Another one bites the dust: faecal silica
levels in large herbivores correlate
with high-crowned teeth
Ju ¨rgen Hummel1,*, Eva Findeisen1, Karl-Heinz Su ¨dekum1,
Irina Ruf2, Thomas M. Kaiser3, Martin Bucher4,
Marcus Clauss5and Daryl Codron5
1Institut fu ¨r Tierwissenschaften, and2Steinmann-Institut fu ¨r Geologie, Mineralogie und Pala ¨ontologie,
Universita ¨t Bonn, 53115 Bonn, Germany
3Biozentrum Grindel und Zoologisches Museum, Universita ¨t Hamburg, Germany
4Zoo Zu ¨rich, Zu ¨rich, Switzerland
5Klinik fu ¨r Zoo-, Heim-, und Wildtiere, Vetsuisse Faculty, Universita ¨t Zu ¨rich, Switzerland
The circumstances of the evolution of hypsodonty (¼ high-crowned teeth) are a bone of contention.
Hypsodonty is usually linked to diet abrasiveness, either from siliceous phytoliths (monocotyledons) or
from grit (dusty environments). However, any empirical quantitative approach testing the relation of
ingested silica and hypsodonty is lacking. In this study, faecal silica content was quantified as acid detergent
insoluble ash and used as proxy for silica ingested by large African herbivores of different digestive types,
feeding strategies and hypsodonty levels. Separate sample sets were used for the dry (n ¼ 15 species)
and wet (n ¼ 13 species) season. Average faecal silica contents were 17–46 g kg21dry matter (DM) for
browsing and 52–163 g kg21DM for grazing herbivores. No difference was detected between the wet
(97.5+14.4 g kg21DM) and dry season (93.5+13.7 g kg21DM) faecal silica. In a phylogenetically
controlled analysis, a strong positive correlation (dry season r ¼ 0.80, p , 0.0005; wet season r ¼ 0.74,
p , 0.005) was found between hypsodonty index and faecal silica levels. While surprisingly our results
do not indicate major seasonal changes in silica ingested, the correlation of faecal silica and hypsodonty
supports a scenario of a dominant role of abrasive silica in the evolution of high-crowned teeth.
Keywords: phytolith; grit; abrasiveness; hypsodonty
Along with the spread of open landscapes and radiation of
grasses during the Cenozoic (probably best documented
for the Miocene), a striking morphological characteristic
of dentitions evolved in different herbivore lineages
[1–3]: hypsodonty, or high-crowned teeth. While the
20 Ma, differences in crown height are also very obvious
(brachydont ¼ low-crowned) [4–6].
It is generally agreed that the ultimate explanation for
hypsodonty is the maintenance of functionality of teeth
under conditions of increased wear . The most
accepted cause of increased wear is a rise of dietary
silica content as a consequence of a higher proportion
of grass in diets and/or foraging in open landscapes,
respectively. Silica is harder than tooth enamel, and there-
fore critical for tooth wear . There are several plant
groups that are known for particularly high silica con-
tents, like liver mosses or horsetails [9,10]. However,
among angiosperms, grasses are best known to be silica
accumulators, while dicots are generally characterized
by lower silica contents. Surprisingly little data are avail-
able from directcomparisons,
to develop nearly
but the difference
between grasses and browse (trees, shrubs, herbs) can
generally be considered substantial: for example, in a
study on East African vegetation, silica contents have
been quantified to be 4.95 per cent dry matter (DM) in
grasses compared with only 0.56–1.46% DM in browse
 or in a sample of alpine plants to be 2.66+1.60
than C3 grasses [13,14].
Principally, dietary silica can occur as characteristic
crystals in plant cell walls (phytoliths), or can be ingested
as dust or contaminations of soil [5,15,16]. But while
much of the discussion on the causes of hypsodonty
focuses on whether phytoliths or grit should be con-
sidered the major abrasive agent (e.g. ), it should
not be forgotten that even for a scenario disregarding
this distinction and simply considering total silica, several
inconsistencies and alternative explanations appear to
exist: for example, if the rise of grasses is considered as
the dominant trigger of hypsodonty, it is surprising that
in the prime example of evolution of hypsodonty (Early
to Middle Miocene of North America), the major rise
of grasses appears to happen much earlier (4 Ma) than
the onset of hypsodonty , described as ‘adaptive lag’
by Janis . Increased tooth wear was also hypothesized
to be caused not only by ingestion of abrasive silica, but
also by higher general occlusal stress in combination
* Author for correspondence (firstname.lastname@example.org).
