Dietary Reconstruction of Pygmy Mammoths from Santa Rosa Island of California

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Quaternary International xxx (2015) 1e14

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Dietary reconstruction of pygmy mammoths from Santa Rosa Island of California

* Gina M. Semprebon a, , Florent Rivals b, c, d, Julia M. Fahlke e, William J. Sanders f, Adrian M. Lister g, Ursula B. Gohlich€ h a Bay Path University, Longmeadow, MA, USA b Institucio Catalana de Recerca i Estudis Avançats (ICREA), Barcelona, Spain c Institut Catala de Paleoecologia Humana i Evolucio Social (IPHES), Tarragona, Spain d Area de Prehistoria, Universitat Rovira i Virgili (URV), Tarragona, Spain e Museum für Naturkunde, Leibniz-Institut für Evolutions- und Biodiversitatsforschung,€ Berlin, Germany f Museum of Paleontology and Department of Anthropology, University of Michigan, MI, USA g Natural History Museum, London, UK h Natural History Museum of Vienna, Vienna, Austria article info abstract

Article history: Microwear analyses have proven to be reliable for elucidating dietary differences in taxa with similar Available online xxx gross tooth morphologies. We analyzed enamel microwear of a large sample of Channel Island pygmy mammoth (Mammuthus exilis) molars from Santa Rosa Island, California and compared our results to Keywords: those of extant proboscideans, extant ungulates, and mainland fossil mammoths and mastodons from Island Rule North America and Europe. Our results show a distinct narrowing in mammoth dietary niche space after Niche occupation mainland mammoths colonized Santa Rosa as M. exilis became more specialized on browsing on leaves Proboscidea and twigs than the Columbian mammoth and modern elephant pattern of switching more between Tooth microwear Paleodiet browse and grass. Scratch numbers and scratch width scores support this interpretation as does the Pleistocene vegetation history of Santa Rosa Island whereby extensive conifer forests were available during the last glacial when M. exilis ﬂourished. The ecological disturbances and alteration of this vegetation (i.e., diminishing conifer forests) as the climate warmed suggests that climatic factors may have been a contributing factor to the extinction of M. exilis on Santa Rosa Island in the Late Pleistocene. © 2015 Elsevier Ltd and INQUA. All rights reserved.

1. Introduction super-island, dubbed Santarosae by Orr (1968) and lay closer to the mainland than today's Channel Islands. Even during periods of 1.1. Background glaciation in the Pleistocene when sea levels were much lower than they are today, the islands were separated from the California coast Endemic to the California Channel Islands, the pygmy mammoth by a relatively small water gap of around 6.5e8km(Roth, 1996; (Mammuthus exilis, Maglio, 1970) was initially discovered on the Muhs et al., 2015). As sea levels rose due to the melting of conti- Island of Santa Rosa and later on Santa Cruz and San Miguel in the nental ice, 76% of Santarosae disappeared (Johnson, 1972) leaving Channel Island archipelago of California. M. exilis is a small only the highest elevations exposed e now known as the islands of mammoth considered to be a dwarfed form of its likely ancestor, San Miguel, Santa Cruz, Santa Rosa, and Anacapa. Of these modern the Columbian mammoth (M. columbi), which occupied the main- islands, all but Anacapa have produced mammoth remains land of North America (Madden, 1977, 1981; Johnson, 1978). Today, (Agenbroad, 2001). The breakup of Santarosae is believed to have the Channel Islands are comprised of eight islands (Fig. 1). In the taken place about 11,000 cal. BP (Kennett et al., 2008). Late Pleistocene, the four Northern Channel Islands formed a single Researchers have long been interested in the Channel Islands for several reasons. First, the islands are part of one of the richest marine ecosystems in the world and are home to over 150 endemic species such as the island fox (Urocyon litteralis) e a small fox with * Corresponding author. E-mail addresses: [email protected], [email protected] six subspecies each unique to the island it lives on. Hence, the (G.M. Semprebon). Channel Islands are often referred to as the North American http://dx.doi.org/10.1016/j.quaint.2015.10.120 1040-6182/© 2015 Elsevier Ltd and INQUA. All rights reserved.

Fig. 1. The Channel lslands and Southern California Coast (Modiﬁed from Rick et al. (2012) (Fig. 1)). Dotted line indicates Late Pleistocene shoreline of the “super island” of Santarosae.

Galapagos. Second, because island species are generally regarded as There has been much speculation regarding the origin of more susceptible to human-induced extinctions than those on mammoths on the Northern Channel Islands, and the finding of continents, and the Channel Islands were initially occupied by Columbian mammoth remains is intriguing given that these re- humans during a period of extensive extinction in North America mains may represent remnants of an ancestral population, unless (and elsewhere) around 13,000 cal. BP (Erlandson et al., 2011), data they represent later migrants to the island. The oldest remains are from such islands has proven useful for providing context for late found in the basal conglomerate of the Garanon Member of the Quaternary extinctions on continents such as the Americas and Santa Rosa Island Formation. U/Th results formerly suggested an Australia (Steadman and Martin, 2003; Wroe et al., 2006). Third, age of at least 200 ka (Orr, 1968), but these are not now considered islands are invaluable for studying evolution and diversification, reliable and new U/Th data indicate an age of ca. 80 ka (Muhs et al., including the effects of insularity on fauna (Palombo, 2008) such as 2015). Mammoth remains attributed to both M. columbi and M. the so-called “Island Rule”. The Island Rule was first stated by Foster exilis have been found throughout the entire Formation (the latest (1964) after comparing numerous island species to their mainland calibrated direct radiocarbon date on M. exilis being 10,700 ± 90 BP varieties. He proposed that the body size of a species becomes (B-14660), equivalent to c. 12,600 cal BP (Agenbroad, 2012). smaller or larger depending on the resources available to it in its Also intriguing is the speculation as to how mainland mam- environment. The Island Rule posits that certain island species moths arrived on the islands. Initially, it was assumed that the evolve larger size when predation pressure is relaxed (due to the ancestral form of M. exilis was either Mammuthus (formerly Archi- absence of some mainland predators), while others evolve smaller diskodon) imperator or Mammuthus columbi. It has now been shown size due to resource constraints regarding availability of food and that M. imperator and M. columbi are conspecific(Slaughter et al., land area (Whittaker, 1998; McNab, 2010). 1962; Miller, 1971, 1976; Agenbroad, 2003) and further research The history of the discovery and excavation of pygmy mam- has suggested that M. columbi represents the likely ancestor of M. moths from the islands is chronicled in Agenbroad (2001). exilis (Johnson, 1978; Madden, 1981; Roth, 1982, 1996). This sug- Mammoth remains have been known from the Northern Channel gests that M. exilis evolved according to the Island Rule (Foster, Islands of Santa Rosa, San Miguel, and Santa Cruz since 1856 1964). That is, a large continental species (M. columbi) adapted to (Stearns,1873). A spectacular find was made in 1994 by Park Service an island environment becoming in time a new smaller species e researchers led by Larry Agenbroad (a Santa Barbara Museum M. exilis (Fig. 2). research associate at the time) of a nearly complete adult male M. The question remains e how did Columbian mammoths reach exilis skeleton e a mature male of about 50 years of age (Agenbroad, the islands? Historically, it was assumed that ancestral mammoths 1998). After this discovery, a thorough pedestrian survey of the could not have swum to the islands. Consequently, various land islands using GPS was begun, to document and pinpoint each dis- bridges linking the Northern Channel Islands to the mainland have covery. More than 160 new localities were recorded with the ma- long been hypothesized (e.g., Clements, 1955; Van Gelder, 1965; jority of localities found on Santa Rosa Island (Agenbroad et al., Valentine and Lipps, 1967; von Bloeker, 1967; Remington, 1971). 2007). Several mainland-size mammoth (Mammuthus columbi) el- This early idea, that insular mammoth remains proved the exis- ements in addition to remains of M. exilis were recovered as a result tence of a land bridge, persisted for many decades (see synopsis by of this survey. The survey of Santa Rosa revealed a ratio of Johnson, 1978). The idea was deeply entrenched but began to give approximately 3:10 large mammoth:small mammoth remains way in light of accumulating geological and biological evidence (Agenbroad, 2012). (Savage, 1967; Johnson, 1978). For example, Johnson (1972, 1978) As many as three species ostensibly of different sizes have been pointed out that a land bridge was not a sine qua non for explain- proposed by researchers over the years (Orr, 1956a,b, 1968; Roth, ing mammoths on the Northern Channel Islands, citing research 1982, 1996). However, Agenbroad (2009) showed convincingly, that elephants are excellent distance swimmers, among the best of using less fragmentary material, that only two species are likely all land mammals and highly skilled at crossing water gaps. Hence, present e M. columbi and M. exilis (Fig. 2). currently it is now understood that sea-level fall brought the

