Dental microwear texture analysis of Pliocene Suidae from Hadar and Kanapoi in the context of early hominin dietary breadth expansion

Journal of Human Evolution 132 (2019) 80e100

Contents lists available at ScienceDirect

Journal of Human Evolution journal homepage: www.elsevier.com/locate/jhevol

Dental microwear texture analysis of Pliocene Suidae from Hadar and Kanapoi in the context of early hominin dietary breadth expansion Ignacio A. Lazagabaster a, b, * a b

The Leon Recanati Institute for Maritime Studies and Departments of Maritime Civilizations and Archaeology, University of Haifa, Haifa 3498838, Israel Institute of Human Origins and School of Human Evolution and Social Change, Arizona State University, Tempe, AZ 85282, USA

a r t i c l e i n f o

a b s t r a c t

Article history: Received 6 August 2018 Accepted 29 April 2019

Stable carbon isotope studies suggest that early hominins may have diversified their diet as early as 3.76 Ma. Early Pliocene hominins, including Australopithecus anamensis, had diets that were dominated by C3 resources while Late Pliocene hominins, including Australopithecus afarensisda putative descendant of A. anamensisdhad diets that included both C3 and C4 resources. It has been hypothesized that the expansion of C4 grasslands in eastern Africa during the Pliocene could have prompted hominins to incorporate C4 resources in their diets. However, dental microwear analyses suggest that diet diversification did not involve changes in the mechanical properties of the foods consumed. To provide contextual and comparative information on this issue, the diet of suids from the A. anamensis site of Kanapoi and the A. afarensis site of Hadar is investigated. Using dental microwear texture analyses, it is shown that despite significant dietary overlap, there is evidence for dietary niche partitioning among suids. Based on comparisons with the diet of extant African suids, it is inferred that Nyanzachoerus pattersoni (n ¼ 21) was a mixed feeder, Nyanzachoerus jaegeri (n ¼ 4) and Notochoerus euilus (n ¼ 61) were habitual grazers, and Kolpochoerus afarensis (n ¼ 34) had a broad diet that included hard brittle foods and underground resources. The dental microwear of Ny. pattersoni and Ny. jaegeri/No. euilus do not differ significantly between Kanapoi and Hadar. Most differences are driven by K. afarensis, a suid absent at Kanapoi but present at Hadar. Food availability probably differed between Hadar and Kanapoi, and it is likely that A. afarensis did not exploit some of the foods (e.g., underground resources) consumed by suids. It is hypothesized that despite the incorporation of C4 resources in the diet, a significant dietary change towards flexible diets in the hominin lineage had yet to come. © 2019 Elsevier Ltd. All rights reserved.

Keywords: Australopithecus Paleodiet Mammal Suid Pig Kanapoi

1. Introduction Dietary changes likely played a critical role in shaping early hominin evolutionary history (Teaford and Ungar, 2000; Sponheimer and Dufour, 2009; Lee-Thorp et al., 2010, 2012; Ungar and Sponheimer, 2011; Cerling et al., 2013; Sponheimer et al., 2013; Levin et al., 2015). Stable carbon isotope studies show that the earliest hominins for which there is data, Ardipithecus ramidus and Australopithecus anamensis, had diets that were strongly dominated by C3 resources (Ungar and Sponheimer, 2011; LeeThorp et al., 2010, 2012; Cerling et al., 2013; Sponheimer et al., 2013), while late Pliocene hominins, including Kenyanthropus platyops and Australopithecus afarensis, had diets with more varied

* Corresponding author. E-mail address: [email protected]. https://doi.org/10.1016/j.jhevol.2019.04.010 0047-2484/© 2019 Elsevier Ltd. All rights reserved.

stable carbon isotopic signatures that included a mix of both C3 and C4 resources (Sponheimer et al., 2013; Wynn et al., 2013, 2016). The incorporation of C4 resources in hominin diets occurred as early as 3.76 Ma, as evidenced by data from Woranso-Mille (Afar, Ethiopia; Levin et al., 2015). The hominin fossil remains from Woranso-Mille between 3.76 and 3.57 Ma have affinities to both A. anamensis and A. afarensis (Haile-Selassie and Melillo, 2015) and, for this reason, they have been argued to occupy a phyletic intermediate position (Haile-Selassie et al., 2010) in the hypothesized anagenetic lineage formed by these two hominin species (Kimbel et al., 2006). This supports the notion that the stable carbon isotopic changes that occurred at this time in the A. anamensiseA. afarensis lineage (Sponheimer and Dufour, 2009; Sponheimer et al., 2013; Levin et al., 2015) were coupled with morphological changes in the masticatory apparatus (Ward et al., 1999, 2001, 2010, 2013; Kimbel et al., 2004, 2006; White et al., 2006; Kimbel and Delezene, 2009). These craniodental changes suggest an adaptive shift to a diet

I.A. Lazagabaster / Journal of Human Evolution 132 (2019) 80e100

involving heavier mastication with the postcanine dentition and to a different use of the anterior dentition in food processing (Kimbel and Delezene, 2009; Ward et al., 2010). The craniodental anatomical repertoire of A. anamensis and A. afarensis is also indicative of the processing of hard foods, including nuts, seeds, and hard seasonal fruits (McHenry, 1984; Kay, 1985; Grine and Martin, 1988; Ward et al., 1999, 2001; Wood and Richmond, 2000; White et al., 2000; Ungar, 2004; Macho et al., 2005). The occlusal and buccal molar microwear exhibited by these two hominins, however, resembles that of living primates that consume softer fruits and foliage, like Pan troglodytes, Gorilla gorilla, Alouatta palliata, and Trachypithecus cristatus (Teaford and Ungar, 2000; Grine et al., 2006a, b; Estebaranz et al., 2009; Ungar et al., 2010; Delezene et al., 2013; but see Estebaranz et al., 2012). The occlusal microwear textures of A. afarensis premolars do not manifest a regular consumption of hard food objects either (Delezene et al., 2013). There is no strong evidence that diversity in dietary resources, as indicated by increasing C4 foods in hominin diets, was paralleled by significant changes in the physical properties of those foods. The apparent incongruence between the craniodental morphology, the stable carbon isotopes, and the dental microwear of A. anamensis and A. afarensis, lacks a consensual explanation. It has been suggested that the specialized craniodental morphology of A. anamensis and A. afarensis would have allowed for the use of hard brittle resources as fallback foods (Grine et al., 2006a, b; Ungar et al., 2010). The absence of dental microwear values indicative of hard brittle food consumption could be due to the low probability of registering an occasional feeding behavior through dental microwear analyses, a technique which only captures the last days or weeks of the individual's activity before death (Teaford and Oyen, 1989). The variability in d13C values of A. afarensis could have been the result of this species' proclivity to forage in different microhabitats, like it has been observed in modern chimpanzees (Pruetz and Bertolani, 2009), or its ability to change the main foods exploited depending on their availability through time. The fossil record at hominin sites usually spans hundreds of thousands of years and it is conceivable that environmentally-driven diet changes occurred in narrower temporal intervals (Hopley and Maslin, 2010; Cerling et al., 2013; Sponheimer et al., 2013). Such habitat selectivity might have buffered A. afarensis in the face of environmental change (Sponheimer et al., 2013; Wynn et al., 2016). It is unclear to what extent did the feeding behavior of A. afarensis differ from A. anamensis and whether environmental change was the main driver behind the increase in stable carbon isotope variabilitydbut not in occlusal dental microweardin A. afarensis. This issue would greatly benefit from a better understanding of the dietary changes in co-occurring mammalian groups, particularly herbivores or omnivores, whose dietary niches could have overlapped with early hominins. One of these mammal groups are the extinct relatives of pigs (Suidae). The rapid evolution of suid dentition, their flexible dietary behaviors, and the large amount of suid fossils recovered from Plio-Pleistocene eastern African sediments alongside hominin remains (Harris and White, 1979; White, 1995), make them an ideal group to examine the relationship between dietary shifts and environmental changes in the evolutionary context of the A. anamensiseA. afarensis lineage. Most of the A. anamensis material (~70%) comes from Kanapoi, a ~4.2e3.9 Ma site in the Turkana Basin, northern Kenya (Fig. 1; Ward et al., 1999, 2001, 2010, 2013; Kimbel et al., 2006; White et al., 2006). This species is also known from Allia Bay (~3.9 Ma), Turkana Basin (Leakey et al., 1995; Ward et al., 2001; Schoeninger et al., 2003), the Middle Awash (4.2e4.1 Ma) in the Afar region of northern Ethiopia (White et al., 2006), and possibly Fejej, in southern Ethiopia (Ward, 2014). Approximately 90% of the fossil sample of A. afarensis has been recovered from Pliocene

81

sedimentary deposits at Hadar (3.45e2.95 Ma), in the Afar (Fig. 1; Kimbel et al., 1994, 2004; Kimbel and Delezene, 2009; Ward and Kimbel, 2012). Remains of A. afarensis have also been found at Maka (~3.4 Ma), in the Middle Awash (White et al., 1993, 2000), at Dikika (3.4e3.3 Ma; Alemseged et al., 2005, 2006) also in the Afar, at Koobi Fora (~3.3 Ma, Tulu Bor Member; Kimbel, 1988), in the Turkana Basin, at Kantis (3.5e3.4 Ma; Mbua et al., 2016), in Kenya, and at Laetoli (3.7e3.5 Ma), in Tanzania (Harrison, 2011). Because Kanapoi and Hadar have produced the largest collection of fossils attributed to A. anamensis and A. afarensis respectively, they have been intensively studied and there is a large body of literature dealing with paleoenvironmental and paleoecological issues at these two sites. Here, dental microwear texture analysis is used to study the diets of fossil suids at Hadar and Kanapoi, expanding the results presented in Ungar et al. (2017). A dental microwear texture baseline on modern suids is used to infer the diet of fossil suids, which are in turn used as a proxy for paleohabitat reconstruction and to examine if changes in suid diets between Kanapoi and Hadar paralleled those seen in early hominins. The results are framed in the context of resource availability, dietary breadth expansion, and paleohabitat reconstructions of A. anamensis and A. afarensis (Bonnefille et al., 1987, 2004; Reed, 1997, 2008; Hailemichael, 2000; Wynn, 2000; Hailemichael et al., 2002; Manthi, 2006; Aronson et al., 2008; Behrensmeyer, 2008; Campisano and Feibel, 2008; Bonnefille, 2010; Wynn et al., 2016; Manthi et al., 2017; Robinson et al., 2017; Ungar et al., 2017; Dumouchel, 2018; Dumouchel and Bobe, 2019). 1.1. Dietary background of extant African suids Extant African suids occupy a wide range of habitats, but they are mostly associated with forested and mixed grassland-woodland settings (Meijaard et al., 2011; Kingdon, 2015). Extant warthogs (Phacochoerus), for example, are well adapted to the savanna grasslands of sub-Saharan Africa but are most often found where there is some tree, bush, or tall grass cover and within range of permanent water sources (Cumming, 1975, 2013). The majority of extant suids are generalized omnivores, capable of exploiting a variety of foods, including underground plant parts (Leus and MacDonald, 1997; Nowak, 1999; Meijaard et al., 2011; Kingdon, 2015), which they access using their long snouts and incisors (i.e., rooting; Ewer, 1958; Lazagabaster, 2013; Kingdon, 2015). Ecological and morphological studies suggest that some fossil suids were also capable of exploiting these underground resources (Cooke, 1978a; Harris and White, 1979; Harris, 1983; Pickford et al., 2004; Lazagabaster, 2013; van der Made, 2013; Hou et al., 2014). Five suid species inhabit sub-Saharan Africa today (Kingdon, 2015): Potamochoerus porcus (red river hog), Potamochoerus larvatus (bushpig), Hylochoerus meinertzhageni (giant forest hog), Phacochoerus africanus (common warthog), and Phacochoerus aethiopicus (dessert warthog). Extant species of the genus Potamochoerus have a typical, generalized suid postcanine dentition like that of wild boars (genus Sus) and are characterized by lowcrowned bunodont teeth with relatively thick enamel. Modern Potamochoerus species are generalist omnivores, capable of effectively exploiting a wide array of foods, including leaves, nuts, tubers, roots, invertebrates, and small vertebrates (Meijaard et al., 2011; Kingdon, 2015). While Po. porcus inhabits mostly forested areas, including the humid rainforests of Sub-Saharan Africa, Po. larvatus can be found in riverine or xeric scrub forests and thicket formations from southern Ethiopia to South Africa (Skinner et al., 1976; Breytenbach and Skinner, 1982; Jones, 1984; Seydack, 1990; Nowak, 1999; Meijaard et al., 2011). There are also areas in Central Africa where populations of both Po. porcus and Po. larvatus are sympatric (Kingdon, 2015). Hylochoerus meinertzhageni is the

82

I.A. Lazagabaster / Journal of Human Evolution 132 (2019) 80e100

Figure 1. Location of Kanapoi and Hadar. A) Map of Africa. B) A section of Eastern Africa with the location of the two sites (green dots). C) A chronogram showing the temporal distribution of hominin taxa (dark gray) and suid taxa (light gray). Discontinued lines denote ancestor-descendant relationships among taxa. (For interpretation of the references to color in this figure legend, the reader is referred to the Web version of this article).

largest of all extant African suids and possesses lophodont-like dentition. It feeds mainly on grasses, sedges, herbs, and foliage, but it prefers fresh short-grasses instead of old or dry grasses (Kingdon, 2015). Stable carbon isotope analyses indicate the consumption of up to 25% of C4 resources at the beginning of the rainy season (Cerling and Viehl, 2004). The populations of H. meinertzhageni are scattered across tropical Africa and mostly occupy forest/grassland mosaics and montane to lowland thickets and forests (d’Huart, 1978; Viehl, 2003; d’Huart and Yohannes, 2014; Kingdon, 2015). Phacochoerus species (Ph. Africanus and Ph. Aethiopicus) are characterized by extremely hypsodont and elongated third molars formed by multiple rows of columnar pillars. In line with the dental evidence, observational and isotopic data show that Phacochoerus species are mainly grazers (Cumming, 1975, 2013; Harris and Cerling, 2002; Meijaard et al., 2011), though some populations feed on fruits, nuts, and underground resources seasonally (Cumming, 1975, 2013). Some individuals have been seen feeding on vertebrate prey and carcasses (Roberts, 2012). Phacochoerus species mostly inhabit grasslands, open bushlands, and woodlands in sub-Saharan Africa (Cumming, 2013), though some populations occupy more forested habitats in certain parts of eastern Africa (Butynski and de Jong, 2017; Teklehaimanot and Balakrishnan, 2017). Both H. meinertzhageni and Phacochoerus lack the specific craniodental adaptations for rooting found in other suids, but while Phacochoerus are still able to dig using the tusks and snout, H. meinertzhageni rarely engages in rooting (Meijaard et al., 2011; Lazagabaster, 2013). 1.2. The importance of fossil Suidae in paleoanthropology Suids initially rose to importance in human evolutionary studies when they helped to resolve a controversy in the 1970s regarding the age of the early Homo skull KNM-ER 1470 recovered from Koobi Fora, Kenya (White, 1995). Since then, suid fossils have continued to be intensively studied for biochronological purposes (White and

Harris, 1977; Cooke, 1978b, 1985; Harris and White, 1979), but also for hominin habitat reconstructions (Bishop, 1994, 1999; Bishop et al., 1999; Bobe et al., 2002; Lazagabaster et al., 2018a) and other paleoecological issues relevant to human evolution (White, 1995; Cooke, 2007; Souron, 2012; Geraads and Bobe, 2017a; Lazagabaster et al., 2018a). One of the main reasons that suids are so useful in the context of human evolution is that their dentition underwent rapid and significant evolution during the PlioPleistocene in Africa (Harris and White, 1979; Cooke, 1978b, 2007; Souron, 2012, 2017), possibly in response to dietary shifts triggered by global and/or regional climatic changes (deMenocal, 1995, 2004; Bobe et al., 2002; Wynn et al., 2016; Robinson et al., 2017; Lazagabaster et al., 2018a). As grasslands and bushlands
galen et al., 2007; Bonnefille, 2010; Cerling et al., 2011, expanded (Se 2015; Feakins et al., 2013), some suid lineages presumably adapted their masticatory apparatus to the consumption of foods with a higher content of abrasive particles, such as silica and grit associated with grasses. Some of the most evident morphological changes are exemplified by the increase in third molar length and height, the reduction and loss of premolars and incisors, thinner enamel, and the elongation of canine-premolar diastema (Harris and White, 1979; Van der Made, 1999; Cooke, 2007). Other synchronous suid lineages retained less-specialized, short bunodont molars and likely had broader, omnivorous diets probably associated with more wooded and mixed habitats (Harris and White, 1979; Harris, 1983; Cooke, 2007; Cuddahee, 2008; Souron, 2012). Considering the significant disparity in the morphology of the masticatory apparatus and in body size among the different species of fossil suids, some degree of dietary niche partitioning between fossil species is expected. Stable carbon isotope analyses have shown, however, that the relationship between C4 resource consumption (e.g., C4 grasses) and dental morphology (e.g., length and height of the third molar) in suids is not straightforward (Harris and Cerling, 2002; Souron, 2017). There are several explanations for this mismatch. Dental morphology is driven mostly by food fracture