Proc. R. Soc. B (2011) 278, 1742–1747
Published online 10 November 2010
Received 8 September 2010
Accepted 20 October 2010
This journal is q 2010 The Royal Society
with large quantities of low-quality food  or poten-
tially also higher occlusal stress loads owing to a longer
lifespan , the latter hypothesis being both rejected
 and supported  later on. In addition, looking
at the data of silica contents at the level of individual
plant species, it appears that at least some dicots can
reach fairly high silica levels , like Cucurbitaceae
and Urticales  potentially rendering the ranking of
grass and browse concerning their silica contents less
unequivocal as often perceived. In fact, silica has been
discussed as causing abrasion in dicot diets, too [22,23],
and among hypsodont notoungulates, microwear indi-
cated a browsing feeding style . Once evolved,
hypsodonty appears not to be decreased irrespective of a
later shift to a less abrasive diet , which could imply
a less tight connection of grass diets and hypsodonty
and a generally high benefit/cost ratio of this dental
Several studies have shown hypsodonty to be positively
correlated to grass content of diet [5,25]. By contrast, it
can be stated that while the focus of discussions is already
on the distinction of the significance of different silica
sources (exogenous dust versus endogenous plant phyto-
liths) for abrasiveness of herbivore diets, not even the
relation of total ingested silica (sum of exogenous and
endogenous silica) and hypsodonty has been tested yet
in an empirical, quantitative assay.
A potential approach to tackle this data gap makes use
of the fact that besides its mechanical resistance, a striking
property of silica is its chemical stability and inertness. It
is known to pass through the digestive tract without any
significant degradation or absorption , characteristics
qualifying silica as one of the standard markers in animal
digestibility trials. This also opens the door for an estimate
of tooth wear constraints faced by individual species owing
to ingested silica: faecal silica should reflect ingested silica
(as the sum of phytoliths and exogenous silica), integrating
both diet (e.g. browse or grass) and habitat choice (e.g.
open versus closed), and offering a way to approach the
relation of ingested silica and hypsodonty.
Based on a sample of African herbivores, we tested
how faecal silica levels reflect the degree of hypsodonty
of a species, and to what extent faecal silica levels
change between the wet and dry season.
2. MATERIAL AND METHODS
Faecal samples were collected from 10 ruminants and five
hindgut fermenters (table 1). In general, they were sampled
for the dry and wet season at Kruger National Park, South
Africa, except the two rhino taxa, which were both sampled
at Lewa Wildlife Reserve, Kenya, and only for the dry
season. All faeces were collected fresh shortly after observing
defecation; care was taken not to contaminate samples with
soil. After drying at 608C they were milled through a 1 mm
sieve. Silica content was quantified by using residual ash
after boiling in acid detergent solution as used for acid
detergent fibre (ADF) determination. All silica (biogenic
and dust/soil) is recovered in this fraction (acid detergent
insoluble ash—ADIA) , and according to Van Soest
, the method is considered equivalent or even preferable
to the classical method of acid insoluble ash (AIA) after
Van Keulen & Young . In the following, ADIA values
are referred to as silica values if not explicitly indicated
differently. The fibre bag system (Gerhardt, Ko ¨nigswinter,
Germany) was used for sample analysis.
Hypsodonty indices of the respective species were taken
from the literature (primarily ; if the data of Mendoza &
Palmqvist  differed, the average of both studies was
used). Dietary information for each species was derived
from stable carbon isotope analysis of faeces [30,31].
d13C data from faeces were converted to estimates of the
ratio of C3browse to C4grass in the diet of each sample
using a simple linear mixing model that controls for spatio-
temporal variations in the isotope composition of dietary
baselines (plants) (see  and references therein).
We tested the hypothesis that hypsodonty is reflected in
the silica content of faeces by correlating the hypsodonty
index with the mean silica content of each species. In
the same way, we tested the hypotheses that faecal silica
content reflects proportions of browse and grass in the diet
(estimated %C4grass intake with the mean faecal silica con-
tent ofeach species),and
proportions of browse and grass intake. d13C data were
Table 1. Faecal silica contents of large African herbivores (mean+s.d.; DM, dry matter).
dry seasonwet season
greater kudu (Tragelaphus scriptus)
giraffe (Giraffa camelopardalis)
nyala (Tragelaphus angasi)
impala (Aepyceros melampus)
waterbuck (Kobus ellipsiprymnus)
sable antelope (Hippotragus niger)
roan antelope (Hippotragus equinus)
blue wildebeest (Connochaetes taurinus)
tsessebe (Damaliscus lunatus)
African buffalo (Synceros caffer)
black rhino (Diceros bicornis)
African elephant (Loxodonta africana)
warthog (Phacochoerus aethiopicus)
plains zebra (Equus burchelli)
white rhino (Ceratotherium simum)
Faecal silica and hypsodonty
J. Hummel et al.
Proc. R. Soc. B (2011)
bimodally distributed, and we thus used Spearman’s rank
correlations for the analyses. We controlled for phylogenetic
effects in the analyses by linear regression through the
origin of the independent contrasts of these same variables.