Fig. 2. Comparative sizes of the mainland mammoth (Mammuthus columbi) and the pygmy mammoth of the Channel Islands (Mammuthus exilis). Modified from Agenbroad (2012) (Fig. 2). Estimated height data from Agenbroad (2009). islands only a few kilometers from the shore, enabling mainland proboscideans and other mammals known to ingest large quanti- mammoths an opportunity to gain access even if a land bridge was ties of twigs and bark. not present. Today the local vegetation of the Northern Channel Islands is 1.3. Microwear dominated by grasslands and shrublands with some patchy woodlands, and mild temperatures with little annual temperature Microwear has been employed for over three decades as a fluctuation (Junak et al., 2007). To date, studies of the vegetation technique to visualize scars in dental enamel caused by food items history of the island have included pollen analyses on Santa Rosa such as plant phytoliths or by exogenous grit or dust coating the Island (Cole and Liu 1994; Kennett et al., 2008), San Miguel Island surface of vegetation (e.g., Rensberger, 1978; Walker et al., 1978; (West and Erlandson, 1994), continuous offshore pollen cores from Solounias and Semprebon, 2002; Semprebon et al., 2004; the Santa Rosa Basin (Heusser, 1995, 2000) and paleobotanical Merceron et al., 2004, 2005; Scott et al., 2005, 2006; Ungar et al., studies on Santa Cruz Island (Cheney and Mason, 1930). During the 2008, 2010) including studies of mammoths and other pro- Late Pleistocene, when these islands existed as the single super- boscideans (Rivals et al., 2012, 2015). Microwear turns over rela- island of Santarosae, forest vegetation was present including cy- tively rapidly, thus giving insight into the dietary behavior of the press, pine, and Douglas fir(Cheney and Mason, 1930; Anderson last days, or weeks, before an animal's death e the so-called “Last et al., 2008). Climatic changes at the end of the Pleistocene have Supper Effect” (Grine, 1986). As such, it provides a window into the been invoked as the cause for the loss of coastal forest (Anderson short-term dietary behavior of a taxon as opposed to the deep-time et al., 2008), and major fires coincident with the last known adaptation of gross tooth morphology, giving insight into what a occurrence of pygmy mammoths (around 13,000 cal BP) have been taxon was actually eating despite what it might originally have demonstrated (Kennett et al., 2008). Anderson et al. (2010) com- been adapted to eat (Rivals and Semprebon, 2011). Importantly, this bined pollen analysis with an analysis of the fire disturbance snapshot into the habitat and dietary behavior of a taxon is largely regime of Santa Rosa Island and reported that a coastal conifer taxon-independent. forest covered the highlands of Santa Rosa during the last glacial While microwear analyses have proven to be very reliable in but that by ca. 11,800 cal. BP Pinus stands, coastal sage scrub and diagnosing dietary behavior of mammals, two considerations are grassland replaced the forest as the climate warmed. relevant to all microwear approaches: 1) potential error involved in the analyses, and 2) the causal factors producing microwear scars. 1.2. Aims of the study Different microwear methodologies have different strengths and weaknesses, but all have value depending on questions being The purpose of this study is twofold: 1) to explore the paleo- studied. The three methods currently used involve scanning elec- dietary ecology of Mammuthus exilis from Santa Rosa Island, Cali- tron microscopy (SEM), light microscopy for dental microwear fornia using stereomicrowear analysis, and 2) to compare (LDM), and dental microwear texture analysis (DMTA). Because microwear patterns of M. exilis to those of extant elephants and to SEM and LDM rely on observer measurements, while DMTA em- other mammoths and mastodons from North America and Europe, ploys an automated approach, studies have been done to identify especially its ancestor M. columbi. To test the hypothesis that M. and/or quantify both inter- and intra-observer error involved in exilis was exploiting the forest vegetation during the Late Pleisto- each (e.g., Grine et al., 2002; Galbany et al., 2005; Fraser et al., 2009; cene, we employed light microscopy dental microwear on a large Mihlbachler et al., 2012 DeSantis et al., 2013; Williams and Geissler, sample of pygmy mammoth teeth from Santa Rosa Island. If forest 2014; Hoffman et al., 2015). vegetation including woody browse was exploited on Santa Rosa While these studies have provided valuable insight regarding Island during the Late Pleistocene, we predict that: 1. M. exilis elucidating potential error in microwear studies, it is important to would exhibit more scratches in the low scratch range (i.e., be- not generalize results utilizing one methodology to another. Thus, tween 0 and 17) typical of extant mammals that feed on leaves; 2. microwear error studies aimed at testing LDM (other than Some individuals of M. exilis would display the unusually deep and Semprebon et al., 2004), while adding to the cannon of knowledge, wide scratches (i.e., hypercoarse scratches) found in extant have not duplicated the original LDM methodological regime (i.e.,

