NEW APPROACHES

Testing Parallel Laser Image Scaling for Remotely MeasuringBody Dimensions on Mantled Howling Monkeys (Alouatta palliata)

NANCY L. BARRICKMAN1, AMY L. SCHREIER2, AND KENNETH E. GLANDER3

1Department of Anthropology, University of Waterloo, Waterloo, Ontario, Canada2Department of Biology, Regis University, Denver, Colorado3Department of Evolutionary Anthropology, Duke University, Durham, North Carolina

Body size is a fundamental variable for many studies in primate biology. However, obtaining bodydimensions of wild primates through live capture is difficult and costly, so developing an alternativeinexpensive and non-invasive method is crucial. Parallel laser image scaling for remotely measuringbody size has been used with some success in marine and terrestrial animals, but only one arborealprimate. We further tested the efficacy of this method on the arboreal mantled howling monkey(Alouatta palliata) in La Pacifica, Costa Rica.We calculated interobserver error, as well as themethod’srepeatability when measuring the same animal on different occasions. We also compared measure-ments obtained physically through live capture with measurements obtained remotely using parallellaser image scaling. Our results show that the different types of error for the remote technique areminimal and comparable with the error rates observed in physical methods, with the exception of somedimensions that vary depending on the animals’ posture. We conclude that parallel laser image scalingcan be used to remotely obtain body dimensions if careful consideration is given to factors such asspecies-specific morphology and postural habits. Am. J. Primatol. 77:823–832, 2015.© 2015 Wiley Periodicals, Inc.

Key words: body size; remote measurement; parallel laser photo scale; measurement error;mantled howling monkey

INTRODUCTIONBody size is a crucial variable in behavioral

ecology, providing data that are imperative tounderstanding adaptations such as clutch/offspringsize, sexual selection, growth, and life history, aswellthe intersection between these variables and ecologi-cal parameters such as habitat quality and dietarypreferences [e.g., Bergeron, 2007; Caillaud et al.,2008; Lourie et al., 2014; Rothman et al., 2008;Wijeyamohan et al., 2012]. In addition, data on bodysize have significant implications for conservationpolicy, contributing to our understanding of relation-ships between habitat quality and alteration withvariables such as growth rates and population-levelchanges in body size over time [e.g., Berger, 2012;Rohner et al., 2011]. Measuring body size in captivitydoes not provide adequate information to addressthese questions because, in many species, body sizeand growth rates can differ considerably from wildconspecifics due to environmental circumstancesincluding provisioning and lack of predator pressure[e.g., Altmann&Alberts, 2005; Leigh, 1994; Smith &Jungers, 1997]. However, measuring body size ofwild animals is challenging. Live capture of animalsthrough methods such as traps and darting is costly

and potentially harmful to the animals [e.g., Bossonet al., 2012; Glander, 2013; Pelletier et al., 2004].Thus, several researchers have developed techniquesfor remotely and noninvasively estimating body sizeof wild animals.

DESCRIPTIONPhotogrammatic methods, which involve taking

measurements of body dimensions from photo-graphs, have been tested in whale sharks [Graham& Roberts, 2007; Jeffreys et al., 2013; Rohner et al.,2011], marine mammals [Durban & Parsons, 2006;

conflict of interest : None

�Correspondence to: Nancy L. Barrickman, Department ofAnthropology, University of Waterloo, 200 University AveWest, Waterloo, Ontario N2L 3G1, Canada.E-mail: nlbarric@uwaterloo.ca

Received 10 October 2014; revised 2 February 2015; revisionaccepted 13 March 2015

DOI: 10.1002/ajp.22416Published online 30 April 2015 in Wiley Online Library(wileyonlinelibrary.com).

American Journal of Primatology 77:823–832 (2015)

© 2015 Wiley Periodicals, Inc.

