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JOURNAL OF QUATERNARY SCIENCE (2016) 31(7) 799808 ISSN 0267-8179. DOI: 10.1002/jqs.


Dental mesowear reflects local vegetation and niche

separation in Pleistocene proboscideans from Britain
Natural History Museum, Cromwell Road, London SW7 5BD, UK
Department of Geosciences and Geography, University of Helsinki, Finland
Received 7 April 2016; Revised 29 August 2016; Accepted 11 September 2016

ABSTRACT: Proboscideans, and elephants in particular, played a key role in Pleistocene mammal communities in
Europe. The British Pleistocene fossil record provides a unique opportunity to study changes in proboscidean
feeding ecology associated with environmental proxy data such as pollen records and the presence of competitors.
Here we utilize a recently introduced dietary analysis method, mesowear angle analysis, for studying relationships
between dietary variation in proboscideans, changes in available vegetation and the presence of sympatric
proboscidean species. The method is based on recording the relief of worn molar surfaces as angle measurements,
which reflect attrition- vs. abrasion-dominated feeding and serve as a proxy for grazing vs. browsing diets. By
comparison with pollen records, we show that blunt mesowear angles specifically reflect grass eating rather than
open-ground feeding in general. We further find that all British Pleistocene proboscidean species were relatively
flexible feeders able to shift their dietary preference according to local vegetation composition. Nonetheless, when
more than one proboscidean species occurred in the same environment, they always show significantly different
mean mesowear signal, suggesting dietary niche separation. Copyright # 2016 John Wiley & Sons, Ltd.
KEYWORDS: diet; Pleistocene; pollen; Proboscidea; mesowear angles.

Introduction lamellae in the last molar increased from the 810 of

M. rumanus to 1214 (Lister et al., 2005). Dietary analyses
Proboscideans were the largest land mammals in Europe based on microwear indicate that M. meridionalis was a
during the Pleistocene, living in various habitats, often repre- mixed-feeder (Rivals et al., 2015). In the early Middle
sented by more than one sympatric species. Pleistocene Pleistocene, ca. 0.80.6 Ma, there was a turnover in the
deposits from Britain contain abundant remains of fossil proboscidean fauna of Britain, during which the last
elephants, with other proboscideans in the earliest levels, and M. meridionalis populations were replaced by two immigrat-
often include associated information on the environments. In ing elephant species, the straight-tusked elephant Palaeolox-
this study we utilize the mesowear angle method (Saarinen odon antiquus and the steppe mammoth Mammuthus
et al., 2015) for analysing diets of British Pleistocene probosci- trogontherii (Lister, 2004; Lister et al., 2005). Both P. antiquus
dean species and populations. There are two main objectives and M. trogontherii had more specialized, hypsodont denti-
to this study. First, we evaluate dietary niche separation tions than M. meridionalis, with last molars comprising
between sympatric proboscidean species by comparing mean typically 1621 lamellae in P. antiquus (Dubrovo, 1977;
mesowear signals of populations. Second, we compare the Herridge and Lister, 2012) and 1722 in M. trogontherii
mesowear signals of the proboscideans with local vegetation (Lister et al., 2005), and they may have outcompeted M.
proxy data from pollen records. This enables us to evaluate meridionalis in wooded and open habitats, respectively
how local vegetation structure is reflected in the dietary pre- (Lister, 2004). Environmental data indicate that despite the
ferences of the proboscideans at the level of local populations. increased hypsodonty inherited from its African precursors
British Pleistocene localities provide a valuable opportunity to (Lister, 2013), P. antiquus inhabited relatively wooded tem-
analyse mammalvegetation interactions because they are well perate habitats and was on average a mixed-feeder, based on
stratified and contain abundant pollen and mammal remains. microwear and other dietary analyses (e.g. Grube et al.,
In the latest Pliocene to earliest Pleistocene (ca. 32.5 Ma) 2010; Rivals et al., 2012). M. trogontherii typically occupied
the proboscidean fauna of Britain included the mastodon more open, savanna or steppe-like habitats and demonstrates
Mammut borsoni, the gomphotheriid Anancus arvernensis significant increase in grazing adaptations compared to
and the early mammoth Mammuthus rumanus (Lister and M. meridionalis (Lister, 2004, 2005), although microwear
van Essen, 2003; Kahlke et al., 2011; Rivals et al., 2015). analyses indicate variable mixed-feeding diets for this species
Dental microwear studies (Rivals et al., 2015) have indicated too (Rivals et al., 2012). P. antiquus and M. trogontherii
browse-dominated diets for these species, and their denti- were the common elephant species in Britain in the Middle
tions brachydont with relatively few lamellae or cusps Pleistocene, occasionally coexisting, e.g. in the Marine
compared to later elephantids do not show highly special- Isotope Stage 7 (MIS 7) locality of Ilford. P. antiquus persisted
ized grazing adaptations (Lister et al., 2005). By the Early in warm phases of the Late Pleistocene, but M. trogontherii
Pleistocene, Mammut borsoni was extinct in Britain, but the was replaced by the woolly mammoth M. primigenius in the
last populations of A. arvernensis persisted until ca. 1.85 Ma late Middle Pleistocene. M. primigenius shows extreme
in the Norwich Crag. The earliest European mammoth species grazing adaptations in its dentition with very hypsodont
M. rumanus was replaced during the Early Pleistocene by the molars inherited from M. trogontherii and the last molar
southern mammoth Mammuthus meridionalis, which still comprising on average 2324 lamellae in Europe, higher in
had relatively low-crowned molars but with the number of Siberia (Lister et al., 2005). M. primigenius mostly inhabited

