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2013 SOUTHEASTERN NATURALIST 12(2):297–306
Age and Gender Affect Epiphyseal Closure in
Emily B. Flinn1,2,*, Bronson K. Strickland1, Stephen Demarais1,
and David Christiansen3
Abstract - Timing of epiphyseal closure determines length of long bones and thus body
size, but factors affecting epiphyseal closure in Odocoileus virginianus (White-tailed
Deer) have not been conclusively quantified. We collected morphometric data and radiographic
images of the distal humerus, proximal radius, distal radius, and metacarpus on
approximately 0.5-, 1.5-, 2.5-, and 3.5-year-old optimally nourished captive deer. Age
affected closure of distal radial and metacarpal epiphyseal plates (P < 0.001), with all
individuals exhibiting epiphyseal closure by 3.5 years of age. Gender affected closure of
the distal radial epiphyseal plates (P = 0.036), with females closing prior to males. Differential
bone growth rate prior to epiphyseal closure may be one mechanism by which
individual and cohort phenotypic effects are manifested in cervids.
Examination of long bones for ossification of epiphyseal growth plates is
used to determine age class (Grant et al. 1972, Marks and Erickson 1966) and
skeletal maturity (Vulcano et al. 1997), and to assess factors affecting morphological
variation in mammals (Serrano et al. 2007, Silberberg and Silberberg
1949). Timing of epiphyseal plate ossification (i.e., closure) in Odocoileus
virginianus Zimmerman (White-tailed Deer) has been investigated to determine
effects of geographic location, gender, and age on growth patterns (Purdue 1983).
However, limitations of previous studies of epiphyseal closure in deer included
inadequate sample size or the use of individuals with estimated ages (Lewall
and Cowan 1963, Purdue 1983). In cervids, body mass influences dominance
and mating success (Clutton-Brock et al. 1988, Jones et al. 2011, Townsend and
Bailey 1981); thus, skeletal development may influence fitness by limiting ultimate
body size and mass (Gill 1956). Knowledge of factors affecting epiphyseal
closure may aid our understanding of how morphological variation and fitness
are related in White-tailed Deer.
Previous studies have shown epiphyseal closure in mammals is influenced
by age, environment (i.e., nutrition), and the endocrine system (Malina and
Bouchard 1991). Lewall and Cowan (1963) suspected a delay in epiphyseal
closure in Odocoileus hemionus columbianus Rafinesque (Black-tailed Deer)
caused by restricted nutrition (i.e., 70% of ad libitum diet). In Cervus elaphus L.
1Mississippi State University, Department of Wildlife, Fisheries, and Aquaculture, Mississippi
State, MS 39762. 2Current address - Missouri Department of Conservation, 3500
East Gans Road, Columbia, MO 65201. 3Mississippi State University, College of Veterinary
Medicine, Mississippi State, MS 39762. *Corresponding author - emily.flinn@mdc.
298 Southeastern Naturalist Vol. 12, No. 2
(Red Deer), gender variation suggested a female adaptation to prioritize energy
needs for reproduction over those for growth (Clutton-Brock et al. 1982). In deer,
age is thought to be the primary factor affecting timing of epiphyseal closure, followed
by gender (Purdue 1983) and possibly nutrition (Lewall and Cowan 1963).
The goal of this research was to quantify effects of age and gender on
epiphyseal closure in known-aged White-tailed Deer (hereafter, deer) raised
on an optimum quality diet. We used radiographs to evaluate closure rates of the
epiphyseal plate at four locations in the forelimb of male and female captive deer
from 3.6 months to 3.4 years of age. We hypothesized that age would correlate
positively with epiphyseal closure at each location and that epiphyseal plates of
females would close earlier than those of males.