Ireland et al., 2006; Lourie et al., 2014; Perryman &Lynn, 1993; Perryman and Westlake, 1998; Websteret al., 2010], large terrestrial mammals such aselephants [Lee & Moss, 1995; Morgan & Lee, 2003;Shrader et al., 2006; Wijeyamohan et al., 2012] andartiodactyls [Bergeron, 2007; Berger, 2012; Willischet al., 2013], terrestrial primates such as baboons[Domb & Pagel, 2001], macaques [Kurita et al.,2012], gorillas [Breuer et al., 2007; Caillaud et al.,2008], and chimpanzees [Deschner et al., 2004;Emery & Whitten, 2003;], as well as one arborealprimate—red colobus monkeys [Rothman et al.,2008]. Several techniques have been developed,and they primarily differ regarding how the scaleof the objects in the photograph is determined. Someresearchers use scaling poles or an object of knownsize, including other animals that have been physi-cally measured, in the photograph [e.g., Domb &Pagel, 2001; Deschner et al., 2004; Graham &Roberts, 2007; Ireland et al., 2006; Kurita et al.,2012; Lee & Moss, 1995; Morgan & Lee, 2003;Willisch et al., 2013]. This technique is feasible forterrestrial primates, but not for most arborealspecies because the substrates are often difficult toaccess. Another method of photogrammetry consistsof determining the relationship between a pixel and aknown unit of measure through a formula calculatedusing the distance between the photographer and thesubject, and the focal length of the camera lens [e.g.,Breuer et al., 2007; Berger, 2012; Caillaud et al.,2008; Emery & Whitten, 2003; Perryman & Lynn,1993; Shrader et al., 2006]. However, as Rothmanand colleagues [2008] have noted, distance from asubject can be difficult to accurately obtain in anarboreal environment.

The technique of using parallel laser imagescaling for photogrammetry involves the use of adevice with two laser beams at a fixed distance fromeach other that are projected onto the animal ornearby surface. Photographs are taken of the animalwith the laser points included in the frame.Measure-ments of the animal are then taken directly from thephotographs using the distance between the laserpoints as a photo scale. Several researchers haveused this technique in marine [Durban & Parsons,2006; Jeffreys et al., 2013; Rohner et al., 2011;Webster et al., 2010], terrestrial [Bergeron, 2007;Lourie et al., 2014; Wijeyamohan et al., 2012], andarboreal environments [Rothman et al., 2008]. Someof the details vary, such as the distance between thelasers and whether the lasers are horizontal orvertical relative to each other, but the principleremains the same. There are several potentialsources of error that must be carefully consideredduring the construction and use of the device[Bergeron, 2007; Durban & Parsons, 2007; Jeffreyset al., 2013; Lourie et al., 2014; Rothman et al., 2008;Rohner et al., 2011; Webster et al., 2010; Wijeyamo-han et al., 2012]. The laser beams must be precisely

parallel, such that they are equidistant regardless ofthe distance between the photographer and thesubject. The animal must be in a position in whichlandmarks are visible and the dimension is notdistorted by posture (e.g., laterally flexed spine orsplayed hindlimbs). The animal must be in a positionrelative to the photographer that minimizes errorfrom parallax (e.g., the lateral surface of the animalperpendicular to the photographer’s line of sight). Inaddition, the lasers must be projected on a surfacethat is perpendicular to the laser beams to minimizeparallax distortion of the distance between the laserpoints. The surface of the projection must be fairlysmooth, as an overly bumpy surface can distort thelaser points and make their centers difficult todetermine.

EXAMPLEAll research reported compliedwith the protocols

approved by the Institutional Animal Care and UseCommittees at Duke University (Protocol A130-13-05) and Regis University (Protocol 14-005), and theAnimal Care Committee at the University of Water-loo (Protocol 13-10). In addition, all research con-formed to the American Society of Primatologists(ASP) Principles for the Ethical Treatment of NonHuman Primates. All research conducted in thisreport complied with legal requirements for conduct-ing research in Costa Rica.

In this study we investigated the effectiveness ofparallel laser image scaling to measure bodydimensions of an arboreal primate, the mantledhowling monkey (Alouatta palliata). Because arbo-real primates are more difficult to remotely measurethan terrestrial primates due to their relativeinaccessibility, it is thus paramount to develop asuitable method for the arboreal environment. Roth-man and colleagues [2008] tested this method on anarboreal primate, the red colobus monkey (Procolo-bus rufomitraus), and their results showed minimalerror (mean error rate of 1.7%). However, theyfocused on tail length, and we seek to expand thedemonstration of this method to additional bodydimensions. Howlers provide some advantages forthis method as they are found in social groups andthus several animals can be photographed in a singledata collection bout, and they are relatively inactive[Di Fiore et al., 2011] allowing for time to positionthe camera and lasers. In testing the accuracy of thismethod, our research determined the degree of threetypes of error: (i) interobserver error, i.e., the errorassociated with multiple researchers measuring thesame photograph; (ii) repeatability error, i.e., theerror across multiple photographs of the sameanimal; (iii) accuracy error, i.e., the error betweenmeasurements obtained physically from live cap-tures and the measurements of the same animalusing parallel laser image scaling.