I.A. Lazagabaster / Journal of Human Evolution 132 (2019) 80e100

properties and phylogeny whereas stable carbon isotopes depend on the photosynthetic pathway of the plants consumed by the animals and can reveal only what type of plant the animals consumed during a variable timespan during crown formation (Cerling and Harris, 1999; Ehleringer and Osmond, 2000; Brugnoli and Farquhar, 2000; Du et al., 2019). The time interval recorded by stable carbon isotopes is also dependent upon how the enamel was sampled. A single drill at a given height of the tooth may capture a period of a few months, while a larger sample area could capture multiple years, therefore missing possible seasonal variations in diet that are important to test hypotheses on the relationship between craniodental morphology and the seasonal use of fallback foods. As mentioned before, most suidsdat least the extant onesdare very flexible in terms of diet and capable of exploiting a wide array of dietary resources depending on the habitat and the season (Meijaard et al., 2011; Souron, 2017). These reasons complicate the reconstruction of suid diets in the past and exemplify the importance of capturing seasonal variations in diet. To capture a larger amount of the complexity of suid paleodiets, dental microwear analysis is an excellent complement to stable carbon isotope data. In the context of suid paleodiets, dental microwear analysis has been applied to the study of fauna from fossil assemblages (Hunter and Fortelius, 1994) and archaeological sites (Vanpoucke et al., 2009), and has been used in paleoecological studies of human evolution in eastern Africa (Bishop et al., 2006; Medin et al., 2015; Ungar et al., 2017). Three-dimensional microwear texture analysis is the most recent dental microwear approach, yet only Souron et al. (2015a), Ungar et al. (2017), and Yamada et al. (2018) have applied this methodology to the study of suid diets. Here, this technique is applied to the analysis of Hadar suid diets and compare the microwear metrics with those of the Kanapoi suids partially published in Ungar et al. (2017). 1.3. Geological and ecological background Kanapoi Kanapoi is situated in the lower Kerio River valley of northern Kenya, southwest of Lake Turkana (Fig. 1). This site has yielded the largest fossil sample of A. anamensis to date and it is also the earliest site where this hominin is found (Wynn, 2000; Dumouchel, 2018). The Kanapoi Formation dates from 4.4 to 3.4 Ma, but the major fossiliferous deposits, which include hominin remains, date to between 4.195 and 4.108 Ma (McDougall and Brown, 2008) and consist of floodplain paleosols and deltaic sand bodies associated with the ancestral Kerio River and Lonyumun Lake, a precursor of Lake Turkana (Feibel, 2003). Lonyumun Lake was probably shallow and likely experienced periods of isolation, but the discovery of shared fish taxa between Lonyumun Lake and the Nile River suggest that a connection existed between this river and the Turkana Basin in relatively short but humid time periods (Stewart and Rufolo, 2018). Substantial remains of aquatic fossil avifauna from Kanapoi corroborate this site's proximity to a lake (Field, 2017). The depositional setting and the paleosols from Kanapoi suggest a mosaic of habitats similar to those seen today in the modern Omo River Delta at the north end of Lake Turkana, ranging from sparsely vegetated and arid grasslands to gallery woodland (Wynn, 2000; Quinn and Lepre, 2019). While most paleoenvironmental reconstructions support a mixture of woodlands and grasslands (Andrews and Humphrey, 1999; Wynn, 2000; Harris and Leakey, 2003a; Behrensmeyer et al., 2007; Behrensmeyer and Reed, 2013; Ungar et al., 2017; Dumouchel and Bobe, 2019; Quinn and Lepre, 2019), there has been considerable disagreement on the relative abundances of grass to woody vegetation. The proportion of soil carbonates from C4 plants runs between 25% and 40% (Wynn, 2000; Quinn and Lepre, 2019). The taxonomic composition of micromammals provides evidence for

83

the presence of numerous vegetation types. These vegetation types were predominantly arid savannas, dry Acacia bush and scrub, and grasslands, but also included moist forests and riverine woodlands or thickets (Manthi, 2006). The study of the Chiroptera (bats) from Kanapoi revealed a diverse assemblage of insectivorous and fruiteating bats whose modern counterparts live in trees both in forested areas and near open woodlands (Gunnell and Manthi, 2018). The high relative abundance of grazing-adapted mammals led Harris et al. (2003), Bobe (2011), and Geraads and Bobe (2017b) to suggest the presence of drier and more open conditions. The overall composition of the squamate record is more consistent with shrub savanna than closed-canopy habitats (Head and Müller, 2018). Recent analyses of bovid mesowear, and analyses of bovid, suid, and rhinocerotid hypsodonty, indicate that grassy habitats were a dominant component of the Kanapoi ecosystem (Dumouchel and Bobe, 2019). On the other hand, ecological structure analysisdbased on locomotor adaptation and trophic ecovariablesdsuggests a mainly closed, woodland habitat (Reed, 1997), and the diet of large mammalsdas indicated by d13C values of dental enameldsuggests an ecosystem with a high proportion of mixed feeders and browsers (Manthi et al., 2017). In general, Kanapoi provided A. anamensis with a wide range of habitats (Wynn, 2000; Behrensmeyer et al., 2007; Behrensmeyer and Reed, 2013; Quinn and Lepre, 2019). Hadar The Hadar Research Project area is located along the lower course of the Awash River, in the west-central part of the Awash Valley, Ethiopia (Fig. 1). The Pliocene deposits of Hadar date to ~3.45e2.95 Ma (Campisano and Feibel, 2008) and constitute the main source of fossils attributed to A. afarensis (Kimbel and Delezene, 2009), including the partial skeleton A.L. 288-1 (‘Lucy’). The ~155 m of Hadar Formation strata consist of floodplain paleosols, fluvial and deltaic sands, and lacustrine clays and silts (Taieb et al., 1976; Campisano and Feibel, 2008). A paleolake existed east and northeast of Hadar, but lacustrine transgressions occurred in the region. Most of the vertebrate remains at Hadar are recovered from fluvial-deltaic deposits (Campisano and Feibel, 2008; Campisano, 2007, 2012). The presence of multiple tephra in the Hadar sequence have allowed detailed dating of the sediments. The Sidi Hakoma Tuff (~3.42 Ma) is close to the base of the sequence and the BKT-2 Complex (~2.95 Ma) caps the strata at the top of the sequence. The Hadar Formation is divided into four members: the Basal Member (BM, ~3.45e3.42 Ma), the Sidi Hakoma Member (SH, ~3.42e3.24 Ma), the Denen Dora Member (DD, ~3.24e3.20 Ma), and the Kada Hadar Member (KH, ~3.20e2.95 Ma; Campisano and Feibel, 2008; Campisano, 2012), most of which is additionally divided in several submembers (e.g., SH-1, SH-2, SH-3, etc.). Based on ecomorphology and community structure analysis, Reed (2008) identified fluctuating paleoenvironments across the Hadar sequence timespan, ranging from intermediate cover bushland, open woodland, to shrubland habitats with varying regions of wetlands and edaphic grasslands across space. Reed (2008) characterized the BM as a mixture of woodlands, grasslands, and some riverine forest. This reconstruction is consistent with the rich riverine pollen record from BM (Bonnefille et al., 2004) and with data from paleosol carbonates indicating only ~30% C4 grass cover (Hailemichael, 2000; Aronson et al., 2008). The overlying SH had the most forested and closed habitats in SH-1, with high rainfall and low seasonality, as reconstructed from the fossil mammals (Reed, 2008). This characterization is supported by pollen analyses (Bonnefille et al., 1987, 2004) and dental microwear analyses of Hadar bovids (Scott, 2012). The SH-3 and SH-4 submembers probably consisted of woodlands and wet grasslands (Reed, 2008). In fact, mollusk shell analyses indicate that the SH-3 had the least evaporated condition of the Hadar paleolake (Hailemichael et al., 2002), which would also indicate the presence of wetlands. The

84

I.A. Lazagabaster / Journal of Human Evolution 132 (2019) 80e100

DD member consisted mostly of edaphic or wetland grasslands and DD-1 was still influenced by the presence of the lake (Campisano and Feibel, 2008). The pollen record indicates a transition from woodland to wetlands, open woodlands, and grasslands (Bonnefille et al., 2004; Bonnefille, 2010) associated with fluvial systems in DD (Campisano and Feibel, 2008). The wetland dominated habitats in the DD were replaced by more xeric conditions in KH (~3.20e2.95 Ma; Reed, 2008), but the pollen record and various spatial analyses of the submembers (Campisano, 2007) suggest that a riverine forest was still present at this time. 1.4. Fossil suids from Kanapoi and Hadar The Kanapoi suids were first studied by Cooke and Ewer (1972), who described two new suid species of the subfamily Tetraconodontinae, Nyanzachoerus pattersoni and Nyanzachoerus plicatus. Harris and White (1979) considered Ny. pattersoni a junior synonym of Nyanzachoerus kanamensis and Ny. plicatus a junior synonym of Nyanzachoerus jaegeri. Nyanzachoerus pattersoni is a generalized suid, showing typical tetraconodontine molar morphology and large premolars. The molars are like those of extant Potamochoerus and Sus in general structure but present a more sublophodont aspect when unworn. Though most authors agree with Harris and White (1979) in considering Ny. pattersoni part of the hypodigm of Ny. Kanamensis (Cooke, 1985, 2007; Hlusko and Haile-Selassie, 2007; Bishop, 2010; Geraads et al., 2013; Boisserie et al., 2014; Geraads and Bobe, 2017a; Reda et al., 2019), this study follows van der Made's (1999) argument to restrict the name Ny. Kanamensis (or Sivachoerus kanamensis in van der Made's own view) to the suids with narrower premolars from the western branch of the eastern African Rift Valley. It is worth mentioning that this argument is partially based on the holotype of Ny. Kanamensis, a specimen that displays significant enamel erosion, making the premolars appear narrower than they probably were when the animal was alive. The valid status of Ny. pattersoni was recognized in Cooke (1978a, b), Cooke and Wilkinson (1978), Harris et al. (2003), Kullmer (2008), and Lazagabaster et al. (2018a). Nyanzachoerus pattersoni is broadly considered a browser (Harris, 1983) or a browser to mixed feeder when only considering stable carbon isotope data (Harris and Cerling, 2002; Bishop, 2010; Wynn et al., 2016; Manthi et al., 2017). The taxonomic status of the other suid present at Kanapoi, Ny. jaegeri, is also a matter of unresolved debate. Virtually all researchers agree that Ny. jaegeri is the valid name for Cooke and Ewer's (1972) Ny. plicatus and that this species is the most likely ancestor of the genus Notochoerus (White and Harris, 1977; Cooke, 1978a, 1978b; Harris and White, 1979; Van der Made, 1999; Pickford, 1993; Kullmer et al., 2008; Bishop, 2010, 2011). The derived dental morphology of Ny. jaegeri has led some researchers to include this taxon within Notochoerus (Fessaha, 1999; Kullmer, 1999, 2008; Harris and Leakey, 2003a; b; Harris et al., 2003; Kullmer et al., 2008; Bishop, 2010, 2011; Ungar et al., 2017; Geraads and Bobe, 2017a) contra Harris and White (1979), Pickford (1993), and van der Made (1999), among others. New cranial material from Woranso-Mille with definitive affinities to Nyanzachoerus has been attributed to this species (Reda et al., 2019). The generic name Nyanzachoerus is retained here for Ny. jaegeri though future work may again reshuffle the taxonomy of the Tetraconodontinae. Nyanzachoerus jaegeri has longer and taller third molars and relatively reduced premolars in comparison to Ny. pattersoni, suggesting a shift towards grazing feeding behaviors (Harris and White, 1979; Harris et al., 2003; Ungar et al., 2017). The Pliocene deposits of Hadar are dominated by two suids from the subfamily Tetraconodontinae, Ny. pattersoni and Notochoerus euilus, and one suid from the subfamily Suinae, Kolpochoerus afarensis (Cooke, 1978a; Fessaha, 1999). The fossil material of Ny.

pattersoni at Hadar is indistinguishable from that at Kanapoi in terms of craniodental morphology (Cooke, 1978a; Harris and White, 1979; Fessaha, 1999; Reda et al., 2019). The genus Nyanzachoerus represents a stem group from which Notochoerus likely evolved. In many respects, the craniodental morphology of Notochoerus is convergent with extant Phacochoerus (e.g., vertical and tall occipital, orbits situated high up in the cranium, hypsodont third molars, reduced premolars and incisors, and dorsoventrally flattened anterior mandibular symphysis), which suggests that the diet of Notochoerus was also dominated by grazing. Throughout the Hadar sequence, there is a trend towards premolar reduction in No. euilus, as well as larger and more hypsodont third molars (Fessaha, 1999). Kolpochoerus afarensis was overall similar in morphology and size to extant Potamochoerus (Cooke, 1978a; Bishop, 2010; Souron, 2012). Kolpochoerus afarensis had bunodont and brachyodont molars, and hypsodont incisors that were likely useddas in the case of Potamochoerusdto acquire underground resources like roots, rhizomes, and earthworms (Lazagabaster, 2013). Pliocene representatives of the genus Kolpochoerus were smaller than contemporaneous tetraconodontines and possessed similar dental adaptations to those seen in extant Potamochoerus or Sus, including low-crowned bunodont third molars (Harris and White, 1979; Harris, 1983; Fessaha, 1999; Bishop et al., 2006; Souron, 2012; Haile-Selassie and Simpson, 2013; Souron et al., 2015b; Lazagabaster et al., 2018a).

2. Materials and methods 2.1. Sample All suitable suid lower third molars from the Hadar collection housed at the Authority for Research and Conservation of Cultural Heritage (ARCCH) were examined for this study. The fossils were recovered during several decades of fieldwork by the International Afar Research Expedition and the Hadar Research Project (Kimbel and Delezene, 2009; Johanson, 2017). The suitable lower third molars were those that preserved at least the first two pair of cuspids, had visible wear facets or minimal dentine exposure, and had well-preserved enamel on the occlusal surface. Those specimens with obvious postmortem damage or with an obscuring, irremovable layer of matrix or preservative were excluded from the analysis. The lower third molar was chosen as the target of the analysis for several reasons. Third molars display the most dramatic evolutionary trends in African Suidae and therefore, they have received major emphasis in systematic studies of the family (Harris and White, 1979). Some African suids have large and robust third molars, which explains why they are well preserved in the fossil record, and because of their taxonomic value, they are frequently collected in the field. Furthermore, the adult individuals of some suid species, such as extant Phacochoerus spp. or fossil Metridiochoerus spp., have most of their dentition worn down with age and they can lose most of the cheek teeth, except for the third molars. The third molar mesial cusps are closer to the center of the molar row (especially in species with elongated third molars), an area targeted in most microwear studies (second molars in the case of primatesdincluding homininsdand carnivorans; Teaford, 1985; Scott et al., 2006; Ungar et al., 2008; Scott, 2012; Peterson et al., 2018; Stynder et al., 2018). The lower third molar was the tooth used by Ungar et al. (2017) and this is the sole published study of dental microwear texture analysis that has been carried out on fossil Suidae. The selection of this tooth, therefore, maximizes the possibility of comparing dental microwear across different suid genera in the fossil record. In other studies of dental microwear texture in extant suids, Souron et al. (2015a, b) targeted both lower

I.A. Lazagabaster / Journal of Human Evolution 132 (2019) 80e100

and upper third and second molars while Yamada et al. (2018) included lower third, second, and first molars. Within the lower third molars, the buccal enamel band of the protoconid (Phase II of mastication) was analyzed in this work. When the protoconid lacked an appropriate surface for analysis (i.e., because of taphonomic damage), the lingual enamel band of the metaconid (Phase I of mastication) was analyzed. During mastication in domestic pigs, mandibular translations are largely propalinal along the anteroposterior axis and during nut-cracking, jaw motion is largely restricted to propalinal translations and elevation/depression of the mandible (Menegaz et al., 2015). In rodents, propalinal chewing has been shown to produce continuous wear facets across the occlusal surface (Lazzari et al., 2008) and negligible variation in scratch orientation among facets (Charles et al., 2007). However, during the power stroke of mastication in domestic pigs, occlusal displacements during chewing along the mesiodistal axis accounted for approximately 1/3 of mandibular movements and the other 2/3 of mandibular movements occurred along the buccolingual axis (Menegaz et al., 2015). Therefore, it is not possible to exclude the existence of two distinct phases of masticationdone buccal and one lingualdin suids. In primates, there are significant differences between buccal and lingual facets (Krueger et al., 2008) and experimentation on sheep with controlled diets indicate that tooth and facet selection, even when only analyzing facets related to one phase of mastication, can have an impact on dietary discrimination (Ramdarshan et al., 2017). For this reason, the possible interaction of cusp selection is tested below. Mastication biomechanics is expected to vary among different suid taxa. The morphology of the mandible, the temporomandibular fossa, the zygomatic arch, and the temporal and parietal regions, differ considerably among modern and fossil species (Ewer, 1958, 1970; Harris and White, 1979; Reda et al., 2019; Herring, 1980, 1985; Lazagabaster et al., 2018b). This can potentially have an impact on the interpretation of dental microwear texture data, but further research is necessary to account for the interplay of chewing biomechanics and the formation of dental facets in suids. A sample of 148 fossil lower third molars from Hadar were molded, casted, and analyzed under confocal microscopy, but only 109 had well-preserved microwear with no sign of taphonomic alteration and were included in the final analysis. The final sample from Hadar is composed of Nyanzachoerus pattersoni (n ¼ 14), Notochoerus euilus (n ¼ 61), and K. afarensis (n ¼ 34). The collection number and stratigraphic provenience of each of these fossils can be found in the Supplementary Online Material (SOM) Table S1. The Hadar submembers are notated with the name of the member followed by a letter (e.g., “T”) or a number (1e4; Campisano and Feibel, 2008; Campisano, 2012). In addition, the relatively small stratigraphic layer separating the BM and SH members is known as SHT (Sidi Hakoma Tuff). Due to the uncertainty of the stratigraphical provenience of some areas of Hadar, some fossils are assigned to more than one submember. For simplicity and standardization, the youngest member or submember of each specimen was used. All submembers were then pooled together in their correspondent member. For example, a specimen with stratigraphic assignation BM/SHT, is considered BM, while SH1/SH2 is considered SH. Most of the specimens with more than one submember assigned, however, were within the same member (e.g., DD2/DD3) and therefore, a different chronological arrangement would not have had a great impact on the results (SOM Table S1). With the purpose of comparing the suid diets between Hadar and Kanapoi, a total of 19 fossil specimens from Kanapoi were included in the analyses. These belong to two species: Ny. pattersoni (n ¼ 15) and Ny. jaegeri (n ¼ 4) and are housed at the