Please cite this article in press as: Semprebon, G.M., et al., Dietary reconstruction of pygmy mammoths from Santa Rosa Island of California, Quaternary International (2015), http://dx.doi.org/10.1016/j.quaint.2015.10.120 4 G.M. Semprebon et al. / Quaternary International xxx (2015) 1e14 have employed different magnifications, used different counting primates, marsupials, ungulates, and rodents) into their known areas, have not counted all features visible, and/or assessed micro- trophic groups (Semprebon et al., 2004; Merceron et al., 2004, wear from photographs e sometimes using untrained observers). 2005; Rivals et al., 2007, 2012; Townsend and Croft, 2008; Fraser The original methodology developed by Semprebon, 2002 and et al., 2009; Williams and Patterson, 2010; Fraser and Theodor, Solounias and Semprebon, 2002 (and utilized in this study) in- 2011, 2013; Williams and Holmes, 2011; Bastl et al., 2012; Fahlke volves counting pits and scratches directly using a stereoscope at 35 et al., 2013; Christensen, 2014; Williams and Geissler, 2014). times magnification following the same standard microscope cali- The causal factors involved in producing microwear scars are bration and systematic counting methods employed every day in only beginning to be understood. Microwear patterns must be diagnostic medicine and life science research to accurately count influenced by the differing physical properties of enamel and substances such as blood cells and platelets using light microscopy ingested abrasives such as biogenic silica (i.e., phytoliths) from (where differential light refraction as used in this study is used to plants, or abiotic silica from dust or grit. While it is also possible identify the objects being counted). that differing tooth morphologies and masticatory biomechanics For example, the procedure used to construct the comparative may impact the nature of microwear scars, a similar pattern of extant ungulate and proboscidean databases (Semprebon, 2002; microwear scars have been observed across various orders of Rivals et al., 2012) and to analyze the fossil proboscideans used in mammals consuming similar dietary items which seems to argue this study relies on employing a calibrated ocular reticle subdivided that such effects are relatively minor (e.g., Semprebon et al., 2004) into 9 subsquares which greatly enhances the ability to not lose although further study is needed. A number of studies have tested track of features counted rather than attempting to count numerous the effects of abrasives in producing microwear scars and have features scattered within a larger, undivided field of view. Addi- expanded our thinking away from considering phytoliths alone as tionally, features are counted according to a strict protocol that contributing to microwear scar topography (Covert and Kay, 1981; ensures that features present are not skipped over or counted more Kay and Covert, 1983; Maas, 1991, 1994; Gügel et al., 2001; than once (Estridge and Reynolds, 2012). Also, a relatively large Mainland, 2003; Sanson et al., 2007; Lucas et al., 2013; Schulz counting area is employed and features are counted twice (to et al., 2013; Müller et al., 2014; Hoffman et al., 2015). Studies reduce error due to potential variable scar distribution). When this examining the relative hardness of enamel versus phytoliths have, protocol is followed, both interobserver and intraobserver error has however, produced contradictory results (Baker et al., 1959; Sanson been demonstrated to be low (Semprebon et al., 2004). et al., 2007; Rabenold and Pearson, 2014; Xia et al., 2015). The most In some studies, however, feature counts have been made from promising studies regarding teasing apart causal factors involve images using much higher magnifications than used in Semprebon controlled feeding experiments. These studies have elucidated et al. (2004) and counting error would naturally be expected to be patterns in such widely diverse taxa as American opossums (Covert higher due to the greater number of features visible at higher and Kay, 1981; Kay and Covert, 1983), rabbits (Schulz et al., 2013), magnifications. For example, Mihlbachler et al. (2012) reported that and ungulates (Hoffman et al., 2015). Such studies have docu- interobserver error was higher than that reported by Semprebon mented an increase in scratch numbers in rabbits when their diet et al., 2004, although evidence was found (2012) that error dimin- contained grass with more biogenic abrasives (Schulz et al., 2013) ished significantly with increased experience of the observer and and in opossums that were fed fine-grained pumice (Covert and data collected by all observers was highly correlated (Mihlbachler Kay, 1981; Kay and Covert, 1983). Hoffman et al. (2015) provided et al., 2012). Also, while DMTA has been employed to extract 2D the controlled feeding experiment with domesticated sheep, and microwear data from photosimulations of scanned areas of DMTA, tested the effects of abiotic abrasives of different sizes. This study (e,g., DeSantis et al., 2013), stereomicroscopy was invented to pro- reported a significant increase in pit features that was correlated vide depth of field and a three dimensional visualization of an object with an increase in grain size. This observed grit effect supports the being examined and thus is widely used in microsurgery, dissection, interpretation of increased grit consumption by extant ungulates forensics, medicine, industry, and quality control. In microwear from semi-arid and arid environments due to increased pitting analysis as employed here and in Solounias and Semprebon (2002) observed in these forms (Solounias and Semprebon, 2002). and Semprebon et al. (2004), stereomicroscopy allows relative LDM (after Semprebon, 2002; Solounias and Semprebon, 2002) depth and 3D shape of different features to be assessed. was used in this study as it allows for the attainment of relatively While fully automated methodologies such as DMTA have been large sample sizes (numbers of specimens), and a very large developed and have proven useful to reduce subjectivity and comparative stereomicrowear database exists which is comprised interobserver error (Ungar et al., 2003; Galbany et al., 2005)itis of extant artiodactyls, perissodactyls, and proboscideans of known important to note, that DMTA reduces interobserver error only diets compiled by a single observer (GMS). Relatively few studies when the same exact location on the same tooth surface is scanned have concerned themselves with proboscidean microwear patterns twice, as results obtained on the same tooth and same facet may be (examples are Palombo and Curiel (2003), Palombo (2005), Green quite different when different regions of that tooth and facet are et al. (2005), Todd et al. (2007) and Calandra et al. (2008, 2010)). scanned (see Fig. 8 in Scott et al., 2006). This difference is due to the Rivals et al. (2012, 2015) studied dietary diversity patterns in natural heterogeneity of microwear on tooth surfaces, a propensity Pleistocene representatives of Mammut, Anancus, Palaeoloxodon which affects all microwear methodologies but is more problematic and Mammuthus from a variety of localities in Europe and North at higher versus lower magnifications and when only small areas of America. In this study, we test the effect of insular dwarfism on a tooth are analyzed. If relatively low magnification and a large dietary niche occupation by comparing Pleistocene mammoths counting area is assessed such as in the Solounias and Semprebon from the North American mainland with island mammoths from (2002) methodology, both inter- and intra-observer error may be the Channel Islands off the coast of California. minimized (see Williams and Geissler, 2014). Regardless, the effects of potential error should be evaluated 2. Materials and methods within the context of whether accurate dietary categorization of living mammals with known diets can be obtained by single ob- 2.1. Sample servers. A variety of different variations on the original LDM methodology have produced great fidelity in terms of partitioning Molar teeth of Mammuthus exilis from the Channel Islands of living mammals (e.g., carnivores, cetaceans, proboscideans, California were sampled from the collections of the Santa

