CRC Press Taylor and Francis Group, Boca Raton, Florida, pp. 107e133. Cordova, C.E., Chase, B.M., Smith, G.F. Can phytoliths provide an insight into past vegetation of the Middle Kalahari Paleolakes during the Quaternary? Comment on “Burrough, S.E., Breman, E., and Dodd, C.” Journal of Arid Environments, in press. Cowling, R.M., 1983. Phytochorology and vegetation history in the south-eastern Cape, South Africa (fynbos, renosterveld). Journal of Biogeography 10, 393e419. Dansgaard, W., Johnsen, S.J., Clausen, H.B., Dahl-Jensen, D., Gundestrup, N.S., Hammer, C.U., Hvidberg, C.S., Steffensen, J.P., Sveinbjörnsdottir, A.E., Jouzel, J., Bond, G., 1993. Evidence for general instability of past climate from a 250 kyr ice core record. Nature 364, 218e220. DeNiro, M.J., Epstein, S., 1978. Carbon isotope evidence for different feeding patterns in two hyrax species occupying the same habitat. Science 201, 906e908. Díaz, F.P., Latorre, C., Maldonado, A., Quade, J., Betancourt, J.L., 2012. Rodent middens reveal episodic, long-distance plant colonizations across the hyperarid Atacama Desert over the last 34,000 years. Journal of Biogeography 39, 510e525. Duffin, K.I., 2008. The representation of rainfall and fire intensity in fossil pollen and charcoal records from a South African savanna. Review of Palaeobotany and Palynology 151, 59e71. Dupont, L.M., Behling, H., Jahns, S., Marret, F., Kim, J.-H., 2007. Variability in glacial and Holocene marine pollen records offshore from west southern Africa. Vegetation History and Archaeobotany 16, 87e100. Dupont, L.M., Donner, B., Vidal, L., Pérez, E.M., Wefer, G., 2006. Linking desert evolution and coastal upwelling: pliocene climate change in Namibia. Geology 33, 461e464. Dupont, L.M., Linder, H.P., Rommerskirchen, F., Schefuß, E., 2011. Climate-driven rampant speciation of the Cape flora. Journal of Biogeography 38, 1059e1068. Eglinton, T.I., Eglinton, G., Dupont, L.M., Sholkovitz, E.R., Montluçon, D., Reddy, C.M., 2002. Composition, age, and provenance of organic matter in NW African dust over the Atlantic Ocean. Geochemistry, Geophysics, Geosystems 3, 27 pp. Ehleringer, J.R., Cerling, T.E., 1995. Atmospheric CO2 and the ratio of intercellular to ambient CO2 concentrations in plants. Tree Physiology 15, 105e111. Ehleringer, J.R., Cooper, T.A., 1988. Correlations between carbon isotope ratio and microhabitat of desert plants. Oecologia 76, 562e566. Ehleringer, J.R., Cerling, T.E., Helliker, B.R., 1997. C4 photosynthesis, atmospheric CO2, and climate. Oecologia 112, 285e299. Eitel, B., Kadereit, A., Blümel, W.D., Hüser, K., Kromer, B., 2005. The Amspoort Silts, northern Namib Desert (Namibia): formation, age and palaeoclimatic evidence of river-end deposits. Geomorphology 64, 299e314. Fall, P.L., 1990. Deforestation in southern Jordan: evidence from fossil hyrax middens. In: Entjes-Nieborg, G., van Zeist, W. (Eds.), Man’s role in shaping the eastern Mediterranean landscape. Balkema, Rotterdam. Fall, P.L., Lindquist, C.A., Falconer, S.E., 1990. Fossil hyrax middens from the Middle East: a record of paleovegetation and human disturbance. Packrat Middens, 408e427.