85

National Museums of Kenya (NMK), Nairobi, Kenya. Partial results of the microwear analysis of Kanapoi suids were published in Ungar et al. (2017). Nyanzachoerus pattersoni from Hadar and Ny. pattersoni from Kanapoi are treated as different analytical units throughout the rest of this paper, while Ny. jaegeri and No. euilus are treated as a single anagenetically-evolving lineage (Harris and White, 1979). A total of 47 specimens of extant African suid species with known diets were included in the analyses and used as a baseline for fossil comparisons. The extant sample includes five extant suid species: H. meinertzhageni (n ¼ 3), Phacochoerus africanus (n ¼ 9), Phacochoerus aethiopicus (n ¼ 4), Potamochoerus larvatus (n ¼ 23), and Potamochoerus porcus (n ¼ 6). Five additional specimens of Phacochoerus were analyzed but their identification to the species rank was uncertain. No significant microwear differences between Ph. aricanus and Ph. aethiopicus were found. Therefore, all Phacochoerus samples were grouped together in Phacochoerus spp. (n ¼ 18; SOM S1). All specimens are housed at the osteological collections of the Field Museum of Natural History (Chicago, USA), the NMK (Nairobi, Kenya), and the ARCCH (Addis Ababa, Ethiopia). All suitable specimens available at these collections were examined but the availability of these specimens varied depending on the species, hence the disparity in sample size. The sample distributions in this study do not represent the actual abundance of these species in modern African ecosystems; rather, they only represent the abundance of suitable lower third molars in the institutions that were visited during this research. A complete dataset of the dental microwear texture raw data obtained in this study and more information on the specimens analyzed have been uploaded to Mendeley Data repository and can be retrieved through the following link: https://doi.org/10.17632/ x5v9mk72y5.1. 2.2. Dental microwear texture variables High fidelity casts of all suitable third molars were created and analyzed under confocal microscopy. Detailed information on the casting procedures and the methodological aspects of the confocal microscopy used can be found in SOM S2 and S3. This study considered a total of thirteen dental microwear texture variables. Data for five variables were derived from scalesensitive fractal analysis (SSFA), including area scale fractal complexity (Asfc), anisotropy (epLsar), textural fill volume (Tfv), and two measures of heterogeneity of complexity (HAsfc9 and HAsfc81). The way these variables are calculated is explained in detail in Scott et al. (2006). Additionally, surface textures were characterized by eight International Organization for Standardization (2012) texture measurements (ISO 25178-2), which are increasingly being employed in microwear analyses to complement SSFA (e.g., Calandra et al., 2012; Schulz et al., 2013). The International Organization for Standardization (ISO) parameters were generated using Sensomap v6 and include five-point pit height (S5v), maximum pit height (Sv), mean dale area (Sda), mean dale volume (Sdv), pit void volume (Vvv), texture-aspect ratio (Str), developed interfacial area ratio (Sdr), and skewness of the height distribution (Ssk)dISO/FDIS 25178-2 (International Organization for Standardization, 2012; T ̧alu et al., 2013). For the ISO variables, the curvature of the scanned surface was removed by using the default polynomial approximation (‘form removal’ operator) of Sensomap. An extended explanation of all variables used can be found in Table 1. In summary, the variables analyzed in this study include two measures of feature complexity (Asfc, Sdr), two measures of feature anisotropy (epLsar, Str), two measures of heterogeneity of textures (HAsfc9, HAsfc81), three measures of feature volume

86

I.A. Lazagabaster / Journal of Human Evolution 132 (2019) 80e100

Table 1 Microwear variables used in this work. Measure Feature complexity

Feature anisotropy

Texture heterogeneity Feature volume

Feature area Feature depth Feature density

Var.

Variable name

Analysis

Asfc

Area of scale fractal complexity

SSFA

Sdr

Developed interfacial area ratio

ISO

epLsar

SSFA

Str

Anisotropy exact proportion length-scale anisotropy of relief Texture-aspect ratio

ISO

HAsfc9 HAsfc81 Tfv

Heterogeneity of Asfc in 3  3 squares Heterogeneity of Asfc in 9  9 squares Textural fill volume

SSFA SSFA SSFA

Vvv Sdv Sda Sv S5v Ssk

Void volumes of valleys Mean dale volume Mean dale area Maximum pit height Five-point pit height Skewness of the height distribution

ISO ISO ISO ISO ISO ISO

Explanation Changes in surface roughness with the scale of observation Percentage difference between surface area and surface cross sectional area Extent to which microwear surface texture is aligned in a specific direction The orientation of patterns on a surface calculated as the ratio of the maximum and minimum radii of the central peak Assessment of variance in complexity among subdivisions of the scanned area in 3  3 and 9  9 grids Aggregated volume of the surface calculated by filling the scanned area with cuboids of known volumes Total fill volume of valleys Average fill volume of valleys Area occupied by the average-size dale Maximum depth of pits Mean value of the five deepest pits Density of valleys (meriting negative values) or peaks (meriting positive values)

Abbreviations: Var. ¼ abbreviated variable name; SSFA ¼ variables associated with scale-sensitive fractal analysis; ISO ¼ variables associated with the International Organization for Standardization (2010) ISO/FDIS 25178-2.

(Tfv, Vvv, Sdv), a measure of feature area (Sda), two measures of feature depth (Sv, S5v), and a measure of feature density (Ssk). 2.3. Statistical analyses Nine groups that represent species or geographical variants of species were used as units of statistical analyses: H. meinertzhageni, Phacochoerus spp., Po. larvatus, Po. porcus, Ny. jaegeri, Ny. pattersoni (Kanapoi), Ny. pattersoni (Hadar), No. euilus, and K. afarensis. For simplicity, these groups will be referred to as species throughout the rest of the text, while acknowledging that they include a generic assignation (Phacochoerus spp). and a speciesdNy. pattersonidwith two geographical variants. A series of two-way multivariate analysis of variance (MANOVAs) were carried out to check for microwear differences between groups and account for the interaction of different factors. The first one compares tooth cusp (protoconid or metaconid) and species (all species), the second one compares geological unit (Ka, BM, SH, DD, KH) and species (all fossil species), and the third one compares geological unit and species (only Hadar). Differences in central tendencies between species and between geological units were assessed using a one-way MANOVA for all variables, with individual analyses of variance (ANOVAs) and multiple comparisons post hoc tests (Dunn's tests) used to determine the sources of significant variation (Dunn, 1958) among extant species, extant vs. fossil species, and among fossil species. Data were rank-transformed to mitigate violation of assumptions inherent to parametric statistics (Conover and Iman, 1981). To be conservative in the comparisons, Bonferroni corrections on pvalues were used to decrease Type I errors (Cabin and Mitchell, 2000). A p-value  0.05 was considered significant. In addition to comparisons of central tendency, the homogeneity of variances was compared among species. In past studies of primatesdincluding homininsdand other mammals, differences in the homogeneity of variances have been suggested to be important for inferring fallback food choice and seasonality (e.g., Scott et al., 2005; Ungar et al., 2010; DeSantis and Haupt, 2014; Shapiro et al., 2016; Peterson et al., 2018). Levene's tests were used, following Plavcan and Cope's (2001) method, where each value is subtracted from the sample mean before analysis: 0

X ¼ jX  mean ðXÞj

Following Levene's transformations, the same analyses used to compare central tendencies (one-way MANOVAs, ANOVAs, and post-hoc Dunn's tests) were performed. A principal component analysis (PCA) with all continuous variables was carried out first, solely on the extant species using the ^ et al., 2008). ‘prcomp’ function in the ‘FactoMineR’ library in R (Le The transformed coordinates were then used to plot rescaled values of the fossil species in the frozen PCA graph. One-way ANOVAs were performed on the first two principal components (PC1 and PC2), first comparing extant species, secondly comparing fossil species (all fossil species first and then Kanapoi and Hadar species separated), and finally comparing geological units. In addition, a linear discriminant analysis (LDA) with all continuous variables was performed to visualize differences between species using the ‘lda’ function in the ‘MASS’ library in R (Venables and Ripley, 2002). All statistical analyses were performed in R environment v. 3.4.1. (R Core Team, 2018). 3. Results The results of two-way MANOVAs are presented in SOM Table S2. Differences among species are significant in all analyses. There are no significant differences between cusps and there is no significant interaction of cusp when comparing microwear variables among species. There are differences among geological units when considering both Kanapoi and Hadar, but no significant differences when the comparisons are made among Hadar members only. In both cases, there is no significant interaction of geological unit and species. 3.1. Univariate comparisons among extant African suid species Summary statistics for the extant African suid species analyzed are presented in Table 2 and in Figures 2 and 3. Results of ANOVAs are presented in SOM Table S3. Post-hoc comparisons can be found in Table 3 and in SOM Tables S4 and S5. Of the thirteen variables analyzed, seven yielded significant differences in central tendencies within the extant African suid sample used in this work, including measures of surface complexity (Asfc), surface anisotropy (epLsar), surface heterogeneity (HAsfc9 and HAsfc81), feature volume (Vvv), feature depth (Sv) and feature density (Ssk). The microwear

I.A. Lazagabaster / Journal of Human Evolution 132 (2019) 80e100

87

Table 2 Summary statistics of microwear texture variablesa for extant African suid species analyzed in this work. Taxon

n

Hylochoerus meinertzhageni

3

Phacochoerus spp.

18

Potamochoerus larvatus

23

Potamochoerus porcus

6

a

Median Mean SD Median Mean SD Median Mean SD Median Mean SD

Complexity

Anisotropy

Heterogeneity

Volume

Area

Depth

Density

Asfc

Sdr

epLsar

Str

HAsfc9

HAsfc81

Tfv

Vvv

Sdv

Sda

Sv

S5v

Ssk

1.33 1.40 0.24 1.73 1.73 0.57 4.04 5.24 3.93 8.46 9.07 3.35

0.93 0.93 0.08 0.88 0.93 0.38 1.37 1.70 1.02 0.91 0.97 0.22

0.0065 0.0064 0.0006 0.0044 0.0046 0.0014 0.0023 0.0026 0.0011 0.0011 0.0012 0.0006

0.30 0.38 0.24 0.32 0.35 0.16 0.35 0.43 0.21 0.49 0.46 0.14

0.71 0.66 0.41 0.44 0.62 0.49 0.21 0.43 0.45 0.98 1.28 0.88

2.34 4.31 4.14 0.58 1.33 1.50 0.43 1.79 2.68 2.88 4.08 2.80

29075.94 28708.69 23626.26 41136.70 40090.09 10751.74 42604.92 40653.02 10079.44 43159.40 41991.33 8953.52

0.12 0.12 0.04 0.08 0.10 0.06 0.13 0.15 0.07 0.07 0.08 0.03

9.02 12.35 7.96 7.44 31.18 63.89 18.84 28.62 31.91 4.71 5.08 3.43

655.97 624.64 271.33 473.42 834.94 736.38 724.35 815.14 555.23 289.85 307.19 146.97

2.78 2.60 0.62 2.15 2.57 1.28 3.11 3.86 1.75 1.71 1.98 0.77

2.01 1.96 0.71 1.48 1.56 0.76 2.45 2.45 1.18 1.45 1.46 0.46

1.25 1.05 0.42 0.08 0.21 0.58 0.46 0.45 0.39 0.53 0.45 0.48

See Table 2 for abbreviations of the microwear variables.

variables that better differentiate extant suid species (p < 0.0001) are complexity (Asfc) and anisotropy (epLsar). The Asfc means of Po. porcus and Po. larvatus are significantly higher than in Phacochoerus and H. meinertzhageni. On the contrary, the epLsar mean values are significantly higher in H. meinertzhageni and Phacochoerus in comparison to Po. porcus and Po. larvatus. The mean and standard error of Asfc and epLsar for all suid species are plotted in Figure 4. With respect to measures of surface heterogeneity, Po. porcus shows higher mean values of HAsfc9 than the other three species though the only significant difference (p < 0.01) occurs with Po. larvatus. Similarly, Po. porcus shows the highest mean value of HAsfc81, which is significantly higher than in Po. larvatus and Phacochoerus. The mean value of feature volume (Vvv) is significantly higher in Po. larvatus than in Po. porcus while the values of feature depth (Sv) are significantly higher in Po. larvatus than in Po. porcus and Phacochoerus. In the case of feature density (Ssk), Phacochoerus has significantly higher mean values than H. meinertzhageni. The analysis of variance using Levene's test uncovered statistical differences in Asfc, epLsar, and Sdr. The Asfc variance is significantly higher in Po. porcus and Po. larvatus than in Phacochoerus and H. meinertzhageni, while the opposite occurs in epLsar, where the variance is larger in the former than in the latter. The Sdr variance is significantly larger in Po. larvatus than in the other three species. 3.2. Univariate comparisons between extant and fossil suid species The fossil species from Kanapoi Ny. jaegeri differs from Po. larvatus in having lower values of complexity (Asfc and Sdr), and heterogeneity (HAsfc9), and from Po. porcus in having lower values of Asfc and higher values of anisotropy (epLsar; Figs. 2e4; Tables 2 and 4; SOM Tables S3eS5). No significant differences occur between Ny. jaegeri and Phacochoerus or Hylochoerus meinzetzhageni. The other suid from Kanapoi, Ny. pattersoni, differs from Phacochoerus and Po. larvatus in having lower values of anisotropy (epLsar and Str), heterogeneity (HAsfc9 and HAsfc81), and density (Ssk), but also differs from Po. larvatus in having lower values of feature volume (Sdv) and feature area (Sda). It differs from Po. porcus in having lower values of Asfc, and from H. meinertzhageni in having lower values of epLsar. In a similar vein, Ny. pattersoni from Hadar also has significantly lower values of Asfc in comparison to Po. porcus and Po. larvatus and significantly higher values of epLsar in comparison to Phacochoerus and H. meinertzhageni, as well as significantly lower values of feature volume (Vvv and Sdv) and feature depth (S5v) in comparison to Po. larvatus. Notochoerus euilus has significantly lower values of complexity (Asfc and Sdr) in comparison to Po. larvatus and Po. porcus. Notochoerus euilus also has significantly lower values of

feature volume (Vvv and Sdv), feature area (Sda) and feature depth (Sv and S5v) than Po. larvatus and Phacochoerus. In fact, with respect to these variables, the values of No. euilus are closer to those of Po. porcus (except S5v) but differ from the latter in having significantly lower values of heterogeneity (HAsfc9 and HAsfc81). Finally, K. afarensis differs from Phacochoerus and H. meinertzhageni in having significantly higher values of Asfc and lower values of epLsar. The values of epLsar, Sdr, Vvv, Sdv, Sda, Sv, and S5v are also significantly lower in K. afarensis than in Po. larvatus and more similar to those of Po. porcus. The values of heterogeneity (HAsfc9, HAsfc81) are significantly higher in K. afarensis than in Po. larvatus. In Figure 4, Ny. jaegeri and No. euilus plot closer to modern Phacochoerus due to its high values of epLsar and low values of Asfc. On the other hand, Ny. pattersoni (both in Kanapoi and Hadar) occupies a unique bivariate space that is somewhat intermediate between Phacochoerus, Po. larvatus, and Po. porcus, and which is characterized by low values of both Asfc and epLsar. Kolpochoerus afarensis plots closer to Po. porcus, due to its high values of Asfc and low values of epLsar.

3.3. Univariate comparisons among fossil suid species As in the case of extant suids, the measures of complexity (Asfc) and anisotropy (epLsar) largely drive separations between fossil species (Figs. 2 and 4), but in this case heterogeneity (HAsfc9 and HAsfc91) also plays a large role (p < 0.0001; Tables 3 and 4; SOM Tables S3, S6, and S7). The mean values of Asfc are significantly higher in K. afarensis than in Ny. jaegeri and No. euilus. Conversely, Ny. jaegeri and No. euilus have significantly higher mean values of epLsar in comparison to Ny. pattersoni (both in Kanapoi and Hadar) and K. afarensis. With respect to feature depth (S5v), Ny. jaegeri and Ny. pattersoni (both in Kanapoi and Hadar), have significantly higher mean values than No. euilus and K. afarensis. Nyanzachoerus jaegeri and Ny. pattersoni (both in Kanapoi and Hadar) also have the highest values of Sv, Vvv, Ssk, and Sdr. In the case of heterogeneity (HAsfc9 and HAsfc91), Ny. jaegeri, Ny. pattersoni from Kanapoi, and K. afarensis have significantly higher mean values than Ny. pattersoni from Hadar and No. euilus. The variances of Asfc, Ssk, HAsfc9 and HAsfc81 are also significantly different between fossil species. For Asfc, differences were only statistically significant between Ny. jaegeri and Ny. pattersoni from Hadar (p < 0.001), and K. afarensis and No. euilus (p < 0.01). Nyanzachoerus jaegeri and Ny. pattersoni from Hadar also differ in the variance of Ssk (p < 0.01). The heterogeneity (HAsfc9 and HAsfc81) variance is different between No. euilus and Ny. jaegeri, but also between No. euilus and K. afarensis.

88

I.A. Lazagabaster / Journal of Human Evolution 132 (2019) 80e100

Figure 2. Boxplots showing the central tendencies and dispersion of the raw values of the texture microwear variables derived from scale-sensitive fractal analysis (SSFA), for each extant and fossil suid groups analyzed in this work. The boxes represent the interquartile range (IQR), which account from the 25th percentile to the 75th percentile of the data. The median is represented by the horizontal line separating the boxes in two portions. The mean is represented by the rhombus symbol. The ends of the lines extending from the IQR are the extreme values (within 1.5 times of the IQR from the upper or lower quartile).

3.4. Multivariate comparisons A multivariate principal components analysis (PCA) including all variables for all species was performed to investigate groupings within the sample. The three first PCs explain 67.3% of the variance (SOM Table S8) but separation between species is more evident when the first (PC1) and second (PC2) principal components are plotted together (Fig. 5). In multivariate space, there is considerable overlap between all of the extant and fossil suid species textures. PC1 explains most of the variance (36.2%) and the variables that load most significantly in PC1 are Sdr, Vvv, Sdv, Sda, S5v, and Sv.

Most of the separation between extant species occurs in PC2, though this component explains only 18.1% of the variance. The four variables that load most significantly in PC2 are complexity (Asfc), anisotropy (epLsar) and heterogeneity (HAsfc9 and HAsfc81). Potamochoerus porcus is well separated from Phacochoerus and H. meinertzhageni while Po. larvatus occupies a larger area in the multivariate space (Fig. 5A). Although most K. afarensis points are restricted to the lower part of the PC1ePC2 plot (where most of Po. porcus points group) and most of the No. euilus points cluster in the upper part of the graph (closer to Phacochoerus), about one third of No. euilus values overlap with K. afarensis. The four specimens of Ny.