intensity fiber-optic light source (Dolan-Jenner) was directed across the surface of casts at a shallow angle to the occlusal surface. The mean number of pits (rounded features) versus mean number of scratches (elongated features) per taxon were counted within a 0.4 mm square area (0.16 mm2) by GMS. It was also noted if more than four large pits (i.e., deep pits with low refractivity that are at least twice the diameter of highly refractive small pits) were present or absent per microscope field (within the 0.4 mm square area) and whether gouges (i.e., depressions with ragged, irregular edges that are 2e3 times larger than large pits) were present or absent (after Semprebon, 2002; Solounias and Semprebon, 2002). Results were compared with extant ungulate and proboscidean microwear databases to determine the dietary categories of browser versus grazer (Semprebon, 2002; Solounias and Semprebon, 2002). Scratch textures were assessed as being either fine, coarse, hypercoarse, a mixture of fine and coarse, or a mixture of coarse and hypercoarse scratch types per tooth surface using the differential light refractivity of each type of scratch to categorize them (after Semprebon et al., 2004). In addition, a scratch width score (SWS) was obtained by assigning a score of 0 to teeth with Fig. 3. Mandible of Mammuthus exilis from Santa Rosa Island, California (Specimen predominantly fine scratches per tooth surface, 1 to those with a from Santa Barbara Museum of Natural History e catalogue number SBMNH-VP 1078). mixture of fine and coarse types of textures, 2 to those with pre- Arrow depicts area sampled for microwear analysis (i.e., the central portion of the dominantly coarse scratches, 3 to those with a mixture of coarse central enamel bands of the grinding facet of the occlusal surface). Scale bar ¼ 5 cm. and hypercoarse textures, and 4 to those with predominantly hypercoarse scratches. Univariate statistics, ANOVA, and Tukey's fi Barbara Museum of Natural History, California. The specimens post-hoc test for honest signi cant differences were calculated were screened under a stereomicroscope for potential tapho- using PAST software (Hammer et al., 2001). nomic alteration of dental surfaces. Those with badly preserved Because extant seasonal mixed feeders and those that alternate enamel or taphonomic defects (i.e., features displaying unusual their diet when migrating to different regions alternately feed on morphologies or fresh features made during the collecting pro- browse and grass may overlap the browsing or grazing mean cess or during storage) were removed from the analysis scratch/pit morphospaces, the percentage of individuals within a following King et al. (1999). We also excluded slightly or heavily taxon that possess raw scratch values falling into the low scratch worn teeth. range (i.e., between 0 and 17) were calculated, since extant leaf Fifty-one M. exilis adult molar casts from Santa Barbara Island, browsers, grazers, and mixed feeders show distinctive and two from San Miguel Island, and one from Santa Cruz Island, as well discriminating low scratch range patterns (Semprebon, 2002; as one tooth of M. columbi from Santa Rosa Island, were determined Semprebon and Rivals, 2007). to be suitable for analysis and subjected to microwear analysis by a single observer (GMS) who also analyzed the extant ungulate and 3. Results proboscidean comparative samples. 3.1. Comparative extant proboscidean microwear

2.2. Microwear technique Results of the microwear analysis are shown in Table 1. It is clear from Fig. 4A that extant Loxodonta africana and Elephas maximus Tooth surfaces were cleaned, molded, cast and examined at 35 exhibit a varied dietary behavior e taking both grass and browse, times magniﬁcation with a Zeiss Stemi-2000C stereomicroscope whereas the forest elephant, Loxodonta cyclotis, exhibits less vari- after the methodology of Solounias and Semprebon (2002). The ability and is more focused on the browse end of the spectrum analysis was made from the central portion of the central enamel (note, however, that fewer specimens were available for L. cyclotis bands of the occlusal surface (Fig. 3). Microscopic scars were than for the others). This corroborates what is known from ﬁeld visualized using external oblique illumination. An M1-150 high- studies (Sukumar, 2003).

Table 1 Microwear summary data for the second molars of extant and fossil proboscidean samples.

Species N Pit mean Pit SD Scratch mean Scratch SD SWS % LP % G %F % C % M % CH % H % 0e17 S Diet

Loxodonta africana 33 22.9 3.9 17.4 5.3 3.1 54.6 36.4 0.0 0.0 0.0 87.9 12.1 39.4 MF Loxodonta cyclotis 6 29.8 4.0 12.9 5.1 2.8 50.0 33.3 0.0 0.0 16.7 66.7 16.7 83.3 B Elephas maximus 10 20.9 2.6 18.3 4.3 3.1 70.0 50.0 0.0 0.0 0.0 90.0 10.0 40.0 MF Mammuthus exilis e Santa Rosa Island 51 26.9 5.99 10.78 4.59 2.0 37.3 13.7 7.84 11.77 33.33 47.06 0.0 94.1 B Mammuthus exilis e San Miguel Island 2 24.0 e 7.8 e 4.0 50.0 0.0 0.0 0.0 0.0 0.0 100 100 B Mammuthus exilis e Santa Cruz Island 1 22.0 e 8.5 e 1.0 0.0 0.0 0.0 0.0 100 0.0 0.0 100 B Mammuthus columbi e Santa Rosa Island 1 31.5 e 19.5 e 2 100 0 0 100 0 0 0 0 G

Abbreviations: N ¼ Number of specimens; Pit Mean ¼ Mean number of pits; Pit SD ¼ standard deviation of Pits; Scratch ¼ Mean number of scratches; Scratch SD ¼ standard deviation of scratches; SWS ¼ Mean Scratch width score from 0 to 4 (0 ¼ fine scratches only, to 4 ¼ hypercoarse scratches only; %LP ¼ Percentage of individuals per taxon with large pits; %G ¼ Percentage of individuals per taxon with gouges; %F ¼ Percentage of individuals per taxon with fine scratches; %C ¼ Percentage of individuals per taxon with coarse scratches; %M ¼ Percentage of individuals per taxon with a mixture of fine and coarse scratches; %CH ¼ Percentage of individuals per taxon with a mixture of coarse and hypercoarse scratches; %H ¼ Percentage of individuals per taxon with hypercoarse scratches; %0-17S ¼ low scratch percentage (i.e., Percentage of individuals per taxon with scratch counts between 0 and 17; B ¼ leaf browser; MF ¼ mixed feeder; G ¼ grazer. All extant and extinct specimens were scored by GMS.