the open, grass-dominated steppetundra habitats of the last
Correspondence: J. Saarinen, 2 Department of Geosciences and Geography,
as above.
glacial (e.g. Lister, 1991; Allen et al., 2009) and had on
E-mail: average a relatively grass-dominated diet with significant

Copyright # 2016 John Wiley & Sons, Ltd.


non-grass herbaceous content, based on microwear analyses, digital angle meter to 0.1 precision. The angle meter was
plant remains and DNA samples analysed from teeth, modified to allow measuring the mesowear angles from worn
stomach contents of frozen carcasses and fossilized faeces dentine valleys by making both of the arms of the device
(Guthrie, 1990, 2001; van Geel et al., 2008; Rivals et al., extendable and attaching narrow metal plates to their proxi-
2010, 2012; Willerslev et al., 2014; Kirillova et al., 2016). mal ends, so that the tips of the metal plates meet. In this
Many studies have shown that sympatric species of way, any angle could be fitted by placing the tips at one point
proboscideans had separated dietary niches, presumably in the bottom of the worn dentine valley (see Saarinen et al.,
allowing them to coexist (Calandra et al., 2008, 2010; Rivals 2015). The angles from three central lamellae of each
et al., 2012, 2015). Based on dental microwear, Rivals et al. specimen were averaged to give a mean mesowear angle. In
(2012) noted opposite temporal trends in the dietary prefer- the case of fragmentary specimens, a minimum of one central
ences of the straight-tusked elephant (P. antiquus) and the lamella or loph was used for recording the mesowear angle.
mammoth lineage (Mammuthus) during the Pleistocene of Means of the mean mesowear angles of individual teeth
Europe, with Palaeoloxodon shifting from a mixed feeder to a were calculated for all palaeopopulations, and they were
browser and Mammuthus from a browser to a grazer. compared using pairwise Wilcoxon tests. This allowed us to
However, this result was based on data from only one or two evaluate differences in dietary preferences and the role of
localities for each time interval, and these localities represent dietary niche separation between species at a locality. We
widely separate geographical regions (Greece, Germany and also compared the mean mesowear angles of proboscidean
the UK), so there might be a spatial signal contributing to the species and guilds at locality level with published non-
result. Rivals et al. (2015) suggested that the sympatric Early arboreal pollen (NAP) and Graminae (grass) percentages in
Pleistocene proboscideans M. rumanus and A. arvernensis pollen records from the localities. The correlations of mean
had separated dietary niches despite their both being mixed- mesowear angle with NAP on the one hand and Graminae
feeders with relatively flexible dietary preferences. In this on the other allow us to evaluate whether the mesowear
study we address the question of how far this kind of dietary signals reflect specifically the amount of grass in the diets
flexibility reflects niche separation or how much it is a or open-ground feeding in general. To examine this, we
response to changes in local vegetation. used stepwise multiple linear regressions to analyse how
much of the variation in the mesowear angles is explained
Materials and methods by mean Graminae %, mean non-Graminae NAP % and
total mean NAP %.
We utilized the mesowear angle method introduced by Materials
Saarinen et al. (2015) for dietary analyses of fossil probosci-
The material for this study comprises fossil proboscidean
deans from Pleistocene localities of Britain. Mesowear (mac-
molar teeth from latest Pliocene and Pleistocene localities of
roscopic relief and shape of worn molar surfaces) serves as a
Britain, housed at the Natural History Museum and Norwich
proxy for the relative amount of abrasive plant material
