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A Comparison of Scan and Focal Sampling for the Description of Wild Primate
Activity, Diet and Intragroup Spatial Relationships

Article in Folia Primatologica · March 2013

DOI: 10.1159/000348305 · Source: PubMed

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 Original Article

Folia Primatol 2013;84:87–101 Received: September 26, 2012

DOI: 10.1159/000348305 Accepted after revision: January 23, 2013
Published online: March 28, 2013

A Comparison of Scan and Focal Sampling

for the Description of Wild Primate Activity,
Diet and Intragroup Spatial Relationships
Katherine R. Amato a, b Sarie Van Belle b, d Brianna Wilkinson c
a
Program in Ecology, Evolution and Conservation Biology, and b Department of
Anthropology, University of Illinois, Urbana-Champaign, Ill., and c Department of Biology,
Dartmouth College, Hanover, N.H., USA; d Estación de Biología Tropical Los Tuxtlas,
Instituto de Biología, Universidad Nacional Autónoma de México, México, México

Key Words
Alouatta · Activity budget · Instantaneous focal sampling · Continuous focal
sampling · Group scan · Proximity · Nearest neighbor

Abstract
We used data collected during two concurrent studies of black howler monkeys
(Alouatta pigra) in Palenque National Park, Mexico, to compare systematically three
methods of behavioral data collection [group activity scan sampling (group scans), in-
stantaneous focal individual sampling (instantaneous focals) and continuous focal indi-
vidual sampling (continuous focals)] and three methods of proximity data collection
[group proximity scan sampling (group proximity scans), focal individual proximity scan
sampling (focal proximity scans) and instantaneous focal individual nearest neighbor
sampling (focal nearest neighbor samples)]. We conducted pairwise comparisons of
data among methods using Pearson correlations and one-sample t tests. A series of
Kruskal-Wallis tests were performed to compare the activity and proximity patterns of
adult males, adult females and juveniles described by each method. The three behav-
ioral data collection methods generally provided similar information about activity and
diet. However, important differences for both activity and proximity data existed among
methods. Instantaneous focals overestimated the percentage of time spent in social in-
teractions, while group scans overestimated time spent moving and underestimated
time spent feeding. Group proximity scans and focal proximity scans provided similar
spatial data, while focal nearest neighbor samples were more appropriate for determin-
ing the influence of one individual on another at any given moment. These biases sug-
gest the importance of deliberate method selection during project design and highlight
the need for taking methods into account when comparing studies.
Copyright © 2013 S. Karger AG, Basel

© 2013 S. Karger AG, Basel Katherine R. Amato

0015–5713/13/0842–0087$38.00/0 109 Davenport Hall
E-Mail karger@karger.com 607 S. Matthews Avenue
www.karger.com/fpr Urbana, IL 61801 (USA)
E-Mail amato1 @ illinois.edu
 Introduction

Focal individual observations and scan sampling are used almost universally by
primatologists to describe non-human primate behavior in a variety of wild and cap-
tive contexts. Scan samples are traditionally used to survey activity budget, diet, or
spatial arrangements of all or a subgroup of individuals in a social group simultane-
ously at specified time intervals. In contrast, focal individual samples are primarily
used to collect detailed data describing behaviors that might be overlooked by meth-
ods that do not require the observer to follow an individual in all situations. Altmann
[1974] was the first to outline primate focal and scan sampling in detail. According
to her, data describing complex behaviors (e.g. social interactions) are difficult to re-
cord with scan samples due to the challenge of locating and identifying the activity of
each individual in a group in a short amount of time. However, she notes that research
requiring information regarding easily recognizable behaviors and/or group syn-
chrony of behaviors can benefit greatly from scan sampling. In contrast, focal data
may be more useful for detecting behavioral differences between individuals in a so-
cial group or for describing patterns of subtle social interactions. Focal samples can
be recorded continuously or instantaneously, and how well the two methods corre-
spond depends on the interval between instantaneous records of behavior during a
focal sample, the type of behavioral data being recorded, and the frequency at which
individuals of the species being observed shift behaviors [Altmann, 1974].
Despite the general acceptance of focal and scan sampling for behavioral data
collection, little work has been done formally to compare them. Although the litera-
ture commonly cited [Altmann, 1974; Martin and Bateson, 1993; Lehner, 1996; Pat-
erson, 2001] by authors employing these methods describes them in great detail and
suggests ideal contexts for each, it does not provide systematic comparisons to sup-
port these suggestions and to guide researchers more effectively in project design. In
fact, comparisons of methods for collecting activity and diet data are rare in the pri-
mate literature in general [Dunbar, 1976; Rhine and Flanigon, 1978; Rhine and Ender,
1983; Bernstein, 1991; Fragaszy et al., 1992; Kawanaka, 1996; Zinner et al., 1997; Rose,
2000; Stevenson and Quinones, 2004; Hernández-Lloreda and Colmenares, 2006; Ed-
wards et al., 2010; Gilby et al., 2010], and studies comparing methods for describing
spatial proximity patterns among individuals are completely absent (but see Haddadi
et al. [2011] for a discussion on temporal and spatial criteria for accurately construct-
ing social networks). Because data describing interindividual relationships may de-
pend heavily on proximity data, especially in primates with low frequencies of social
interaction [Di Fiore and Fleischer, 2005; Van Belle et al., 2008; Takuda et al., 2012],
a thorough understanding of the techniques available for estimating spatial relation-
ships among primate individuals is critical. Without systematic comparisons of these
techniques, such an understanding is impossible.
The aim of this paper is to evaluate several commonly used primate behavioral
sampling techniques in the field. Specifically, we compare the use of group activity
scan sampling (hereafter group scans), continuous focal individual sampling (here-
after continuous focals), and instantaneous focal individual sampling (hereafter in-
stantaneous focals) in describing activity and diet in two groups of wild black howler
monkeys (Alouatta pigra) in Palenque National Park, Mexico. We also compare the
use of group proximity scan sampling (hereafter group proximity scans), focal indi-
vidual proximity scan sampling (hereafter focal proximity scans), and instantaneous

