Corrigendum: The influence of habitat on body size and tooth wear in Scottish red deer (Cervuselaphus)

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ARTICLE
The influence of habitat on body size and tooth wear in
Scottish red deer (Cervus elaphus)
F.J. Pérez-Barbería, S.L. Ramsay, R.J. Hooper, E. Pérez-Fernández, A.H.J. Robertson, A. Aldezabal,
P. Goddard, and I.J. Gordon
Abstract: Body size has profound implications for ecology and life-history traits of mammalian species. Tooth wear is an
indicator of food-processing investment and diet properties, with fitness consequences through differences in comminution
efficiency, nutrient gain, and senescence. We investigate the relationships between mandible length (a proxy of skeletal body
size), molar dentine thickness (a measure of tooth wear), and faecal neutral detergent fibre with residual ash (NDF–ash, a
combined proxy of fibre and mineral components in the diet) in 874 male and female red deer (Cervus elaphus L., 1758) from
21 locations in moorland and woodland habitats across Scotland. Significant differences in mandible length occurred between
habitats: woodland deer having larger mandibles than moorland deer. Within habitats, larger mandibles were related to higher
rates of dentine wear, suggesting increased body size was associated with greater intake and processing of food. Both dentine
wear and faecal NDF–ash were higher in moorland deer than in woodland deer, suggesting that fibre and (or) mineral abrasives
in the diet may have contributed towards habitat differences in dentine wear. Between habitats, higher dentine wear was not
associated with larger mandibles, in contrast to the relationship within habitats, indicating the precedence of additional
environmental factors between habitats.
Key words: age, Cervus elaphus, diet, faecal ash, faecal fibre, moorland, red deer, senescence, tooth wear, woodland.
Résumé : La taille du corps est étroitement liée a
`l’écologie et aux caractéristiques du cycle biologique des espèces de mam-
mifères. L’usure des dents est un indicateur de l’investissement dans la transformation de la nourriture et des propriétés du
régime alimentaire, avec des conséquences associées a
`l’aptitude découlant de variations de l’efficacité de la comminution, des
gains en nutriments et de la sénescence. Nous avons examiné les liens entre la longueur de la mandibule (une variable
substitutive de la taille du squelette du corps), l’épaisseur de la dentine des molaires (une mesure de l’usure des dents) et la
concentration de fibres au détergent neutre avec cendres résiduelles dans les fèces (NDF–ash, une variable substitutive combinée
des contenus en fibres et en minéraux de l’alimentation) chez 874 cerfs élaphes (Cervus elaphus L., 1758) mâles et femelles de
21 emplacements dans des habitats marécageux et forestiers a
`la grandeur de l’Écosse. Des différences significatives de la
longueur de la mandibule ont été relevées entre les différents habitats, les cerfs des forêts ayant des mandibules plus grandes que
les cerfs de milieux marécageux. Au d’habitats semblables, des mandibules plus grandes étaient associées a
`de plus hauts taux
d’usure de la dentine, donnant a
`penser qu’une plus grande taille du corps serait associée a
`une ingestion et une transformation
de nourriture plus importantes. L’usure de la dentine et le NDF–ash dans les fèces étaient tous deux plus élevés chez les cerfs
d’habitats marécageux que chez ceux d’habitats forestiers, donnant a
`penser que les abrasifs fibreux et (ou) minéraux dans
l’alimentation pourraient en partie expliquer les variations d’usure de la dentine entre habitats. Entre les habitats, une plus
grande usure de la dentine n’était pas associée a
`des mandibules plus grandes, contrairement a
`la relation observée au sein
d’habitats semblables, indiquant des effets plus importants d’autres facteurs ambiants sur les différences entre habitats. [Traduit
par la Rédaction]
Mots-clés : âge, Cervus elaphus, régime alimentaire, cendres dans les fèces, fibres dans les fèces, milieu marécageux, cerf élaphe,
sénescence, usure des dents, milieu forestier.
Introduction
In mammalian herbivores, the rate of food intake and efficiency
of nutrient release from forage are determined by characteristics
of the plant material consumed and the animals’ feeding and
processing apparatus (Robbins 1993;Pérez-Barbería and Gordon
1998a). In different habitats, the interaction between these intrin-
sic and extrinsic factors, together with variation in an individual’s
energy demand, can result in variation in somatic growth and
condition and there is a plethora of evidence that body size is
strongly related to reproductive success and other life-history
traits (Clutton-Brock et al. 1982;Peters 1983), which underlie indi-
vidual performance and population dynamics. For herbivores,
mastication is a key element in utilising the nutrients from in-
gested forage (Poppi et al. 1980;Pond et al. 1984;Pérez-Barbería
and Gordon 1998a); therefore, reported biometric differences be-
tween herbivore populations occupying different habitats may be
reflected in patterns of tooth wear.
Tooth wear is caused by attrition (tooth–tooth contact) and
abrasion (tooth–food contact) (Lucas 2004). In ruminants, the rate
Received 6 June 2014. Accepted 12 November 2014.