Castle Museum. A map of the localities studied here is shown
(mainly grass) eaten by herbivorous mammals (Fortelius and
in Fig. 1. The pollen data for the localities were gathered
Solounias, 2000). The reason why grasses in particular cause
from previously published literature (Table 1). Detailed
abrasion-dominated mesowear on molar surfaces is still
information about the localities, with discussion on the
debated but it most likely includes factors such as the high
association of pollen records and the proboscidean material,
fibre and phytolith content of grass leaves (e.g. Lucas and
is provided in the Supporting Information (Appendix S1). NAP
Omar, 2012; Damuth and Janis, 2014; Lucas et al., 2014).
and Graminae (grass) pollen percentages were obtained,
Empirical evidence has demonstrated that mesowear analysis
where possible, from exact pollen counts given in the
does reflect grazing in particular, without being significantly
publications, or else read from pollen diagrams where pollen
altered by other factors such as external grit on plants (Kaiser
counts were not listed. For our purposes, NAP is calculated to
et al., 2013). We use the term grazing here in the strict sense
include only herbs and grasses, not shrubs. This is because
of eating grass. Consequently, feeding on low-growing herbs
the dominant shrubs in British Pleistocene environments (e.g.
is considered browsing, together with feeding on leaves of
Corylus) are often associated with closed habitats along with
shrubs and trees. For convenience, considering proboscidean
trees, and because browsing on shrubs would not drastically
species we use generalized dietary classes, defined here as:
differ in terms of feeding ecology, or mesowear signal, from
browsers (<10 % grass in diet), browse-dominated mixed-
browsing on trees. Because it is often not possible to connect
feeders (1030% grass in diet), generalized mixed-feeders
particular proboscidean specimens to exact strata in the
(3070% grass in diet), grass-dominated mixed-feeders
pollen sequences, we compared the mean mesowear angles
(7090% grass in diet) and grazers (>90% grass in diet),
from the proboscidean assemblages against mean, minimum
similar to the conventional dietary categorization of herbivo-
and maximum NAP and Graminae percentages in the pollen
rous mammals (e.g. Fortelius and Solounias, 2000).
sequences from the localities. This approach enables us to
Mesowear angles were measured on the occlusal surface of
compare similarly time-averaged and roughly associated
molar lamellae by placing the vertex of the angle at the
proboscidean and vegetation records at locality level.
bottom of the dentine valley and the sides at the top edge of
the adjacent enamel ridges (see Saarinen et al., 2015). In
some less heavily worn teeth of Mammut borsoni the angles
were measured from worn enamel facets by placing the side There is considerable variation in mesowear angle values, not
of the angle parallel to the surface of the facet. These angles only between proboscidean species, but also between palae-
record the relief (relative height) of the enamel ridges, serving opopulations of each species and within the populations
as a proxy for diet abrasiveness, by the same principle as (Table 1; Fig. 2). This indicates relatively flexible feeding
traditional mesowear analysis (Fortelius and Solounias, 2000), behaviours in Pleistocene proboscideans, despite different
and they have been demonstrated to correlate with grazing dietary adaptations of the species. The Late Pliocene masto-
on C4-grasses in tropical elephant populations (Saarinen et don Mammut borsoni from the Red Crag Nodule Bed has the
al., 2015). The mesowear angles were measured with a sharpest mean mesowear angle (ca. 94) of all the

Copyright # 2016 John Wiley & Sons, Ltd. J. Quaternary Sci., Vol. 31(7) 799808 (2016)

Figure 1. Locality map.