Study animals originated from wild lineages across Mississippi. Fawns were
born at the Mississippi State University Rusty Dawkins Memorial Deer Unit
(MSU Deer Unit) located in Oktibbeha County, MS. This facility was subdivided
into five 0.4–1.3-ha pens that contained natural forages, Trifolium repens
L. (White Clover), water, and two feeders supplied with ad libitum 20%-protein
deer pellets (Purina AntlerMax Professional High Energy Breeder 59UB, Purina,
St. Louis, MO). Fawns were weaned naturally by their dam or when removed
from their dam at an average age of 5.5 months. Female fawns remained within
the MSU Deer Unit. Male fawns were randomly assigned to similar research facilities
located in Noxubee, Attala, and Copiah counties, MS. Each of these three
facilities consisted of 2 pens of 0.9 ha with vegetation and husbandry identical
to MSU Deer Unit protocols, to insure there was no confounding effect due to
specific pen location. All of the eleven pens used to confine study animals were
located away from high traffic areas and any other factors that potentially could
have caused a stress reaction in animals.
During February–April 2005 and 2006, the Mississippi Department of Wildlife,
Fisheries, and Parks captured and relocated wild-bred adult females (>1.5
year-old) from across Mississippi to the MSU Deer Unit. These wild-caught
females produced first generation offspring in 2005 and 2006, and the first-generation
deer produced second-generation offspring in 2007 and 2008. All fawns
were located and tagged within 24 hours of birth.
We used a VR 8020 mobile radiograph machine (Vet-Ray Inc., Arlington
Heights, IL) to process 706 radiographic images of long bones from 128 deer
with known birth dates to determine age- and gender-specific timing of epiphyseal
closure, with 58 individuals undergoing repeated sampling. Ages at the time
of sampling were 3.6–6.7 months (108–201 days), 1.1–1.4 years (402–511 days),
2.2–2.4 years (803–876 days); and 3.2–3.4 years (1168–1241 days) (hereafter,
these will be referred as 0.5, 1.5, 2.5, and 3.5 years, respectively). We collected
2013 E.B. Flinn, B.K. Strickland, S. Demarais, and D. Christiansen 299
176–178 usable radiographic images for each epiphyseal plate. Sample sizes differed
among epiphyseal plates because not all radiographs developed properly
We processed images of adults (1.5–3.5 years-old) during October–November
2007 and 2008. We recorded images of 0.5-year-old fawns during January 2008,
December 2008, and January 2009. For each deer, we examined one radiographic
image for each of four epiphyseal plates of the forelimb: distal humerus, proximal
radius, distal radius, and metacarpal (i.e., 4 images/deer). Each epiphyseal
plate was independently assigned a classification by 2 veterinarians using a system
similar to Purdue’s (1983). The plates received 1 of 3 classifications: open
(growth is occurring), partial (growth has ceased but epiphyseal plate has not
completely ossified), or closed (growth has ceased, epiphyseal plate is fully ossified).
When a closure ranking differed, the evaluators conferred to establish a
Additionally, we collected morphometric measurements of all deer to examine
the relationship between bone growth and limb length. We measured elbow-tohoof
length, which is from the proximal tip of the ulna, to the tip of the longest
nail of the front hoof. This measurement incorporated the proximal and distal
radial as well as the metacarpal epiphyseal plates. We also measured scapulato-
hoof length, which is from the most dorsal point of the scapula to the tip of
the longest nail of the front hoof. This measurement incorporated all evaluated
epiphyseal plates. All handling and marking techniques were approved by the
Mississippi State University Institutional Animal Care and Use Committee under
protocol numbers 04-068 and 07-036.
We modeled the effects of age (days) and gender on epiphyseal closure using
an analysis of covariance model with the GLIMMIX procedure in SAS (SAS
Institute, Cary, NC). We modeled each epiphysis as open or closed with gender
as a fixed effect and days since birth as a continuous covariate. Experimental
units were individual deer with known birth dates. We attempted to evaluate
gender*days interactions in our analysis, but models failed to converge, likely
due to sample size limitations. Because many animals were sampled repeatedly
from birth year up to 4 years of age, we included deer ID as a random effect.