I.A. Lazagabaster / Journal of Human Evolution 132 (2019) 80e100

89

Figure 3. Boxplots showing the central tendencies and dispersion of the raw values of the texture microwear variables characterized by eight International Organization for Standardization (2010) texture measurements (ISO 25178-2) for each extant and fossil suid groups analyzed in this work. Configuration of boxplots as in Figure 2.

jaegeri are closer to No. euilus and Phacochoerus than to Po. porcus or K. afarensis. Finally, Ny. pattersoni occupies an intermediate area between K. afarensis and No. euilus. The results are better visualized in Figure 5B, where each point is the mean value for the first two components (PC1 and PC2), and the lines represent the standard error of the mean. Information regarding geological unit is also included in this graph. The separation between the group formed by Po.porcus and K. afarensis on the one hand, and the group formed by Phacochoerus, H. meinertzhageni, No. euilus, and Ny. jaegeri on the other hand, is more evident when only looking at mean values. Interestingly, Ny. pattersoni from Kanapoi has values closer to K. afarensis in the KH member, but intermediate between Po.larvatus, Po. porcus, and K. afarensis in the BM member. Nyanzachoerus pattersoni in Hadar is closer to No. euilus and Ny. jaegeri. A series of ANOVAs were performed to account for differences between species in PC1 and PC2 (SOM Table S9). There are significant differences in PC1 and PC2 when comparing extant species only and when comparing all fossil species and fossil species from

Hadar. However, there are no differences in PC1 among species in Kanapoi. There are statistical differences in PC1 when grouping all fossil species by geological unit but not in PC2. In general, these results support that the separation between species is more consistent in PC2 than in PC1. On the contrary, geological units are better separated in PC1. In order to maximize the differences between species, a linear discriminant analysis (LDA) was also carried out. The results are presented in SOM Table S10 and Figure 6. Though there is separation between groups to a certain extent, there is also considerable overlap. 4. Discussion 4.1. Extant suid microwear texture baseline This study shows that despite substantial overlap in the microwear signal in extant African suid species, preferred food

e (3) Sdr, epLsar, Sv (5) Asfc,c HAsfc9b, HAsfc81b

(2) e (4) Asfc,c epLsar,c HAsfc9,c HAsfc81c

(2) epLsar (3) Asfcb See Table 2 for abbreviations of the microwear variables. p < 0.001. p < 0.0001. c

(3) epLsarc (1) epLsarb Nyanzachoerus pattersoni (H)

a

(8) epLsar, Vvv, Sdv, Sda, Sv, S5v (5) Notochoerus euilus (H)

b

(2) HAsfc9 (5) Asfc,c epLsar, HAsfc9, HAsfc81

(7) Sdr,b HAsfc9,c HAsfc81,c Vvv, Sv, S5v, Ssk (2) HAsfc9, HAsfc81

(2) (4) Asfc, HAsfc81 e (7) Asfc,b Sdr,b Ssk (2) Asfc.b epLsar (0) (4) Asfc,c epLsarb

epLsar

Kolpochoerus afarenis (H)

(5) Asfc, Vvv, S5v

HAsfc9 HAsfc9 HAsfc9,c HAsfc81, Sda

(9) Sdr,c epLsar,b HAsfc9,c HAsfc81,b Vvv,c Sdv,c Sda,b Sv,c S5vc (7) Asfc,c Sdr, Vvv,c Sdv,c Sda,c Sv,c S5vc

(1) (0) (5) Sdr, epLsar, S5v (1) Asfc (2) Asfc,b Ssk (3) HAsfc9 epLsar, Vvv Asfc HAsfc9, HAsfc81 (2) (1) (4) Asfc (0) (1) (1) (3) epLsar (2) Asfc, epLsar (2) (1) Asfcc (1) e (3) (1) (4) Sv (1) e (1) (1) (1) (2) Asfc,b Sdr e (2) Asfc, epLsar (1) Asfc Sdr, epLsarb epLsarb

(1) e (5) Asfc,c epLsar (4) Asfc,c epLsarc (0) (7) epLsar,b Str, HAsfc81, Sskc (9) Asfc,c epLsar,c HAsfc9, HAsfc81,b Sda, Ssk Asfc Asfc,b epLsarb

e (1) (2) (2) (0) (1) Hylochoerus meinertzhageni Phacochoerus spp. Potamochoerus larvatus Potamochoerus porcus Nyanzachoerus jaegeri (K) Nyanzachoerus pattersoni (K)

Phacochoerus spp.

(4) (3) e (7) (3) (6)

Potamochoerus larvatus

Potamochoerus porcus

Nyanzachoerus jaegeri (K)

Nyanzachoerus pattersoni (K)

Kolpochoerus afarenis (H)

(2) (2) (3) (3) (3) (1)

Notochoerus euilus (H)

Nyanzachoerus pattersoni (H)

I.A. Lazagabaster / Journal of Human Evolution 132 (2019) 80e100

Hylochoerus meinertzhageni

Table 3 Summary of post-hoc multiple comparisons for the microwear texture data within and between extant African suid taxa and fossil suid taxa from Kanapoi (K) and Hadar (H) using non-parametric Dunn's test. Comparisons of central tendencies are noted to the left, while comparisons of variance are noted to the right. The number in parenthesis refers to the total number of significant comparisons where p < 0.05. Only comparisons of microwear variablesa where p < 0.01 are shown.

90

differences are reflected to a certain extent in microwear texture variation. Differences in the microwear of extant suid species are especially notable in two texture variables, complexity (Asfc) and anisotropy (epLsar). These variables are among the most widely used features to account for diet variability in these types of analyses in other ungulate groups and in primates, including hominins (Ungar et al., 2007, 2008, 2010, 2012, 2017; Grine et al., 2010; Merceron et al., 2010; Scott, 2012; Shearer et al., 2015; Martin et al., 2018; Peterson et al., 2018; Rowan et al., 2018; Stynder et al., 2018). In general, microwear textures featuring high complexity and low anisotropydwhich correspond with the presence of a large quantity of pitsdare associated with hard object specialists or browsers (Strait, 1993; Silcox and Teaford, 2002; Ungar et al., 2007, 2008; Daegling et al., 2011; Calandra et al., 2012; Scott, 2012; Calandra and Merceron, 2016). In contrast, low complexity values and high anisotropy valuesdwhich correspond with the presence of a large quantity of scratchesdare associated with species that graze or consume tough leaves (Ungar et al., 2007, 2008; Merceron et al., 2009; Scott et al., 2009; Scott, 2012; Calandra et al., 2012; Calandra and Merceron, 2016), although some woody seeds can also be tough (Teaford and Walker, 1984; Teaford, 1988; Lucas, 2004; Lucas et al., 2008). Scott's (2012) microwear texture analysis of a large sample of African bovids found that tough and abrasive herbaceous monocotyledon plants produce more anisotropic textures (high epLsar), whereas the consumption of brittle browse that is less tough and less abrasive results in more isotropic textures (low epLsar). In extant African suids, Souron et al. (2015a) found that omnivorous species have higher texture complexity (Asfc) than herbivores but contrary to the results presented here, they did not find any significant difference in anisotropy (epLsar) between species. Furthermore, the omnivore suid species studied by Souron et al. (2015a) had similar dental microwear signals, while the two extant omnivore species included in this study (Po. larvatus and Po. porcus) differ considerably in this regard. These mismatches are likely due to geographical and/or seasonal differences between the sample of modern suids analyzed here and the one analyzed by Souron et al. (2015a). Ward and Mainland (1999) showed that the dental microwear of free-range boars in large grassland areas were characterized by a high frequency of scratches and Yamada et al. (2018) reported that the textures of a population of wild boars rooting in deciduous forests were also dominated by scratches, whereas those of a stall-fed population (which fed on corn hay and did not perform rooting), were dominated by pits. Another population of wild boars studied in Yamada et al. (2018), however, failed to confirm this pattern. Two of the extant African suid species analyzed in this work, Po. porcus and Po. larvatus, yielded high mean values of complexity (Asfc) and low mean values of anisotropy (epLsar) (Figs. 3 and 4). These species are known for having broad omnivorous diets that regularly include hard foods such as fruits, nuts, roots, and tubers (Meijaard et al., 2011). Potamochoerus porcus shows more extreme values (higher Asfc and lower epLsar) in comparison to Po. larvatus, but these two suids are also distinguished in measures of texture heterogeneity (HAsfc9 and HAsfc81), which are higher in Po. porcus, and measures of feature volume (Vvv and Sdv), feature area (Sda) and feature depth (Sv), which are higher in Po. larvatus. Souron et al. (2015a) suggested that higher values of heterogeneity could be related to more variable diets but also argued that the presence of grit in the diet associated with rooting behaviors could have the effect of homogenizing the dental microwear signal, hence producing lower values of heterogeneity. It is worth noting that controlled experiments with leporids (rabbits) show that high variability in microwear textures does not necessarily imply dietary diversity; instead, it can also be related to uniform, low-abrasion

I.A. Lazagabaster / Journal of Human Evolution 132 (2019) 80e100

91

Figure 4. Bivariate plot of anisotropy (epLsar) and complexity (Asfc) of extant and fossil suid taxa. Each point represents the mean and the lines represent the standard error. Abbreviation of geological units in chronological order (from older to younger): Ka ¼ Kanapoi; BM ¼ Basal Member; SH ¼ Sidi Hakoma; DD ¼ Denen Dora; KH ¼ Kada Hadar.

Table 4 Summary statistics of microwear texture variablesa for fossil suid species from Kanapoi and Hadar. Taxon

n

Nyanzachoerus jaegeri (Kanapoi)

4

Nyanzachoerus pattersoni (Kanapoi)

15

Nyanzachoerus pattersoni (Hadar)

14

Notochoerus euilus (Hadar)

61

Kolpochoerus afarensis (Hadar)

34

a

Median Mean SD Median Mean SD Median Mean SD Median Mean SD Median Mean SD

Complexity

Anisotropy

Heterogeneity

Volume

Area

Depth

Density

Asfc

Sdr

epLsar

Str

HAsfc9

HAsfc81

Tfv

Vvv

Sdv

Sda

Sv

S5v

Ssk

1.83 1.76 0.19 2.54 2.61 0.82 2.12 2.56 1.35 1.66 2.13 1.21 5.79 6.15 2.63

0.75 0.77 0.04 1.21 1.25 0.51 0.91 1.02 0.31 0.71 0.79 0.32 0.70 0.74 0.30

0.0040 0.0041 0.0008 0.0020 0.0021 0.0010 0.0016 0.0017 0.0015 0.0027 0.0032 0.0020 0.0014 0.0014 0.0008

0.37 0.43 0.18 0.55 0.52 0.15 0.49 0.51 0.18 0.49 0.46 0.20 0.38 0.41 0.20

1.96 1.73 0.82 1.11 1.30 0.59 0.29 0.44 0.35 0.18 0.60 1.24 1.08 1.85 1.75

2.26 2.66 2.02 2.84 3.65 2.41 0.40 1.57 2.28 0.35 1.53 2.25 3.45 3.79 2.07

45206.42 42995.58 7006.55 39410.82 33662.88 30717.39 40266.00 42692.82 14311.35 44306.90 44261.68 9745.87 43582.62 43427.66 11505.46

0.07 0.08 0.02 0.09 0.10 0.05 0.07 0.08 0.04 0.05 0.06 0.03 0.07 0.07 0.03

5.80 8.24 6.39 5.65 18.83 46.97 4.80 34.30 87.79 2.90 5.53 6.19 3.64 5.80 7.76

396.44 457.36 230.96 313.13 482.27 570.88 400.29 621.84 515.11 305.54 382.03 259.76 281.71 408.96 323.07

2.14 2.27 0.40 2.18 2.75 1.62 2.12 2.55 1.09 1.51 1.66 0.70 1.72 1.81 0.80

1.45 1.59 0.40 1.35 1.64 0.83 1.25 1.25 0.38 0.91 1.02 0.44 0.97 1.09 0.55

0.50 0.40 0.77 0.84 0.98 0.65 0.65 0.75 0.87 0.27 0.39 0.48 0.37 0.46 0.50

See Table 2 for abbreviations of the microwear variables.

diets (Schulz et al., 2013). In primate molar occlusal facets, higher values of microwear feature volume, area, and depth, are associated with larger and deeper pits that are often produced during the mastication of hard objects (Ragni et al., 2017). Similar results were obtained when looking at the occlusal facets of canines and incisors in New World monkeys (Delezene et al., 2016). The microwear textures of the two Potamochoerus species in the analyses reported here may well be reflecting the ecological preferences and the environments inhabited of these two suids. Food availability, vegetation structure, and soil composition can vary dramatically between different habitats across sub-Saharan Africa. While Po. porcus regularly feeds on tropical fruits and seeds in forested and rainforest-like habitats of central and western Africa (Leus and MacDonald, 1997; Magliocca et al., 2003; Beaune et al., 2012; Melletti et al., 2017), Po. larvatus inhabits more open woodlands

and savanna-type habitats in eastern and southern Africa (Leus and MacDonald, 1997; Meijaard et al., 2011; Seydack, 2017). The differences in microwear texture in the two Potamochoerus species is visible in the PCA and LDA plots (Figs. 5 and 6), where it is noticeable that Po. larvatus has values that are more spread in comparison to Po. porcus. This is due to the high degree of variance in some of the microwear texture variables in Po. larvatus, as shown by Levene's tests (SOM Tables S5 and S7). One possible explanation of these results is that, while both species have broad diets that include hard-object feeding, Po. larvatus inhabits more seasonal environments, where some of these resources (seeds, fruits, nuts) are only available in some parts of the year, in contrast to the tropical rainforests inhabited by Po. porcus, where these resources are available almost year-round. It is also possible that the highly heterogenous surfaces of Po. porcus are indicative of its rooting

92

I.A. Lazagabaster / Journal of Human Evolution 132 (2019) 80e100

Figure 5. Bivariate plots of the first and second principal components (PC1 and PC2) derived from principal component analysis (PCA). The PCA was carried out first on extant suid taxa only. The data on fossil taxa were then rescaled to fit the PCA based on extant suid taxa. A) All data points represented. B) Each point represents the mean and the lines represent the standard error. Abbreviation of geological units as in Figure 4.

behaviors. Although there is no documentation in the literature that Po. porcus engages more actively in rooting than Po. larvatus (Skinner et al., 1976; Breytenbach and Skinner, 1982; Jones, 1984; Seydack, 1990; Leus and MacDonald, 1997; Nowak, 1999; Meijaard et al., 2011), the incisors of Po. porcus show a considerable amount of wear when compared with the molar row (Lazagabaster and van der Made, under review). This observation will contradict the expectation of Souron et al. (2015a) that high heterogeneity values are related to weak rooting behaviors. It may well be that the type of soil is having an impact in the results; the loose soils of rainforests may favor the ingestion of hard particles of soil and the abrasion of teeth in comparison to the more compacted and

harder soils of savannahs. In favor of this explanation is the result that Phacochoerus also shows high mean values and high variance for some of these microwear texture variables (e.g., HAsfc81, Sdv, and Sda), which could be capturing the seasonal consumption of hard objects by this suid (Cumming, 1975, 2013). Though Phacochoerus has been categorized as a grazer specialist (Harris and Cerling, 2002), in the driest month of the year it can switch completely to a diet composed of seeds, nuts, and underground resources such as tubers and roots (Cumming, 1975, 2013). A critical limiting factor of the modern extant baseline built here is that the date of death of many of the specimens is unknown. Dental microwear only preserves information on what the animal ate

I.A. Lazagabaster / Journal of Human Evolution 132 (2019) 80e100

93

Figure 6. Bivariate plots of the first and second linear discriminants (LD1 and LD2) derived from linear discriminant analysis (LDA). The LDA was carried on all modern and fossil suid taxa together.

during a limited time frame in the order of weeks before the animal's death, a phenomenon that has been called the ‘Last Supper effect’ (Grine, 1986; Teaford and Oyen, 1989). The results presented here could be mostly showing the microwear textures of these suids in a certain season and thus, biasing the results. Seasonality has been shown to be an important factor in primate diets (Percher et al., 2018) and should be considered in future studies of suid microwear. Otherwise, the results presented here are consistent with Phacochoerus having a grazer diet, including low values of Asfc and high values of epLsar (Figs. 3 and 4). Phacochoerus also shows high values of heterogeneity, which is not consistent with what was found by Souron et al. (2015a). The values of Asfc and epLsar in Phacochoerus are similar to those shown by H. meinertzhageni, though the values of heterogeneity (especially HAsfc81) are higher in the latter than in the former. H. meinertzhageni is a mixed feeder feeding both on graze and browse but is not considered to be proficient good at exploiting underground resources (Meijaard et al., 2011). In the PCA and LDA plots, H. meinertzhageni occupies an intermediate position between Po. larvatus and Phacochoerus (Figs. 5 and 6). Unfortunately, the low sample size (n ¼ 3) does not allow for a good characterization of the microwear signal of H. meinertzhageni. It is worth noting that Souron et al. (2015a, b) only included five specimens of H. meinertzhageni in their study. The low availability of specimens of this suid in zoological collections hampers the correct understanding of the microwear profile of this species. 4.2. Dietary ecology of Hadar Suidae The extant African suid microwear texture dataset serves as a baseline to categorize and infer aspects of the diet of fossil species. In the same way as it occurs with extant species, the fossil species from Hadar show substantial overlap in their microwear textures. However, there are also significant differences in several of the

microwear variables studied. As in the case of extant suids, fossil species are also better distinguished based on values of complexity (Asfc) and anisotropy (epLsar; Fig. 4), but similar groupings are observed when considering all variables in the PCA and LDA plots (Figs. 5 and 6). Kolpochoerus afarensis has dental microwear textures (e.g., high values of Asfc and low values of epLsar) that resemble those of extant Po. porcus and are closer to the values of Po. larvatus than they are to those of Phacochoerus and H. meinertzhageni. The suid K. afarensis is a suine that has craniodental characteristics overall comparable to extant Potamochoerus or Sus (Cooke, 1978a; Bishop, 2010; Souron, 2012). For example, both K. afarensis and Potamochoerus have low-crowned bunodont molars with thick enamel that presumably represent adaptive traits for resisting the heavy loads of breaking up hard foods, as in primates (Lambert et al., 2004; Lucas, 2004; Lucas et al., 2008). These suids also share craniodental adaptations designed for rooting, as evidenced by the marked impressions of the rostral muscles that move the snout, and the hypsodont and complex incisors (Cooke, 1978a; Lazagabaster, 2013). In light of the high values of Asfc for both Po. porcus and K. afarensis, it makes sense to infer that K. afarensis was also exploiting foods with hard physical properties, as its extant counterpart does. This feeding behavior is congruent with the carbon isotope data available for this suid in the Hadar Formation. The d13C average of 4.16 ± 1.45‰ (n ¼ 10) for K. afarensis from Dikika (Bedaso et al., 2013), and 3.76 ± 2.57 (n ¼ 29) for K. afarensis from Hadar (Wynn et al., 2016), suggests that K. afarensis had a mixed C3eC4 diet with a relatively high contribution of C4 resources. The C4 photosynthetic pathway is typical of tropical monocotyledon grasses as well as some trees and shrubs from warm regions (Heaton, 1999; Harris and Cerling, 2002; Passey and Cerling, 2002; Cerling et al., 2003). It is likely that contemporaneous mammals at Hadar and Dikika that have yielded similar positive d13C values, such as equids and bovids of the tribes Alcelaphini, Hippotragini, and Reduncini, were mostly grazing on C4 grasses more than eating browse or fruits from trees (Bedaso