123

Farmer, E.C., deMenocal, P.B., Marchitto, T.M., 2005. Holocene and deglacial ocean temperature variability in the Benguela upwelling region: implications for lowlatitude atmospheric circulation. Paleoceanography 20. http://dx.doi.org/ 10.1029/2004PA001049. Farquhar, G.D., Richards, R.A., 1984. Isotopic composition of plant carbon correlates with wtaer-use efficiency of wheat genotypes. Australian Journal of Plant Physiology 11, 539e552. Farquhar, G.D., Sharkey, T.D., 1982. Stomatal conductance and photosynthesis. Annual Review of Plant Physiology 33, 317e345. Finné, M., Norström, E., Risberg, J., Scott, L., 2010. Siliceous microfossils as late Quaternary paleo-environmental indicators at Braamhoek wetland, South Africa. The Holocene. 0959683610362810. Gayo, E.M., Latorre, C., Santoro, C.M., Maldonado, A., De Pol-Holz, R., 2012. Hydroclimate variability in the low-elevation Atacama Desert over the last 2500 yr. Climate of the Past 8, 287e306. Gil-Romera, G., Scott, L., Marais, E., Brook, G.A., 2006. Middle- to late-Holocene moisture changes in the desert of northwest Namibia derived from fossil hyrax dung pollen. Holocene 16, 1073e1084. Gil-Romera, G., Scott, L., Marais, E., Brook, G.A., 2007. Late Holocene environmental change in the northwestern Namib Desert margin: new fossil pollen evidence from hyrax middens. Palaeogeography, Palaeoclimatology, Palaeoecology 249, 1e17. Gil-Romera, G., Turton, D., Sevilla-Callejo, M., 2011. Landscape change in the lower Omo valley, southwestern Ethiopia: burning patterns and woody encroachment in the savanna. Journal of Eastern African Studies 5, 108e128. Gil-Romera, G., Lamb, H.F., Turton, D., Sevilla-Callejo, M., Umer, M., 2010. Long-term resilience, bush encroachment patterns and local knowledge in a Northeast African savanna. Global Environmental Change 20, 612e626. Goldblatt, P., Manning, J.C., 2002. Plant diversity of the Cape region of southern Africa. Annals of the Missouri Botanical Garden 89, 281e302. Grimm, E.C., Maher Jr., L.J., Nelson, D.M., 2009. The magnitude of error in conventional bulk-sediment radiocarbon dates from central North America. Quaternary Research 72, 301e308. Haltenorth, T., Diller, H., 1977. A Field Guide to the Mammals of Africa Including Madagascar. Collins, London. Handley, L.L., Austin, A.T., Stewart, G.R., Robinson, D., Scrimgeour, C.M., Raven, J.A., Heaton, T.H.E., Schmidt, S., 1999. The 15N natural abundance (d15N) of ecosystem samples reflects measures of water availability. Functional Plant Biology 26, 185e199. Heaton, T.H.E., Vogel, J.C., von la Chevallerie, G., Collet, G., 1986. Climate influence on the isotopic composition of bone nitrogen. Nature 322, 822e823. Hedges, R.E.M., Stevens, R.E., Richards, M.P., 2004. Bone as a stable isotope archive for local climatic information. Quaternary Science Reviews 23, 959e965. Hedges, R.E.M., Stevens, R.E., Richards, M.P., 2006. Isotopes in bones and teeth. In: Leng, M.J. (Ed.), Isotopes in Palaeoenvironmental Research, pp. 117e145. Higuera, P.E., Gavin, D.G., Bartlein, P.J., Hallett, D.J., 2010. Peak detection in sediment-charcoal records: impacts of alternative data analysis methods on fire-history interpretations. International Journal of Wildland Fire 19, 996e 1014. Hoeck, H.N., 1975. Differential feeding behaviour of the sympatric hyrax: (Procavia johnstoni and Heterohyrax brucei). Oecologia 22, 15e47. Hofreiter, M., Mead, J.I., Martin, P., Poinar, H.N., 2003. Molecular caving. Current