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Laser Device DescriptionWe adapted our design from similar devices used

by other researchers [e.g., Bergeron, 2007; Durban &Parsons, 2006; Jeffreys et al., 2013; Rothman et al.,2008; Wijeyamohan et al., 2012]. The engineeringmachine shop at the University of Waterloo con-structed the device. Two lasers were mountedhorizontally at 4 cm apart in two aluminum barrelswhich were encased in an aluminum body with PVCstruts on either side to provide stability when thedevice was resting on a flat surface (Fig. 1a). Thedevice was attached to a Canon EOS 7D camera withEFS 55–250mm zoom lens using a standard tripodbolt. We used green lasers (Apinex, Montreal, modelGM-CW02) because of their greater visibility in thecanopy as compared with red lasers [Rothman et al.,2008].

We chose to orient the lasers horizontally ratherthan vertically. In the case of mantled howlers’

typical positional behavior, the lasers aremost easilyprojected onto a branch below the animal, a treetrunk next to the animal, or on the caudal portion ofthe animal’s body. Horizontal orientation is prefera-ble for branches located underneath the animal, andeither vertical or horizontal is acceptable for projec-tion onto a tree trunk or the body. We tested thismethod on tree trunks of various sizes by projectingthe lasers onto the trunk and photographing themalongwith an object of known size. The error was lessthan 1%—calculated as the difference between theremotemeasurement and the physical measurementof the object divided by the physical measurement—for tree trunkswith diameters as small as 20 cm, so inthis study we used tree trunks that were larger than20 cm in diameter. Furthermore, horizontal place-ment does not necessitate the use of an inclinometerfor the calculation of parallax due to the angle oforientation of the lasers.

Fig. 1. A schematic of the laser device is shown mounted to a camera; credit Sean Docherty (A); a sample photograph of a howler withlaser point (B).

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Aluminum can expand and contract due toambient conditions, so the laser position wasadjustable using a set of four small screws per laser.A hex key was used to tighten and loosen the screws.We calibrated the lasers’ position by projecting thelasers onto a metal ruler, and adjusting them untilthe laser beams were 4 cm apart at three distances:5m, 10m, and 20m. Calibration was performedbefore, after, and during each photo session. If wefound that the distance between the lasers wasmiscalibrated, all photos taken since the previouscalibration session were discarded.

Other potential sources of parallax that couldalter the distance between the laser beams includethe angle of the surface that the points are projectedon, and the angular orientation between the photog-rapher on the ground and the subject in an arborealenvironment. We tested the error produced by thefirst issue by projecting the laser on a board held atvarious angles tilted away from the observer, andincluded an object of known size in the photograph asa scale. The distance between the laser points did notincrease by more than 2% of 4 cm until the board wasmore than 15° from perpendicular. We took careduring data collection to project the lasers onsurfaces, such as tree branches, that were perpen-dicular to the line-of-sight, but small deviations canbe tolerated. The angle between the photographerand the subject was tested by projecting the lasersonto an object of known size that was held at variousheights on a three-story building. The resulting errorwas less than 1% for all angles fromhorizontal to 60°,and there was no significant increase or decrease inthe error with increasing angular position.

Study Sites, Subjects, and ProcedureHacienda La Pacifica is a privately owned ranch

in western Costa Rica (10°280N, 85°070W) includingdisturbed secondary growth in corridors that inter-sect cleared pasture. It is a lowland tropical dry forestecozone with deciduous seasonally dry forest[Thompson et al., 2014]. Several generations of adulthowlers have been darted, captured, and tagged atthis site from 1972 to 2014, and details of theprocedure are outlined elsewhere [Glander et al.,1991]. Physical measurements of captured howlerswere taken using a measuring tape, and the land-marks are described in Table I. In July 2014, wephotographed, using the laser device, 8 knownanimals from a well-studied group that had beenphysicallymeasured onmultiple occasions (Table II).We used these photographs to determine interob-server error, repeatability, and accuracy compari-sons between physical and remote measurements.We also determined interobserver error rates in thephysical measurements of animals that were dartedon 3 or more occasions since 1972 (Table III) for

comparison to interobserver and repeatability meas-ures using the remote parallel laser image scaling.All the animals included in this analysis were adultsat the time measurements were taken.