F.J. Pérez-Barbería, S.L. Ramsay, R.J. Hooper, E. Pérez-Fernández, A.H.J. Robertson, P. Goddard, and I.J. Gordon. James Hutton Institute,
Craigiebuckler, AB15 8QH, Aberdeen, Scotland, UK.
A. Aldezabal. Landare Biologia eta Ekologia Saila, Zientzia eta Teknologia Fakultatea, Euskal Herriko Unibertsitatea (UPV–EHU), 644 p.k., 48080 Bilbo
(Bizkaia), Euskal Herria, Spain.
Corresponding author: F.J. Pérez-Barbería (e-mail: javier.perez-barberia@hutton.ac.uk).
61
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of tooth wear is mainly determined by two factors. The first factor
is how much time the animal invests in chewing and ruminating,
which is directly related to the quality and volume of food ingested.
Diets of lower nutritional quality will require the consumption of
greater volumes of food (Robbins 1993), necessitating more chewing
and concomitant exposure to dental wear (Pérez-Barbería and
Gordon 1998a). In this context, there is often an implicit assumption
that (i) increased fibre content is negatively associated with diet qual-
ity or nutritional value (Robbins 1993) and (ii) diet quality and fibre
content will decrease and increase, respectively, as one moves from a
browse-dominated to a graze-dominated diet (Pérez-Barbería and
Gordon 2001;Pérez-Barbería et al. 2001); both assumptions, however,
are oversimplifications that may not always hold true (Codron et al.
2007;Clauss and Dierenfeld 2008;Clauss et al. 2010;Damuth and
Janis 2011).
The second factor concerns the wear-inducing properties of the
material ingested, which is related to either intrinsic properties of
the forage itself (such as the presence of hard silica phytoliths) or
to extrinsic material ingested simultaneously (such as soil or dust)
(Mayland et al. 1975;van Soest 1994;Williams and Kay 2001;
Massey and Hartley 2006;Damuth and Janis 2011;Strömberg 2011;
Jardine et al. 2012;Kaiser et al. 2013). While most recent studies
concerning the evolution of hypsodonty have tended to focus on
the relative importance for tooth wear of intrinsic abrasive silica
in grasses versus increased extrinsic abrasive material in more
open, drier habitats (Mayland et al. 1975;van Soest 1994;Williams
and Kay 2001;Massey and Hartley 2006;Damuth and Janis 2011;
Hummel et al. 2011;Strömberg 2011;Jardine et al. 2012;Kaiser
et al. 2013), ecological studies of tooth-wear variation in extant
ungulates have often emphasised supposed differences in plant-
tissue properties, with the suggestion that increasing fibre con-
tent results in increased tooth wear (e.g., Veiberg et al. 2007a).
Although fibre itself is not sufficiently hard to directly abrade
tooth enamel, it can increase plant-tissue toughness, such that
higher occlusal forces and greater mastication time are needed to
process forage (Pérez-Barbería and Gordon 1998a,1999), poten-
tially increasing attrition and the impact of any abrasive particles
present (Damuth and Janis 2011).
Worn teeth may reduce comminution efficiency (Pérez-Barbería
and Gordon 1998a,1998b), reducing the nutritional gain from in-
gested forage (Skogland 1988;Kojola et al. 1998). Indeed, loss of
function in the molar teeth associated with excessive wear is a
potential proximate ecological mechanism of senescence in rumi-
nants (Skogland 1988;Gaillard et al. 1993;Kojola et al. 1998;
Ericsson and Wallin 2001;Loe et al. 2003;Carranza et al. 2004;
Nussey et al. 2007;Ozaki et al. 2010). Senescence has been docu-
mented in many wild ungulates (Gaillard et al. 1993;Bérubé et al.
1999;Loison et al. 1999;Mysterud et al. 2001;Nussey et al. 2006;
Nussey et al. 2011) and significant correlations have been demon-
strated between molar height (an indicator of tooth wear) and life
expectancy (Carranza et al. 2004;Ozaki et al. 2010).
In Scotland, red deer (Cervus elaphus L., 1758) occupy a number of
different habitats, but the most contrasting and abundant are
woodland and moorland (Watson and Staines 1978;Clutton-Brock
and Albon 1989;Hester et al. 1999;Pérez-Barbería et al. 2013). Red
deer resident in woodland are often considered to show faster
rates of early development, greater adult masses, larger antlers,
and greater reproductive output than those on moorland (Mitchell
et al. 1977;Clutton-Brock and Albon 1989). However, rigorous com-
parisons of these variables between populations that occur in
these habitats are somewhat lacking; data for different habitats
often coming from independent studies with different sampling
methodologies.
Differences in tooth wear between such contrasting habitats
can result from a nonexclusive combination of two factors: (1) her-
bivores have to eat more in one habitat than the other, either due
to greater energy demands or due to reduced energy or nutrient
density of the diet, and (or) (2) diets differ in their wear-inducing
properties between habitats.