94

I.A. Lazagabaster / Journal of Human Evolution 132 (2019) 80e100

et al., 2013; Wynn et al., 2016; Robinson et al., 2017). However, the consumption of foods from animal origin, like carrion, eggs, and insects, could have also contributed to the relatively positive d13C values of K. afarensis. Extant Po. larvatus has d13C values that span the whole range of stable carbon isotopic variability, from almost pure C3 feeder to almost pure C4 feeder (Ambrose and DeNiro, 1986; Harris and Cerling, 2002; Cerling et al., 2004; Sealy et al., 2014; Souron, 2017). The d13C values of K. afarensis are compatible with an omnivore diet and the microwear signal points towards the consumption of harddbut not excluding toughdfoods. It is likely that K. afarensis, like Po. porcus, actively exploited underground resources that included harder parts of C4 plants or that involved the ingestion of soil particles that contributed to its low anisotropic, highly complex, and heterogenous dental surface textures. Nevertheless, the craniodental morphology, the stable carbon isotope data, and the dental microwear textures, all point towards K. afarensis having a diverse and omnivore diet. It is important to point out that extant Po. porcus have d13C mean values that are significantly more negative than K. afarensis, but this is most likely related to habitat differences. While Po. porcus inhabits densely forested areas with mostly C3 vegetation (Meijaard et al., 2011), K. afarensis presumably inhabited mixed woodland settings at Hadar with an abundant presence of C4 vegetation (Bonnefille et al., 1987, 2004; Reed, 1997, 2008; Aronson et al., 2008; Behrensmeyer, 2008; Campisano and Feibel, 2008; Behrensmeyer and Reed, 2013; Wynn et al., 2013, 2016; Du et al., 2019). Another Hadar suid, No. euilus has a microwear signal that is closer to that of extant Phacochoerus, including high values of anisotropy (epLsar). This is congruent with the a priori expectation based on the morphology of the masticatory apparatus; both No. euilus and Phacochoerus share similar craniodental characteristics. These shared characteristics include elongated and hypsodont third molars, reduced premolars and incisors, thin dental enamel, widened anterior portion of the mandibular symphysis, long postcanine diastemata, elevated orbits, and vertical occipitals, among others. These traits are characteristic of species that consume large quantities of graze, and some of them are convergent in other grazer mammals, such as bovids and horses (Janis and
rez-Barbería and Gordon, 1999; Mendoza et al., Thomason, 1995; Pe 2002; Damuth and Janis, 2011; Lazagabaster et al., 2016). When looking at Figures 5 and 6, however, part of the range (roughly 20%) of No. euilus microwear values overlaps with those of K. afarensis. This is surprising because the expectation was that No. euilus would likely have a restricted microwear signal reflective of its specialized grazing habits, as suggested by stable carbon isotopes. Notochoerus euilus has an average d13C of 2.29 ± 2.20‰ (n ¼ 18) at Dikika (Bedaso et al., 2013; Wilson, 2013), of 1.75 ± 1.45‰ (n ¼ 39) at Hadar (Wynn et al., 2016), and of 0.98 ± 1.07‰ (n ¼ 19) at Woranso-Mille (Levin et al., 2015). A possible explanation is that the microwear textures of some No. euilus specimens that overlap with Po. porcus are capturing a seasonal pattern, where No. euilus was exploiting underground food items, just as extant Phacochoerus does when graze is not available during the driest month of the year (Cumming, 1975, 2013). Finally, Ny. pattersoni is characterized as having a microwear signal that is somewhat intermediate between K. afarensis and No. euilus, and intermediate among extant African suid species. This suid has also been argued to be mostly a grazer, based on stable carbon isotope data. The d13C average of Ny. pattersoni is 3.89 ± 1.57‰ (n ¼ 6) at Dikika (Bedaso et al., 2013; Wilson, 2013 and 3.80 ± 1.46‰ (n ¼ 6) at Hadar (Wynn et al., 2016). The dentition of Ny. pattersoni resembles that of Potamochoerus, but Ny. pattersoni is much larger in general body size and has third molars that are more hypsodont and sublophodont in aspect, and especially in early stages of wear (Cooke and Ewer, 1972; Cooke, 1978a;

Harris and White, 1979; Reda et al., 2019; Geraads and Bobe, 2017a, b). In addition, Ny. pattersoni has wide and bulky premolars (both lower and upper third and fourth premolars) and shorter third molars in comparison to No. euilus, which suggests that this suid did not specialize in grazing to the extent that No. euilus did, and probably had a different diet. Considering its craniodental features, the stable carbon isotope signature, and its dental microwear signal, it is hypothesized here that Ny. pattersoni was probably a mixed feeder, eating plant material both from graze and browse, and occasionally exploiting hard food items. Nevertheless, Ny. pattersoni does not show as much variability in microwear textures as No. euilus. Following the argument above, this indicates that Ny. pattersoni probably had a less marked seasonal dietary pattern. Nyanzachoerus pattersoni does not show the specialized craniodental adaptations for rooting present in K. afarensis, Potamochoerus, and Sus (Cooke and Ewer, 1972; Cooke, 1978a; Reda et al., 2019). It is important to note that sample size of dental microwear among different suid species from Hadar varies in this study. There are 61 samples of No. euilus, 34 samples of K. afarensis, and only 14 samples of Ny. pattersoni. The microwear results reported in this study indicate that in spite of considerable overlap, there was certain dietary niche partitioning among suids at Hadar, which was not evident from carbon stable isotope analyses alone (Wynn et al., 2016; Lazagabaster et al., 2018a). 4.3. Comparisons of suid diets between Kanapoi and Hadar: implications for habitat reconstructions The suid Ny. pattersoni from Hadar has a similar microwear signal to Ny. pattersoni from Kanapoi, but surface heterogeneity (HAsfc) is significantly higher in the Kanapoi sample. The spread of the microwear signal in the PCA plot (Fig. 5), however, is larger for the sample from Hadar. Following the argument of Souron et al. (2015a) heterogenous surfaces may indicate either more dietary variability or less intense rooting activity (Souron et al., 2015a). In the PCA plot, the mean values of Ny. pattersoni at Kanapoi are intermediate between Po. larvatus and Po. porcus, and closer to K. afarensis, while the sample of Ny. pattersoni at Hadar groups closer to Phacochoerus, Ny. jaegeri, and No. euilus. It is possible that this suid had a narrower dietary niche at Hadar, but the microwear spread of microwear values may also be reflecting a slight change to a diet closer to that of No. euilus, and either including more intense grazing or more seasonal feeding (though an increase in C4 grazing is not supported by stable carbon isotopes; Bedaso et al., 2013; Wilson, 2013; Wynn et al., 2016). Nyanzachoerus pattersoni is relatively abundant in the Sidi Hakoma Member, when habitats have been reconstructed as more wooded and closed, with higher rainfall and shorter dry seasons in comparison to younger Hadar members (Reed, 2008). This suid virtually disappears from Hadar (there are only three specimens) in the overlying Denen Dora Member ~3.24 Ma, when the habitats became more open and grasslands spread (Bonnefille et al., 2004; Reed, 2008). The Denen Dora Member is dominated by No. euilus (>80% of relative suid abundance). It is possible that Ny. pattersoni was unable to compete for grassy resources with No. euilus and for underground resources with K. afarensis. The microwear signal of No. euilus is also like that of its hypothesized ancestor from Kanapoi, Ny. jaegeri. The overall microwear signal in No. euilus is quite variable, yet, as previously mentioned, some of these microwear signals may be the product of occasional or seasonal feeding on underground foods. Kolpochoerus afarensis, which is present across all the Hadar members, has a microwear signal consistent with a variable diet that probably included hard objects such as fruits or nuts, or underground resources. The slight trend in this species towards lower values of complexity and higher values of anisotropy through the

I.A. Lazagabaster / Journal of Human Evolution 132 (2019) 80e100

Hadar sequence indicates a small increase in grazing resources in the Kada Hadar Member ~3.1 Ma. Notochoerus euilus also has higher values of anisotropy in this member, suggesting more grazing at the end of the Hadar sequence, which is compatible with the paleoenvironmental reconstruction of Reed (2008). When compared with extant African suid species, the microwear texture evidence across Hadar suid species is consistent with diverse diets that may relate to both the presence of woodland/bushland habitats and grasslands at Hadar, with grasslands perhaps becoming more abundant after ~3.24 Ma (Bonnefille, 2010). In general, the dental surface textures of the two suid species present in Kanapoi do not differ significantly from that of their younger relatives at Hadar. It is the inclusion of a third speciesdK. afarensisdthat has an impact on the overall microwear signal. This suid exploited a different dietary niche to that of Ny. pattersoni and Ny. jaegeri/No. euilus that could have included the exploitation of underground resources year-round. The absence of some of these resources at Kanapoi may explain why Kolpochoerus has not been found at Kanapoi (Cooke and Ewer, 1972; Geraads and Bobe, 2017a, b). Kolpochoerus is present, though in low abundance, in sites contemporaneous with Kanapoi, such as Allia Bay (n ¼ 3) in the Turkana Basin (Dumouchel, 2018) and Galili (n ¼ 1), in Ethiopia (Kullmer et al., 2008), though it is absent from Mursi, in Ethiopia (Drapeau et al., 2014). Another hypothesis is that Kolpochoerus is absent from Mursi and Kanapoi not because of differences in environment/food resources, but because of physical or environmental barriers that prevented it to disperse into certain areas. The hypothesized ancestors of K. afarensis are found in localities close to Hadar, including those in Woranso-Mille, Gona, Galili, and the Middle Awash (Brunet and White, 2001; Kullmer et al., 2008; White et al., 2009; Haile-Selassie and Simpson, 2013). But if such barriers existed, they did not seem to have limited the dispersion of other mammalsdincluding hominins. It is also possible that the ecological niche of K. afarensis in Mursi and Kanapoi was occupied by other omnivorous animals (hominins, monkeys, carnivorans, and other suids). Nevertheless, suines become more abundant through the African Plio-Pleistocene as tetraconodontines and other extinct suid groups decline (Harris and White, 1979; Cooke, 2007; Rannikko et al., 2017; Lazagabaster et al., 2018a). The dental microwear texture differences between K. afarensis and all other fossil species studied here suggests an opening of a potential niche due to environmental differences between Hadar and Kanapoi, rather than direct competition for food resources among suids. 4.4. Dietary breadth expansion in the Australopithecus anamensiseA. afarensis lineage The dietary breadth expansion in the A. anamensiseA. afarensis lineage is characterized by the incorporation of C4 resources in the diet (Sponheimer et al., 2013; Wynn et al., 2013, 2016), but with no apparent change in the food textural properties consumed (Ungar et al., 2010). With respect to suids, both stable carbon isotopes and the microwear texture analyses presented here do not provide evidence for a significant dietary change between Kanapoi and Hadar in N. pattersoni and in Ny. jaegeri/No. euilus. However, the microwear textures of K. afarensisda suid that is present at Hadar but not Kanapoiddiffer considerably from the other suid species (Nyanzachoerus pattersoni and Ny. jaegeri/No. euilus). Kolpochoerus afarensis has a microwear signal closer to that of extant Po. porcus and to a lesser extent Po. larvatus, which suggests that this suid was actively exploiting hard foods and/or underground resources. Stable carbon isotope data indicate that Kolpochoerus afarensis was consuming a high quantity of C4 resources (Bedaso et al., 2013; Wynn et al., 2016). Therefore, it is reasonable to infer that either hard parts of C4 plants were part of

95

the diet of K. afarensis, or that this suid combined grazing with intense rooting behaviors. The absence of K. afarensis at Kanapoi may be explained by the absence at Kanapoi of certain resources this species exploited at Hadar. Given the available microwear texture of A. afarensis, it opens the door to speculate that hominins did not exploit such resources at Kanapoi or Hadar (as reflected by the low values of Asfc) and focused on the consumption of tough vegetation (leaves or grasses, as reflected by the low values of epLsar; Ungar et al., 2010). As open habitats and grasslands spread
galen et al., 2007; Cerling et al., 2011, 2015), hominins started to (Se exploit C4 resources in addition to C3 resources, but the bulk of the diet probably remained quite similar (leaves or grasses). From the standpoint of dental microwear texture analysis, suid diets did not change dramatically either, but the hypothesized differences in the environment could have allowed for a new dietary niche to be occupied by K. afarensis. The two most important limiting factors in the comparisons between Kanapoi and Hadar are time and space. These two sites are located in different regions and they are temporally separated by more than half a million years. These also affects the interpretation of paleoecological data on suids and other mammals. Understanding the evolutionary and paleoenvironmental context of the geographic and temporal midpoint is crucial. The stable carbon isotopic analyses on hominins and other mammals from WoransoMille, which is located close to Hadar, revealed that hominins were already exploiting C4 resources ~3.8 Ma (Levin et al., 2015), a pattern also observed in Theropithecus (Levin et al., 2015). Without dental microwear texture data of Woranso-Mille hominins, it can only be speculated that hominins were expanding the types of food resources and potentially the environments that they were able to exploit at this time. Woranso-Mille is located farther away from the large Hadar paleolake (Haile-Selassie et al., 2007) and it is possible that it supported different habitats than Hadar in the same time interval (~3.5e3.0 Ma). The combined evidence of the reconstructed habitats and the suid isotopes and microwear suggests that the habitats at Hadar were different from those present at Kanapoi. The increase in the presence of C4 plants and the expansion of C4 grasslands in Hadar, especially after ~3.24 Ma, may explain why hominins incorporated C4 resources in the diet. In turn, this habitat change could have opened a new dietary niche for K. afarensis and favored the disappearance of Nyanzachoerus pattersoni from the area. While the habitats at Hadar could have been more heterogeneous and the climate more seasonal (Bonnefille et al., 2004), Kanapoi already shows a high degree of fragmentation (Wynn, 2000; Ungar et al., 2017; Quinn and Lepre, 2019). Moreover, the spread of C4 plants does not imply a change in the ratio of forested vs. open settings but rather, a change in vegetation and foods available (Bibi et al., 2013; Blondel et al., 2018; Souron, 2018). If this is the case, both the suids and the hominins needed to seek out different food resources due to these climatic variables that affected C3 resources between the two localities. 5. Conclusions The considerable overlap in the microwear texture of extant African suids reflects the complexity of suid diets and the challenging task of reconstructing the dietary ecology of fossil suids. Most suids have generalized diets and even when they have the craniodental morphology that allows specialization in a specific food resource, they still opportunistically or seasonally feed on other foods. The microwear results on extant suids in this study are not in full agreement with those found by Souron et al. (2015a). While it is clear that microwear texture analyses have the potential to be used to infer aspects of diet in fossil suids

96

I.A. Lazagabaster / Journal of Human Evolution 132 (2019) 80e100

(Ungar et al., 2017), further research is needed to understand the relationship between dental microwear textures and feeding behaviors in extant suids (Ward and Mainland, 1999; Souron et al., 2015a; Yamada et al., 2018). Despite the overlap in the microwear signal, the results suggest that suids occupied different dietary niches within Hadar (~3.45e2.95 Ma). This was not evident from analyses of stable isotopes alone. Notochoerus euilus was likely a habitual grazer but it could have occasionally fed on underground resources and harder foods either opportunistically or seasonally, like extant Phacochoerus. In Kanapoi, there are indications that Ny. jaegeri, the hypothesized ancestor of No. euilus, could have relied more on graze than Nyanzachoerus pattersoni but the dietary niche partitioning among suids is less evident in Kanapoi than in Hadar. Nyanzachoerus pattersoni probably had a mixed diet consisting of both browse and graze, and there is no indication that it routinely fed on hard brittle foods. The diet of Nyanzachoerus pattersoni did not significantly change between Kanapoi and Hadar, suggesting that the food and habitat used by this suid were present at both sites. Kolpochoerus afarensis likely had a generalized diet similar to extant Po. porcus and to a lesser extent Po. larvatus, which may have included hard brittle foods and underground resources. The dietary inferences derived from dental microwear textures are congruent to a certain extent with what is known of the craniodental morphology of these species. While K. afarensis and Nyanzachoerus pattersoni had low-crowned bunodont molars that resemble extant Potamochoerus or Sus, No. euilus had elongated and hypsodont third molars more comparable to extant Phacochoerus, and K. afarensis had craniodental adaptations for rooting. The dental microwear and carbon stable isotope values in Nyanzachoerus pattersoni and in Ny. jaegeri/No. euilus did not change significantly between Kanapoi and Hadar. The main driver of the differences between Kanapoi and Hadar is the microwear signal of K. afarensis. There are no specimens attributable to the genus Kolpochoerus at Kanapoi, raising the possibility that the dietary niche occupied by Kolpochoerus was not available at Kanapoi or that the ancestors of K. afarensis lacked the necessary adaptations to cope with the habitats present at Kanapoi. Considering the temporal and spatial separation between Kanapoi and Hadar, a biogeographical explanation for the absence of Kolpochoerus at Kanapoi cannot be excluded. The presumed increase in the presence of open habitats, probably grasslands, especially after ~3.24 Ma, could have caused the disappearance of Nyanzachoerus pattersoni in Hadar and the peak in abundance of No. euilus. Potentially, the habitats at Hadar were more heterogenous or fragmented and the climate was probably more seasonal than at Kanapoi, which would have favored the availability of certain underground resources. In this setting, hominins could have been forced to incorporate C4 resources in the diet, but given the available evidence, A. afarensis did not take advantage of all the dietary resources in the environment. Rather, its diet was limited to tough food. If this is the case, the transition towards flexible dietary behaviors that marked a milestone in human evolution had not yet occurred. Acknowledgements I thank the curators and staff of the Authority for Research and Conservation of Cultural Heritage in Addis Ababa, Ethiopia, for access to the Hadar fossil collection in their care. I thank P. Ungar for facilitating the instruments and software necessary to carry out this research, and all the students and faculty at the Microwear Lab at the University of Arkansas, especially E. Abella and L. Delezene. I would like to thank P. Ungar, K. Reed, W. Kimbel, and J. Van der Made, for their helpful suggestions and for directing my work. This manuscript was vastly improved by the comments and edits of G.