The phylogenetic tree was based on the phylogeny proposed
by Bininda-Emonds et al. , and branch lengths trans-
formed by Pagel’s (1992) method (dry season data) or
Grafen’s r (wet season data). Raw data were analysed with
STATISTICA v. 8.0 , and independent contrasts analysis
with the PDAP module for MESQUITE v. 2.5 [34,35]. In all
tests, dry and wet season data were analysed separately.
For the comparison of wet and dry season data, the
non-parametric Wilcoxon test for matched pairs was used.
Faecal silica values ranged between 20 and 146 g kg21
DM in ruminants and between 17 and 163 g kg21DM
in hindgut fermenters (table 1). Values for browsers
(17–46 g kg21DM) were lower than those of grazers
(52–163 g kg21
DM), with non-overlapping ranges.
There was no overall difference in faecal silica contents
between the dry and wet season (dry season: 93.5+
13.7 g kg21DM; wet season 97.5+14.4 g kg21DM;
p ¼ 0.639) for all species, and also the exclusion of
resulted in no significant difference (dry season: 111+
36.0 g kg21DM; wet season 107+42.0 g kg21DM;
p ¼ 0.297).
As predicted, hypsodonty increased across species with
increasing C4intake, and with increasing faecal silica con-
tent (figure 1). These relationships were consistently
significant in both seasons (although slightly more pro-
nounced in the dry season), and were evident in raw
data and the independent contrasts (table 2). For the
phylogenetically controlled analysis, faecal silica content
faecal silica content (g kg–1 DM)
Figure 1. Correlation of faecal silica level and hypsodonty index  in large African herbivores (dry season: n ¼ 15, r ¼ 0.80,
p , 0.0005; wet season: n ¼ 13, r ¼ 0.74, p , 0.005; phylogenetically controlled analysis 1, greater kudu; 2, giraffe; 3, nyala; 4,
impala; 5, waterbuck; 6, sable antelope; 7, roan antelope; 8, blue wildebeest; 9, tsessebe; 10, African buffalo; 11, black rhino;
12, African elephant; 13, warthog; 14, plains zebra; 15, white rhino). Filled squares, dry season; open triangles, wet season.
Table 2. Correlation analyses of relationships between faecal silica content and hypsodonty (hypsodonty index HI) and %C4
grass in the diet and between %C4grass in diet and hypsodonty. rs, Spearman’s correlation coefficient; rp, Pearson’s product-
moment correlation coefficient; %C4in diet are data derived from d13C of faeces [30,31]; HI, hypsodonty index (,
combined with ).
analysis of raw dataindependent contrasts analysis
faecal silica, HIdry
%C4in diet, faecal silica 11
%C4in diet, HI11
1744 J. Hummel et al. Faecal silica and hypsodonty
Proc. R. Soc. B (2011)
also was positively correlated to C4grass in the diet in
both dry and wet season data (table 2).
Dietary silica is considered to exhibit negative effects on
herbivores ; the mechanisms are discussed to work
on several levels like diet digestibility [37,38], diet prefer-
ence [39,40], bite rate  and even the development of
pathological conditions like urolithiasis ; however, the
negative effect of ingested silica (phytoliths plus dust and
grit) is most renowned for a corresponding increase in
diet abrasiveness (e.g. [5,8,42]). It is generally believed
that tooth wear and dental abnormalities are important
factors limiting the lifespan, the reproductive success
and the body condition of free-ranging wild animals
, although actual studies documenting this are still
limited in number [20,44–50]. The effect of grit on
tooth wear in vivo has, so far, only been investigated
once in several populations of Australian sheep, in
which tooth wear on incisors was a direct function of
the amount of soil ingested , while laboratory
approaches also found evidence for the abrasive effect of
plants rich in phytoliths [39,52].
(a) Correlation between faecal silica content
Browsing or grazing feeding style was well reflected by
faecal silica content in this study, on an overall species
basis as well as when comparing browsing and grazing
rhinos or ruminants like African buffalo and giraffe.
The major goal of this study was to quantitatively
approach the hypothesis of a direct correspondence
between silica content (¼ abrasiveness) of the ingested
material and the incidence of hypsodonty. We can state
that the relation of hypsodonty and silica content was
almost more obvious than we anticipated. The significant
positive correlation between these traits was true for both
seasons, and these results imply a considerable influence
of ingested silica on hypsodonty.