88 Folia Primatol 2013;84:87–101 Amato /Van Belle /Wilkinson

DOI: 10.1159/000348305
focal individual nearest neighbor sampling (hereafter focal nearest neighbor samples)
to describe proximity patterns among individuals.
Howler monkeys provide an interesting system for the comparison of behav-
ioral observation methods because they are characterized by cohesive social groups
with relatively low interindividual distances and variation in activity [Pavelka, 2011].
As a result, howler monkey group members should be easier to locate and observe for
group scans compared to other primates. Additionally, as energy minimizers [Milton,
1981], howler monkeys generally change behaviors less frequently than more active
primate species, lowering the probability of missing a behavior during group scans
and instantaneous focal intervals. Therefore, we predicted that for our comparison
all methods for sampling activity, diet and proximity would provide the same results.
Any differences detected would indicate strong biases in the methods which may in-
fluence the interpretation of howler behavioral studies, and are likely to confound
results in studies of primates with less cohesive groups and high intra- and interindi-
vidual behavioral variability. We hope that by providing this information, this study
will contribute to our general knowledge regarding primate behavioral data collec-
tion procedures and improve the design and interpretation of future studies.

Methods

Study Site and Subjects

This study was conducted in Palenque National Park, Mexico (17°28ⴕN, 92°03ⴕW), which
encompasses 1,771 ha. Approximately 1,000 ha are covered by continuous primary tall evergreen
tropical rainforest and forest vegetation in various stages of regeneration. Detailed data on cli-
mate and the black howler population are provided by Estrada et al. [2002].
Over the course of 9 months (September 2010 through June 2011), two independent re-
search projects on black howler monkeys took place at the study site; both groups of researchers
were collecting data on two howler groups (Balam and Motiepa). At times during this period, the
two research teams collected data from the same group, but used different observation methods.
This happened for 28 days for the Balam group and 25 days for the Motiepa group, all days being
dawn-to-dusk follows. Before data collection began, interobserver reliability tests were per-
formed in which the observers used the same observation method to record data on the same
focal individual. After observers obtained 90% agreement, they were permitted to collect data
independently. The principal investigators of each project also performed interobserver reliabil-
ity tests together before training assistants in their respective sampling methods. All researchers
were always close enough to communicate verbally, and they occasionally overlapped in observa-
tions of a single focal individual. We did not include any days when the researchers observed
separate groups in the analysis. A scattering of overlap days occurred in the fall of 2010, but be-
came more consistent in the period from February 2011 through June 2011, when observations
of the Balam and Motiepa groups coincided on an average of 4.2 and 4.4 days per month, respec-
tively. Both groups inhabited areas of primary forest, and all members of both groups could be
individually identified based on factors such as body size, permanent scars, genital pigmentation
and botfly marks. The composition of each group is provided in figure 1.

Data Collection
Behavioral data collection from the two research projects used three observation methods,
each of which was associated with its own protocol for recording proximity among group mem-
bers. For the purpose of the comparisons reported in this paper, we grouped activities into five
categories: feeding, howling, moving, resting, and engaging in social interaction. During feeding
bouts, we identified the food item and analyzed data from five food categories (young and mature
leaves, young and mature fruits, and stems) for the comparison among data collection methods.