proboscideans analysed here, indicating a pure browsing with mean, minimum and maximum grass percentages in the
diet. The gomphothere A. arvernensis shows more variable associated pollen records (Fig. 3). At the species level also,
mesowear angles (ca. 90120), giving a browse-based mesowear angles of the Early and Middle Pleistocene
dietary signal for the population in the Red Crag but a mixed- elephant species, M. meridionalis, P. antiquus and
feeding signal in the Norwich Crag, although the latter M. trogontherii, all show statistically significant positive
sample comprises only two specimens. correlations with mean grass pollen percentages (Fig. 4). The
Among the elephants, the Early Pleistocene M. meridionalis gomphothere A. arvernensis consumed more grass in
shows on average intermediate mesowear angles, varying the relatively open and grassy palaeoenvironment of Norwich
between ca. 115 and 124 between localities, indicating Crag than in the more forested Red Crag.
mixed-feeding diets. P. antiquus shows on average relatively Importantly, our analyses support the hypothesis that
sharp mean mesowear angles (102110), indicating browse- proboscidean mesowear angles reflect specifically the
dominated mixed-feeding diets. However, the population amount of grass in the environment, not just general vegeta-
from Ilford shows significantly higher than average mean tion openness. In stepwise multiple linear regressions model-
mesowear angle (114) implying generalized mixed-feeding ling of locality mean mesowear with Graminae %, mean
diet. M. trogontherii shows on average significantly blunter non-Graminae NAP % and mean NAP % (Table 2), Graminae
mean mesowear angles than P. antiquus or M. meridionalis % shows the most significant P-value and the lowest Akaike
(typically ca. 120140), indicating heavily grass-dominated Information Criterion (AIC), together with the highest correla-
mixed-feeding diets. Nonetheless, there is considerable varia- tion coefficient. Non-Graminae NAP % is not correlated at all
tion in the dietary signal of M. trogontherii between and with mesowear, whereas the total mean NAP % shows a
within localities, indicating some flexibility in the choice of significant positive correlation, but higher AIC and P-value,
diet. M. primigenius shows blunt mean mesowear angles (on and lower correlation coefficient than Graminae % alone.
average ca. 126137), indicating a very grass-dominated This demonstrates that the correlation with total NAP %
diet, which at Kents Cavern is essentially pure grazing, and is caused by grasses (Graminae) specifically, not by non-
at Lea Valley strongly grass-dominated. Graminae NAP.
In deposits where more than one species of proboscidean
occurred sympatrically, such as the Red Crag, Norwich Crag
and Ilford, there is always a statistically significant difference
in the mean mesowear angles between the species (Fig. 2; The results from the mesowear angle analyses provide
Table S1), indicating dietary niche separation among sympat- quantitative corroboration of the dietary adaptations and
ric species. preferences that have been assumed for Pleistocene probosci-
Nonetheless, it is clear that proboscideans generally dean species. They also, however, reveal considerable dietary
consumed more grass in open environments where plant flexibility in these megaherbivores, indicating the ability to
communities were more grass-dominated. Taking the mean shift to more grazing diets in grass-dominated environments
mesowear angle of the whole proboscidean assemblage at and to avoid resource competition by dietary niche separa-
each locality, there is a statistically significantly correlation tion. Furthermore, there is considerable variation among

Copyright # 2016 John Wiley & Sons, Ltd. J. Quaternary Sci., Vol. 31(7) 799808 (2016)
Table 1. Sample means and ranges of individual mean mesowear angles in the proboscidean palaeopopulations from British Plio-Pleistocene localities. Mean percentages of NAP and Graminae associated with the

proboscidean populations in the localities are shown, with minimum and maximum values in parentheses.

Family Species Locality Age n Mean mesowear Mesowear angle NAP % Graminae % Ref. for age Ref. for pollen
angle () range ()

Mammutidae Mammut borsoni Red Crag Nodule Bed ca. 2.7 Ma 4 93.7 83.6102.7 9.4 (8.710.1) 0.6 (0.20.9) Kahlke et al. (2011) Head (1998)
Gomphotheriidae Anancus Red Crag ca. 2.5 Ma 9 106.2 88.2126.1 28.1 (1850) 6.6 (410) Kahlke et al. (2011) Zalasiewicz et al.
arvernensis (1988)
Gomphotheriidae Anancus Norwich Crag ca. 2.31.85 Ma 2 115 109.9120.1 48 (2172) 28.4 (7.450) Richards et al. Richards et al. (1999)
arvernensis (1999)
Elephantidae Palaeoloxodon Happisburgh Early Middle 5 102.1 90.9108.3 No record No record West (1980), Lister

Copyright # 2016 John Wiley & Sons, Ltd.