Analyses of interobserver error and repeatabilityof the remote laser method were supplemented withdata from La Suerte Biological Research Station innortheastern Costa Rica (10°260N, 83°470W). The siteis a tropical premontane wet forest, includingprimary forest and advanced secondary growth[Bezanson, 2009]. During May–June 2014, we took108 usable photographs from two mantled howlersocial groups, including adults, juveniles, and in-fants. Because individuals are not known, we couldonly test interobserver error in most of these photo-graphs. There were, however, two sets of photo-graphs of adult females in which we observed theindividual changing positions, and these two sets of 2and 3 photographs, respectively, were included in theanalysis of repeatability (Table II).

Several photographs were taken of each individ-ual in multiple positions at both La Pacifica and LaSuerte. We sought out animals that were eitherwalking horizontally across a branch, lying pronewith their limbs dangling, or hanging by their tailsbecause these positions allow for several landmarksto be easily located. We also measured the distancebetween the photographer and the animal using aNikon ACULON laser rangefinder to ensure that wewere within 20m, as we had calibrated the 4 cmdistance between the two laser beams up to 20m. Atthe end of each photo session, we reviewed eachphotograph to determine its suitability. If anyresearcher detected a problem, the photograph wasdiscarded. Problems included blurriness, bad projec-tion of the lasers (e.g., on leaves or not visible),inability to determine body landmarks, and animalsnot situated perpendicular to the plane of thephotograph.

Image AnalysisAn example of an image of a howler with laser

points is shown in Figure 1b. Photographs weredownloaded and analyzed on ImageJ 1.44o, designedby the National Institutes of Health, USA, andavailable online at their website: http://imagej.nih.gov/ij. The software has the ability to set the scale of aspecified distance. We measured the distance be-tween the two laser projections, and converted thepixel length to 4 cmusing this function.Wewere thenable to measure the distances between the anatomi-cal landmarks for each of the body measurements(Table I). We defined the landmarks and practicedmeasuring distances on a set of photographs notincluded in the present study [Barrickman &Schreier, 2014]. We measured all of the photographsin this study independently in order to determineinterobserver error.

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Statistical AnalysisTo determine interobserver error for the remote

measurements, we calculated the percentage errorfor each individual measurement by subtractingmeasurer 10s datum from measurer 20s datum, anddividing this difference by measurer 10s datum. Wecalculated means and standard deviations of errorrates for a given measurement (e.g., all the errorrates for measurements of the distal forelimb). Wecreated boxplot distributions showing medians,quartiles, and outliers of error rates for eachmeasurement. Pearson’s correlation coefficient wasalso calculated to determine the correlation betweenthe two researchers’ datasets (P value of � 0.05 wasconsidered statistically significant). Percentage errorwas also calculated to determine interobserver errorfor the physical measurements, calculated by sub-tracting the minimum value obtained for a givenmeasurement on a specific animal from the maxi-mum value, and dividing the difference by themaximum value. Means and standard deviations ofinterobserver error rates for measurements (e.g.,mean of errors from measurements of distal fore-limbs) were compared between remote and physicalmeasurements using Mann–Whitney U rank-sumtest (P value of �0.05 was considered significant;two-tailed). Spearman’s rank correlation coefficient

was performed to determine whether error rateswere related to themagnitude of themeasurement (Pvalue of � 0.05 was considered significant).

Percentage errorwas used to determine degree ofrepeatability (i.e., multiple photographs of the sameanimal in differing positions) and the error rates foraccuracy (i.e., the differences between physical andremote methods in measurements of the sameanimal). We compared means, standard deviations,and boxplots of error distributions for each measure-ment using each method. Spearman’s rank correla-tion coefficient was performed to determine whetherrepeatability was related to the magnitude of themeasurement (P value of �0.05 was consideredsignificant).