Biology 13, R693eR695. Hofreiter, M., Poinar, H.N., Spaulding, W.G., Bauer, K., Martin, P.S., Possnert, G., Pääbo, S., 2000. A molecular analysis of ground sloth diet through the last glaciation. Molecular Ecology 9, 1975e1984. Holmgren, C.A., Rosello, E., Latorre, C., Betancourt, J.L., 2008. Late-Holocene fossil rodent middens from the Arica region of northernmost Chile. Journal of Arid Environments 72, 677e686. Holmgren, K., Lee-Thorp, J.A., Cooper, G.R.J., Lundblad, K., Partridge, T.C., Scott, L., Sithaldeen, R., Talma, A.S., Tyson, P.D., 2003. Persistent millennial-scale climatic variability over the past 25,000 years in Southern Africa. Quaternary Science Reviews 22, 2311e2326. Holmgren, C.A., Betancourt, J.L., Rylander, K.A., Roque, J., Tovar, O., Zeballos, H., Linares, E., Quade, J., 2001. Holocene vegetation history from fossil rodent middens near Arequipa, Peru. Quaternary Research 56, 242e251. Horowitz, A., 1992. Palynology of Arid Lands. Elsevier, Amsterdam. Hubbard, R.N.L.B., Sampson, C.G., 1993. Rainfall estimates derived from the pollen content of modern hyrax dung: an evaluation. South African Journal of Science 89, 199e204. Indermühle, A., Stocker, T.F., Joos, F., Fischer, H., Smith, H.J., Wahlen, M., Deck, B., Mastroianni, D., Tschumi, J., Blunier, T., Meyer, R., Stauffer, B., 1999. Holocene carbon-cycle dynamics based on CO2 trapped in ice at Taylor Dome, Antarctica. Nature 398, 121e126. IUCN, 2011. IUCN Red List of Threatened Species, Version 2011.2. IUCN. Jouzel, J., Masson-Delmotte, V., Cattani, O., Dreyfus, G., Falourd, S., Hoffmann, G., Minster, B., Nouet, J., Barnola, J.M., Chappellaz, J., Fischer, H., Gallet, J.C., Johnsen, S., Leuenberger, M., Loulergue, L., Luethi, D., Oerter, H., Parrenin, F., Raisbeck, G., Raynaud, D., Schilt, A., Schwander, J., Selmo, E., Souchez, R., Spahni, R., Stauffer, B., Steffensen, J.P., Stenni, B., Stocker, T.F., Tison, J.L., Werner, M., Wolff, E.W., 2007. Orbital and millennial Antarctic climate variability over the past 800,000 years. Science 317, 793e797. Kaufman, A., Broecker, W., 1965. Comparison of Th230 and C14 ages for carbonate materials from lakes Lahontan and Bonneville. Journal of Geophysical Research 70, 4039e4054.

124

B.M. Chase et al. / Quaternary Science Reviews 56 (2012) 107e125

Kawamura, K., Ishimura, Y., Yamazaki, K., 2003. Four years’ observations of terrestrial lipid class compounds in marine aerosols from the western North Pacific. Global Biogeochemical Cycles 17, 1003. Keeley, J., Pausas, J., Rundel, P., Bond, W., Bradstock, R., 2011. Fire as an evolutionary pressure shaping plant traits. Trends in Plant Science 16, 406e411. King, J.E., van Devender, T.R., 1977. Pollen analysis of fossil packrat middens from the Sonoran Desert. Quaternary Research 8, 191e204. Kingdon, J., 1971. East African Mammals. Academic Press, London. Kleinschmidt, T., Czelusniak, J., Goodman, M., Braunitzer, G., 1986. Paenungulata: a comparison of the hemoglobin sequences from elephant, hyrax, and manatee. Molecular Biology and Evolution 3, 427e435. Kniseley, R.N., Fassel, V.A., Farquhar, E.L., Gray, L.S., 1962. Infrared spectra of nitrogen containing compounds I e benzamide. Spectrochimica Acta 18, 1217e1229. Kotler, B.P., Brown, J.S., Knight, M.H., 1999. Habitat and patch use by hyraxes: there’s no place like home? Ecology Letters 2, 82e88. Kuch, M., Rohland, N., Betancourt, J.L., Latorre, C., Steppan, S., Poinar, H.N., 2002. Molecular analysis of a 