antiquus Pleistocene (1996)
Elephantidae Palaeoloxodon Waverley Wood Early Middle 4 110.7 102.6114.5 50.2 (2080) 20.8 (935) Shotton et al. Shotton et al. (1993)
antiquus Pleistocene (1993)
Elephantidae Palaeoloxodon Swanscombe MIS 11 18 107.3 98.8116.5 No record No record Schreve (2001)
Elephantidae Palaeoloxodon Clacton (bed 2) MIS 11 10 106.3 100.5111.1 22 (1037) 10.6 (320) Schreve (2001) Bridgland et al.
antiquus (1999)
Elephantidae Palaeoloxodon Grays Thurrock MIS 9 14 109.4 97.7132.1 19.2 (1226) 13.7 (1017) Schreve (2001) Gibbard (1994)
Elephantidae Palaeoloxodon Ilford MIS 7 6 114.8 105.7128.5 44.6 (1872) 21.7 (565) Schreve (2001) West et al. (1964)
Elephantidae Palaeoloxodon Waterhall Farm MIS 5e 12 106.6 96116.8 No record No record Currant and Jacobi
antiquus (2001)
Elephantidae Palaeoloxodon Trafalgar Square MIS 5e 3 107.7 105111.7 35.3 12.5 Schreve (2001) Franks (1960), Stuart
antiquus (1976)
Elephantidae Mammuthus Norwich Crag ca. 2.31.85 Ma 7 123.2 105130.5 48 (2172) 28.4 (7.450) Richards et al. Richards et al. (1999)
meridionalis (1999)
Elephantidae Mammuthus Bacton (Elephant Bed) Early Pleistocene 23 115.2 107.7127.5 17.4 (530) 11.6 (422) West (1980), Lister West (1980)
meridionalis (1996)

Elephantidae Mammuthus Mundesley (bed f) Early Pleistocene 7 116.3 108.6121.9 27 (1055) 14.9 (735) West (1980), Lister West (1980)
meridionalis (1996)
Elephantidae Mammuthus Overstrand (bed g) Early Pleistocene 8 117.6 111.7127.7 22.3 (2025) 16.8 (1520) West (1980), Lister West (1980)
meridionalis (1996)
Elephantidae Mammuthus West Runton MIS 17 1 124 44.6 (3755) 32.8 (2039) Stuart and Lister Field and Peglar
meridionalis (2010) (2010)
Elephantidae Mammuthus Bacton (Estuarine Forest Early Middle 5 119.5 111.4131.5 15.7 (528) 10.1 (715) West (1980), Lister West (1980)
trogontherii Bed) Pleistocene (1996)
Elephantidae Mammuthus Mundesley (beds h and i) Early Middle 5 128.1 120.1144.3 24.6 (1070) 14.5 (445) West (1980), Lister West (1980)
trogontherii Pleistocene (1996)
Elephantidae Mammuthus Overstrand (Cromerian cliff Early Middle 18 122.2 111.2134.7 17 (1022) 7.3 (710) West (1980), Lister West (1980)
trogontherii deposits) Pleistocene (1996)
Elephantidae Mammuthus West Runton MIS 17 1 143.9 44.6 (3755) 32.8 (2039) Stuart and Lister Field and Peglar
trogontherii (2010) (2010)
Elephantidae Mammuthus Pakefield MIS 15 5 122.9 117.7127.5 33.3 (2057) 22.4 (1832) Penkman et al. West (1980)
trogontherii (2011)
Elephantidae Mammuthus Ilford MIS 7 21 128 113.1143.9 44.6 (1872) 21.7 (565) Schreve (2001) West et al. (1964)

J. Quaternary Sci., Vol. 31(7) 799808 (2016)


Allison et al. (1952)

individuals within local palaeopopulations, which could
Ref. for pollen indicate either different individual dietary choices or, perhaps
more probably, seasonal variation in diet. Mesowear records
the dietary signal over the last few months (Rivals et al.,
2007; M. Fortelius pers. comm.), and can probably capture
seasonal variation in diet. Modern Asian elephant (Elephas
Currant and Jacobi maximus) and African savanna elephant (Loxodonta africana)
tend to have mixed-feeding diets that are on average browse-
Scott et al. (2011)

Lister (1991) dominated (<50% grass), but vary seasonally and through the
Ref. for age


animals life (Sukumar and Ramesh, 1992; Cerling et al.,

1999; Saarinen et al., 2015). Their physiology and dental
morphology have adapted to the grassy or open-ground
element of their diet, but evidently do not preclude the
consumption of a substantial browse element as well.
Graminae %

Despite high intraspecific variation, British Pleistocene

No record

No record

proboscidean species show interspecific differences in mean


mesowear angle that reflect different dietary preferences.