However, including the random effect caused some models not to converge. In
these cases, we excluded the random effect. For models with a significant gender
Table 1. Sample sizes of White-tailed Deer radiographic images of four epiphyseal plates classified
by gender (male and female) and mean age (days) taken in Mississippi during 2007–2009.
Distal Distal Proximal
radius humerus radius Metacarpus
Age M F M F M F M F
168 39 39 39 39 38 40 39 36
469 18 28 17 29 17 29 19 29
842 19 19 20 18 20 18 18 19
1198 9 7 7 7 7 7 10 6
300 Southeastern Naturalist Vol. 12, No. 2
or age effect, we output the probability of the epiphysis being open at 4 ages:
168, 469, 842, and 1198 days. These categories represented the mean age (days)
of deer measured each year. Differences were considered significant at α = 0.05.
We modeled scapula-to-hoof and elbow-to-hoof lengths with an exponential
function using the NLIN procedure in SAS (SAS Institute, Cary, NC). This
approach was necessary to model the non-linear growth of these measurements
by age and gender. We did not determine if these equations differed statistically,
as there is no readily available procedure to accomplish this. Instead, we
provided 95% confidence intervals for the parameter estimates a and b in the
respective exponential equations (measurement = a × exp([b / days]) for gender
Age and gender affected closure patterns for the distal radial growth plate,
and age affected closure of the metacarpal growth plate. However, neither affected
the distal humeral and proximal radial growth plates (Table 2). By 0.5
years of age (168 days), 100% of the distal humeral and 98% of the proximal
radial epiphyseal plates had ceased longitudinal growth and were classified as
partial or closed. The metacarpus ceased longitudinal growth by 2.5 years of
age (842 days), with ≥0.97 probability of the epiphyseal plates classified as
partial or closed. The distal radius ceased longitudinal growth by 3.5 years of
age (1198 days), with a probability of 1.0 that epiphyseal plates were closed
Table 2. Effect of age (days) and gender on timing of epiphyseal closure in four growth plates of
male (n = 85) and female (n = 93) White-tailed Deer in Mississippi from 2007 to 2009. Values
represent the probability of an open epiphysis.
168 469 842 1198
Epiphyseal plate F M F M F M F M
Distal radius 0.992 0.999 0.790 0.957 0.046 0.225 0.001 0.005
Metacarpus 0.995 0.992 0.805 0.699 0.031 0.018 0.010 0.007
F-valueA P-value F-valueA P-value
Distal radius 32.04 less than 0.001 4.64 0.036
Metacarpus 27.87 less than 0.001 0.78 0.377
ADegrees of freedom were as follows: Distal radius = 1, 55; Metacarpus = 1, 173.
BNo model computed. Most (proximal radius) or all (distal humerus) epiphyses were closed at the
first sampling period.
2013 E.B. Flinn, B.K. Strickland, S. Demarais, and D. Christiansen 301
Both age and gender influenced growth patterns of skeletal length measurements
(Fig. 1). The 95% CIs of parameter estimates for growth curves of
scapula- and elbow-to-hoof equations for males and females did not overlap,
indicating leg bones in males grew for a longer period of time than in females
Figure 1. Exponential growth curve of scapula-to-hoof and elbow-to-hoof length measurements
(mm) of male (n = 85) and female (n = 93) White-tailed Deer by age (days)
from Mississippi from 2007 to 2009. Arrows depict the mean age (days) measurements
were taken for each age class of deer (i.e., 0.5, 1.5, 2.5, and 3.5 years).
Table 3. Parameter estimates of the exponential equations (measurement = a × exp[b / days]) used
to model scapula- and elbow-to-hoof measurements of male and female White-tailed Deer from 168
to 1198 days of age in Mississippi from 2007 to 2009.