There is evidence that woodland provides shelter from expo-
sure to wind (Staines 1976;Wood 1988;Irvine et al. 2009), whereas
moorland is an open habitat, more exposed to the weather, with
little shelter available (Duncan et al. 2001). Therefore, we might
expect greater food intake, and so higher tooth wear, in deer that
occur in moorland than in woodland to compensate for increased
thermoregulatory energy costs. Alternatively, reduced diet qual-
ity in one habitat may result in increased intake levels, while
differences in the wear-inducing properties of the diet between
habitats may also influence rates of tooth wear.
In this paper, we examine the relationships between body size,
sex, tooth wear, and dietary fibre with residual ash in two con-
trasting habitats (moorland and woodland) across Scotland. We
test whether red deer are larger in woodland than in moorland
and whether this is directly associated with differing rates of
tooth wear that may indicate differences in rates of food intake
and dietary quality.
Materials and methods
We analysed the mandibles of 874 Scottish red deer (males and
females) that were shot in 10 moorland locations (n= 450) and
11 woodland areas (n= 424), representing two contrasting habitats
across the red deer distribution range in Scotland between 2006
and 2010 (Table 1,Fig. 1). Locations were sufficiently spatially sep-
arated to be considered independent for analysis purposes, and
GIS analysis of cull location data and vegetation spatial coverage
data at each location confirmed the assigned habitat category to
be the predominant habitat type for deer culled there. Woodland
habitat in Scotland predominantly comprises mixed coniferous
plantations (mainly exotic species such as Sitka spruce, Picea
sitchensis (Bong.) Carrière, and Douglas-fir, Pseudotsuga menziesii
(Mirb.) Franco) and a smaller proportion of seminatural woodlands;
understories may typically comprise grasses, forbs, and heaths such
as common heather (Calluna vulgaris (L.) Hull) and species of the genus
Vaccinium L. Moorland is generally dominated by a mosaic of heath
(principally C. vulgaris, but also other heather (genus Erica L.) species
and blaeberry (Vaccinium myrtilus L.)) and grass.
All the samples came from deer shot during sport hunting ac-
tivities on private estates or from the legal culling operations of
the Forestry Commission for Scotland to reduce deer numbers in
woodland areas. The mandibles were extracted by the stalkers at
the shooting site or in the associated game larder and kept frozen
or left outdoors, for the flesh to decompose, until they were col-
lected and transported to the laboratory. Shooting date, sex, car-
cass mass (i.e., body mass minus head, internal organs, genitals,
udders, fore- and hind legs, and bleedable blood) and location (at
the moorland estate or at the Forestry Commission larder) of each
animal were also recorded by the stalker. Information on deer
densities was generally not available or, when it was available,
was not comparable across locations and consequently could not
be included in the analysis.
Body size and age estimation
Once in the laboratory, the length of the mandible (±1 mm) was
measured (from the mesial border of the first incisor socket to
the vertical part of the ramus, after removal of any flesh from the
two points) as a proxy of skeletal animal size independent of sea-
sonal changes in body mass (Blant and Gaillard 2004). To estimate
age and tooth wear (see Tooth wear), mandibles were sectioned
through a frontal plane between the paraconid and the metaconid
of the first permanent molar M
1
using a Labotrom circular dia-
mond saw fitted with a water cooling system and an especially
modified clamp (Struers Labotrom, http://www.struers.com). The
age (in years) was estimated by counting the cement layers on the
root pad of the M
1
mesial section, aided by a reflected light micro-
scope at magnification × 20 to × 25 (Mitchell 1963,1967). We used
62 Can. J. Zool. Vol. 93, 2015
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only samples from deer older than 2 years of age because tooth
wear on the occlusal surface of M
1
is negligible in younger age
classes. The maximum age found was 16 years in females and
15 years in males (Table 1); samples from animals older than
12 years old were also removed because the numbers were small
and unbalanced between sexes.
Tooth wear
Tooth wear was estimated by measuring, with the aid of a cal-
liper (±0.1 mm) and a magnifying glass, the dentine thickness on
the M
1
mesial section after having sectioned the mandible, from
the top of the cementum of the radicular pad to the middle point
of the sectioned crown (Fig. 2). If the middle point of the crown
coincided with the infundibulum, then the middle point was the
occlusal surface of the infundibulum and not its bottom, as this
would underestimate the thickness of the dentine (Carranza et al.
2008). The thinner the layer of dentine, the more worn the tooth
is, and we assumed that this measurement would be representa-
tive of the overall wear of all cheek teeth of the animal (Lowe 1967;
Veiberg et al. 2007c). However, dentine thickness is dependent
of the size of the tooth. To ensure that our response variable is
strictly a measure of tooth wear, we included in the model a
tooth-size covariate, the width of the M
1
taken across its frontal
plane. This measurement is hardly affected by tooth wear within
the age range used in this study.
Dentine thickness was also determined for an additional sam-
ple of mandibles taken from deer aged <2 years to check for any
difference in the initial emerged height of unworn molars be-
tween habitats.
Faecal fibre with residual ash
We estimated the neutral detergent fibre with residual ash
(NDF–ash) content in 379 samples of hinds (Hummel et al. 2011).