Merceron, A. Souron, and an anonymous reviewer. I would also like to thank A. McGrosky, E. Hallett, I. Smail, J. Rowan, and E. Locke, for helpful comments. This study was possible thanks to a research grant from the School of Human Evolution and Social Change, Arizona State University. This research was also made possible through the support of a grant from the John Templeton Foundation to the Institute of Human Origins at Arizona State University. The opinions expressed in this publication are those of the authors and do not necessarily reflect the views of the John Templeton Foundation. The author was partially supported by Obra Social “la Caixa” Graduate Fellowship during the completion of this work. Supplementary Online Material Supplementary online material to this article can be found online at https://doi.org/10.1016/j.jhevol.2019.04.010. References Alemseged, Z., Wynn, J.G., Kimbel, W.H., Reed, D., Geraads, D., Bobe, R., 2005. A new hominin from the Basal Member of the Hadar Formation, Dikika, Ethiopia, and its geological context. Journal of Human Evolution 49, 499e514. Alemseged, Z., Spoor, F., Kimbel, W.H., Bobe, R., Geraads, D., Reed, D., Wynn, J.G., 2006. A juvenile early hominin skeleton from Dikika, Ethiopia. Nature 443, 296e301. Ambrose, S.H., DeNiro, M.J., 1986. The isotopic ecology of East African mammals. Oecologia 69, 395e406. Andrews, P.J., Humphrey, L., 1999. African Miocene environments and the transition to early hominines. In: Bromage, T.G., Schrenk, F. (Eds.), African Biogeography, Climate Change, and Human Evolution. Oxford University Press, Oxford, pp. 282e300. Aronson, J.L., Hailemichael, M., Savin, S.M., 2008. Hominid environments at Hadar from paleosol studies in a framework of Ethiopian climate change. Journal of Human Evolution 55, 532e550. Beaune, D., Bollache, L., Fruth, B., Bretagnolle, F., 2012. Bush pig (Potamochoerus porcus) seed predation of bush mango (Irvingia gabonensis) and other plant species in Democratic Republic of Congo. African Journal of Ecology 50, 509e512. Bedaso, Z.K., Wynn, J.G., Alemseged, Z., Geraads, D., 2013. Dietary and paleoenvironmental reconstruction using stable isotopes of herbivore tooth enamel from middle Pliocene Dikika, Ethiopia: implication for Australopithecus afarensis habitat and food resources. Journal of Human Evolution 64, 21e38. Behrensmeyer, A.K., 2008. Paleoenvironmental context of the Pliocene AL 333 “first family” hominin locality, Hadar Formation, Ethiopia. Geological Society of America Special Papers 446, 203e214. Behrensmeyer, A.K., Reed, K.E., 2013. Reconstructing the habitats of Australopithecus: Paleoenvironments, site taphonomy, and faunas. In: Reed, K.E., Fleagle, J.G., Leakey, R.E. (Eds.), The Paleobiology of Australopithecus. Springer, Dordrecht, pp. 41e60. Behrensmeyer, A.K., Bobe, R., Alemseged, Z., 2007. Approaches to the analysis of faunal change during the East African Pliocene. In: Bobe, R., Alemseged, Z., Behrensmeyer, A.K. (Eds.), Hominin Environments in the East African Pliocene: An Assessment of the Faunal Evidence. Springer, Dordrecht, pp. 1e24. Bibi, F., Souron, A., Bocherens, H., Uno, K., Boisserie, J.-R., 2013. Ecological change in the lower Omo Valley around 2.8 Ma. Biology Letters 9, 20120890. Bishop, L.C., 1994. Pigs and the ancestors: hominids, suids and environments during the Plio-Pleistocene of East Africa. Ph.D. Dissertation, Yale University. Bishop, L.C., 1999. Suid paleoecology and habitat preferences at African Pliocene and Pleistocene hominid localities. In: Bromage, T., Schrenk, E. (Eds.), African Biogeography, Climate Change, and Human Evolution. Oxford University Press, Oxford, pp. 99e111. Bishop, L.C., 2010. Suoidea. In: Werdelin, L., Sanders, W.J. (Eds.), Cenozoic Mammals of Africa. University of California Press, Berkeley, pp. 821e842. Bishop, L.C., 2011. Suidae. In: Harrison, T. (Ed.), Paleontology and Geology of Laetoli: Human Evolution in Context. vol. 2: Fossil Hominins and the Associated Fauna. Springer, Dordrecht, pp. 327e337. Bishop, L.C., Hill, A., Kingston, J.D., 1999. Paleoecology of Suidae from the Tugen Hills, Baringo, Kenya. In: Andrews, P.J., Banham, P. (Eds.), Late Cenozoic Environments and Hominid Evolution: a Tribute to Bill Bishop. Geological Society, London, pp. 99e111. Bishop, L.C., King, T., Hill, A., Wood, B., 2006. Palaeoecology of Kolpochoerus heseloni (¼ K. limnetes): A multiproxy approach. Transactions of the Royal Society of South Africa 61, 81e88. Blondel, C., Rowan, J., Merceron, G., Bibi, F., Negash, E., Barr, W.A., Boisserie, J.-R., 2018. Feeding ecology of Tragelaphini (Bovidae) from the Shungura Formation, Omo Valley, Ethiopia: Contribution of dental wear analyses. Palaeogeography, Palaeoclimatology, Palaeoecology 496, 103e120. Bobe, R., 2011. Fossil mammals and paleoenvironments in the Omo-Turkana Basin. Evolutionary Anthropology 20, 254e263.

I.A. Lazagabaster / Journal of Human Evolution 132 (2019) 80e100 Bobe, R., Behrensmeyer, A.K., Chapman, R.E., 2002. Faunal change, environmental variability and late Pliocene hominin evolution. Journal of Human Evolution 42, 475e497. Boisserie, J.-R., Souron, A., Mackaye, H.T., Likius, A., Vignaud, P., Brunet, M., 2014. A new species of Nyanzachoerus (Cetartiodactyla: Suidae) from the late Miocene
nalla, Chad, Central Africa. PLoS one 9, e103221. Toros-Me Bonnefille, R., 2010. Cenozoic vegetation, climate changes and hominid evolution in tropical Africa. Global and Planetary Change 72, 390e411. Bonnefille, R., Vincens, A., Buchet, G., 1987. Palynology, stratigraphy and palaeoenvironment of a Pliocene hominid site (2.9e3.3 my) at Hadar, Ethiopia. Palaeogeography, Palaeoclimatology, Palaeoecology 60, 249e281.
, F., Jolly, D., Peyron, O., 2004. High-resolution vegeBonnefille, R., Potts, R., Chalie tation and climate change associated with Pliocene Australopithecus afarensis. Proceedings of the National Academy of Sciences USA 101, 12125e12129. Breytenbach, G.J., Skinner, J.D., 1982. Diet, feeding and habitat utilization by bushpigs Potamochoerus porcus Linnaeus. South African Journal of Wildlife Research 12, 1e7. Brugnoli, E., Farquhar, G.D., 2000. Photosynthetic fractionation of carbon isotopes. In: Leegood, R.C., Sharkey, T.D., von Caemmerer, S. (Eds.), Photosynthesis. Advances in Photosynthesis and Respiration, vol. 9. Springer, Dordrecht, pp. 399e434. ces de Suini (Mammalia, Suidae) Brunet, M., White, T.D., 2001. Deux nouvelles espe
mie des du continent africain (Ethiopie; Tchad). Comptes Rendus de l'Acade Sciences Paris 332, 51e57. Butynski, T.M., de Jong, Y.A., 2017. Common warthog Phacochoerus africanus (Gmelin, 1788). In: Melletti, M., Meijaard, E. (Eds.), Ecology, Conservation and Management of Wild Pigs and Peccaries. Cambridge University Press, Cambridge, pp. 85e100. Cabin, R.J., Mitchell, R.J., 2000. To Bonferroni or not to Bonferroni: when and how are the questions. Bulletin of the Ecological Society of America 81, 246e248. Calandra, I., Merceron, G., 2016. Dental microwear texture analysis in mammalian ecology. Mammal Review 46, 215e228. Calandra, I., Schulz, E., Pinnow, M., Krohn, S., Kaiser, T.M., 2012. Teasing apart the contributions of hard dietary items on 3D dental microtextures in primates. Journal of Human Evolution 63, 85e98. Campisano, C.J., 2007. Tephrostratigraphy and hominin paleoenvironments of the Hadar Formation, Afar depression, Ethiopia. Ph.D. Dissertation, Rutgers University. Campisano, C.J., 2012. Geological summary of the Busidima Formation (Plio-Pleistocene) at the Hadar paleoanthropological site, Afar depression, Ethiopia. Journal of Human Evolution 62, 338e352. Campisano, C.J., Feibel, C.S., 2008. Depositional environments and stratigraphic summary of the Pliocene Hadar formation at Hadar, Afar depression, Ethiopia. Geological Society of America Special Papers 446, 179e201. Cerling, T.E., Harris, J.M., 1999. Carbon isotope fractionation between diet and bioapatite in ungulate mammals and implications for ecological and paleoecological studies. Oecologia 120, 347e363. Cerling, T.E., Viehl, K., 2004. Seasonal diet changes of the forest hog (Hylochoerus meinertzhageni Thomas) based on the carbon isotopic composition of hair. African Journal of Ecology 42, 88e92. Cerling, T.E., Harris, J., Passey, B.H., 2003. Diets of East African Bovidae based on stable isotope analysis. Journal of Mammalogy 84, 456e470. Cerling, T.E., Hart, J.A., Hart, T.B., 2004. Stable isotope ecology in the Ituri Forest. Oecologia 138, 5e12. Cerling, T.E., Wynn, J.G., Andanje, S.A., Bird, M.I., Korir, D.K., Levin, N.E., Mace, W., Macharia, A.N., Quade, J., Remien, C.H., 2011. Woody cover and hominin environments in the past 6 million years. Nature 476, 51e56. Cerling, T.E., Manthi, F.K., Mbua, E.N., Leakey, L.N., Leakey, M.G., Leakey, R.E., Brown, F.H., Grine, F.E., Hart, J.A., Kaleme, P., Roche, H., 2013. Stable isotopebased diet reconstructions of Turkana Basin hominins. Proceedings of the National Academy of Sciences USA 110, 10501e10506. Cerling, T.E., Andanje, S.A., Blumenthal, S.A., Brown, F.H., Chritz, K.L., Harris, J.M., Hart, J.A., Kirera, F.M., Kaleme, P., Leakey, L.N., Leakey, M.G., 2015. Dietary changes of large herbivores in the Turkana Basin, Kenya from 4 to 1 Ma. Proceedings of the National Academy of Sciences USA 112, 11467e11472. Charles, C., Jaeger, J.-J., Michaux, J., Viriot, L., 2007. Dental microwear in relation to changes in the direction of mastication during the evolution of Myodonta (Rodentia, Mammalia). Naturwissenschaften 94, 71e75. Conover, W.J., Iman, R.L., 1981. Rank transformations as a bridge between parametric and nonparametric statistics. The American Statistician 35, 124e129. Cooke, H.B.S., 1978a. Plio-Pleistocene Suidae from Hadar, Ethiopia. Kirtlandia 29, 1e63. Cooke, H.B.S., 1978b. Suid evolution and correlation of African hominid localities: An alternative taxonomy. Science 201, 460e463. Cooke, H.B.S., 1985. Plio-Pleistocene Suidae in relation to African hominid deposits.
s au Plio-Pleistoce ne. In: Coppens, Y. (Ed.), L'Environnement des Hominide Masson, Paris, pp. 101e117. Cooke, H.B.S., 2007. Stratigraphic variation in Suidae from the Shungura Formation and some coeval deposits. In: Bobe, R., Alemseged, Z., Behrensmeyer, A.K. (Eds.), Hominin Environments in the East African Pliocene: An Assessment of the Faunal Evidence. Springer, Dordrecht, pp. 107e127. Cooke, H.B.S., Ewer, R.F., 1972. Fossil Suidae from Kanapoi and Lothagam, Northwestern Kenya. Bulletin of the Museum of Comparative Zoology 143, 149e296. Cooke, H.B.S., Wilkinson, A.F., 1978. Suidae and Tayassuidae. In: Maglio, J.V., Cooke, H.B.S. (Eds.), Evolution of African Mammals. Harvard University Press, Harvard, pp. 435e482.

97

Cuddahee, R.E., 2008. East African hominin and suid environments in the Turkana basin: An analysis of fossil Suidae (Mammalia, Artiodactyla) mandibular ecomorphology. Ph.D. Dissertation. State University of New York at Buffalo. Cumming, D.H.M., 1975. A Field Study of the Ecology & Behaviour of Warthog. Trustees of the National Museums and Monuments of Rhodesia, Salisbury. Cumming, D.H.M., 2013. Phacochoerus africanus. The common warthog. In: Kingdon, J. (Ed.), Mammals of Africa. Bloomsbury Publishing, London, pp. 54e60. re (Hylochoerus meinertzhageni Thomas) au d'Huart, J.P., 1978. Ecologie de l'hyloche Parc national des Virunga. Fondation pour favoriser les recherches scientifiques en Afrique, Brussels. d'Huart, J.P., Yohannes, E., 2014. Assessment of the present distribution of the forest hog (Hylochoerus meinertzhageni) in Ethiopia. Journal of Mountain Ecology 3, 46e48. Daegling, D.J., McGraw, W.S., Ungar, P.S., Pampush, J.D., Vick, A.E., Bitty, E.A., 2011. Hard-object feeding in sooty mangabeys (Cercocebus atys) and interpretation of early hominin feeding ecology. PLoS One 6, e23095. Damuth, J., Janis, C.M., 2011. On the relationship between hypsodonty and feeding ecology in ungulate mammals, and its utility in palaeoecology. Biological Reviews 86, 733e758. Delezene, L.K., Zolnierz, M.S., Teaford, M.F., Kimbel, W.H., Grine, F.E., Ungar, P.S., 2013. Premolar microwear and tooth use in Australopithecus afarensis. Journal of Human Evolution 65, 282e293. Delezene, L.K., Teaford, M.F., Ungar, P.S., 2016. Canine and incisor microwear in pitheciids and Ateles reflects documented patterns of tooth use. American Journal of Physical Anthropology 161, 6e25. deMenocal, P.B., 1995. Plio-Pleistocene African climate. Science 270, 53e59. deMenocal, P.B., 2004. African climate change and faunal evolution during the PlioceneePleistocene. Earth and Planetary Science Letters 220, 3e24. DeSantis, L.R., Haupt, R.J., 2014. Cougars' key to survival through the Late Pleistocene extinction: insights from dental microwear texture analysis. Biology Letters 10, 20140203. Drapeau, M.S.M., Bobe, R., Wynn, J.G., Campisano, C.J., Dumouchel, L., Geraads, D., 2014. The Omo Mursi Formation: A window into the East African Pliocene. Journal of Human Evolution 75, 64e79. Du, A., Robinson, J.R., Rowan, J., Lazagabaster, I.A., Behrensmeyer, A.K., 2019. Stable carbon isotopes from paleosol carbonate and herbivore enamel document differing paleovegetation signals in the eastern African Plio-Pleistocene. Review of Palaeobotany and Palynology 261, 41e52. Dumouchel, L., 2018. A multi-proxy analysis of Australopithecus anamensis paleoecology in the Omo-Turkana Basin. Ph.D. Dissertation. The George Washington University. Dumouchel, L., Bobe, R., 2019. Paleoecological implications of dental mesowear and hypsodonty in fossil ungulates from Kanapoi. Journal of Human Evolution. https://doi.org/10.1016/j.jhevol.2018.11.004. Dunn, O.J., 1958. Estimation of the means of dependent variables. Annals of Mathematical Statistics 29, 1095e1111. Ehleringer, J.R., Osmond, C.B., 2000. Stable isotopes. In: Pearcy, R.W., Ehleringer, J.R., Mooney, H.A., Rundel, P.W. (Eds.), Plant Physiological Ecology. Springer, Dordrecht, pp. 281e300.
n, D., Pe
rez-Pe
rez, A., 2012. Buccal Estebaranz, F., Galbany, J., Martínez, L.M., Turbo dental microwear analyses support greater specialization in consumption of hard foodstuffs for Australopithecus anamensis. Journal of Anthropological Sciences 90, 163e185.
n, D., Pe
rez-Pe
rez, A., 2009. Testing Estebaranz, F., Martínez, L.M., Galbany, J., Turbo hypotheses of dietary reconstruction from buccal dental microwear in Australopithecus afarensis. Journal of Human Evolution 57, 739e750. Ewer, R.F., 1958. Adaptive features in the skulls of African Suidae. Proceedings of the Zoological Society of London 131, 135e155. Ewer, R.F., 1970. The head of the forest hog, Hylochoerus meinertzhageni. African Journal of Ecology 8, 43e52. Feakins, S.J., Levin, N.E., Liddy, H.M., Sieracki, A., Eglinton, T.I., Bonnefille, R., 2013. Northeast African vegetation change over 12 my. Geology 41, 295e298. Feibel, C.S., 2003. Stratigraphy and depositional setting of the Pliocene Kanapoi Formation, lower Kerio valley, Kenya. Natural History Museum of Los Angeles County, Contributions in Science 498, 9e20. Fessaha, N., 1999. Systematics of Hadar (Afar, Ethiopia) Suidae. Ph.D. Dissertation. Howard University. Field, D.J., 2017. Preliminary paleoecological insights from the Pliocene avifauna of Kanapoi, Kenya: Implications for the ecology of Australopithecus anamensis. Journal of Human Evolution. https://doi.org/10.1016/j.jhevol.2017.08.007. Geraads, D., Bobe, R., 2017a. Suidae from Kanapoi. Journal of Human Evolution. https://doi.org/10.1016/j.jhevol.2017.05.004. Geraads, D., Bobe, R., 2017b. Ruminants (Giraffidae and Bovidae) from Kanapoi. Journal of Human Evolution. https://doi.org/10.1016/j.jhevol.2017.08.006. Geraads, D., Bobe, R., Manthi, F.K., 2013. New ruminants (Mammalia) from the Pliocene of Kanapoi, Kenya, and a revision of previous collections, with a note on the Suidae. Journal of African Earth Sciences 85, 53e61. Grine, F.E., 1986. Dental evidence for dietary differences in Australopithecus and Paranthropus: A quantitative analysis of permanent molar microwear. Journal of Human Evolution 15, 783e822. Grine, F.E., Martin, L.B., 1988. Enamel thickness and development in Australopithecus and Paranthropus. In: Grine, F.E. (Ed.), The Evolutionary History of the “Robust” Australopithecines. Aldine de Gruyter, New York, pp. 3e42.