Mammut borsoni from the Latest Pliocene of the Red Crag
Nodule Bed was a pure browser, based on the ca. 90 mean
mesowear angle and low variation. A. arvernensis and
No record

No record

ca. 100


P. antiquus were on average browse-dominated mixed-

feeders, roughly similar in dietary composition to the extant
African savanna elephant (see Cerling et al., 1999; Saarinen
et al., 2015). M. meridionalis was a flexible mixed-feeder
with mean mesowear values indicating diets which on
Mesowear angle



average fluctuated around ca. 50% grass and browse, roughly

range ()

similarly to the extant Asian elephant (see Sukumar and

Ramesh, 1992). M. trogontherii and M. primigenius were on
average more grass-dominated feeders (>50% grass in diet)
than the extant elephants, although there is remarkable
variation and purely grazing (>90% grass) dietary signal is
not typical for them either.
Mean mesowear

Yet, mean mesowear angles of British Pleistocene probosci-

angle ()




deans and associated Graminae (grass) pollen percentages are

significantly positively correlated, both for the average meso-
wear signals of proboscidean communities, and for the
species separately. This indicates that despite the underlying
differences in dietary preferences and adaptations, probosci-


deans tend to be flexible feeders that are able to consume

relatively more grasses in open, grass-dominated environ-
ments and more browse in wooded environments. This is also
MIS 76?

MIS 2?

seen today in the African savanna elephant (Loxodonta


africana), which has essentially purely browsing diets in

forested areas and mixed-feeding diets in more open savan-
nas with grassy vegetation (Cerling et al., 1999). Our analyses
indicate that blunt mesowear angles reflect grazing (in the
strict sense of eating grass) rather than more broadly feeding
in open environments, because the Graminae pollen %
explains more of the local variation in proboscidean meso-

wear than does NAP %. Moreover, we find that non-

Kents Cavern

Graminae NAP % is not correlated at all with mesowear. This

Lea Valley

supports the hypothesis that mesowear is a proxy of grazing


in particular (e.g. Kaiser et al., 2013; Saarinen et al., 2015).

Of the Pleistocene British proboscidean species, M.
meridionalis, P. antiquus and M. trogontherii clearly demon-
strate dietary flexibility, having on average blunter mean




mesowear in more grass-dominated environments. Also the


gomphothere A. arvernensis has significantly blunter mean

mesowear angles in the grass-dominated pre-Pastonian of the
Norwich Crag than in the forested Late Pliocene environment
of the Red Crag.
Table 1. (Continued)

The locality mean mesowear angles of M. meridionalis

range from 115.2 in the molars from Bacton, indicating



mixed feeding, possibly associated with a wooded Pastonian

environment, to 123.2 in the Norwich Crag, indicating grass-

dominated mixed-feeding, associated with relatively open,

grass-dominated pre-Pastonian strata. These results indicate
Copyright # 2016 John Wiley & Sons, Ltd. J. Quaternary Sci., Vol. 31(7) 799808 (2016)

Figure 2. Means comparison of mesowear angles of sympatric proboscidean species in Early and Middle Pleistocene localities from UK by
pairwise Wilcoxon tests. CF-bF Cromer Forest-bed Formation. The mean values for each palaeopopulation are presented as diamonds where the
middle line shows the mean and the upper and lower lines represent 95% confidence limits. Significantly different means are indicated by
P-values above the figure (Supplementary Table S1 for detailed statistics). Estimated dietary composition (grass/browse) is indicated by dashed
lines, based on threshold values obtained from the regression between mesowear angles and the amount of C4 grasses in the diet of tropical
proboscideans (see Saarinen et al., 2015).