Faecal material was collected from the rectum of the carcass and
kept frozen until transported to the laboratory, where it was dried
and milled toa1mmsieve. NDF–ash content was estimated using
near-infrared (NIR) spectroscopy (Foley et al. 1998;Landau et al.
2006). NIR spectra were recorded of all samples on a FOSS NIRS
5000 spectrometer. A calibration equation was developed using
the spectra of 139 of the samples for which NDF–ash had been
determined by wet chemistry (van Soest and Wine 1967). The NDF–
ash values for the remaining samples were then predicted using
this equation.
Statistical analysis
We used linear mixed-effects models to explore the response of
dentine thickness and NDF–ash to a number of predictors and
control for some sources of variation. Normality and homoscedas-
ticity were verified and identification of outliers carried out by a
preliminary inspection of density plots and quantile–quantile
plots of models of dentine thickness, molar width, mandible
length, and NDF–ash against age, with any extreme outliers re-
moved.
The full linear mixed-effects model on mandible length at-
tempted to fit two random effects (the intercepts of location and
year shot, the latter to account for any cohort effect) and five fixed
effects, namely, molar width, age
2
, sex, habitat (moorland and
woodland), and dentine thickness, as well as their meaningful
interactions. Age was fitted as a quadratic term, rather than using
nonlinear or splines functions, because linear models are pre-
ferred when testing for interactions (McCullagh and Nelder 1989).
Another similar model was fitted using dentine thickness as the
response variable and molar width, age
2
, sex, and habitat, as well
as their interactions, as fixed effects.
The full linear mixed-effects model on faecal NDF–ash fitted
two random effects (the intercepts of location and year shot),
three fixed effects (age
2
, day of year shot, and habitat), and their
meaningful interactions. Only data from females were used in
this analysis, as the data for males were very unbalanced between
season and habitat, making both effects confounded. Fibre con-
tent in plants in temperate climates has a seasonal pattern, fol-
lowing a sinusoidal curve across the year, with a peak in winter
and a minimum in early summer (Grant et al. 1978;Milne et al.
1979;Pérez-Barbería et al. 1997). To capture this seasonal pattern,
we fitted two complementary circular functions of the day of year
(DOY; day 0 = 1st of May) in which the animal was shot (sine DOY,
cosine DOY). Due to the small number of sites (n= 21), there was no
attempt to build any spatial structure into the model.
Despite the recent controversy surrounding the use of pvalues
in model selection in favour of measures such as the difference
Table 1. Number of red deer (Cervus elaphus) by habitat, sex, and age used in this study for the analysis of dentine thickness (DT) and faecal neutral
detergent fibre with residual ash (NDF–ash), which are reported in the table as DT/NDF–ash.
Age (years) Sex 2 3 4 5 6 7 8 9 10 11 12 Total
Woodland Female 70/72 41/48 36/33 21/23 9/9 8/11 14/16 3/3 6/13 5/6 6/8 219/242
Male 73/0 57/0 29/0 14/0 12/0 7/0 4/0 3/0 2/0 2/0 2/0 205/0
Moorland Female 34/32 28/22 28/20 14/11 16/14 13/11 16/11 8/2 4/5 7/4 5/5 173/137
Male 7/0 8/0 23/00 45/0 59/0 41/0 36/0 30/0 13/0 8/0 7/0 277/0
Note: The same animals were used for the DT and NDF–ash analyses, but NDF–ash samples were not available for males. Samples younger than 2 years old and older
than 12 years old have been excluded from the analysis (see the Materials and methods).
Fig. 1. Distribution across Scotland of locations of the woodland
and moorland red deer (Cervus elaphus) used in this study.
1
8
2
7
4
9
6
5
3
19
17
15
20
14
12
18
10
21
16
13
11
200000 300000 400000
600000 700000 800000 900000
2°W3°W4°W5°W6°W
58°N
57°N56°N55°N
050km
Key
Woodland
Moorland
Red deer
distribution
Pérez-Barbería et al. 63
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in Akaike’s information criterion values (⌬AIC) or Bayesian infor-
mation criterion (BIC), their use has been clarified recently
(Murtaugh 2014). Because our objective was to identify the main
drivers of our dependent variables, rather than create predictive
models, we correctly used pvalues to define our final models in
favour of ⌬AIC or BIC approaches. We proceeded by first fitting
full models, as described above, and then using backward elimi-
nation we removed the nonsignificant fixed-effects terms one at a
time following the principle of marginality: the highest order
interactions were tested first and if they were significant, then the
lower order effects were not tested for significance.
The coefficients of the final model were calculated using REML,
as the estimates are more accurate than using maximum likeli-
hood (Nakagawa and Schielzeth 2012). As in linear mixed-effects
models, determining the “correct” value of degrees of freedom
in the estimate of the coefficients is meaningless (Baayen et al.
2008;Nakagawa and Schielzeth 2012); consequently, we used
Satterthwaite’s degrees of freedom approximation. The variance
explained by the model was represented as R
2
marginal (variance
accounted for by the fixed effects; R
2LMM(m)
) and R
2
conditional
(variance accounted for by random and fixed effects; R
2LMM(c)
),
following a method developed for linear mixed-effects models
(Nakagawa and Schielzeth 2012). All analyses and graphics were
conducted in R software (R Development Core Team 2012), mainly
using lme4 (Bates et al. 2013) and lmerTest (Kuznetsova et al. 2013)
packages.