A Comparison of Howler Monkey Observation Folia Primatol 2013;84:87–101 89

Methods DOI: 10.1159/000348305
 Balam group Motiepa group
2010 2011 2010 2011
S O N D J F M A M J S O N D J F M A M J
AM KR AM HG
GZ JP
MF
AF LU KB
TE
JM MIL
RFS AF IS
ML
JM DOS
UNO
JF MAA

Fig. 1. Composition of the two study groups during the study period, excluding infants. Black
circles indicate dispersal of group members. AM = Adult male; AF = adult female; JM = juvenile
male; JF = juvenile female. MIL and DOS were considered adults by June 2011. Both groups in-
cluded infants that were excluded from analyses.

Categories were also used to describe the distance between individuals (except infants) for each
proximity method. This study considers two of these spatial categories: 0–1 and >1–5 m apart.
We limited ourselves to these categories because both research teams used boundaries of 1 and
5 m. We did not include a category for greater distances because the different proximity methods
did not have consistent standards of identifying individuals >5 m apart.
(1) Group Scans and Group Proximity Scans. Instantaneous scan samples were conducted at
15-min intervals to record individual activity data. Three minutes were allotted for the location
of all non-infant group members. The first observed behavior lasting for ≥5 s was recorded for
each group member to avoid a potential bias towards more readily detected activities (e.g. mov-
ing) [Fragaszy et al., 1992; Kortsjens et al., 2005]. A total of 2,241 group scans were completed
(Balam: 1,174 group scans; Motiepa: 1,067 group scans). During each scan sample, the distance
categories between all dyads of non-infant group members were recorded as well. To prevent bi-
asing our results in favor of the most visible group members, we only included scan samples for
which complete data on all non-infant group members were recorded, representing a total of 820
group proximity scans (Balam: 413 group scans, 48.6% of all Balam scans; Motiepa: 407 group
scans, 60.1% of all Motiepa scans).
(2) Continuous Focals and Focal Proximity Scans. Thirty-minute focal individual samples
were conducted to record continuously (to the nearest second) the activity of adults in each
group. Each individual was sampled once before any individual was sampled a second time on
a given day. When focal subjects were out of view for >10 min, the sample was ended, and
focal samples lasting <20 min were discarded. We analyzed 360 focal hours of behavior (Balam:
192.3 h; Motiepa: 167.8 h). Instantaneous proximity scan samples were carried out during the
first 5 s of each focal sample as well as at 15 and 30 min to record the identity and distance cate-
gory of all neighbors of the focal individual. We included only scan samples for which we could
identify all non-infant neighbors, which resulted in 1,691 scan samples (Balam: 893 scan samples;
Motiepa: 798 scan samples).
(3) Instantaneous Focals and Focal Nearest Neighbor Samples. Twenty-minute focal indi-
vidual samples with activity recorded instantaneously at 2-min intervals were used to describe
the behavior of the focal individual. If the focal individual was not visible for more than two time

90 Folia Primatol 2013;84:87–101 Amato /Van Belle /Wilkinson

DOI: 10.1159/000348305
intervals, the focal sample was discarded. Sampling rotated through non-infant group members
over the course of each day. Data collected at each time interval during a focal sample were used
to determine the amount of time dedicated to each activity during a focal sample. In subsequent
analyses, data were represented using these summary values, and not individual time intervals. A
total of 387 focal hours were analyzed (Balam: 202 h; Motiepa: 185 h). When possible, at each
2-min time point during the focal sample, the identity of the neighbor nearest to the focal indi-
vidual was noted, as well as the distance category between the 2 individuals. Proximity data were
recorded during 6,701 time points (Balam: 3,545 time points; Motiepa: 3,156 time points).
This research complied with protocols of the Animal Care Committee of the University of
Illinois at Urbana-Champaign and adhered to the legal requirements of Mexico.