considerable plasticity in the diet of M. meridionalis, which is floodplain environment surrounded by boreal woodland,
particularly strongly correlated with local vegetation (high reconstructed for this site (Shotton et al., 1993).
correlation coefficient and low P-value). The pollen records indicate that although showing cranio-
P. antiquus has a browse-dominated mixed-feeding meso- dental adaptations to open habitats and grazing diet,
wear signal in most of the localities, but a more grass- M. trogontherii inhabited a wide range of environments from
dominated mixed-feeding signal in the relatively open, relatively wooded ones to open grasslands. Its diet, despite
savanna-like MIS 7 environment of Ilford. The MIS 11 being more grass-dominated than that of P. antiquus and
populations from Clacton and Swanscombe, and the MIS 5e M. meridionalis, included some browse as well, especially in
populations from Waterhall Farm and Trafalgar Square have the more wooded environments. The mesowear angle values
relatively sharp mean mesowear angles indicating browse- of M. trogontherii range from ca. 119 at Bacton, plausibly
dominated diets, although the angles are slightly blunter, associated with woodland pollen spectra (see above), to 128
perhaps reflecting the locally more open floodplain environ- in the savanna-like environment of Ilford.
ment, at Trafalgar Square (Franks, 1960). The earliest record Interestingly, both M. meridionalis and M. trogontherii
of this species in Britain comes from the early Middle have relatively blunt mesowear angles in the forested but
Pleistocene of the Cromer Forest-bed Formation (Lister, locally open and grassy early Middle Pleistocene palaeoenvir-
2015), and the sample from the vicinity of Happisburgh onment of the West Runton Freshwater Bed, although this has
shows particularly sharp mesowear angles, indicating mostly to be interpreted with caution because each is represented by
browse-based diet. The Happisburgh assemblage of P. only one specimen. The 124 mean mesowear angle of the
antiquus molars was associated with slabs of clay-ironstone West Runton M. meridionalis specimen indicates grass-
which are full of plant macrofossils (Reid, 1899; S. Parfitt, dominated mixed-feeding, whereas the extremely blunt 143
pers. comm.), dominated by leaves, twigs and cones of trees, mean mesowear angle of the famous large male skeleton of
such as Pinus sylvestris, Picea excelsa, Betula alba, Alnus M. trogontherii from West Runton indicates even more
glutinosa, Quercus robur, Fagus sylvatica and Ulmus sp., abrasive, essentially pure grazing diet.
indicating a forested environment (Reid, 1899). This would The woolly mammoth M. primigenius was a grass-
correspond well with the browsing mesowear signal of dominated feeder but even it shows significant variation in its
P. antiquus from the vicinity of Happisburgh. By contrast, the dietary signal, illustrated especially in the steppetundra
early Middle Pleistocene P. antiquus sample from Waverley environment of the Lea Valley, where the mesowear signal
Wood has a blunter mean mesowear signal, suggesting again indicates a significant component of herb or shrub browse in
more mixed feeding diet in the locally open and grassy the diet. Stomach contents from preserved carcasses from

Copyright # 2016 John Wiley & Sons, Ltd. J. Quaternary Sci., Vol. 31(7) 799808 (2016)

Figure 3. Regressions between the mean mesowear angles of all proboscidean species and mean, minimum and maximum Graminae (grass) %
at locality level.

Siberia mostly demonstrate grass-dominated diets but coexist in the same environments. In the Norwich Crag,
some individuals had eaten significant amounts of browse A. arvernensis and M. meridionalis both show a broadly
(herbs, willows and mosses) (van Geel et al., 2008; Willerslev mixed-feeding mesowear signal, but A. arvernensis has a
et al., 2014; Kirillova et al., 2016). Moreover, microwear significantly more browse-dominated signal than M. meridio-
analyses of Alaskan woolly mammoths indicate grass- nalis. A particularly intriguing case is the significantly different
dominated mixed-feeding rather than strictly grazing diet mean mesowear signals of P. antiquus and M. trogontherii in
(Rivals et al., 2010). the locality of Ilford, where these species co-occurred. The
The Cromer Forest-bed elephants provide a good case significantly different mesowear signals of proboscidean
study to evaluate interspecific trophic relationships. In the species within each locality are supported by dental micro-
early Middle Pleistocene, ca. 0.80.6 Ma, P. antiquus and wear results that also suggest dietary niche separation
M. trogontherii dispersed into Western Europe, the former between the species (Rivals et al., 2012, 2015). Comparing
having originated in Africa (Lister, 2015) and the latter in mesowear with more microwear results from British Pleisto-
eastern Asia (Lister et al., 2005). The mesowear results show cene proboscideans (Rivals and Lister, 2016) further shows
significant differences in the mean mesowear angles of these that these proxies mostly give similar results, but there are a
species in the Cromer Forest-bed Formation, so that few cases where the interpretation is different. For example,
P. antiquus shows a browse-dominated, M. trogontherii grass- at Ilford mesowear analysis suggests a relatively more browse-
dominated and M. meridionalis intermediate dietary signals. dominated diet for P. antiquus and a more grass-dominated
This finding supports the suggestion (Lister, 2004) that the diet for M. trogontherii, than do microwear analyses. This
generalized mixed-feeder M. meridionalis could have been could be due to the different temporal resolution of these
outcompeted in more wooded habitats by the more special- methods, as microwear records only the last few days of
ized woodland form with browse-dominated diet (P. anti- feeding by the animal and mesowear represents a more
quus), and in open habitats by a more specialized open averaged dietary signal over several months (Rivals et al.,
habitat form with grass-dominated diet (M. trogontherii). 2007, 2010; M. Fortelius pers. comm.). Thus, these methods
Our findings also indicate dietary niche separation, which can capture a somewhat different dietary signal, especially if
could have allowed proboscidean species to occasionally there is strong seasonal variation in diet (Rivals et al., 2010).