A limited number of studies have reported faecal silica
values of wild herbivores (table 3), and a small dataset of
five North American ruminants  can be used as a
control of the results of our study: In fact, these data
are in accordance with our results since the hypsodonty
index ranking of the five ruminant taxa is identical with
that of faecal silica.
Obviously, we have to acknowledge that our data
cannot totally exclude a contribution of other parti-
cularities of grasses (like higher occlusal forces) to the
development of high-crowned teeth; however, our pre-
ferred and most likely interpretation is that of a causal
relation of ingested silica levels, abrasiveness of ingested
material and hypsodonty.
(b) Influence of diet digestibility
When using faecal silica as a proxy for ingested silica, DM
digestibility of the ingested diets could potentially inter-
fere with faecal silica as a direct indicator of ingested
silica, via different ‘dilution’ levels by indigestible
material. This would translate in an overestimation of
silica in more digestible, and the opposite in less digestible
samples. When a lower DM digestibility of average
browse compared with grass is assumed , e.g. 45
per cent for browse and 60 per cent for grass, correcting
the average ruminant browser (28 g kg21DM) and
grazer (115 g kg21DM) faecal silica value mathematically
to an intermediate digestibility level results in values of
32 g kg21DM (browser) versus 97 g kg21DM (grazer),
and even when assuming the most extreme imaginable
difference in DM digestibility (40% for browsers versus
70% for grazers), a correction still results in values of
37 g kg21versus 77 g kg21DM of faecal silica in browsers
versus grazers. While any interpretation of the values
should keep in mind that it is concentrations and not
amounts that are actually measured, it can be safely con-
cluded that differences of the magnitude measured here
will hold true irrespective of any realistic difference in
(c) Seasonal differences
Two major effects may influence ingested silica amounts
in the dry season: first, the amount of browse in the
diets of opportunistic feeders will increase, particularly
in diets of mixed feeders, which should lead to an overall
decrease in faecal silica in these taxa. Second, the amount
Table 3. Faecal silica contents reported in literature; hypsodonty index (HI) according to Janis  (DM, dry matter; AIA,
silica content (% DM)HI method reference
bighorn sheep (area 1)
bighorn sheep (area 2)
May–July: 20–30, rest of year: ,4
May–July: ?7–10, rest of year: negligible
aAccording to Jones & Milne .
Faecal silica and hypsodonty
J. Hummel et al.
Proc. R. Soc. B (2011)
of exogenous grit/dust is intuitively assumed to increase,
leading to a general increase in faecal silica levels. In a
study on the influence of overall rainfall on abrasion,
using mesowear as a measure (the latter resulting from
the combination of wear owing to abrasion ¼ tooth–
food contacts and attrition ¼ tooth–tooth contacts),
Kaiser & Ro ¨ssner  were able to show that in the
Miocene of Southern Germany, ruminants with teeth
suggesting a browsing diet in a humid wetland environ-
ment had less abrasion-dominated mesowear signatures
than contemporaneous communities from adjacent drier
karst environments. Climate proxy studies by Kaiser &
Schulz  indicate that this relationship also applies to
zebra habitats in sub-Saharan Africa, where plains
zebras (Equus quagga) from dryer habitats had a more
abrasion-dominated mesowear signal than the same
species in more humid environments. In contrast, in a
study on the influence of different environmental factors
on hypsodonty, no influence of climate (wet, mesic or
arid) on this trait was found in a sample of 57 mainly
African ungulates .
Overall, our data do not imply a significant general
increase in silica load during the dry season. The fact
that even considering grazers only did not lead to a signifi-
cant relation supports a view of a less than expected effect
of changes in rainfall over the seasons on abrasiveness of
diets. Other factors, such as grit transport by wind, cover,
land erosion and the type of soil will probably have a
higher influence on the abrasiveness of plants owing to
grit than changes of the seasons.
The occurrence of hypsodonty through time can be
regarded as one of the most disputed and fascinating
chapters of herbivore evolution. The strong quantitative
support of the view of hypsodonty as a signal of ingested
silica, and hence abrasiveness, is therefore the major
implication and result of this study. While in our data
the sum of all silicates was quantified, the elucidation of
the contribution of biogenic and external silica to overall
intake and the abrasive effect of the respective proportion
should be in the focus of future studies.
Foundation, SU 124/16-1) and is publication no. 23 of the
DFG Research Unit 771 ‘Function and enhanced efficiency
in the mammalian dentition—phylogenetic and ontogenetic
impact on the masticatory apparatus’. We would like to
thank the initiator of this research unit Wighart von
Koenigswald for sharing his dedicated enthusiasm for the
wonders of teeth with us and for proofreading an earlier
version of this manuscript. Lewa Wildlife Reserve, Kenya, is
thanked for providing the rhino samples for this study.
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