3.2. Pygmy mammoth molar microwear compared with extant An ANOVA (Table 2) indicates that M. exilis scratch numbers are proboscideans significantly different (i.e., lower) from those of L. africana (Tukey's ¼ The raw scratch distribution of M. exilis is skewed more toward HSD Test, p 0.0047) and E. maximus (Tukey's HSD Test, p ¼ 0.0011) but are not significantly different from scratch numbers the low scratch browsing range, much like that of Loxodonta cyclotis ¼ (Fig. 4B), indicating a less heterogeneous dietary regime than that of L. cyclotis (Tukey's HSD Test, p 0.6844). Also, M. exilis pit numbers are significantly different (i.e., higher) from those of E. found in L. africana or E. maximus. Two teeth of M. exilis from San ¼ fi Miguel Island and one from Santa Cruz Island were available and maximus (Tukey's HSD Test, p 0.0189) but not signi cantly different from those of L. africana (Tukey's HSD Test, p ¼ 0.193) or these specimens also plot within the extant ungulate browsing ¼ ecospace. L. cyclotis (Tukey's HSD Test, p 0.4508).

Table 2 ANOVA and Tukey's HSD test results for differences in numbers of pits, numbers scratches, and scratch width score. Signiﬁcant differences are indicated in bold.

Number of scratches

ANOVA results e Test for Equal Means: Sum of Squares df Mean square F p Between groups: 1107.22 3 369.075 15.68 <0.001 Within groups: 2259.03 96 23.5315 Total: 3366.25 99 Tukey's honest signiﬁcance test: Pair-wise comparisons e q values below the diagonal, p values above the diagonal. L. cyclotis L. africana E. maximus M. exilis Loxodonta cyclotis e 0.0972 0.0319 0.6844 Loxodonta africana 3.303 e 0.9688 0.0047 Elephas maximus 3.945 0.6417 e 0.0011 Mammuthus exilis 1.57 4.873 5.514 e

Number of pits

ANOVA results e Test for Equal Means: Sum of Squares df Mean square F p Between groups: 636.545 3 212.182 8.388 <0.001 Within groups: 2428.51 96 25.297 Total: 3065.06 99 Tukey's honest signiﬁcance test: L. cyclotis L. africana E. maximus M. exilis Loxodonta cyclotis e 0.0041 0.0002 0.4508 Loxodonta africana 4.936 e 0.7648 0.193 Elephas maximus 6.313 1.377 e 0.01893 Mammuthus exilis 2.099 2.837 4.214 e

Scratch width score

ANOVA results e Test for Equal Means: Sum of Squares df Mean square F p Between groups: 30.7311 3 10.2437 14.85 <0.001 Within groups: 66.2289 96 0.689884 Total: 96.96 99 Tukey's honest signiﬁcance test: L. cyclotis L. africana E. maximus M. exilis Loxodonta cyclotis e 0.8198 0.8511 0.0544 Loxodonta africana 1.232 e 0.9999 0.0046 Elephas maximus 1.141 0.0908 e 0.0056 Mammuthus exilis 3.65 4.882 4.791 e

Gouges

ANOVA results e Test for Equal Means: Sum of Squares df Mean square F p Between groups: 1.73109 3 0.577029 3.164 0.0280 Within groups: 17.5089 96 0.182385 Total: 19.24 99 Tukey's honest signiﬁcance test: L. cyclotis L. africana E. maximus M. exilis Loxodonta cyclotis e 0.998 0.7607 0.6572 Loxodonta africana 0.2522 e 0.8531 0.5448 Elephas maximus 1.387 1.135 e 0.1496 Mammuthus exilis 1.632 1.884 3.019 e

Large pits

ANOVA results e Test for Equal Means: Sum of Squares df Mean square F p Between groups: 1.20661 3 0.402204 1.629 0.1877 Within groups: 23.7034 96 0.24691 Total: 24.91 99 Tukey's honest signiﬁcance test: L. cyclotis L. africana E. maximus M. exilis Loxodonta cyclotis e 0.9957 0.7431 0.9172 Loxodonta africana 0.3252 e 0.8626 0.818 Elephas maximus 1.431 1.106 e 0.3526 Mammuthus exilis 0.9117 1.237 2.342 e

Among Mammuthus exilis from Santa Rosa Island (Table 1, Fig. 5A), 94.1% of individuals have scratches that fall between 0 and 17, a pattern typical of browsing ungulates and those of the extant Loxodonta cyclotis individuals analyzed here, but distinctive from extant species with a greater breadth of scratch values such as ungulate mixed feeders, Loxodonta africana and Elephas maximus. When additional microwear variables are considered, Mam- muthus exilis (Fig. 6), exhibits some distinct patterns from those of extant elephants. Differences in large pitting and gouging (Fig 6A) are not statistically significant when M. exilis is compared to living elephants (Table 2) but there are statistically significant scratch textural differences between M. exilis and Loxodonta africana and Elephas maximus (Fig. 6B), while scratch textural differences between M. exilis and Loxodonta cyclotis are not statistically significant (Table 2). Scratch texture is a reflection of differences in widths and depths of scratches e i.e., fine scratches are the narrowest and shallowest while hypercoarse scratches are the widest and deepest. Thus, the enamel surface of M. exilis typically displays finely textured and mixtures of finely textured and coarse scratches, and fewer mixtures of coarse and hypercoarse scratches or purely hypercoarse scratches than seen in the African savannah and Asian elephants (Table 1, Fig. 6B). Fig. 7 shows that typical extant leaf-dominated ungulate browsers as a group have scratch width scores that range between 0 and 0.46 (i.e., they possess mostly finely textured scratches); whereas typical grazers range from 0.70 to 1.67 (i.e., they have fewer fine and more coarse scratches) and do not overlap leaf browsers. Mixed feeders that consume browse and grass regionally or seasonally predictably overlap both leaf browsers and grazers and range from 0 to 1.14 (data from Semprebon, 2002). What is striking about Fig. 7, is that both modern proboscideans and M. exilis are truly unique in terms of their larger mean scratch width scores when compared to other herbivorous mammals studied with stereomicrowear data thus far (but note that M. exilis has narrower scratches than modern proboscideans).