Results
Mandible length
A mixed linear model on mandible length that included molar
width, quadratic age, sex, habitat, and dentine thickness as fixed
effects indicated that males had longer mandibles than females in
both habitats, and moorland deer had significantly shorter man-
dibles than woodland deer after having controlled for age. Within
habitat, males and females with less dentine thickness had longer
mandibles (Table 2,Fig. 3). The fixed effects explained 42% of the
variance of the data (R
2LMM(m)
;Table 2) and the total variance
explained by fixed effects and the random effects location and
year was 50% (R
2LMM(c)
;Table 2).
Dentine thickness
The fixed effects of the final model included molar width, qua-
dratic age, sex, and habitat, as well as the interaction between age
and sex (Table 3). Dentine thickness decreased with age in a qua-
dratic fashion in both sexes, but in females the rate of tooth wear
attenuated more strongly with age, whereas in males the rate of
Fig. 2. Section of the first lower molar of a red deer (Cervus elaphus), as well as dentine thickness (DT; a proxy of dental wear) as it was
measured in this study.
Table 2. Coefficients of the linear mixed-effects model on mandible
length (cm), which is a proxy of skeletal body size, for red deer (Cervus
elaphus).
Variance SD
Random effects
Location (intercept) 0.1307 0.3615
Year (intercept) 0.0034 0.0582
Residual 0.9108 0.9543
Estimate SE tp
Fixed effects
Intercept 23.338 0.6265 37.25 <0.0001
Molar width 0.122 0.0506 2.42 0.016
Age 0.469 0.0607 7.73 <0.0001
Age
2
−0.026 0.0044 −5.87 <0.0001
Sex (male) 1.293 0.0710 18.22 <0.0001
Habitat (moorland) −0.589 0.1830 −3.22 0.005
Dentine thickness −0.065 0.0223 −2.89 0.004
R
2LMM(m)
0.4243
R
2LMM(c)
0.4965
Note: R
2LMM(m)
is the R
2
marginal (variance account for the fixed effects);
R
2LMM(c)
is the R
2
conditional (variance account for random and fixed effects).
Molar width is a proxy of molar size. Woodland is the reference level in habitat.
64 Can. J. Zool. Vol. 93, 2015
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dentine wear continued at a more similar rate across all age
classes (Table 3,Fig. 4). Moorland deer of both sexes had thinner
dentine than woodland deer (Table 3,Fig. 4). The fixed effects of
the final model explained 67% of the variance of the data
(R
2LMM(m)
;Table 3) and the total variance explained by fixed effects
and the random effect location was 68% (R
2LMM(c)
;Table 3).
To check for any difference between habitats in the initial
emerged height of unworn molars, we examined molars from an
additional sample of animals younger than 2 years. This model
failed to show any habitat difference in molar height in deer
younger than 2 years old (habitat coefficient of the model: moor-
land = –0.3715; highest posterior density (HPD) 95% lower = –1.252;
HPD 95% upper = 0.5282; p
Markov chain Monte Carlo
= 0.3978).
Faecal NDF with residual ash content
The final model for faecal NDF–ash included sine DOY and co-
sine DOY, quadratic age and habitat with no significant interac-
tions between fixed effects (Table 4). Faecal NDF–ash content
varied seasonally across the year (Table 4), with the highest and
lowest values of faecal NDF–ash content occurring around the end
of January (woodland = 69.3%; moorland 72.7%) and September
(woodland = 59.2%; moorland = 62.5%), respectively (Table 4,
Fig. 5a). NDF–ash increased with age, reaching a maximum at
6 years of age in both habitats, and then decreasing (Table 4,
Fig. 5b). Moorland hinds had higher values of NDF–ash than wood-
land hinds (approximately 3%; Table 4). The fixed effects of the
model explained 31% of the variance of the data, and 58% when
fitted in conjunction with the random effects location and year
(Table 4).
Discussion
We found that woodland deer had larger mandibles than moor-
land deer and, within habitats, larger mandibles were related to
higher rates of dentine wear. Rates of dentine wear and faecal
NDF–ash were higher in moorland deer than in woodland deer.
Dentine thickness decreased with age in both sexes, but in fe-
males, the rate of tooth wear attenuated more strongly with age.
Differences in body size between habitats
Mitchell et al. (1977), based on studies by Mitchell (1969) and
Whitehead (1964), reported that woodland deer in Scotland show
Fig. 3. Predictions of the response of mandible length (an index of skeletal body size) against dentine thickness of the first lower molar
(a proxy of tooth wear) for male and female moorland and woodland red deer (Cervus elaphus) using the model in Table 2. Age and molar width
were fixed to their mean values. Figure appears in colour on the Web.
Table 3. Coefficients of linear mixed-effects model on dentine thick-
ness of the first lower molar, which is a proxy of tooth wear, for male
and female red deer (Cervus elaphus).