98

I.A. Lazagabaster / Journal of Human Evolution 132 (2019) 80e100

Grine, F.E., Ungar, P.S., Teaford, M.F., 2006a. Was the Early Pliocene hominin ‘Australopithecus’ anamensis a hard object feeder? South African Journal of Science 102, 301e310. Grine, F.E., Ungar, P.S., Teaford, M.F., El-Zaatari, S., 2006b. Molar microwear in Praeanthropus afarensis: evidence for dietary stasis through time and under diverse paleoecological conditions. Journal of Human Evolution 51, 297e319. Grine, F.E., Judex, S., Daegling, D.J., Ozcivici, E., Ungar, P.S., Teaford, M.F., Sponheimer, M., Scott, J., Scott, R.S., Walker, A., 2010. Craniofacial biomechanics and functional and dietary inferences in hominin paleontology. Journal of Human Evolution 58, 296e308. Gunnell, G.F., Manthi, F.K., 2018. Pliocene bats (Chiroptera) from Kanapoi, Turkana Basin, Kenya. Journal of Human Evolution. https://doi.org/10.1016/j.jhevol.2018. 01.001. Haile-Selassie, Y., Simpson, S.W., 2013. A new species of Kolpochoerus (Mammalia: Suidae) from the Pliocene of Central Afar, Ethiopia: Its taxonomy and phylogenetic relationships. Journal of Mammalian Evolution 20, 115e127. Haile-Selassie, Y., Melillo, S.M., 2015. Middle Pliocene hominin mandibular fourth premolars from Woranso-Mille (Central Afar, Ethiopia). Journal of Human Evolution 78, 44e59. Haile-Selassie, Y., Deino, A., Saylor, B., Umer, M., Latimer, B., 2007. Preliminary geology and paleontology of new hominid-bearing Pliocene localities in the central Afar region of Ethiopia. Anthropological Science 115, 215e222. Haile-Selassie, Y., Saylor, B.Z., Deino, A., Alene, M., Latimer, B.M., 2010. New hominid fossils from Woranso-Mille (Central Afar, Ethiopia) and taxonomy of early Australopithecus. American Journal of Physical Anthropology 141, 406e417. Hailemichael, M., 2000. The Pliocene environment of Hadar. Ethiopia: A comparative isotopic study of paleosol carbonates and lacustrine mollusk shells of the Hadar Formation. Ph.D. Dissertation, Case Western Reserve University. Hailemichael, M., Aronson, J.L., Savin, S., Tevesz, M.J.S., Carter, J.G., 2002. d18O in mollusk shells from Pliocene Lake Hadar and modern Ethiopian lakes: Implications for history of the Ethiopian monsoon. Palaeogeography, Palaeoclimatology, Palaeoecology 186, 81e99. Harris, J.M., 1983. Family Suidae. In: Harris, J.M. (Ed.), Koobi Fora Research Project: The Fossil Ungulates: Proboscidea, Perissodactyla, and Suidae. Clarendon Press, Oxford, pp. 215e302. Harris, J.M., Cerling, T., 2002. Dietary adaptations of extant and Neogene African suids. Journal of Zoology 256, 45e54. Harris, J.M., Leakey, M.G., 2003a. Introduction. In: Harris, J.M., Leakey, M.G. (Eds.), Geology and Vertebrate Paleontology of the Early Pliocene Site of Kanapoi, Northern Kenya. Natural History Museum of Los Angeles County, Los Angeles, pp. 1e8. Harris, J.M., Leakey, M.G., 2003b. Lothagam Suidae. In: Leakey, M.G., Harris, J.M. (Eds.), Lothagam: The Dawn of Humanity in Eastern Africa. Columbia University Press, New York, pp. 485e519. Harris, J.M., White, T.D., 1979. Evolution of the Plio-Pleistocene African Suidae. Transactions of the American Philosophical Society 69, 1e128. Harris, J.M., Leakey, M.G., Cerling, T.E., Winkler, A.J., 2003. Early Pliocene tetrapod remains from Kanapoi, Lake Turkana Basin, Kenya. In: Harris, J.M., Leakey, M.G. (Eds.), Geology and Vertebrate Paleontology of the Early Pliocene site of Kanapoi, Northern Kenya. Natural History Museum of Los Angeles County, Los Angeles, pp. 39e114. Harrison, T., 2011. Hominins from the Upper Laetolil and Upper Ndolanya Beds, Laetoli. In: Harrison, T. (Ed.), Paleontology and Geology of Laetoli: Human Evolution in Context, Fossil Hominins and the Associated Fauna, vol. 2. Springer, Dordrecht, pp. 141e188. Head, J.J., Müller, J., 2018. Squamate reptiles from Kanapoi: Faunal evidence for hominin paleoenvironments. Journal of Human Evolution. https://doi.org/10. 1016/j.jhevol.2018.01.007. Heaton, T., 1999. Spatial, species, and temporal variations in the 13C/12C ratios of C3 plants: Implications for palaeodiet studies. Journal of Archaeological Science 26, 637e649. Herring, S.W., 1980. Functional design of cranial muscles: Comparative and physiological studies in pigs. American Zoologist 20, 283e293. Herring, S.W., 1985. Morphological correlates of masticatory patterns in peccaries and pigs. Journal of Mammalogy 66, 603e617. Hlusko, L.J., Haile-Selassie, Y., 2007. Nyanzachoerus syrticus (Artiodactyla, Suidae) from the late Miocene of Lemudong'o, Kenya. Kirtlandia 56, 152e157. Hopley, P.J., Maslin, M.A., 2010. Climate-averaging of terrestrial faunas: an example from the Plio-Pleistocene of South Africa. Paleobiology 36, 32e50. Hou, S., Deng, T., He, W., Chen, S., 2014. Foraging behavior of Chleuastochoerus (Suidae, Artiodactyla): A case study of skull and mandible morpho-functional analysis. Science China Earth Sciences 57, 988e998. Hunter, J.P., Fortelius, M., 1994. Comparative dental occlusal morphology, facet development, and microwear in two sympatric species of Listriodon (Mammalia: Suidae) from the middle Miocene of western Anatolia (Turkey). Journal of Vertebrate Paleontology 14, 105e126. International Organization for Standardization, 2012. ISO/FDIS 25178-2 e Geometrical product specifications (GPS) e Surface texture: Areal e Part 2: terms, definitions and surface texture parameters. https://www.iso.org/ standard/42785.html. Janis, C.M., Thomason, J.J., 1995. Correlations between craniodental morphology and feeding behavior in ungulates: reciprocal illumination between living and fossil taxa. In: Thomason, J.J. (Ed.), Functional Morphology in Vertebrate Paleontology. Cambridge University Press, Cambridge, pp. 76e98.

Johanson, D.C., 2017. The paleoanthropology of Hadar, Ethiopia. Comptes Rendus Palevol 16, 140e154. Jones, M.A., 1984. Seasonal changes in the diet of bushpig, Potamochoerus porcus Linn., in the Matopos National Park. South African Journal of Wildlife Research, 14, pp. 97e100. Kay, R.F., 1985. Dental evidence for the diet of Australopithecus. Annual Review of Anthropology 14, 315e341. Kimbel, W.H., 1988. Identification of a partial cranium of Australopithecus afarensis from the Koobi Fora Formation, Kenya. Journal of Human Evolution 17, 647e656. Kimbel, W.H., Delezene, L., 2009. “Lucy” redux: A review of research on Australopithecus afarensis. American Journal of Physical Anthropology 140, 2e48. Kimbel, W.H., Johanson, D.C., Rak, Y., 1994. The first skull and other new discoveries of Australopithecus afarensis at Hadar, Ethiopia. Nature 368, 449e451. Kimbel, W.H., Rak, Y., Johanson, D.C., 2004. The Skull of Australopithecus afarensis. Oxford University Press, Oxford. Kimbel, W.H., Lockwood, C.A., Ward, C.V., Leakey, M.G., Rak, Y., Johanson, D.C., 2006. Was Australopithecus anamensis ancestral to A. afarensis? A case of anagenesis in the hominin fossil record. Journal of Human Evolution 51, 134e152. Kingdon, J., 2015. The Kingdon Field Guide to African Mammals, 2nd ed. Princeton University Press, Princeton. Krueger, K.L., Scott, J.R., Kay, R.F., Ungar, P.S., 2008. Dental microwear textures of “Phase I” and “Phase II” facets. American Journal of Physical Anthropology 137, 485e490. Kullmer, O., 1999. Evolution of African Plio-Pleistocene suids (Artiodactyla: Suidae) based on tooth pattern analysis. Kaupia 9, 1e34. Kullmer, O., 2008. The fossil Suidae from the Plio-Pleistocene Chiwondo Beds of northern Malawi, Africa. Journal of Vertebrate Paleontology 28, 208e216. Kullmer, O., Sandrock, O., Bence Viola, T., Hujer, W., Said, H., Seidler, H., 2008. Suids, elephantoids, paleochronology, and paleoecology of the Pliocene hominid site Galili, Somali Region, Ethiopia. Palaios 23, 452e464. Lambert, J.E., Chapman, C.A., Wrangham, R.W., Conklin-Brittain, N.L., 2004. Hardness of cercopithecine foods: implications for the critical function of enamel thickness in exploiting fallback foods. American Journal of Physical Anthropology 125, 363e368. Lazagabaster, I.A., 2013. Microwear analysis on suoid incisors: a new method to study faunal adaptive responses to the environmental changes which shaped human evolution. M.Sc. Dissertation, University of Coimbra. Lazagabaster, I.A., Rowan, J., Kamilar, J.M., Reed, K.E., 2016. Evolution of craniodental correlates of diet in African Bovidae. Journal of Mammalian Evolution 23, 385e396. Lazagabaster, I.A., Souron, A., Rowan, J., Robinson, J.R., Campisano, C.J., Reed, K.E., 2018a. Fossil Suidae (Mammalia, Artiodactyla) from Lee Adoyta, Ledi-Geraru, lower Awash Valley, Ethiopia: Implications for late Pliocene turnover and paleoecology. Palaeogeography, Palaeoclimatology, Palaeoecology 504, 186e200. Lazagabaster, I.A., Brophy, J., Sanisidro, O., Pineda-Munoz, S., Berger, L., 2018b. A new partial cranium of Metridiochoerus (Suidae, Mammalia) from Malapa, South Africa. Journal of African Earth Sciences 145, 49e52. Lazzari, V., Charles, C., Tafforeau, P., Vianey-Liaud, M., Aguilar, J.P., Jaeger, J.J., Michaux, J., Viriot, L., 2008. Mosaic convergence of rodent dentitions. PLoS One 3, e3607. ^, S., Josse, J., Husson, F., 2008. FactoMineR: An R package for multivariate analysis. Le Journal of Statistical Software 25, 1e18. Leakey, M.G., Feibel, C.S., McDougall, I., Walker, A., 1995. New four-million-year-old hominid species from Kanapoi and Allia Bay, Kenya. Nature 376, 565e571. Lee-Thorp, J.A., Sponheimer, M., Passey, B.H., De Ruiter, D.J., Cerling, T.E., 2010. Stable isotopes in fossil hominin tooth enamel suggest a fundamental dietary shift in the Pliocene. Philosophical Transactions of the Royal Society B 365, 3389e3396. Lee-Thorp, J., Likius, A., Mackaye, H.T., Vignaud, P., Sponheimer, M., Brunet, M., 2012. Isotopic evidence for an early shift to C4 resources by Pliocene hominins in Chad. Proceedings of the National Academy of Sciences USA 109, 20369e20372. Leus, K., MacDonald, A.A., 1997. From babirusa (Babyrousa babyrussa) to domestic pig: the nutrition of swine. Proceedings of the Nutrition Society 56, 1001e1012. Levin, N.E., Haile-Selassie, Y., Frost, S.R., Saylor, B.Z., 2015. Dietary change among hominins and cercopithecids in Ethiopia during the early Pliocene. Proceedings of the National Academy of Sciences USA 112, 12304e12309. Lucas, P.W., 2004. Dental Functional Morphology: How Teeth Work. Cambridge University Press, Cambridge. Lucas, P.W., Constantino, P.J., Wood, B.A., 2008. Inferences regarding the diet of extinct hominins: structural and functional trends in dental and mandibular morphology within the hominin clade. Journal of Anatomy 212, 486e500. Macho, G.A., Shimizu, D., Jiang, Y., Spears, I.R., 2005. Australopithecus anamensis: A finite-element approach to studying the functional adaptations of extinct hominins. The Anatomical Record Part A 283, 310e318.
rouil, S., Gautier-Hion, A., 2003. Seed eating in elephant dung by Magliocca, F., Que two large mammals in the Congo Republic. Revue d'Ecologie, Terre et Vie 58, 143e149. Manthi, F.K., 2006. The Pliocene micromammalian fauna from Kanapoi, Northwestern Kenya, and its contribution to understanding the environment of Australopithecus anamensis. Ph.D. Dissertation. University of Cape Town. Manthi, F.K., Cerling, T.E., Chritz, K.L., Blumenthal, S.A., 2017. Diets of mammalian fossil fauna from Kanapoi, northwestern Kenya. Journal of Human Evolution. https://doi.org/10.1016/j.jhevol.2017.05.005. Martin, F., Plastiras, C.A., Merceron, G., Souron, A., Boisserie, J.R., 2018. Dietary niches of terrestrial cercopithecines from the Plio-Pleistocene Shungura