3.3. Pygmy mammoth microwear compared to mainland mammoths and mastodons

Mammuthus exilis clearly has mean scratch and pit results nearly identical to the forest elephant (Loxodonta cyclotis) and distinct from L. africana and Elephas maximus. Mammuthus exilis has mean scratch and pit results that are more similar to those found in prior studies for the mastodon Mammut americanum than those found in mainland mammoths (Figs. 4C and 5B), the latter taxa typically displaying values either intermediate between the browsing and grazing extant morphospaces, or skewed towards grazing, depending on the species (Green et al., 2005; Rivals et al., 2012). In addition, an examination of enamel surfaces (Fig. 8) suggests a more attritive diet for M. exilis compared to most other mammoths studied. Note the relatively polished, ﬂat, and shiny enamel surface with relatively few food scars in M. exilis compared to the relatively dull and more irregular enamel surface with many food scars in M. primigenius. Fortelius and Solounias (2000) provide a Fig. 4. A. Bivariate plot of the number of pits versus the number of scratches for the extant proboscideans analyzed graphed in relation to Gaussian conﬁdence ellipses comprehensive study and discussion of attritive versus abrasive (p ¼ 0.95) on the centroid for extant ungulate browsers (B) and grazers (G) (convex molar wear due to mastication of various types of food items. Taxa hulls) adjusted by sample size (ungulate data from Semprebon (2002) and Solounias that consume relatively soft food items such as browse experience and Semprebon (2002); extant proboscidean data compiled by GMS). B. Bivariate much tooth-on-tooth (attritive) polishing of opposing wear facets plot showing the raw scratch and pit distribution of M. exilis compared to that of extant ungulates from Semprebon (2002) and Solounias and Semprebon (2002). C. Mean as molars cut completely through relatively soft food and produce scratch versus mean pit results for M. exilis from Santa Rosa Island compared to extant ungulates (convex hulls), and living and fossil proboscidean mean scratch/pit values. Key: 1 ¼ Mammut americanum (Phosphate Beds, SC USA); 2 ¼ M. americanum TX, USA); 8 ¼ M. columbi (Quarry G., Sheridan Co., NE, USA); 9 ¼ M. columbi (Grayson, (Ingleside, San Patricio Co., TX, USA); 3 ¼ M. americanum (Various Localities, FL,USA); Sheridan Co., NE, USA); 10 ¼ M. primigenius (Fairbanks Area, AK, USA); 4 ¼ M. exilis, Santa Rosa Island, CA, USA; 5 ¼ M. columbi (Phosphate Beds, SC, USA); 11 ¼ M. primigenius (Brown Bank, North Sea); 12 ¼ M. trogontherii (Crayford - Slade 6 ¼ M. columbi (Santa Rosa Island, CA USA); 7 ¼ M. columbi (Ingleside, San Patricio Col, Green, UK); 13 ¼ M. trogontherii (Ilford, UK). Data: 1e2, 5, 7e14 from Rivals et al. (2012); 3 from Green et al. (2005); 4, 6 from this study).

Fig. 5. Box plot of the percentage of scratches per taxon that fall within the low scratch range (i.e., between 0 and 17). Boxes represent results from extant ungulates. A. Low scratch range scores for Mammuthus exilis (from Santa Rosa Island) compared to results for extant ungulates and extant proboscideans. B. Low scratch range scores for mainland mammoths (key as in Fig. 7 legend). The box represents the central 50% of the scratch values and the bars represent the range (minimal and maximal values). relatively polished and ﬂat enamel facets. Taxa that consume twigs of rainforest trees and varies its diet regionally according to relatively abrasive foods such as grass experience more abrasive the availability of trees and fruits (White et al., 1993; Tangley, 1997; food-on-tooth wear which leads to a less polished and more Eggert et al., 2003). An extensive seven-year observational study of irregular enamel surface. L. cyclotis from the Lope Reserve in Gabon (White et al., 1993) determined that 70% of the diet of L. cyclotis in terms of the number 4. Discussion of species and amounts eaten came from leaves and bark. In contrast, Loxodonta africana (African savannah elephant) and 4.1. Pygmy mammoth microwear compared to extant elephants Elephas maximus (Asian elephant) are more generalist feeders, relying on more widely distributed resources including grasses, In this study, M. exilis exhibited a microwear scratch pattern shrubs, herbs, palms and vines and broadleaved trees (Nowak, similar to (and not signiﬁcantly different from) that of Loxodonta 1999; Osborn, 2005; Archie et al., 2006; Rode et al., 2006; cyclotis (i.e., scratch results concentrated toward the browsing Wittemyer et al., 2007). Loxodonta africana extended historically morphospace), in contrast to that of L. africana or Elephas max- from north of the Sahara Desert to the southern tip of Africa but is imus (scratch results that extend more into the mixed feeding and now found in increasingly fragmented habitats (deserts, savannas, grazing zones). These results are consistent with known differ- forests, river valleys and marshes (Estes, 1999). E. maximus is found ences in habitat and dietary habits of L. cyclotis, L. africana and E. today in Southeast Asia from India to Borneo but was formerly maximus. more widely distributed from the Levant, throughout Southeast Loxodonta cyclotis (African forest elephant), found today in Asia, and in China as far north as the Yangtze River. Like L. africana, western and central Africa, mainly occupies lowland tropical rain- E. maximus used a greater variety of habitats in the past than it does forests, swamps, and semi-evergreen and semi-deciduous tropical today, as currently ecotones with an interdigitation of grass, forests, rainforests. Forest elephants are known to change habitats and low woody plants are favored as continuously forested areas seasonally, occupying lowland rainforest during the wet season and without regular clearings do not support high densities (Shoshani moving to swampy areas during the dry season (Merz, 1986a,b; Fay and Eisenberg, 1982). Both L. africana and E. maximus alternate and Agnagna, 1991; Dudley et al., 1992; White et al., 1993; Tangley, between a predominantly browsing strategy with that of grazing 1997). Loxodonta cyclotis subsists mainly on leaves, bark, fruit, and because of seasonal variation of food plants, seasonally changing

that of the extant L. cyclotis than the more highly migratory L. africana and E. maximus. Thus, some microwear features inscribed into enamel of M. exilis, such as scratch numbers and textures and the appearance of the enamel surfaces themselves, are more congruent with a less abrasive diet than African savannah and Asian elephants. The enamel surface of M. exilis is flatter (enamel band edges sharp and less rounded), more polished and less scarred than African savannah and Asian elephants and more similar to L. cyclotis and other predominantly browsing forms (Solounias and Semprebon, 2002). Interestingly, no individual of M. exilis exhibits mostly hypercoarse scratches as is seen in some individuals of all species of living elephants (Solounias and Semprebon, 2002). Hypercoarse scratches are relatively unusual features that have thus far mainly been reported in those taxa known to consume appreciable amounts of bark (Solounias and Semprebon, 2002; Green et al., 2005) or are known hard-object processors such as primate hard- fruit and seed consumers (Semprebon et al., 2004). It is possible that these scratch textural results are due to bark consumption, as puncture-like large pits typical of fruit and seed consumers were not observed. The fact that fewer individuals of M. exilis possess mixed coarse and hypercoarse or purely hypercoarse scratches than the African savannah and Asian elephants raises interesting questions regarding the relative importance of bark consumption in these forms. It is conceivable, however, that because proboscideans are large animals with large jaw muscles, they might concentrate more pressure when biting on a hard object compared to smaller more selective-feeding mammals and that this, rather than bark consumption, might produce hypercoarse scratches. While this should not be discounted as a possibility or as a contributing factor, hypercoarse scratches are not simply deeper than coarse or fine scratches, they are also wider. This augmented scratch width is Fig. 6. Bar charts showing percentages of individuals per taxon in M. exilis and extant concordant with the tendency of bark to include clustered silica proboscideans with large pits and gouges (Fig. 6A) and the percentage of individuals per taxon of M. exilis and extant proboscideans displaying fine, mixed fine and coarse, whereby soil minerals are concentrated and cemented into silica coarse, mixed coarse and hypercoarse and hypercoarse scratch textures (Fig. 6B). aggregates (Sangster and Hodson, 1992; Albert and Weiner, 2001). Also, if bite force alone were responsible for producing hypercoarse mineral content, and migration habits (Joshi and Singh, 2008; scratches, other microwear scars would be expected to be deeper Mohaptra et al., 2013). and we have not found this to be the case. In addition, an important Our microwear results suggest that pygmy mammoths from finding that bears on this question is the presence of hypercoarse Santa Rosa engaged in a fairly restricted dietary regime more like scratches in the enamel of Florida mastodons with preserved