Variance SD
Random effects
Location (intercept) 0.1044 0.3231
Year (intercept) 0.0736 0.2713
Residual 2.0887 1.4452
Estimate SE tp
Fixed effects
Intercept 10.057 0.9020 11.15 <0.0001
Molar width 0.410 0.0743 5.52 <0.0001
Age −1.195 0.1182 −10.11 <0.0001
Age
2
0.041 0.0094 4.36 <0.0002
Sex (male) −1.045 0.4307 −2.43 0.016
Habitat (moorland) −0.654 0.2037 −3.21 0.004
Age × sex (male) 0.414 0.1629 2.54 0.011
Age
2
× sex (male) −0.03053 0.012948 −2.358 0.019
R
2LMM(m)
0.6658
R
2LMM(c)
0.6817
Note: R
2LMM(m)
is the R
2
marginal (variance account for the fixed effects);
R
2LMM(c)
is the R
2
conditional (variance account for random and fixed effects).
Molar width is a proxy of molar size. Woodland is the reference level in habitat.
Pérez-Barbería et al. 65
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greater rates of growth, higher adult masses, and larger antlers
than those on open moorland. However, they recognised the lim-
itation of their study, as there were few detailed comparisons
between habitats due to lack of comparable published data and
differences in sampling methodology. Our study corroborates
that red deer occupying moorland habitat are, on average, skele-
tally smaller (based on mandible length) than those from a wood-
land habitat. In addition, besides confirming the known sexual
dimorphism of red deer, with males being significantly larger
than females, our findings show that habitat differences in skele-
tal size occur similarly in both sexes.
Mitchell et al. (1977) hypothesised that the most likely cause of
such differences in deer body mass between habitats is that wood-
land is less exposed to harsh weather and, consequently, wood-
land deer are subjected to less thermal stress than moorland deer.
A not incompatible alternative explanation is that the nutritional
quality, or available energy density, of the diet may be lower in
moorland. In both cases, deer on moorland would have to employ
a compensatory increase in their dietary intake to maintain a
similar body size to woodland populations; the observation that
moorland deer are skeletally smaller than woodland deer indi-
cates that they either do not increase their intake or do not in-
crease it sufficiently to fully compensate.
Differences in tooth wear between habitats
Dentine thickness of the M1 molar was found to be significantly
greater in woodland deer than those occupying moorlands, sug-
gesting increased tooth wear in moorland deer. This observation
is supportive of the hypothesis above that deer in moorland have
to increase their dietary intake, relative to those in woodland,
either due to greater energy demands or reduced energy or nutri-
ent density of the diet. An alternative, but compatible, explana-
tion is that diets differ in their wear-inducing properties between
habitats.
For Scottish red deer, in woodland and moorland, graminoids
(principally grass species) and heaths (dominated by C. vulgaris
with some Vaccinium spp.) generally constitute the major part of
the diet, with grasses dominating in summer and their contribu-
tion declining in winter (Staines 1977;Mitchell et al. 1977;Osborne
1984;Clutton-Brock and Albon 1989;Gordon 1989a,1989b,1989c).
However, forbs and tree browse may also make a significant dietary
contribution in forest-dwelling populations, with a concomitant
Fig. 4. Predictions of the response of dentine thickness of the first lower molar against age for male and female moorland and woodland red
deer (Cervus elaphus) using the model in Table 3. Molar width was fixed to its mean value. Age was estimated in years, but to improve
readability, symbols of different age classes have been moved across the xaxis by +0.3 years per class. Figure appears in colour on the Web.
Table 4. Coefficients of linear mixed-effects model on faecal neutral
detergent fibre with residual ash, which is a proxy of the toughness
and abrasiveness of the diet, for female red deer (Cervus elaphus).
Variance SD
Random effects
Location (intercept) 6.3359 2.5171
Year (intercept) 0.5004 0.7074
Residual 10.0901 3.1765
Estimate SE tp
Fixed effects
Intercept 60.970 1.2315 49.51 <0.0001
Sine DOY −5.755 0.6862 −8.39 <0.0001
Cosine DOY 0.287 0.5106 0.56 0.574
Age 0.971 0.2611 3.72 0.0002
Age
2
−0.080 0.0205 −3.88 0.0001
Habitat (moorland) 3.067 1.3320 2.30 0.035
R
2LMM(m)
0.3139
R
2LMM(c)
0.5785
Note: Cosine DOY is the cosine of day of year; sine DOY is the sine of day of
year; R
2LMM(m)
is the R
2
marginal (variance account for the fixed effects); R
2LMM(c)
is the R
2
conditional (variance account for random and fixed effects). Molar
width is a proxy of molar size. Woodland is the reference level in habitat.
66 Can. J. Zool. Vol. 93, 2015
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Fig. 5. Predictions of the response of faecal neutral detergent fibre with residual ash (NDF) for hinds of red deer (Cervus elaphus) against age
and day of year when the animal was shot using the model in Table 4.(a) Three-dimensional surfaces from top to bottom are moorland (dark
grey in print, purple on the Web) and woodland (light grey in print, green on the Web). (b) NDF with residual ash against age as in panel a;
day of year was fixed at 1st of May. Woodland: circles and broken line (grey in print; green on the Web); moorland: triangles and solid line
(grey in print; purple on the Web).