I.A. Lazagabaster / Journal of Human Evolution 132 (2019) 80e100 Formation, Ethiopia: evidence from Dental Microwear Texture Analysis. Scientific reports 8, 14052. Mbua, E., Kusaka, S., Kunimatsu, Y., Geraads, D., Sawada, Y., Brown, F.H., Sakai, T., Boisserie, J.-R., Saneyoshi, M., Omuombo, C., Muteti, S., 2016. Kantis: A new Australopithecus site on the shoulders of the Rift Valley near Nairobi, Kenya. Journal of Human Evolution 94, 28e44. McDougall, I.A.N., Brown, F.H., 2008. Geochronology of the pre-KBS tuff sequence, Omo Group, Turkana Basin. Journal of the Geological Society 165, 549e562. McHenry, H.M., 1984. Relative cheek-tooth size in Australopithecus. American Journal of Physical Anthropology 64, 297e306. Medin, T., Martínez-Navarro, B., Rivals, F., Libsekal, Y., Rook, L., 2015. The late Early Pleistocene suid remains from the paleoanthropological site of Buia (Eritrea): Systematics, biochronology and eco-geographical context. Palaeogeography, Palaeoclimatology, Palaeoecology 431, 26e42. Meijaard, E., d'Huart, J., Oliver, W., 2011. Family Suidae (pigs). In: Wilson, D.E., Mittermeier, R.A. (Eds.), Handbook of the Mammals of the World. Lynx Edicions, Barcelona, pp. 248e291. Melletti, M., Breuer, T., Huffman, B.A., Turkalo, A.K., Mirabile, M., Maisels, F., 2017. Red river hog Potamochoerus porcus (Linnaeus, 1758). In: Melletti, M., Meijaard, E. (Eds.), Ecology, Conservation and Management of Wild Pigs and Peccaries. Cambridge University Press, Cambridge, pp. 134e149. Mendoza, M., Janis, C.M., Palmqvist, P., 2002. Characterizing complex craniodental patterns related to feeding behaviour in ungulates: a multivariate approach. Journal of Zoology 258, 223e246. Menegaz, R.A., Baier, D.B., Metzger, K.A., Herring, S.W., Brainerd, E.L., 2015. XROMM analysis of tooth occlusion and temporomandibular joint kinematics during feeding in juvenile miniature pigs. Journal of Experimental Biology 218, 2573e2584. Merceron, G., Scott, J., Scott, R.S., Geraads, D., Spassov, N., Ungar, P.S., 2009. Folivory or fruit/seed predation for Mesopithecus, an earliest colobine from the late Miocene of Eurasia? Journal of Human Evolution 57, 732e738. Merceron, G., Escarguel, G., Angibault, J.M., Verheyden-Tixier, H., 2010. Can dental microwear textures record inter-individual dietary variations? PLoS One 5, e9542. Nowak, R.M., 1999. Walker's Mammals of the World. Johns Hopkins University Press, Baltimore. Passey, B.H., Cerling, T.E., 2002. Tooth enamel mineralization in ungulates: Implications for recovering a primary isotopic time-series. Geochimica et Cosmochimica Acta 66, 3225e3234.
rez-Barbería, F.J., Gordon, I.J., 1999. The functional relationship between feeding Pe type and jaw and cranial morphology in ungulates. Oecologia 118, 157e165. Peterson, A., Abella, E.F., Grine, F.E., Teaford, M.F., Ungar, P.S., 2018. Microwear textures of Australopithecus africanus and Paranthropus robustus molars in relation to paleoenvironment and diet. Journal of Human Evolution 119, 42e63. Percher, A.M., Merceron, G., Nsi Akoue, G., Galbany, J., Romero, A., Charpentier, M.J., 2018. Dental microwear textural analysis as an analytical tool to depict individual traits and reconstruct the diet of a primate. American Journal of Physical Anthropology 165, 123e138. Pickford, M., 1993. Old World suoid systematics, phylogeny, biogeography and
26e27, 237e269. biostratigraphy. Paleontologia i Evolucio Pickford, M., Liu, J.H., Pan, Y.R., 2004. Systematics and functional morphology of Molarochoerus yuanmouensis (Suidae, Mammalia) from the Late Miocene of Yunnan, China. Comptes Rendus Palevol 3, 691e704. Plavcan, J.M., Cope, D.A., 2001. Metric variation and species recognition in the fossil record. Evolutionary Anthropology 10, 204e222. Pruetz, J.D., Bertolani, P., 2009. Chimpanzee (Pan troglodytes verus) behavioral responses to stresses associated with living in a savanna-mosaic environment: implications for hominin adaptations to open habitats. PaleoAnthropology 252e262. Quinn, R.L., Lepre, C.J., 2019. Revisiting the pedogenic carbonate isotopes and paleoenvironmental interpretation of Kanapoi. Journal of Human Evolution. https://doi.org/10.1016/j.jhevol.2018.11.005. R Core Team, 2018. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org/. Ragni, A.J., Teaford, M.F., Ungar, P.S., 2017. A molar microwear texture analysis of pitheciid primates. American Journal of Primatology 79, e22697. Ramdarshan, A., Blondel, C., Gautier, D., Surault, J., Merceron, G., 2017. Overcoming sampling issues in dental tribology: Insights from an experimentation on sheep. Palaeontologia Electronica 20, 53A.  _ I., Fortelius, M., 2017. Relative abundances and palaeoecology Rannikko, J., Zliobait e, of four suid genera in the Turkana Basin, Kenya, during late Miocene to Pleistocene. Palaeogeography, Palaeoclimatology, Palaeoecology 487, 187e193. Reda, H.G., Lazagabaster, I.A., Haile-Selassie, Y., 2019. Newly discovered crania of Nyanzachoerus jaegeri (Tetraconodontinae, Suidae, Mammalia) from the Woranso-Mille (Ethiopia) and reappraisal of its generic status. Journal of Mammalian Evolution 26, 177e199. Reed, K.E., 1997. Early hominid evolution and ecological change through the African Plio-Pleistocene. Journal of Human Evolution 32, 289e322. Reed, K.E., 2008. Paleoecological patterns at the Hadar hominin site, Afar Regional State, Ethiopia. Journal of Human Evolution 54, 743e768. Roberts, B.A., 2012. An attack by a warthog Phacochoerus africanus on a newborn Thomson's gazelle Gazella thomsonii. African Journal of Ecology 50, 507e508. Robinson, J.R., Rowan, J., Campisano, C.J., Wynn, J.G., Reed, K.E., 2017. Late Pliocene environmental change during the transition from Australopithecus to Homo. Nature Ecology & Evolution 1, 0159.

99

Rowan, J., Martini, P., Likius, A., Merceron, G., Boisserie, J.-R., 2018. New Pliocene remains of Camelus grattardi (Mammalia, Camelidae) from the Shungura Formation, Lower Omo Valley, Ethiopia, and the evolution of African camels. Historical Biology. https://doi.org/10.1080/08912963.2017.1423485. Seydack, A.H., 2017. Bushpig. In: Melletti, M., Meijaard, E. (Eds.), Ecology, Conservation and Management of Wild Pigs and Peccaries, 2017. Cambridge University Press, Cambridge, pp. 122e133. Schoeninger, M.J., Reeser, H., Hallin, K., 2003. Paleoenvironment of Australopithecus anamensis at Allia Bay, East Turkana, Kenya: evidence from mammalian herbivore enamel stable isotopes. Journal of Anthropological Archaeology 22, 200e207. Schulz, E., Piotrowski, V., Clauss, M., Mau, M., Merceron, G., Kaiser, T.M., 2013. Dietary abrasiveness is associated with variability of microwear and dental surface texture in rabbits. PLoS One 8, e56167. Scott, J.R., 2012. Dental microwear texture analysis of extant African Bovidae. Mammalia 76, 157e174. Scott, R.S., Ungar, P.S., Bergstrom, T.S., Brown, C.A., Childs, B.E., Teaford, M.F., Walker, A., 2006. Dental microwear texture analysis: technical considerations. Journal of Human Evolution 51, 339e349. Scott, R.S., Ungar, P.S., Bergstrom, T.S., Brown, C.A., Grine, F.E., Teaford, M.F., Walker, A., 2005. Dental microwear texture analysis shows within-species diet variability in fossil hominins. Nature 436, 693e695. Scott, J.R., Godfrey, L.R., Jungers, W.L., Scott, R.S., Simons, E.L., Teaford, M.F., Ungar, P.S., Walker, A., 2009. Dental microwear texture analysis of two families of subfossil lemurs from Madagascar. Journal of Human Evolution 56, 405e416. Sealy, J., Johnson, M., Richards, M., Nehlich, O., 2014. Comparison of two methods of extracting bone collagen for stable carbon and nitrogen isotope analysis: comparing whole bone demineralization with gelatinization and ultrafiltration. Journal of Archaeological Science 47, 64e69.
galen, L., Lee-Thorp, J.A., Cerling, T., 2007. Timing of C4 grass expansion across Se sub-Saharan Africa. Journal of Human Evolution 53, 549e559. Seydack, A.H.W., 1990. Ecology of the bushpig Potamochoerus porcus in the Cape Province, South Africa. Ph.D. Dissertation. University of Stellenboch. Shapiro, A.E., Venkataraman, V.V., Nguyen, N., Fashing, P.J., 2016. Dietary ecology of fossil Theropithecus: Inferences from dental microwear textures of extant geladas from ecologically diverse sites. Journal of Human Evolution 99, 1e9. Shearer, B.M., Ungar, P.S., McNulty, K.P., Harcourt-Smith, W.E., Dunsworth, H.M., Teaford, M.F., 2015. Dental microwear profilometry of African noncercopithecoid catarrhines of the Early Miocene. Journal of Human Evolution 78, 33e43. Silcox, M.T., Teaford, M.F., 2002. The diet of worms: An analysis of mole dental microwear. Journal of Mammalogy 83, 804e814. Skinner, J., Breytenbach, G., Maberly, C., 1976. Observations on the ecology and biology of the bushpig Potamochoerus porcus Linn. in the northern Transvaal. South African Journal of Wildlife Research 6, 123e128.
volutive du genre Kolpochoerus (Cetartiodactyla:Suidae) Souron, A., 2012. Histoire e
istoce nen Afrique orientale. Ph.D. Dissertation, University of Poitiers. au Plio-Ple Souron, A., 2017. Diet and ecology of extant and fossil wild pigs. In: Melletti, M., Meijaard, E. (Eds.), Ecology, Conservation and Management of Wild Pigs and Peccaries. Cambridge University Press, Cambridge, pp. 29e38. Souron, A., 2018. Morphology, diet, and stable carbon isotopes: on the diet of Theropithecus and some limits of uniformitarianism in paleoecology. American Journal of Physical Anthropology 166, 261e267. re, N., Colyn, M., HofmanSouron, A., Merceron, G., Blondel, C., Brunetie
ska, E., Boisserie, J.-R., 2015a. Three-dimensional dental microwear Kamin texture analysis and diet in extant Suidae (Mammalia: Cetartiodactyla). Mammalia 79, 279e291. Souron, A., Boisserie, J.-R., White, T.D., 2015b. A new species of the suid genus Kolpochoerus from Ethiopia. Acta Palaeontologica Polonica 60, 79e96. Sponheimer, M., Dufour, D.L., 2009. Increased dietary breadth in early hominin evolution: revisiting arguments and evidence with a focus on biogeochemical contributions. In: Hublin, J.J., Richard, M.P. (Eds.), Evolution of Hominin Diets. Springer, Dordrecht, pp. 229e240. Sponheimer, M., Alemseged, Z., Cerling, T.E., Grine, F.E., Kimbel, W.H., Leakey, M.G., Lee-Thorp, J.A., Manthi, F.K., Reed, K.E., Wood, B.A., 2013. Isotopic evidence of early hominin diets. Proceedings of the National Academy of Sciences USA 110, 10513e10518. Stewart, K.M., Rufolo, S.J., 2018. Kanapoi revisited: Paleoecological and biogeographical inferences from the fossil fish. Journal of Human Evolution. https:// doi.org/10.1016/j.jhevol.2018.01.008. Strait, S.G., 1993. Molar microwear in extant small-bodied faunivorous mammals: An analysis of feature density and pit frequency. American Journal of Physical Anthropology 92, 63e79. Stynder, D.D., DeSantis, L.R., Donohue, S.L., Schubert, B.W., Ungar, P.S., 2018. A dental microwear texture analysis of the Early Pliocene African ursid Agriotherium africanum (Mammalia, Carnivora, Ursidae). Journal of Mammalian Evolution. https://doi.org/10.1007/s10914-018-9436-y. Taieb, M., Johanson, D.C., Coppens, Y., Aronson, J.L., 1976. Geological and paleontological background of Hadar hominid site, Afar, Ethiopia. Nature 260, 289e293. lu, S., Stach, S., Mahajan, A., Pathak, D., Wagner, T., Kumar, A., Bedi, R.K., 2013. T¸a Multifractal analysis of drop-casted copper (II) tetrasulfophthalocyanine film surfaces on the indium tin oxide substrates. Surface and Interface Analysis 46, 393e398. Teaford, M.F., 1985. Molar microwear and diet in the genus Cebus. American Journal of Physical Anthropology 66, 363e370.

100

I.A. Lazagabaster / Journal of Human Evolution 132 (2019) 80e100

Teaford, M.F., 1988. A review of dental microwear and diet in modern mammals. Scanning Microscopy 2, 1149e1166. Teaford, M.F., Oyen, O.J., 1989. In vivo and in vitro turnover in dental microwear. American Journal of Physical Anthropology 80, 447e460. Teaford, M.F., Walker, A., 1984. Quantitative differences in dental microwear between primate species with different diets and a comment on the presumed diet of Sivapithecus. American Journal of Physical Anthropology 64, 191e200. Teaford, M.F., Ungar, P.S., 2000. Diet and the evolution of the earliest human ancestors. Proceedings of the National Academy of Sciences USA 97, 13506e13511. Teklehaimanot, G., Balakrishnan, M., 2017. Population status, feeding ecology and habitat association of the common warthog (Phacochoerus africanus) in Bale Mountains National Park, Ethiopia. International Journal of Ecology and Environmental Sciences 43, 185e194. Ungar, P., 2004. Dental topography and diets of Australopithecus afarensis and early Homo. Journal of Human Evolution 46, 605e622. Ungar, P.S., Sponheimer, M., 2011. The diets of early hominins. Science 334, 190e193. Ungar, P., Merceron, G., Scott, R., 2007. Dental microwear texture analysis of Varswater bovids and early Pliocene paleoenvironments of Langebaanweg, Western Cape Province, South Africa. Journal of Mammalian Evolution 14, 163e181. Ungar, P.S., Grine, F.E., Teaford, M.F., 2008. Dental microwear and diet of the PlioPleistocene hominin Paranthropus boisei. PLoS One 3, e2044. Ungar, P.S., Scott, R.S., Grine, F.E., Teaford, M.F., 2010. Molar microwear textures and the diets of Australopithecus anamensis and Australopithecus afarensis. Philosophical Transactions of the Royal Society B 365, 3345e3354. Ungar, P.S., Krueger, K.L., Blumenschine, R.J., Njau, J., Scott, R.S., 2012. Dental microwear texture analysis of hominins recovered by the Olduvai Landscape Paleoanthropology Project, 1995e2007. Journal of Human Evolution 63, 429e437. Ungar, P.S., Abella, E.F., Burgman, J.H.E., Lazagabaster, I.A., Scott, J.R., Delezene, L.K., Manthi, F.K., Plavcan, J.M., Ward, C.V., 2017. Dental microwear and Pliocene paleocommunity ecology of bovids, primates, rodents, and suids at Kanapoi. Journal of Human Evolution. https://doi.org/10.1016/j.jhevol.2017.03.005. van der Made, J., 1999. Biometrical trends in the Tetraconodontinae, a subfamily of pigs. Transactions of the Royal Society of Edinburgh: Earth Sciences 89, 199e225. van der Made, J., 2013. Microstonyx (Suidae, Artiodactyla) from the Upper Miocene of Hayranlı-Haliminanı, Turkey. Turkish Journal of Zoology 37, 106e122. Vanpoucke, S., Mainland, I., De Cupere, B., Waelkens, M., 2009. Dental microwear study of pigs from the classical site of Sagalassos (SW Turkey) as an aid for the reconstruction of husbandry practices in ancient times. Environmental Archaeology 14, 137e154. Venables, W.N., Ripley, B.D., 2002. Modern Applied Statistics with S, 4th ed. Springer, New York. €kologie des Afrikanischen RieViehl, K., 2003. Untersuchungen zur Nahrungso senwaldschweins (Hylochoerus meinertzhageni Thomas) im Queen Elizabeth National Park, Uganda. Ph.D. Dissertation, University of Hannover. Ward, C., Kimbel, W., 2012. New postcranial fossils of Australopithecus afarensis from Hadar, Ethiopia (1990e2007). Journal of Human Evolution 63, 1e51. Ward, C., Leakey, M., Walker, A., 1999. The new hominid species Australopithecus anamensis. Evolutionary Anthropology 7, 197e205.

Ward, C., Leakey, M., Walker, A., 2001. Morphology of Australopithecus anamensis from Kanapoi and Allia Bay, Kenya. Journal of Human Evolution 41, 255e368. Ward, C., Plavcan, J.M., Manthi, F.K., 2010. Anterior dental evolution in the Australopithecus anamensiseafarensis lineage. Philosophical Transactions of the Royal Society B 365, 3333e3334. Ward, C., Manthi, F., Plavcan, J., 2013. New fossils of Australopithecus anamensis from Kanapoi, West Turkana, Kenya (2003e2008). Journal of Human Evolution 65, 501e524. Ward, C.V., 2014. Taxonomic affinity of the Pliocene hominin fossils from Fejej, Ethiopia. Journal of Human Evolution 73, 98e102. Ward, J., Mainland, I.L., 1999. Microwear in modern rooting and stall-fed pigs: the potential of dental microwear analysis for exploring pig diet and management in the past. Environmental Archaeology 4, 25e32. White, T.D., 1995. African omnivores: global climatic change and Plio-Pleistocene hominids and suids. In: Vrba, E.S., Denton, G., Partridge, T., Burckle, L. (Eds.), Paleoclimate and Evolution, with Emphasis on Human Origins. Yale University Press, New Haven, pp. 369e384. White, T.D., Harris, J.M., 1977. Suid evolution and correlation of African hominid localities. Science 198, 13e21. White, T.D., Hart, W.K., Walter, R.C., WoldeGabriel, G., de Heinzelin, J., Clark, J.D., Asfaw, B., Vrba, E., 1993. New discoveries of Australopithecus at Maka in Ethiopia. Nature 366, 261e265. White, T.D., Suwa, G., Simpson, S., Asfaw, B., 2000. Jaws and teeth of Australopithecus afarensis from Maka, Middle Awash, Ethiopia. American Journal of Physical Anthropology 111, 45e68. White, T.D., WoldeGabriel, G., Asfaw, B., Ambrose, S.H., Beyene, Y., Bernor, R.L., Boisserie, J.-R., Currie, B., Gilbert, H., Haile-Selassie, Y., Hart, W.K., Hlusko, L.J., Howell, F.C., Kono, R.T., Lehmann, T., Louchart, A., Lovejoy, C.O., Renne, P.R., Saegusa, H., Vrba, E.S., Wesselman, H., Suwa, G., 2006. Asa Issie, Aramis and the origin of Australopithecus. Nature 440, 883e889. White, T.D., Ambrose, S.H., Suwa, G., Su, D.F., DeGusta, D., Bernor, R.L., Boisserie, J.R., Brunet, M., Delson, E., Frost, S., Garcia, N., 2009. Macrovertebrate paleontology and the Pliocene habitat of Ardipithecus ramidus. Science 326, 67e93. Wilson, J.N., 2013. Stable isotopes and trace elements in tooth enamel bioapatite: Effects of diagenesis and pretreatment on primary paleoecological information. M.S. Dissertation, University of South Florida. Wood, B., Richmond, B.G., 2000. Human evolution: Taxonomy and paleobiology. The Journal of Anatomy 197, 19e60. Wynn, J., 2000. Paleosols, stable carbon isotopes, and paleoenvironmental interpretation of Kanapoi, Northern Kenya. Journal of Human Evolution 39, 411e432. Wynn, J.G., Sponheimer, M., Kimbel, W.H., Alemseged, Z., Reed, K.E., Bedaso, Z.K., Wilson, J.N., 2013. Diet of Australopithecus afarensis from the Pliocene Hadar formation, Ethiopia. Proceedings of the National Academy of Sciences USA 110, 10495e10500. Wynn, J.G., Reed, K.E., Sponheimer, M., Kimbel, W.H., Alemseged, Z., Bedaso, Z.K., Campisano, C.J., 2016. Dietary flexibility of Australopithecus afarensis in the face of paleoecological change during the middle Pliocene: Faunal evidence from Hadar, Ethiopia. Journal of Human Evolution 99, 93e106. Yamada, E., Kubo, M.O., Kubo, T., Kohno, N., 2018. Three-dimensional tooth surface texture analysis on stall-fed and wild boars (Sus scrofa). PLoS One 13, e0204719.