11 700-year-old rodent midden from the Atacama Desert, Chile. Molecular Ecology 11, 913e924. Lancaster, N., 1979. Evidence for a widespread Late Pleistocene humid period in the Kalahari. Nature 279, 145e146. Lancaster, N., 2002. How dry was dry? Late Pleistocene palaeoclimates in the Namib Desert. Quaternary Science Reviews 21, 769e782. Latorre, C., Betancourt, J.L., Rylander, K.A., Quade, J., Matthei, O., 2003. A vegetation history from the arid prepuna of northern Chile (22e23 S) over the last 13,500 years. Palaeogeography, Palaeoclimatology, Palaeoecology 194, 223e246. Latorre, C., Betancourt, J.L., Arroyo, M.T.K., 2006. Late Quaternary vegetation and climate history of a perennial river canyon in the Rio Salado basin (22 S) of northern Chile. Quaternary Research 65, 450e466. Lee-Thorp, J.A., Hohngren, K., Lauritzen, S.-E., Linge, H., Moberg, A., Partridge, T.C., Stevenson, C., Tyson, P.D., 2001. Rapid climate shifts in the southern African interior throughout the mid- to late Holocene. Geophysical Research Letters 28, 4507e4510. Leon, B., Belonje, P.C., 1979. Calcium, phosphorus and magnesium excretion in the rock hyrax, Procavia capensis. Comparative Biochemistry and Physiology Part A: Physiology 64, 67e72. Louw, E., Louw, G.N., Retief, C.P., 1972. Thermolability, heat tolerance and renal function in the dassie or hyrax (Procavaia capensis). Zoologie Africana 7, 451e 469. Maldonado, A., Betancourt, J.L., Latorre, C., Villagran, C., 2005. Pollen analyses from a 50 000-yr rodent midden series in the southern Atacama Desert (25 30 S). Journal of Quaternary Science 20, 493e507. Maloiy, G.M.O., 1972. Renal salt and water excretion in the camel (Camelus dromedarius). Symposium of the Zoological Society of London 31, 243e259. Maloiy, G.M.O., Eley, R.M., 1992. The Hyrax. Regal Press, Nairobi. Maloiy, G.M.O., Sale, J.B., 1976. Renal function and electrolyte balance during dehydration in the hyrax. Israel Journal of Medical Sciences 12, 852e853. McCarthy, L., Head, L., Quade, J., 1996. Holocene palaeoecology of the northern Flinders Ranges, South Australia, based on stick-nest rat (Leporillus spp.) middens: a preliminary overview. Palaeogeography, Palaeoclimatology, Palaeoecology 123, 205e218. Meadows, M.E., Baxter, A.J., 1999. Late Quaternary palaeoenvironments of the southwestern Cape, South Africa: a regional synthesis. Quaternary International 57 (8), 193e206. Meadows, M.E., Sugden, J.M., 1991. A vegetation history of the last 14,000 years on the Cederberg, southwestern Cape Province. South African Journal of Science 87, 34e43. Meadows, M.E., Chase, B.M., Seliane, M., 2010. Holocene palaeoenvironments of the Cederberg and Swartruggens mountains, Western Cape, South Africa: pollen and stable isotope evidence from hyrax dung middens. Journal of Arid Environments 74, 786e793. Meltzer, A., 1976. Water economy of the hyrax. Isreal Journal of Medical Science 12, 862e863. Monnin, E., Indermühle, A., Dällenbach, A., Flückiger, J., Stauffer, B., Stocker, T.F., Raynaud, D., Barnola, J.