Measurement Gender a L95% CL U95% CL b L95% CL U95% CL
Scapula Male 931.6 911.1 952.1 -44.5 -50.2 -38.7
Female 829.2 809.6 848.8 -25.4 -31.5 -19.3
Elbow Male 616.9 604.5 629.2 -39.2 -44.4 -34.0
Female 554.3 542.3 566.3 -22.5 -28.0 -16.9
302 Southeastern Naturalist Vol. 12, No. 2
Age is the primary factor affecting epiphyseal closure in mammals (Hale
1949, Thomsen and Mortensen 1946). Closure rates for the distal radial and
metacarpal epiphyseal plates support the importance of age in epiphyseal ossification.
The lack of age effect on distal humeral and proximal radial epiphyseal
plates was due to the high rate of closure by the first sampling period at 0.5 years.
Sampling prior to this age may have more clearly defined possible variation in
When epiphyseal plates cease growth and complete ossification, the elongation
of the long bone and the limb is complete. In most specimens, the distal humerus
and proximal radius growth plates clearly ceased involvement in bone elongation
by 0.5 years, although the metacarpal epiphyseal plate contributed to bone elongation
until 2.5 years of age. Longitudinal growth of the metacarpal bone ceased
when this plate closed because it is the only epiphyseal plate present in the metacarpal
bone (Lewall and Cowan 1963). The distal radial growth plate contributed
for the longest period to growth of the evaluated epiphyseal plates by continuing
growth in females until 2.5 years of age and in males until 3.5 years of age.
Consistencies in epiphyseal closure are present between our study on optimally
nourished captive deer with known birth dates and Purdue’s (1983) study
on wild-range deer from various environments. Purdue (1983) found the proximal
and distal radial epiphyseal plates for males closed within 2 months of the
closure timings in our study. Similarly, Purdue (1983) found the proximal and
distal radial and metacarpal epiphyseal plates for females closed within 1 month
of the closure timings in our study.
Inconsistencies in the timing of epiphyseal closure were also present between
our study and Purdue’s (1983). He reported that male metacarpal epiphyseal
plates closed at 29 months, although our study found closure at 38 months. This
discrepancy is likely a result of our sampling schedule, as a gap existed between
28.9 and 38.0 months for male deer. Additionally, a discrepancy in Purdue’s
(1983) report of the distal humerus closure timing prevents an accurate comparison.
Although he reported (Purdue 1983:1210, Table 3) that the distal humeral
epiphyseal plate closed at 12 and 20 months for males and females, respectively,
he stated in the results that this epiphyseal plate fused before and during the animal’s
first autumn (i.e., less than 7 months-old; Purdue 1983).
Our results support the conclusion that gender is a secondary factor affecting
epiphyseal closure (Malina and Bouchard 1991, Purdue 1983, Serrano et al.
2006). Epiphyseal plates closed earlier in female Ursus americanus Pallas (Black
Bear; Marks and Erickson 1966) and Capra pyrenaica Schinz (Iberian Ibex; Serrano
et al. 2006), similar to our proximal and distal radial epiphyseal data and
forelimb leg measurements. We may have missed gender effects in the distal
humeral and metacarpal epiphyseal plates because we did not sample throughout
the year. Year-round sampling would have provided a clearer depiction of variation
among year classes and gender groups.
2013 E.B. Flinn, B.K. Strickland, S. Demarais, and D. Christiansen 303
Gender effects on the timing of epiphyseal closure may result from differences
in the onset of sexual maturity (Silberberg and Silberberg 1949, Iuliano-Burns et
al. 2009). Female Red Deer ceased growth earlier than males, perhaps to prioritize
allocation of energy to reproduction (Clutton-Brock et al. 1982). Many more
female than male deer fawns reached sexual maturity during their first winter,
demonstrating the gender variation in sexual maturity (Cheatum and Morton
1946). Our data suggest that female deer do not invest in body size as long as
males do, possibly because investment in reproduction is more beneficial. Additionally,
females may stop growing sooner because additional body size offers no
advantage to them. Conversely, male body size directly affects fitness thru malemale
intraspecific competition (i.e., combat) to establish dominance and breeding
access (Demarais and Strickland 2011, Jones et al. 2011). Gender variation in
epiphyseal closure timing, forelimb length, and age when longitudinal growth
ceases is a primary mechanism for sexual dimorphism.