We also calculated absolute error (i.e., length oferror in cm rather than as a percentage) to compareerror rates with the sex-specific means and standarddeviations of the body dimensions among all theanimals our study group.

RESULTSThe distributions of the two trunk measure-

ments demonstrate some sexual dimorphism in themeasurements that include the skull (Glabella toRump, GR, and Body Length, BL; Fig. 2; Table IV).

TABLE I. Description of Measurements and Landmarks

Measurement Description

Glabella to rump (GR)a From most caudal projection of brow in lateral profile to base of tailNeck to rump (NR)a From bend between skull and vertebral column when cervical spine is extended to base

of tailBody length (BL)a From crown of skull when neck is flexed to base of tailDistal forelimb (DF) Straight line from elbow to bend in wrist or proximal edge of palmar surface if visible;

for physical measurements, the styloid process on the ulnar side was used as thedistal landmark

Distal hindlimb (DH) Straight line from knee joint to bend in center of ankle joint when viewed laterally; forphysical measurements, the lateral malleolus was used as the distal landmark

aGR and NR were not physically measured. BL was not measured remotely because animals were never positioned correctly. These measurements areincluded in the analysis to test repeatability and interobserver error only.

TABLE II. Sample Composition; All Animals Were Measured Physically and Remotely Except for the Two AdultFemales from La Suerte and Zen from La Pacifica, Who Were Measured Remotely Only

Name/Identifier Site Sex Sets of photographs

Talia La Pacifica F 2Zanahoria La Pacifica F 2Fuschia La Pacifica F 3Mimosa La Pacifica F 4Hibiscus La Pacifica F 6AF 1 La Suerte F 2AF 2 La Suerte F 3Rambo II La Pacifica M 2Zen La Pacifica M 3Aguacate La Pacifica M 6

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Physical and remote measurements cannot bedirectly compared for trunk measurements becausethe landmarks differed between the two techniques.The distributions of limb measurements also showsome sexual dimorphism using both methods (Fig. 3;Table IV). There was considerable overlap in DistalForelimb (DF) measurements between the physicaland remote methods, but not in the Distal Hindlimb(DH) measurements. The remote method consistent-ly resulted in shorter DH measurements than thephysical method.

Analyses of interobserver error using the remoteparallel laser method showed an average percentageof error across all measurements of 3.62% with astandard deviation of 2.90%. Themean interobservererror rates and correlation coefficients in remotemeasurements varied depending on the measure-ment (Fig. 4). Analyses of physical measurementstaken at La Pacifica revealed higher levels ofinterobserver error than the remote method (mean¼ 7.08%; SD¼4.81%; Fig. 5). The results of theMann-WhitneyU rank-sum test revealed significantdifferences between the interobserver error rates oftrunk length measurements, with physical measure-ments resulting in higher error rates (mean errorrate for body length¼6.13%) than remote measure-ments (mean error rates for GR¼2.75% and NR

¼2.74%) (Mann-Whitney U rank-sum of trunklength error rate v. GR error rate: U¼�438, d.f.¼47, P<0.0001, two-tailed; trunk length v. NR:U¼�430, d.f.¼47, P< 0.0001, two-tailed). Therewere no significant differences between interobserv-er error rates for limb measurements across theremote and physical measurements (mean error ratephysical measurement of DF¼ 4.25%, mean errorrate for remote measurement¼3.52%, Mann-Whit-ney U rank-sum: U¼�2.5, d.f.¼ 4, P¼ 0.6, two-tailed; mean error rate of physical measurement ofDH¼5.79%, mean for remote measurement¼4.16%, Mann-Whitney U rank-sum: U¼�7.0, d.f.¼6, P¼0.28, two-tailed).

Measurements of a smaller magnitude (i.e.,limbs) resulted in a greater percentage of interob-server error than trunk measurements using boththe physical and remote methods. The error ratesfrom both the remote and physical methods werecombined to test for relationships with the magni-tude of measurement, and the non-parametricSpearman’s rank correlation was significant(r¼�0.57, N¼ 14, P¼0.03, two-tailed). However,the absolute error was smaller in the case of smallermeasurements. Using the remote method, the aver-age error in the trunk lengthmeasurements (GR andNR) was 1.2 cm, DF was 0.75 cm, and DH was0.56 cm. As with the remote method, the absoluteerror using the physical method was higher amongthe greater measurements (e.g., absolute error ofbody length was 3.4 cm as compared to 0.7 cm in thehindlimb and 0.4 cm in the pollex).