-M., 2001. Atmospheric CO2 concentrations over the last glacial termination. Science 291, 112e114. Murphy, B.P., Bowman, D.M.J.S., 2006. Kangaroo metabolism does not cause the relationship between bone collagen d15N and water availability. Functional Ecology 20, 1062e1069. Murphy, B.P., Bowman, D.M.J.S., 2009. The carbon and nitrogen isotope composition of Australian grasses in relation to climate. Functional Ecology 23, 1040e1049. Murray, D.C., Pearson, S.G., Fullagar, R., Chase, B.M., Houston, J., Atchison, J., White, N.E., Bellgard, M.I., Clarke, E., Macphail, M., Gilbert, M.T.P., Haile, J., Bunce, M., Deep Sequencing of Ancient Plant and Mammal DNA Preserved in Arid and Semi-Arid Zone Middens. Quaternary Science Reviews, submitted for publication. Partridge, T.C., Scott, L., Hamilton, J.E., 1999. Synthetic reconstructions of southern African environments during the Last Glacial Maximum (21e18 kyr) and the Holocene Altithermal (8e6 kyr). Quaternary International 57 (8), 207e214. Pate, J.S., 2001. Carbon isotope discrimination and plant water-use efficiency: case scenarios for C3 plants. In: Unkovich, M., Pate, J., McNeill, A., Gibbs, D.J. (Eds.), Stable Isotope Techniques in the Study of Biological Processes and Functioning of Ecosystems. Kluwer Academic Publishers, Dordrecht, pp. 19e37. Pearson, S., 1999. Late Holocene biological records from the middens of stick-nest rats in the central Australian arid zone. Quaternary International 59, 39e46. Pearson, S., Betancourt, J.L., 2002. Understanding arid environments using fossil rodent middens. Journal of Arid Environments 50, 499e511.

Pearson, S., Dodson, J.R., 1993. Stick-nest rat middens as sources of paleoecological data in Australian deserts. Quaternary Research 39, 347e354. Peters, K.E., 2005. The Biomarker Guide. In: Biomarkers and Isotopes in the Environment and Human History, vol. 1. Cambridge University Press, Cambridge, UK. Poinar, H., Kuch, M., McDonald, G., Martin, P., Pääbo, S., 2003. Nuclear gene sequences from a Late Pleistocene sloth coprolite. Current Biology 12, 1150e 1152. Polley, H.W., Johnson, H.B., Marinot, B.D., Mayeux, H.S., 1993. Increase in C3 plant water-use efficiency and biomass over Glacial to present C02 concentrations. Nature 361, 61e64. Pons, A., Quézel, P., 1958. Première remarques sur l’étude palynologique d’un guano fossile du Hoggar. Comptes Rendus des Scéances de L’Académie des Sciences 244, 2290e2292. Prinsloo, L.C., 2007. Rock hyraces: a cause of San rock art deterioration? Journal of Raman Spectroscopy 38, 496e503. Prinsloo, P., Robinson, T.J., 1992. Geographic mitochondrial DNA variation in the rock hyrax, Procavia capensis. Molecular Biology and Evolution 9, 447e456. Quick, L.J., Chase, B.M., Meadows, M.E., Scott, L., Reimer, P.J., 2011. A 19.5 kyr vegetation history from the central Cederberg Mountains, South Africa: palynological evidence from rock hyrax middens. Palaeogeography, Palaeoclimatology, Palaeoecology 309, 253e270. Richards, M.P., Hedges, R.E.M., 2003. Variations in bone collagen d13C and d15N values of fauna from Northwest Europe over the last 40,000 years. Palaeogeography, Palaeoclimatology, Palaeoecology 193, 261e267. Rommerskirchen, F., Eglinton, G., Dupont, L., Güntner, U., Wenzel, C., Rullkötter, J., 2003. A north to south transect of Holocene southeast Atlantic continental margin sediments: relationship between aerosol transport and compoundspecific d13C land plant biomarker and pollen records. Geochemistry, Geophysics, Geosystems 4, 1101. Rossouw, L., 2009. The Application of Fossil Grass-phytolith Analysis in the Reconstruction of Cainozoic Environments in the South African Interior. Department of Plant Sciences. University of the Free State, Bloemfontein. Rübsamen, K., Kettembeil, S., 1980. Effect of water restriction on oxygen uptake, evaporative water loss and body temperature of the rock hyrax. Journal of Comparative Physiology 138B, 315e320. Rübsamen, K., Heller, R., Lawrenz, H., Engelhardt, W., 1979. Water and energy metabolism in the rock hyrax (Procavia habessinica). Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology 131, 303e309. Rübsamen, K., Hume, I.D., Engelhardt, W.V., 1982. Physiology of the rock hyrax. Comparative Biochemistry and Physiology Part A: Physiology 72, 271e277. Rudnai, J., 1987. The enigmatic hyrax. Swara 10, 33e34. Rundel, P.W., Esler, K.J., Cowling, R.M., 1999. Ecological and phylogenetic patterns of carbon isotope discrimination in the winter-rainfall flora of the Richtersveld, South Africa. Plant Ecology 142, 133e148. Sale, J.B., 1960. The Hyracoidea: a review of the systematic position and biology of the hyrax. Journal of the East African Natural History Society 23, 185e188. Sale, J.B., 1965a. The feeding behaviour of rock hyraxes (Genera Procavia and Heterohyrax) in Kenya. East African Wildlife 3, 1e18. Sale, J.B., 1965b. Some Aspects of the Behaviour and Ecology of the Rock Hyraxes (Genera Procavia and Heterohyrax) in Kenya. University of London. Sale, J.B., 1966a. Daily food consumption and mode of ingestion in the hyrax. Journal of the East African Natural History Society 3, 215e224. Sale, J.B., 1966b. The habitat of the rock hyrax. Journal of the East African Natural History Society 3, 205e214. Sale, J.B., 1970. The behaviour of the resting rock hyrax in relation to its environment. Zoologica Africana 5, 87e99. Schade, J.D., Hobbie, S.E., 2005. Spatial and temporal variation in islands of fertility in the Sonoran Desert. Biogeochemistry 73, 541e553. Schefuß, E., Schouten, S., Schneider, R.R., 2005. Climatic controls on central African hydrology during the past 20,000 years. Nature 437, 1003e1006. Schmitt, J., Schneider, R., Elsig, J., Leuenberger, D., Lourantou, A., Chappellaz, J., Köhler, P., Joos, F., Stocker, T.F., Leuenberger, M., Fischer, H., 2012. Carbon isotope constraints on the deglacial CO2 rise from ice cores. Science 336, 711e714. Schoeninger, M.J., DeNiro, M.J., 1984. Nitrogen and carbon isotopic composition of bone collagen from marine and terrestrial animals. Geochimica et Cosmochimica Acta 48, 625e639. Schwarcz, H.P., Dupras, T.L., Fairgrieve, S.I., 1999. 15N enrichment in the Sahara: in search of a global relationship. Journal of Archaeological Science 26, 629e636. Schwark, L., Zink, K., Lechterbeck, J., 2002. Reconstruction of postglacial to early Holocene vegetation history in terrestrial Central Europe via cuticular lipid biomarkers and pollen records from lake sediments. Geology 30, 463e466. Scott, L., 1990a. Hyrax (Procaviidae) and dassie rat (Petromuridae) middens in palaeoenvironmental studies in Africa. In: Betancourt, J.L., van Devender, T.R., Martin, P.S. (Eds.), Packrat Middens: The Last 40,000 Years of Biotic Change. University of Arizona Press, Tucson, pp. 408e427. Scott, L., 1990b. Palynological evidence for late Quaternary environmental change in southern Africa. Palaeoecology of Africa 21, 259e268. Scott, L., 1994. Palynology of Late Pleistocene hyrax middens, southwestern Cape Province, South Africa: a preliminary report. Historical Biology 9, 71e81. Scott, L., Bousman, C.B., 1990. Palynological analysis of hyrax middens from Southern Africa. Palaeogeography, Palaeoclimatology, Palaeoecology 76, 367e379. Scott, L., Cooremans, B., 1992. Pollen in recent Procavia (hyrax), Petromus (dassie rat) and bird dung in South Africa. Journal of Biogeography 19, 205e215.