Copyright # 2016 John Wiley & Sons, Ltd. J. Quaternary Sci., Vol. 31(7) 799808 (2016)

Figure 4. Regressions between mean mesowear angles and mean Graminae (grass) % at locality level for Palaeoloxodon antiquus, Mammuthus
meridionalis and Mammuthus trogontherii.

Table 2. Stepwise multiple linear regression modelling of locality retained a component of browse in their diet as well. Our
mean mesowear angles of Proboscidea against mean Graminae %, results indicate that proboscidean mean mesowear angles
mean non-Graminae NAP % and total mean NAP %. AIC Akaikes specifically reflect the abundance of grasses in their
information criterion. Statistically significant correlations are in bold environments, not just general openness of the environ-
ments. This gives additional support to the status of
Parameter P R2 AIC mesowear as a proxy of grazing.
3. Despite the usually high intraspecific variation in mesowear
Mean Graminae % 0.0001 0.88 65 angles, there are also significant differences in mean meso-
Mean non-Graminae NAP % 0.88 0.003 83 wear angles between proboscidean species, which point to
Mean NAP % 0.02 0.51 79 different dietary preferences. These interspecific differences
would have allowed the species to occasionally coexist in
the Pleistocene environments without outcompeting each
Conclusions other, which seems to have been the case, for example, in
Norwich Crag (A. arvernensis and M. meridionalis),
The main findings in this study can be summarized as
West Runton (M. meridionals and M. trogontherii) and
Ilford (M. trogontherii and P. antiquus).
1. Variation in mesowear angles indicates considerable die-
tary plasticity in the proboscidean species from British
Pleistocene localities.
Supplementary Material
2. Mean mesowear angles, both in proboscidean assemblages Appendix S1. Locality information.
and in individual species, reflect local vegetation patterns. Table S1. Wilcoxon test results of the means comparison of
Elephants in particular consumed significant amounts of proboscidean species. Significant P-values are marked in bold
grass when it was abundantly available, but typically type.

Copyright # 2016 John Wiley & Sons, Ltd. J. Quaternary Sci., Vol. 31(7) 799808 (2016)

Acknowledgements. We thank the curators Pip Brewer and Spyr- Kahlke R, Garca N, Kostopoulos DS et al. 2011. Western Palaearctic
idoula Pappa for providing access to the fossil proboscidean palaeoenvironmental conditions during the Early and early Middle
collections of the NHM (London), and David Waterhouse for Pleistocene inferred from large mammal communities, and impli-
providing access to study the West Runton mammoth in the Norwich cations for hominin dispersal in Europe. Quaternary Science
Castle Museum. These people also helped in locating and studying the Reviews 30: 13681395.
specimens. This work was funded by Oskar Huttunen Foundation, Kaiser TM, M uller DWH, Fortelius M et al. 2013. Hypsodonty
Helsinki, Finland, and Jenny and Antti Wihuri Foundation, Helsinki, and tooth facet development in relation to diet and habitat in
Finland. herbivorous ungulates: implications for understanding tooth wear.
Mammal Review 43: 3446.
Abbreviations. AIC, Akaikes information criterion; MIS, Marine Kirillova IV, Argant J, Lapteva EG et al. 2016. The diet and
Isotope Stage; NAP, non-arboreal pollen. environment of mammoths in North-East Russia reconstructed from
the contents of their feces. Quaternary International 406: 147161.
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