The results of tests of repeatability, or multiplemeasurements of the same individual taken fromdifferent photographs in varying positions, revealthat error varied depending on the measurement(Fig. 6). Themeasurements of trunk length had lowererror rates (GR mean¼6%; NR mean¼5.4%) thanthe limb measurements (DF mean¼ 8.4%; DH mean¼18%). Thus, hindlimb measurements had a partic-ularly low repeatability. Absolute rates showed anaverage error of 3.1 cm for GR, 2.1 cm for NR, 1.4 cmfor DF, and 2.6 cm for DH. Spearman’s rank

TABLE III. Sample Composition of Animals Used to Determine Error Rate in Physical Measurements. AnimalsWere Captured and Measured Between 1972 and 2014

Number of occasions animal was captured and physically measured N (number of animals)

3 264 125 16 67 38 19 112 1

Total 51

Fig. 2. Distribution of trunk measurements taken physically(BL) and remotely (GR and NR). Sample sizes are indicated inparentheses. Open boxes denote females and shaded boxesdenote males. BL¼body length; GR¼glabella to rump; NR¼neckto rump.

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correlation test showed no significant relationshipbetween the degree of repeatability error and themagnitude of the measurement (r¼ -0.80, N¼5,P¼ 0.20, two-tailed). However, the sample size (i.e.,number of measurements) was small, and it isdifficult to determine whether a correlation existswithout a larger sample.

Only measurements of DF and DH were compa-rable between the physical and remote methods. Forother physical measurements, remote measure-ments were not possible because either landmarkscould not be reliably located in the photographs, aswas the case for proximal limbs, or the animals didnot naturally assume the proper position for meas-urements such as body length. The results showeddiffering distributions of error depending on themeasurement (Fig. 7). The DFmeasurements had anaverage error of 6.3%, resulting in an absolute errorof 1.0 cm. The DH measurement had a considerablyhigher average error of 13.1%, resulting in anabsolute error of 1.9 cm.

A comparison between measurement distribu-tions and absolute errors (i.e., length of error in cm)

showed that the error was less than the standarddeviation of sex-specific distributions in most casesexcept DH (Table IV). These results indicate that thenatural variation in most body dimensions of thepopulation exceeded the error variation of bothphysical and remote methods.

COMPARISON AND CRITIQUEThe interobserver error rates using the remote

parallel laser image scaling are lower than those ofthe physical method, and significantly lower in thecase of trunk measurements. The difference betweenthe interobserver rates could be because two observ-ers measured animals using the remote methodduring a single field season, whereas severalresearchers performed physical measurements overseveral field seasons from 1972 to 2014. Waite andMellish [2009] emphasize that interobserver errorrates in physical measurements are rarely comparedwith error rates in photogrammetry. In their studycomparing these two measurement methods in sealions, they found no significant differences betweeninterobserver rates [Waite & Mellish, 2009].However, to be comparable to multiple occasions oflive capture and measurement, the repeatability(multiple photographs of the same individual) of the

TABLE IV. Comparison of Measurement Means and Standard Deviations with Error Rates; All Values Are in cm

Measurementa

Male Mean,StandardDeviationa

Female Mean,StandardDeviationa

Mean InterobserverError (physical)

MeanInterobserverError (remote)

MeanRepeatability

Error

Mean ErrorPhysical v.Remote

BL 49.43, 2.73 44.79, 2.45 3.44 b b b

GR 52.70, 4.25 50.30, 3.29 b 1.39 3.08 b

NR 40.24, 4.91 39.68, 1.83 b 1.06 2.15 b

DF 17.57, 1.09 15.82, 1.57 0.62 0.76 1.37 1.01DH 14.01, 1.54 13.57, 1.59 0.65 0.56 2.57 1.86

aThe means and standard deviations provided in this table are frommeasurements taken using the remote method with the exception of BL, which is fromphysical measurements. Details regarding sample size are provided in the text and Tables II and III.bThese error rates were not calculated for this study. See text for details.

