Supplementary Methods file for Young, Fernàndez and Fleagle (2009)

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Supplementary Methods file for Young, Fernàndez and Fleagle (2009)
Animal husbandry and sample composition
The data for this study were taken from a mixed-longitudinal series of radiographs and
associated morphometrics originating from a long-term study of capuchin monkey growth at the
Harvard School of Public Health. This dataset has constituted the primary resource for research
on capuchin monkey growth for more than 30 years (Ausman et al. 1982; Cole 1992; Elias and
Samonds 1977; Fleagle and Samonds 1975; Fleagle et al. 1975; Fleagle and Schaffler 1982;
Jungers and Fleagle 1980; Samonds and Hegsted 1973; Thurm et al. 1975; Watts 1990; Wood
2003; Young 2005). Newborn monkeys were removed from their mothers following birth and
were hand-reared for 3-5 years under controlled conditions in a primate nursery. All animals
were fed a diet known to promote optimal growth, housed in non-restrictive cages that were large
relative to body size, and were permitted frequent (2-3 times per week) periods of exercise on a
large tree positioned in one corner of the laboratory (Thurm et al. 1975; K. Samonds and C.
Samonds, pers. comm.). Lateral-view uniplanar radiographs and morphometric measurements
were taken weekly during the first eight weeks of life, biweekly during the following year, and at
one to two month intervals for several years thereafter. Radiographic and placement procedures
have been described in detail elsewhere (Fleagle and Samonds, 1975; Thurm et al., 1975).
From this larger project, a subset of 15 male C. albifrons and three male C. apella were
selected for the current study (i.e., all available control group males from the original study).
Data from animals younger than one month of age were excluded due to difficulty identifying
long bone epiphyses. In total, measurements were recorded on 493 C. albifrons radiographs and
147 C. apella radiographs. Measurements were combined across individuals to create speciesspecific mixed longitudinal samples spanning the first five years of life (Table S1). In the wild,
capuchin monkeys typically wean between 9 and 14 months of age and begin reproductive
activity at around three years of age (Robinson and Janson 1987). The sample used in this study
therefore includes animals of all age stages, from infant to adult.
Measurement protocols
Right humeral and femoral maximum lengths, total (i.e., external) diameters, and
medulary (i.e., internal) diameters were measured on digitally scanned radiographs (resolution:
150 ppi) using NIH ImageJ software (Abramoff et al. 2004). Brass scale bars, cut at millimeter
intervals and placed in each radiograph, were used to calibrate measurments from pixels to
millimeters. Radiographs were discarded in cases where it was difficult to distinguish between
left and right limbs or when the proximal or distal ends of the limbs were blurred. In addition,
radiographs were not used when the date the radiograph was taken and the date body weight was
measured differed by more than 10 days. Humerus length was measured as the distance from the
most proximal point of the humeral head and the most distal end of the trochlea, whereas femur
length was measured as the to the distance from the most proximo-dorsal point on the femoral
head to the most distal point of the condylar surfaces. External and “internal” (i.e., medullary)
diameters were measured at midshaft on an axis perpendicular to the longitudinal axis of the
bone. Measuring diameters at midshaft ensured that measurements were easily repeatable and
that measurements of humerus diameter were not biased by inclusion of the deltopectoral crest.
To facilitate the identification of bone-air boundaries, image edges were also enhanced using the
ImageJ “Find Edges” macro prior to taking diameter measurements. Interrater reliability was
high across all length and diameter measurements (Kendall’s [63]=0.78-0.93, all p<0.001).
Statistical methodology
To investigate the ontogenetic scaling of cross-sectional dimensions, log-transformed
limb measurements were fit to the standard allometric power function:
log Y = log  +  log X
where Y represents the parameter of interest, X is an overall size variable,  is the slope (i.e.,
scaling coefficient) and  is the intercept. Allometry was recognized if the 95% confidence
intervals on scaling coefficients did not encompass the expected values for isometric scaling (as
defined in Table 1 of the manuscript).
Age-related changes in GSF were fit to a non-linear Gompertz model (German and
Meyers 1989):
Y  Aebe
kt
where Y represents the parameter of interest, t is postnatal age in days and e is the base of the
natural logarithm.
A, b and 
k are constants, calculated iteratively, that are respectively
proportional to the lower asymptote of the curve, the exponential rate of decay and the tangential
slope at birth. Capuchin monkeys exhibit a pronounced growth spurt at approximately three
years of age, coincident with the onset of sexual maturity (Leigh 1996; Robinson and Janson
1987).
Such a pronounced growth spurt necessarily affected Gompertz fits, possibly
confounding growth assessments at earlier ages. Therefore, when examining age related changes
in GSF we truncated the dataset to only include measurements taken prior to three years of age,
at which time the monkeys had reached approximately 70% of adult body mass.
We adopted a mixed-effects approach when fitting all regression models (Pinheiro and
Bates 2000), allowing us to formally incorporate “random” intraspecific variation and
accommodate autoregressive and heteroscedastic error structures.
For each relationship of
interest, a variety of models, correlation structures and error structures were tested using iterative
maximum likelihood estimation, retaining the model with highest explanatory power, as gauged
by comparing Akaike Information Criteria across models. The goodness-of-fit for each was also
assessed using a likelihood-ratio reformulation of the standard coefficient of determination (i.e.,
R2):
 2