200
250
300
2
4
6
8
10
12
55
60
65
70
75
day of year (1 = 1st May)
age (years)
NDF content in faeces (%)
(a)
24681012
50
55
60
65
70
75
age (years)
faecal NDF-ash (%)
(b)
Pérez-Barbería et al. 67
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reduction in proportions of both grass and heath (Latham et al. 1999).
If such dietary differences between habitats resulted in the moor-
land diet being of lower nutritional quality, then this might require
the consumption of greater volumes of food, necessitating more
chewing and concomitant exposure to tooth wear. Additionally, dif-
ferences in the wear-inducing properties of forest browse, forbs,
heath, and grasses might result in differential rates of tooth wear
between red deer occupying moorland and woodland, reflecting
their differing contribution to diet in respective habitats. More open
habitats may also tend to promote the probability of ingesting soil
and grit, increasing tooth wear (Strömberg 2002,2011;Mendoza and
Palmqvist 2008;Damuth and Janis 2011;Jardine et al. 2012;Kaiser
et al. 2013).
A number of studies comparing tooth wear rates between un-
gulate species with different feeding types have reported higher
rates of wear for grazers, followed by mixed feeders, and then
browsers (Solounias et al. 1994;van Soest 1994;Veiberg et al.
2007a;Damuth and Janis 2014). Furthermore, several studies have
reported significant intraspecific variation in tooth wear between
populations in different geographic areas (Skogland 1988;Kojola
et al. 1998;Loison et al. 2001;Nussey et al. 2007;Veiberg et al. 2007a;
Ozaki et al. 2010;Kubo and Yamada 2014). This has been attributed
either to perceived differences in quality of habitat or available for-
age, or to differences in population density and associated resource
competition leading to variation between individuals in access to
higher quality forage (Fowler 1987;Freeland and Choquenot 1990).
Differences in faecal NDF–ash between habitats
Differences in faecal NDF–ash were examined among a subset
of hinds in our deer samples. These values represent a combined
proxy of both fibre and potentially abrasive silicate mineral com-
ponents in the diet.
Some caution must be exercised in interpreting the analysis find-
ings in relation to habitat and tooth wear: (i) while measured tooth
wear reliably represents cumulative wear integrated over a long pe-
riod of time, measured NDF–ash reflects only the diet consumed in
the few days immediately prior to sampling (Pérez-Barbería and
Gordon 1998b); (ii) while our analyses control for seasonal varia-
tion in the fibre content of plants or prevalence of extrinsic min-
eral abrasives through the year, interpretation rests on the
assumption that observed differences in faecal NDF–ash content
between habitats are broadly representative of general differ-
ences in fibre and ash contents of available diets between habi-
tats; and (iii) the analyses on faecal NDF–ash were carried out only
for hinds, so may not be applicable to males.
A significant difference in faecal NDF–ash was found between
habitats (Table 4), with levels higher for moorland than woodland
deer, in accordance with expectations. The difference in faecal
NDF–ash content between habitats, however, was relatively small,
at only around 3% (Fig. 5b). Furthermore, whereas all fixed terms
in the model explained around 31% of variation in faecal NDF–ash
(R
2marginal
), when analysed in conjunction with the random terms
location and year, this rose to 58% (R
2conditional
), indicating consid-
erable variation in dietary fibre with residual ash contents between
locations and years. By contrast, R
2
marginal and conditional val-
ues for the analysis of tooth wear show that the amount of ex-
plained variation in tooth wear only increased from 67% to 68%,
due to location and year. Thus, it would appear that while there is
considerable variation in dietary fibre and ash contents between
locations within habitats, there is only very minor variation in
tooth wear. Although not conclusive, these observations suggest
that variation in tooth wear between locations may not be closely
related to variation in fibre and ash content and that differences
in tooth wear between habitats may be predominantly influenced
by environmental factors besides dietary NDF–ash content. It is
also possible, however, that a component of NDF–ash, such as
abrasive silicate levels, significantly influence tooth wear between
habitats, but the relationship is largely masked by unrelated vari-
ation in another component such as fibre.
Part of the faecal NDF–ash variance was explained by age. Faecal
NDF–ash increased with age, reaching a maximum at 6 years of
age and then decreasing. We hypothesise that this could be due to
differences in diet selection related to age: young and very old
hinds selecting diets with lower NDF–ash content, and thus less
abrasive, than hinds in their prime age when they need to maxi-
mise their intake for reproduction investment. Although there
is some evidence that time investment in mastication can be
adapted as an attempt to compensate for reduced chewing effec-
tiveness associated with changes in age-related tooth morphol-
ogy, there is no evidence of a similar compensation process by
changes in diet composition or the physical structure of the feed
in red deer (Pérez-Barbería and Gordon 1998b). Further work is
needed to provide support to these hypotheses.