Fig. 7. Box plot of scratch width scores for extant ungulates and proboscideans and M. exilis. A score of 0 ¼ teeth with mostly ﬁne scratches, 1 ¼ those with a mixture of ﬁne and coarse scratches, 2 ¼ those with mostly coarse scratches, 3 ¼ those with a mixture of coarse and hypercoarse scratches, and 4 ¼ those with mostly hypercoarse scratches. In each plot, the center vertical line marks the median of the sample, the central 50% of the scratch values fall within the range of the box, and the top and bottom bars represent the range of scratch values.

Fig. 8. Photomicrographs of molar enamel surfaces (@35X magniﬁcation) of M. exilis e SBMNH e VPN 838 (left) compared to M. primigenius e AMNH 651012-1952 (right). Note the relatively ﬂat and polished enamel surface of M. exilis, typical of attritive feeders versus the uneven topography and duller enamel surface of M. primigenius which is typical of abrasion-dominated feeders. Both specimens were analyzed using the same lighting regime. Scale bar ¼ 0.4 mm. digesta consisting of a heavy concentration of cypress twigs (Webb Rivals et al., 2012) which indicate more seasonal or regional mixed et al., 1992; Mihlbachler, 1998; Green et al., 2005). While the above feeding (i.e., alternate consumption of browse and grass) in the are consistent with hypercoarse scratches being caused by bark majority of forms, although exceptions do exist. For example, consumption, further study is needed to tease apart the contrib- Mammuthus columbi from the Phosphate Beds of South Carolina in uting factors that produce such distinctive scratches in North America apparently browsed (Fig. 4C, point labeled 5; Rivals proboscideans. et al., 2012).

4.2. Pygmy mammoth microwear compared to mainland 4.3. Channel Island Paleoecology mammoths and mastodons Today the local vegetation of the Northern Channel Islands is Our results indicate that M. exilis most likely engaged in a diet of dominated by grasslands and shrublands with some patchy relatively low abrasion (polished enamel) and less dietary breadth woodlands, and mild temperatures with little annual temperature (few scratches) than the majority of mainland mammoths studied fluctuation (Junak et al., 2007). To date, studies of the vegetation thus far, including its likely ancestor e M. columbi. history of the island have included pollen analyses on Santa Rosa Our data show (Table 1 and Fig. 4B) that 94% of individuals in our Island (Cole and Liu 1994; Kennett et al., 2008) and San Miguel sample of M. exilis have scratch numbers that fall within a relatively Island (West and Erlandson, 1994), and paleobotanical studies on narrow low scratch (browsing type) range while only the forest Santa Cruz Island (Cheney and Mason, 1930). During the Late elephant (L. cyclotis) and one of the mammoth samples we studied Pleistocene, when these islands existed as the single super-island of (Mammuthus columbi from the Phosphate Beds of South Carolina e Santarosae, forest vegetation was present including cypress, pine, Fig. 4C) also fall within this range. Two questions to consider when and Douglas fir(Cheney and Mason, 1930; Anderson et al., 2008). interpreting these data are: (1) do the relatively narrow browse- Climatic changes at the end of the Pleistocene have been invoked as dominated scratch results of M. exilis reflects its actual dietary the cause for the loss of coastal forest (Anderson et al., 2008), and range or were the specimens analyzed collected from a particular major fires coincident with the last known occurrence of pygmy horizon or facies that may underrepresent the diversity of habitats mammoths (around 13,000 cal. BP) have been demonstrated (and diets), and (2) since microwear represents a snapshot in time (Kennett et al., 2008). Anderson et al. (2010) combined pollen of dietary behavior (i.e., the diet at the time of an animal's death), is analysis with an analysis of the fire disturbance regime of Santa it possible that a concentration of deaths in a particular season Rosa Island and reported that a coastal conifer forest covered the might have led to a “last supper effect” (Grine, 1986)? highlands of Santa Rosa during the last glacial but that by ca. Firstly, the sample available to us was drawn from a variety of 11,800 cal. BP Pinus stands, coastal sage scrub and grassland facies (Agenbroad, 2001) so our results most likely show fidelity to replaced the forest as the climate warmed. the actual dietary range of M. exilis. However, if food supply or Our molar microwear results support our hypothesis that M. climate were highly seasonal on Santa Rosa Island during the exilis was exploiting forest vegetation on Santa Rosa during the Late tenure of M. exilis on the island, it is quite plausible that deaths Pleistocene since M. exilis individuals possessed scratches mainly in would not have been spread evenly throughout the year, especially the low scratch range typical of leaf browsing extant ungulates and on an island where seasonal migration is not possible. other mammals as well as the unusually deep and wide scratches Interestingly, the enamel surfaces and mean scratch/pit patterns typical of bark and twig consumers such as extant proboscideans of M. exilis are more similar to those found in prior studies for the and black rhinos (see Solounias and Semprebon, 2002). These re- American Mastodon e Mammut americanum (Green et al., 2005) sults are consistent with what is known of the Pleistocene vege- than to the results reported for Middle to Late Pleistocene Mam- tation history of Santa Rosa Island whereby extensive coastal muthus from North America and Europe (Perez-Crespo et al., 2012; conifer forests were available during the last glacial as well as Pinus