R 2   (log LUM  log LRM )
 N

where logLUM is the log-likelihood of the full model and logLRM is the log-likelihood of the

intercept-only model (Magee
1990). All statistical procedures were implemented using the
freely-available, open source R Statistical Package (R Development Core Team 2008).
Table S1. Composition of the longitudinal radiographic samples in Cebus albifrons and C.
apella
Cebus albifrons (N=15)
Cebus apella (N=3)
Minimum Maximum Median
Minimum Maximum Median
Starting age (days)
30
344
41
34
40
39
Duration (years)
1.3
5.5
3
4.3
4.7
4.5
N radiographs
15
52
35
48
50
49
References
Abramoff MD, Magelhaes PJ, and Ram SJ. 2004. Image processing with ImageJ. Biophotonics
Int 11:36-42.
Ausman LM, Powell EM, Mercado DL, Samonds KE, Lozy M, and Gallina DL. 1982. Growth
and developmental body composition of the cebus monkey (Cebus albifrons). Am J
Primatol 3:211-227.
Cole TM. 1992. Postnatal heterochrony of the masticatory apparatus in Cebus albifrons and
Cebus albifrons. J Hum Evol 23:253-252.
Elias MF, and Samonds KW. 1977. Protein and calorie malnutrition in infant cebus monkeys:
growth and behavioral development during deprivation and rehabilitation. The American
Journal of Clinical Nutrition 30:355-366.
Fleagle JG, and Samonds K. 1975. Physical growth of cebus monkeys (Cebus albifrons) during
the first year of life. Growth 39:35-52.
Fleagle JG, Samonds KW, and Hegsted DM. 1975. Physical growth of cebus monkeys, Cebus
albifrons, during protein or calorie deficiency. The American Journal of Clinical
Nutrition 28:246-253.
Fleagle JG, and Schaffler MB. 1982. Development and eruption of the mandibular cheek teeth in
Cebus albifrons. Folia Primatol (Basel) 38:158-169.
German RZ, and Meyers LL. 1989. The role of time and size in ontogenetic allometry: I.
Review. Growth Dev Aging 53:101-106.
Jungers WL, and Fleagle JG. 1980. Postnatal growth allometry of the extremities in Cebus
albifrons and Cebus apella: a longitudinal and comparative study. Am J Phys Anthropol
53:471-478.
Leigh SR. 1996. Evolution of human growth spurts. Am J Phys Anthropol 101:455-474.
Magee L. 1990. R2 measures based on Wald and likelihood ratio joint significance tests. Am Stat
44:250-253.
Pinheiro JC, and Bates DM. 2000. Mixed-Effects Models in S and S-PLUS. New York, NY:
Springer.
R Development Core Team. 2008. R: A language and environment for statistical computing.
2.7.1 ed. Vienna, Austria: R Foundation for Statistical Computing.
Robinson JG, and Janson CH. 1987. Capuchins, squirrel monkeys, and atelines: socioecological
convergence with old world primates. In: Smuts BB, Cheney DL, Seyfarth RM,
Wrangham RW, and Struhsaker TT, editors. Primate Societies. Chicago and London: The
University of Chicago Press.
Samonds KW, and Hegsted DM. 1973. Protein requirements of young cebus monkeys (Cebus
albifrons and apella). American Journal of Clinical Nutrition 26:30-40.
Thurm D, Samonds KW, and Fleagle JG. 1975. An atlas of the skeletal maturation of the cebus
monkey: the first year. Boston: Harvard School of Public Health.
Watts ES. 1990. A comparative study of neonatal skeletal development in Cebus and other
primates. Folia Primatol (Basel) 54:217-224.
Wood HT. 2003. Energetics, encephalisation and Weaning: Modelling Growth and Maturation in
Primate and Human Evolution [Ph.D. Dissertation]. University College London:
University College London.
Young JW. 2005. Ontogeny of muscle mechanical advantage in capuchin monkeys (Cebus
albifrons and Cebus apella). J Zool Lond 267:351-362.
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