Relationship of age, sex, and body size with tooth wear
Within habitats, males and females of larger skeletal body size
had significantly more worn teeth, after controlling for the effects
of age and molar size. This suggest that larger deer consumed
greater quantities of forage to grow and maintain their increased
body size, with the penalty of increased tooth wear; a finding
which has not been reported in other deer populations (Nussey
et al. 2007;Ozaki et al. 2010). It is interesting that while this was
observed within habitats, between habitats moorland deer were
both smaller and exhibited greater tooth wear. This supports the
conclusions of Ozaki et al (2010) and Veiberg et al (2007a)that diet
type is generally of greater influence than body size on tooth wear.
In males and females of both habitats, dentine thickness showed
a decelerating decline with age, as reported in other studies (Loe
et al. 2003;Carranza et al. 2004;Nussey et al. 2007;Veiberg et al.
2007b), although the rate of tooth wear attenuated more strongly
with age in females. There are a number of studies in deer that
have reported faster rates of molar wear and incisor wear in males
than females (Loe et al. 2003;Carranza et al. 2004,2008;Kubo et al.
2013). Differences in rates of tooth wear between sexes in ungu-
lates have often been predicted according to four compatible
hypotheses: (1) sexual dimorphism in body size and increased
consumption by larger animals (e.g., Clutton-Brock and Albon
1989;Carranza et al. 2004); (2) dietary niche separation between
sexes (often linked to size dimorphism) and concomitant differ-
ences in diet quality (Clutton-Brock and Albon 1989;Kubo et al.
2013); (3) differences in life-history strategies, with females se-
lected to favour longer term survival and multiple breeding years,
while males selected more for enhanced short-term performance
during the prime breeding years (Promislow 1992;Gaillard and
Yoccoz 2003;Carranza et al. 2004;Carranza et al. 2008); (4) com-
bining elements of hypotheses 1 and 3, molariform teeth in male
red deer (Carranza et al. 2004), as well as in other sexually dimor-
phic ungulates (Carranza and Pérez-Barbería 2007), are smaller
and less durable than expected from body size dimorphism, lead-
ing to steeper wear rate and earlier depletion than in females,
consistent with greater sexual selection on polygynous males for
body size than tooth size. Our analyses on skeletal size support
hypothesis 1 above and our results for dentine thickness partially
support hypothesis 3 above, as females had more durable teeth at
their old age by decreasing their rate of dentine wear after approx-
imately 8 years of age in comparison with males (Loe et al. 2003;
Carranza et al. 2004;Nussey et al. 2007;Veiberg et al. 2007b).
However, in hypothesis 3, we should expect higher rates of den-
tine wear before and during the prime age of males, as polygynous
males invest heavily in growth and reproduction at their prime,
but this was not supported by our data. However, as indicated by
Kubo et al. (2013), relative levels of dietary niche separation be-
tween sexes (hypothesis 2 above) may also vary between habitats
and locations contributing to variation between studies.
68 Can. J. Zool. Vol. 93, 2015
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Finally, as tooth wear is cumulative during an animal’s life, one
would expect a small difference in dentine thickness between
habitats in young deer and that this difference should increase as
deer get older and teeth are exposed to differential wear rates for
longer; our data, however, showed a lack of interaction between
habitat and age. Analysis of molars from animals younger than
2 years confirmed that there was no difference in initial emerged
height of unworn molars and, thus, observed differences in adult
molar height between habitats most likely reflect differences in
wear rates; the lack of detected interaction between age and hab-
itat may simply reflect insufficient sensitivity in the analysis be-
cause of the small sample size in the oldest age classes.
Conclusion
This study confirmed that Scottish red deer occupying moor-
land habitat are, on average, skeletally smaller that woodland
deer. This likely reflects increased energy demands and (or) poorer
quality diet in moorland. Dentine wear was also higher in moor-
land deer, indicating a possible increase in intake and processing
in moorland deer to partially mitigate any such energy demand or
diet-quality differences. Differences in dentine wear between hab-
itats may also reflect inherent differences in toughness and abra-
siveness of the diet. This was supported by significantly higher
faecal NDF–ash contents in deer from moorland habitat.
Within habitats, larger deer of both sexes had higher rates of
dentine wear, suggesting that deer grew larger through ingesting
more food or spending more time chewing and ruminating to
enhance processing of food. The fact that between habitats moor-
land deer were both smaller and had higher rates of tooth wear
suggests that environmental effects have a stronger influence on
tooth wear than body size.
Acknowledgements
Thanks to all stalkers of private estates and the Forestry Com-
mission for Scotland that collected and prepared the samples used
in this study. An early version of this paper was significantly im-
proved by the comments of C. Marcus and M.O. Kubo. We are also
indebted to the European Commission Leonardo da Vinci Pro-
gramme and the students that the programme supported to par-
ticipate in this work, as well as the Scottish Government’s Rural
and Environment Science and Analytical Services Division (RESAS)
and the Scottish Natural Heritage (SNH) for funding this project.
A.A. and E.P.-F. were supported by funding from the Department
of Education, Universities and Research of the Basque Govern-
ment, and k-Egokitzen07 and Unesco07/07 projects.
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