Please cite this article in press as: Semprebon, G.M., et al., Dietary reconstruction of pygmy mammoths from Santa Rosa Island of California, Quaternary International (2015), http://dx.doi.org/10.1016/j.quaint.2015.10.120 G.M. Semprebon et al. / Quaternary International xxx (2015) 1e14 11 stands and sage scrub as the climate warmed (Anderson et al., MIS2/1 transition occurred (reduction in pine and other trees; 2010). Therefore, abundant browse was apparently available to M. expansion of open vegetation). Muhs et al. (2015) conclude that exilis, and consumption of leaves and twigs, as hypothesized here is climate and vegetation change may not have been a major compatible with available Pleistocene vegetation on the island. contributor to M. exilis extinction. It remains plausible, however, that habitat change, especially in the situation of a small island 4.4. Extinction of M. exilis area, would have reduced population size, making the species more likely to go extinct from these causes either stochastically or via There is much debate surrounding the extinction of Late Qua- another agent (Lister and Stuart, 2008). While our results suggest ternary megafauna. The leading hypotheses are human overkill, that climatic factors may have played a role in the extinction of climatic fluctuations, or vegetational change, with widespread Channel Island pygmy mammoths on Santa Rosa Island, the disease, or extraterrestrial impact events sometimes invoked determination of the relative contribution of climatic factors versus (Martin and Klein, 1984; Grayson, 2001, 2007; Grayson and Meltzer, human overkill would benefit from futher study. These suggestions 2002; Koch and Barnosky, 2006; Firestone et al., 2007; Haynes, require further work including on the diet of the early (M. columbi) 2007; Faith and Surovell, 2009). It has long been thought that is- immigrants in comparison with M. exilis. land species are more susceptible to human-induced extinctions than those on continents and, consequently, the Channel Islands 5. Conclusions have generated much interest to proponents of overkill hypotheses. While early researchers reported that the Northern Channel Islands This analysis has provided for the first time microwear evidence were colonized by humans at least 40,000 years ago and claimed an of feeding behavior (i.e., mainly browsing on leaves and twigs) in M. association between human artifacts and mammoth remains as exilis from Santa Rosa Island of California. This strongly suggests well as what were interpreted as “fire features” (Berger and Orr, that a constrained niche was imposed upon M. exilis, compared to 1966; Orr and Berger, 1966; Orr, 1968), closer scrutiny puts the the broader dietary breadth apparent in its mainland ancestor (M. date of the first occupation of the islands by humans at around columbi). Lastly, our analysis offers a glimpse into a possible 13,000 cal. BP), and what were interpreted as “mammoth roasting contributing factor for the extinction of Channel Island pygmy pits” are now thought to be natural burn features or due to other mammoths, as the woodland dietary preferences of this taxon were natural processes (Wendorf, 1982; Cushing et al., 1986; Rick et al., beginning to diminish and be replaced by grasslands as the climate 2012; Pigati et al., 2014). warmed. While a possible minimum temporal overlap between mammoth and Homo sapiens of 250 years has been suggested for Santa Rosa Island using radiocarbon dating (Agenbroad et al., Acknowledgements 2005), faunal remains associated with archeological sites dated between 12,200 and 11,500 cal. BP on the Channel Islands are We thank Paul Collins from the Santa Barbara Museum of Nat- devoid of large mammals (Erlandson et al., 2007; Rick et al., 2012) ural History for access to the specimens and Jelena Hasjanova, and there is no direct evidence of human hunting of mammoths on Michaela Tarnowicz, Kristina Rogers, and Mia Russo from Bay Path the Channel Islands (Rick et al., 2012). University for assistance in making casts. Much is known about Channel Island mammoths. It is likely that Columbian mammoths gained access to the Northern Channel References Islands during a low stand of MIS 6, ca. 130 ka (Muhs et al., 2015) and gave rise to island pygmy mammoths via an approximately 50 Agenbroad, L.D., 1998. New pygmy mammoth (Mammuthus exilis) localities and percent linear size reduction (Agenbroad, 2009). This decrease in radiocarbon dates from San Miguel, Santa Rosa, and Santa Cruz Islands, Cali- size would provide the advantage of a lesser need for food intake fornia. In: Weigand, P. (Ed.), Contributions to the Geology of the Northern Channel Islands, Southern California. Pacific Section of the American Associa- which might have proven to be an advantage in times of environ- tion of Petroleum Geologists, Bakersfield, California, pp. 169e175. mental stress (McNab, 2010; Lister and Hall, 2014). Agenbroad, L., 2003. New absolute dates and comparisons for California's Mam- e However, the survival ability of the pygmy mammoths would muthus exilis. Deinsea 9, 1 16. Agenbroad, L.D., 2001. Channel Islands (USA) pygmy mammoths (Mammuthus have been compromised by the vast reduction of island land area as exilis) compared and contrasted with M. columbi, their continental ancestral sea levels rose at the end of the Pleistocene. The super-island of stock. In: Cavarretta, G., Gioia, P., Mussi, M., Palombo, M.R. (Eds.), The World of Santarosae shrank to about 75% of its original landmass as sea levels Elephants: International Conference, Rome, pp. 473e475. Agenbroad, L.D., 2009. Mammuthus exilis from the Channel Islands: height, mass, rose (Kennett et al., 2008) causing inevitable ecological distur- and geologic age. In: Damiani, C.C., Garcelon, D.K. (Eds.), Proceedings of the bances and alteration of available vegetation and freshwater sour- Seventh California Islands Symposium. Institute for Wildlife Studies, Arcata, ces. In addition, the results of this study clearly show that M. exilis pp. 15e19. Agenbroad, L.D., 2012. Giants and pygmies: mammoths of Santa Rosa Island, Cali- mainly browsed on leaves and twigs, a clear shift in niche from its fornia (USA). Quaternary International 255, 2e8. mainland ancestor. As warming ensued, conifer forests were Agenbroad, L.D., Johnson, J.R., Morris, D., Stafford, T.W., 2005. Mammoths and replaced by sage scrub, Pinus stands and grasslands by about humans as Late Pleistocene contemporaries on Santa Rosa island. In: Garcelon, D., Schwemm, C. (Eds.), Proceedings of the Sixth California Islands 11,800 cal. BP (Heusser, 1995, 2000; Anderson et al., 2010). Our Symposium (National Park Service Technical Publication CHIS-05-01. Institute microwear results are consistent with the last glacial (MIS4-2) for Wildlife Studies, pp. 3e7. vegetative history of Santa Rosa Island and suggest that climatic Agenbroad, L.D., Johnson, J., Morris, D., Stafford, T.W., 2007. Mammoths and humans factors contributed to the extinction of Channel Island Pygmy as late Pleistocene contemporaries on Santa Rosa Island. In: American Geophysical Union Spring Meeting, pp. 3e7. Mammoths on Santa Rosa Island as the shrinking of the forest Albert, R.M., Weiner, S., 2001. Study of phytolith in prehistoric ash layers from habitat would have impacted a species that relied heavily on leaves, Kebara and Tabun caves using a quantitative approach. In: Meunier, J.D., and twigs. Colin, F. (Eds.), Phytolith: Applications in Earth Sciences and Human History. A.A. Balkema Publishers, Lisse, pp. 251e256. Muhs et al. (2015) point out that since the earliest dated remains Anderson, R.L., Byrne, R., Dawson, T., 2008. Stable isotope evidence for a foggy of Mammuthus from the California Channel islands are in late MIS 5 climate on Santa Cruz Island, California at̴ 16,600 cal. yr. B.P. 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