Fig. 3. Distribution of limb measurements taken physically andremotely (DF¼distal forelimb, and DH¼distal hindlimb).Measurements of females are indicated by white boxes andmales by shaded boxes. Physical measurements are denoted by“p” following the measurement code and do not have speckledpattern in the boxes, and remote measurements are denoted by“r” and have speckled pattern in the boxes. Sample sizes areindicated in parentheses.

Fig. 4. Interobserver error percentages using the remotemethod. The first value in parentheses is the sample size (i.e.,number of times the measurement was taken by each observer;multiple animals are included), followed by the Pearson’scorrelation coefficient. GR¼ glabella to rump; NR¼neck torump; DF¼distal forelimb; DH¼distal hindlimb.

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remote method must be considered. The repeatabili-ty error rates in our study are similar to theinterobserver error rates for physical measurementsof trunk measurements, but the repeatability errorrates for limb measurements are higher using theremote method. This result is likely explained by thegreater variability of limb position as compared withtrunk position. The howlers’ limbs were not alwaysprecisely perpendicular to the camera’s line-of-sight.We eliminated many of the photographs with thisproblem before the image analysis stage, but somedegree of error was difficult to avoid in fieldconditions as the animals are rarely in an idealposition for the measurement of certain bodydimensions. Specifically, we noted that the animals’hindlimbswere often splayedwhen resting in a prone

position on a horizontal branch with the limbshanging down, a common resting posture in howlers.

The repeatability error rates in this study arehigher than those found by some other researcherswho tested methods of photogrammetry. Forinstance, Bergeron [2007] found a particularly lowmean repeatability error of 3.1% when measuringthe annuli of ibex using parallel laser image scaling.In contrast, ourmean repeatability error rate rangedfrom 5.4% (2.1 cm) for NR to 18% (2.6 cm) for DHmeasurements. Other studies, however, found amean absolute repeatability error that is similar toor greater than our results. Caillaud and colleagues[2008] remotely measured gorillas, determiningscale through a calculation involving distance fromobject and focal lens length. Theirmean repeatabilityerror was 5.07 cm for body length (percentage notprovided; approximately 5% given a mean bodylength of 89.4 cm). Durban and Parsons [2006] foundsimilar repeatability error rates to the present studywhen they remotelymeasured dorsal fin size in killerwhales using parallel laser image scaling. Error infemales averaged 9% (6 cm), whereas error in malesaveraged 16% (23 cm). They attribute their errorrates to several factors, primarily the parallax fromorientation of photographer above the whale and finsthat were not positioned perpendicular to the surfaceof water [i.e., tilted towards the photographer;Durban & Parsons, 2006]. These factors also affectedour study. In an arboreal environment, there isparallax as the photographer is always below theanimal. In addition, postural issues were present inour study, as noted above—limbs were rarelyprecisely perpendicular to the camera’s line-of-sight.The distal hindlimbs, exhibiting the highest meanrepeatability error, were particularly problematicbecause of the postural variation. Because livecapture is often not possible, many studies validatedtheir remote measurements by using objects ofknown size such as boards rather than studyanimals, and obtained low error rates [e.g., Jeffreys

Fig. 5. Interobserver error percentages using the physicalmethod, separated by measurement. The sample size, in termsof number of animals that were measured on multiple occasions,was 51 animals for all measurements except for distal hindlimb(4 animals) and distal forelimb (6 animals). See text andTable IIIfor details regarding sample composition.

Fig. 6. Distribution of repeatability error, i.e., measurementsfrom multiple photographs of the same individual in differentpositions. Sample sizes are as follows: GR consists of 2 individualsmeasured twice and 2 individual measured 3 times; NR consistsof 3 individuals measured twice and 1 individual measured 3times; DF consists of 5 individuals measured twice; DH consists of3 individuals measured twice, 2 individuals measured 3 times,and 2 individuals measured four times. GR¼nglabella to rump;NR¼neck to rump; DF¼distal forelimb; DH¼distal hindlimb.

Fig. 7. Distribution of error between measurements of sameanimals using physical and remotemethods. The sample size is 7animals for each measurement. DF¼distal forelimb; DH¼distal hindlimb.