B.M. Chase et al. / Quaternary Science Reviews 56 (2012) 107e125 Scott, L., Vogel, J.C., 2000. Evidence for environmental conditions during the last 20,000 years in Southern Africa from 13C in fossil hyrax dung. Global and Planetary Change 26, 207e215. Scott, L., Woodborne, S., 2007a. Pollen analysis and dating of late Quaternary faecal deposits (hyraceum) in the Cederberg, Western Cape, South Africa. Review of Palaeobotany and Palynology 144, 123e134. Scott, L., Woodborne, S., 2007b. Vegetation history inferred from pollen in late Quaternary faecal deposits (hyraceum) in the Cape winter-rain region and its bearing on past climates in South Africa. Quaternary Science Reviews 26, 941e953. Scott, L., Marais, E., Brook, G.A., 2004. Fossil hyrax dung and evidence of Late Pleistocene and Holocene vegetation types in the Namib Desert. Journal of Quaternary Science 19, 829e832. Sealy, J.C., van der Merwe, N.J., Thorp, J.A.L., Lanham, J.L., 1987. Nitrogen isotopic ecology in southern Africa: implications for environmental and dietary tracing. Geochimica et Cosmochimica Acta 51, 2707e2717. Shi, N., Dupont, L.M., Beug, H.-J., Schneider, R., 2000. Correlation between vegetation in southwestern Africa and oceanic upwelling in the past 21,000 years. Quaternary Research 54, 72e80. Shi, N., Schneider, R., Beug, H.-J., Dupont, L.M., 2001. Southeast trade wind variations during the last 135 kyr: evidence from pollen spectra in eastern South Atlantic sediments. Earth and Planetary Science Letters 187, 311e321. Simpson, G.G., 1945. The principles of classification and a classification of mammals. Bulletin of the American Museum of Natural History 85, 1e350. Sinninghe-Damsté,, J.S., Verschuren, D., Ossebaar, J., Blokker, J., van Houten, R., van der Meer, M.T.J., Plessen, B., Schouten, S., 2011. A 25,000-year record of climateinduced changes in lowland vegetation of eastern equatorial Africa revealed by the stable carbon-isotopic composition of fossil plant leaf waxes. Earth and Planetary Science Letters 302, 236e246. Smith, B.N., 1972. Natural abundance of the stable isotopes of carbon in biological systems. BioScience 22, 226e231. Smith, H.J., Fischer, H., Wahlen, M., Mastroianni, D., Deck, B., 1999. Dual modes of the carbon cycle since the Last Glacial Maximum. Nature 400, 248e250. Sonzogni, C., Bard, E., Rostek, F., 1998. Tropical sea-surface temperatures during the last glacial period: a view based on alkenones in Indian Ocean sediments. Quaternary Science Reviews 17, 1185e1201. Spaulding, W.G., Betancourt, J.L., Croft, L.K., Cole, K.L., 1990. Packrat middens: their composition and methods of analysis. Packrat Middens, 59e84. Sponheimer, M., Robinson, T.F., Roeder, B.L., Passey, B.H., Ayliffe, L.K., Cerling, T.E., Dearing, M.D., Ehleringer, J.R., 2003. An experimental study of nitrogen flux in llamas: is 14N preferentially excreted? Journal of Archaeological Science 30, 1649e1655. Srivastava, P., Brook, G.A., Marais, E., 2005. Depositional environment and luminescence chronology of the Hoarusib River Clay Castles sediments, northern Namib Desert, Namibia. Catena 59, 187e204. Stone, A.E.C., Thomas, D.S.G., Viles, H.A., Late Quaternary palaeohydrological changes in the northern Namib Sand Sea: new chronologies using OSL dating of interdigitated aeolian and water-lain interdune deposits. Palaeogeography, Palaeoclimatology, Palaeoecology, in press. Stuut, J.-B.W., Prins, M.A., Schneider, R.R., Weltje, G.J., Jansen, J.H.F., Postma, G., 2002. A 300 kyr record of aridity and wind strength in southwestern Africa:

125

inferences from grain-size distributions of sediments on Walvis Ridge, SE Atlantic. Marine Geology 180, 221e233. Swap, R.J., Aranibar, J.N., Dowty, P.R., Gilhooly, W.P., Macko, S.A., 2004. Natural abundance of 13C and 15N in C3 and C4 vegetation of southern Africa: patterns and implications. Global Change Biology 10, 350e358. Taberlet, P., Coissac, E., Pompanon, F., Brochmann, C., Willerslev, E., 2012. Towards next-generation biodiversity assessment using DNA metabarcoding. Molecular Ecology 21, 2045e2050. Telfer, M.W., Thomas, D.S.G., 2007. Late Quaternary linear dune accumulation and chronostratigraphy of the southwestern Kalahari: implications for aeolian palaeoclimatic reconstructions and predictions of future dynamics. Quaternary Science Reviews 26, 2617e2630. Thomas, D.S.G., Burrough, S.L., 2012. Interpreting geoproxies of late Quaternary climate change in African drylands: implications for understanding environmental change and early human behaviour. Quaternary International 253, 5e17. Thomas, D.S.G., Shaw, P.A., 2002. Late Quaternary environmental change in central southern Africa: new data, synthesis, issues and prospects. Quaternary Science Reviews 21, 783e797. Tierney, J.E., Russell, J.M., Huang, Y., 2010. A molecular perspective on Late Quaternary climate and vegetation change in the Lake Tanganyika basin, East Africa. Quaternary Science Reviews 29, 787e800. Tierney, J.E., Russell, J.M., Huang, Y., Damste, J.S.S., Hopmans, E.C., Cohen, A.S., 2008. Northern Hemisphere controls on tropical southeast African climate during the past 60,000 years. Science 322, 252e255. Tinner, W., Hu, F.S., 2003. Size parameters, size-class distribution and area-number relationship of microscopic charcoal: relevance for fire reconstruction. The Holocene 13, 499e505. Tinner, W., Hubschmid, P., Wehrli, M., Ammann, B., Conedera, M., 1999. Long-term forest fire ecology and dynamics in southern Switzerland. Journal of Ecology 87, 273e289. van der Merwe, N.J., Medina, E., 1989. Photosynthesis and 13C/12C ratios in Amazonian rain forests. Geochimica et Cosmochimica Acta 53, 1091e1094. Vogts, A., Moossen, H., Rommerskirchen, F., Rullkötter, J., 2009. Distribution patterns and stable carbon isotopic composition of alkanes and alkan-1-ols from plant waxes of African rain forest and savanna C3 species. Organic Geochemistry 40, 1037e1054. Walker, B.H., Ludwig, D., Holling, C.S., Peterman, R.M., 1981. Stability of semi-arid savanna grazing systems. The Journal of Ecology 69, 473e498. Whitlock, C., Higuera, P.E., McWethy, D.B., Briles, C.E., 2010. Paleoecological perspectives on fire ecology: revisiting the fire-regime concept. The Open Ecology Journal 3, 6e23. Williams, D.H., Fleming, I., 1989. Spectroscopic Methods in Organic Chemistry. McGraw-Hill International. Wilson, D.E., Reeder, D.M., 1993. In: Mammal Species of the World: a Taxonomic and Geographic Reference, second ed. Smithsonian Institution Press, Washington, DC, USA. Zhang, Z., Zhao, M., Eglinton, G., Lu, H., Huang, C.-Y., 2006. Leaf wax lipids as paleovegetational and paleoenvironmental proxies for the Chinese Loess Plateau over the last 170 kyr. Quaternary Science Reviews 25, 575e594.