Nutrition has exhibited varying effects on timing of epiphyseal closure in
ungulates, and additional controlled studies are needed. A restricted diet (70% ad
libitum diet) delayed epiphyseal closure by a minimum of 12 months in Blacktailed
Deer (Lewall and Cowan 1963). In contrast, the metacarpal epiphyseal
plate closed faster in a high-density (92 individuals/km2) population of nutritionally
deprived Dama dama L. (Fallow Deer) compared to deer in a low-density
area (23 individuals/km2) (Serrano et al. 2007). Verme and Ozoga (1980) found
shorter femur lengths in captive deer fawns fed restricted diets but did not evaluate
Bone growth rates prior to epiphyseal closure may be a mechanism
by which cervids develop and maintain cohort effects (Albon et al. 1992,
Pettorelli et al. 2002). Although skeletal measurements are more resistant
to environmental variation than are other body condition indices (e.g., body
mass, antler quality; Klein 1964, Klein et al. 1987), a reduction in skeletal
measurements is expected to be evident when nutrition is severely reduced
(Skogland 1990). Deer fawns increased hind-foot length when their population
was drastically reduced (Ashley et al. 1998), exhibiting density-dependent environmental
effects on skeletal length.
Variation in timing of epiphyseal closure and/or rate of bone growth prior to
closure associated with nutritional intake may be the process by which phenotypic
variation is expressed in cohorts and regional populations of White-tailed
Deer in Mississippi (Strickland and Demarais 2000, Strickland et al. 2008).
Strickland and Demarais (2000) found regional variation in morphometrics,
among which Delta males achieved a larger body mass at a younger age than
males in lower quality regions, including the Lower Coastal Plain. Flinn (2010)
found corresponding patterns in skeletal growth among male White-tailed Deer
from the Delta, Loess, and Lower Coastal Plain regions in Mississippi.
In Mississippi, female deer in lesser-quality habitats had less body mass
that did not increase after 3.5 years of age, whereas female deer within
greater-quality habitat had greater body mass that increased until 4.5 years
304 Southeastern Naturalist Vol. 12, No. 2
of age (Strickland and Demarais 2000). Environments with lower diet quality
may produce females with smaller body size as a trade-off with the costs
of reproduction (Clutton-Brock et al. 1982, Oftedal 1985). Sexual maturation
can cease long-bone growth to increase an individual’s reproductive success
by closing the epiphyseal locations before their genetic potential for skeletal
size is reached in suboptimal conditions (Geist et al. 2000, Silberberg and Silberberg
1949, Taber and Dasmann 1958). Thus, in environments with greater
diet quality, females can afford to invest in larger bodies without jeopardizing
reproduction; conversely, females with decreased available diet quality must
terminate somatic development and invest in reproduction.
We thank the Mississippi Department of Wildlife, Fisheries and Parks for technical
assistance and financial support through the Federal Aid in Wildlife Restoration Project
W 48-55, Study 65. We thank all MDWFP biologists and staff involved in deer capture
and collection, particularly A. Blaylock, L. Castle, C. Dacus, A. Gary, C. McDonald,
W. McKinley, J. Willcutt, and L. Wilf. We appreciate Mississippi State University’s Department
of Wildlife, Fisheries, and Aquaculture and the Forest and Wildlife Research
Center for all administrative and logistical support. We are grateful to Mississippi State
University’s College of Veterinary Medicine for film and developing equipment and M.
Mordecai for evaluating radiographs. We also thank private cooperators for husbandry of
research animals, S. Tucker for university research facility assistance and maintenance,
and M. Belant for manuscript edits. This manuscript is contribution WF350 of the Mississippi
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