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et al., 2013; Perryman & Lynn, 1993; Wijeyamohanet al., 2012]. However, animals have complexmorphologies and tests for accuracy on the actualstudy subjects, as in our study, is ideal. Rothmanand colleagues [2008] demonstrated the efficacy ofparallel laser image scaling in measuring taillength in red colobus monkeys, with a low meanerror rate of 1.7% (1.1 cm) as compared to physicalmeasurements. Physically and remotely obtainedmeasurements of ibex annuli also had low errorrates; Bergeron’s [2007] results showed amean errorrate of 3.9% (0.2 cm), while Willisch and colleagues’[2013] results showed that 88% of the annuli werewithin 0.75 cm of one another. We were able todirectly compare physical and remotemeasurementsof the limbs, and our mean error rates were higherthan previous studies though the absolute error rateswere comparable to the measurements of red colobustails (6.3% or 1.0 cm and 13.1% or 1.9 cm for the DFand DH, respectively). As with previous analyses oferror rates detailed above, the distal hindlimbs wereparticularly problematic, likely the result of thehowlers’ postural behavior. For some body dimen-sions such as distal hindlimbs in howlers, it isdifficult to replicate measurements with smalldegrees of error because of the animals’ positionalbehavior. Tail length in colobus and horn annuli inibex are easier to replicate than trunk or limb lengthbecause the tails and horns are not as variable inposition during the animals’ normal behavior as thetrunk and limbs. However, body dimensions such astrunk and limb length are more pertinent than taillength to many aspects of primate biology, such assexual dimorphism or growth and development.Thus, determining a reliable method for remotelymeasuring these dimensions is paramount, especial-ly as live capture and measurement is prohibitivelyexpensive and potentially dangerous. As long as agiven measurement can be repeated on the sameindividual at different times and different locations(assuming the animal is an adult), they are reliableindicators and provide valuable data. After complet-ing the analyses reported above, we re-examined ourphotographs using stricter criteria regardingconsistency of posture, and eliminated several photo-graphs. We did not have a large enough sample foranalysis, but wewere able to reduce the repeatabilityerror to less than 3% in three individuals for whichwe had multiple photographs.

In line with previous studies, the results of thisstudy reveal both the benefits and limitations ofremotely obtained measurements. For some meas-urements, we foundhigh error rates, primarily due tothree factors. First, the limbs of howlers are smallerthan the dimensions used in other studies, such asbody length in gorillas or tail length in red colobusmonkeys. Our results revealed a strong correlationbetween the magnitude of the measurement and thedegree of error, so the measurement of smaller

species can be difficult. Second, landmarks andappropriate postures can be difficult to obtain forsome body dimensions, as we noted for distalhindlimbs. Thus, the postural habits of the speciesmust be carefully considered before a reasonableassessment of possible measurements can be made.Finally, using remote measurements in an arborealenvironment versus a terrestrial environment addsanother potential source of error—the parallax inbody position created by the angle of the line-of-sightis often inevitable because the photographer must bebelow the animal. Thus, researchers should considerremotely measuring animals on only lowersubstrates.

Despite the limitations, parallel laser imagescaling has substantial advantages. Live capture iscostly and invasive, and remote techniques arerelatively inexpensive and non-invasive. In addition,error from parallel laser image scaling is less thanthe variation in body dimensions in howlers (asindicated by the standard deviation), demonstratingthat the measurements are a reliable biologicalsignal. With careful consideration of factors suchas species-specific morphology and postural habits,remote measurements can be obtained that are asreliable as physical measurements. With time,patience, luck, and strict adherence to posturalcriteria, researchers can obtain body size dimensionsnon-invasively in wild arboreal populations.

ACKNOWLEDGMENTSWe are very appreciative of the respective

owners of both research sites, La Pacifica and LaSuerte, for access to their forests. We also thankMaderasRainforest Conservancy for hosting us at LaSuerte and Ministerio del Ambiente y Energia(MINAE) for granting research permits. Manythanks to Susan Williams, Cynthia Thompson, andChris Vinyard for their skills and assistance in livecapture of the animals at La Pacifica. Our thanksalso to Francisco Campos and The Organization forTropical Studies for their assistance. We are verygrateful to the engineers at the University ofWaterloo’s Engineering Machine Shop, especiallyRichard Forgett, John Boldt, and Sean Docherty fortheir design skills and expertise.

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