Data Analyses
For each data collection procedure, the average percentage of time spent monthly in each
activity and consuming each food type was calculated for all focal individuals (juveniles not in-
cluded in continuous focals). Using these average monthly percentages for each individual, we
then calculated the monthly percentage of time spent in each activity and consuming each food
type for the group overall. To assess how well data collected using each method corresponded,
we compared monthly group averages from each method in a pairwise fashion. For pairwise com-
parisons including continuous focals, monthly means from both methods considered were cal-
culated only from adult individuals.
Because monthly averages for activity and diet approximated a normal distribution, we used
parametric tests to compare them. We first determined a Pearson correlation coefficient for the
average monthly percentage of time spent in each activity and consuming each food type for each
pair of methods [Fragaszy et al., 1992]. Significant correlations indicated high similarity in the
overall patterns described by each method. p values were corrected for multiple comparisons us-
ing a sequential Bonferroni procedure for α = 0.05 [Holm, 1979; Rice, 1989]. Because activity and
diet data were considered separately for each pairwise comparison of methods, p values were ad-
justed for the five tests (one for each activity or diet category) performed on each of these datasets.
Because it is possible for two datasets to be correlated but to report distinct values for each
data point, we also calculated the difference between the monthly average percentage of time
spent in each activity per pair of methods and used one-sample t tests to determine whether these
differences varied significantly from zero [Gilby et al., 2010]. If the methods reported similar val-
ues, we would expect the differences among monthly average values not to differ from zero. Be-
cause we wanted to detect failures to reject the null hypothesis for these tests, p values were not
corrected with sequential Bonferroni corrections to avoid inflating the rate of false negatives.
Because each group of howlers showed the same activity and diet patterns, data from both groups
were combined for both sets of tests.
Similarly, for each procedure, the average percentage of time spent at 0–1 m and at >1–5 m
was calculated per dyad of individuals per month for the two study groups. Using these averages,
we then calculated monthly averages for adult male-adult male dyads, adult female-adult female
dyads, adult male-adult female dyads, adult male-juvenile dyads, and adult female-juvenile dyads
in each group. As with the activity data, the monthly averages approximated a normal distribu-
tion and were compared across methods in a pairwise fashion using Pearson correlations and
one-sample t tests. Because both distance categories were considered part of the same proximity
dataset, correlation p values were adjusted using a sequential Bonferroni procedure to reflect the
ten tests (one for each age-sex dyad at each distance) performed for each pairwise comparison.
p values for t tests were not corrected.
To further assess similarities and differences among the data collection procedures, we ex-
amined whether adult males, adult females and juveniles differed in the monthly mean percent-
age of time spent in each activity and consuming each food type using a series of Kruskal-Wallis
tests for each method separately. The more similar the methods, the fewer differences we would
expect in the behavior patterns reported by each method. For example, if group scans report
males howling significantly more time on average than females, both continuous and instanta-
neous focals should also report males howling significantly more frequently than females. Simi-
larly for the proximity data, the average time spent at each distance category was compared for

A Comparison of Howler Monkey Observation Folia Primatol 2013;84:87–101 91

Methods DOI: 10.1159/000348305
Table 1. Pearson correlation coefficients (r) and p values for pairwise comparisons among the
three data collection procedures for activity budget and diet

Instantaneous focals Instantaneous vs. Continuous focals

vs. group scans continuous focals vs. group scans
r p r p r p

Activity
Feeding 0.908 0.000 0.837 0.000 0.965 0.000
Howling 0.517 0.070 0.340 0.256 0.859 0.000
Moving 0.652 0.016 0.526 0.065 0.608 0.027
Resting 0.838 0.000 0.811 0.001 0.898 0.000
Social interaction 0.753 0.003 0.760 0.003 0.893 0.000
Food type
Young leaves 0.768 0.002 0.508 0.076 0.892 0.000
Mature leaves 0.700 0.008 0.594 0.032 0.927 0.000
Young fruits 0.380 0.201 0.977 0.000 0.480 0.096
Mature fruits 0.893 0.000 0.703 0.007 0.816 0.001
Stems 0.781 0.002 0.613 0.026 0.927 0.000

n = 13 for each test (6- and 7-monthly averages for Balam and Motiepa, respectively). Bold
p values indicate significant correlations between two data collection methods after sequential
Bonferroni corrections with the initial α value set at 0.050.

male-male, female-female, male-female, male-juvenile, and female-juvenile dyads for each meth-
od separately. Small sample sizes and a poor approximation of the normal distribution required
the use of non-parametric Kruskal-Wallis tests for these analyses. Data for these tests were com-
bined for both groups when there were no significant differences between groups, and a sequen-
tial Bonferroni correction was applied to all p values (activity and diet: five categories with three
age-sex pairwise comparisons each; proximity: two categories with five dyad comparisons each).

Results

Activity
The average time spent feeding, resting and being social correlated strongly
among all methods (table 1). However, time spent moving was more weakly corre-
lated among all methods, and time spent howling was weakly correlated between in-
stantaneous focals and continuous focals and between instantaneous focals and group
scans (table 1). t tests indicated several differences for average monthly activity bud-
gets between group scans and both focal methods. Specifically, group scans showed
that the howler monkeys spent on average less time feeding and being social and more
time moving when compared to instantaneous focals (table 2). Group scans also
showed that the howler monkeys spent less time feeding and more time moving than
continuous focals (table 2). Instantaneous focals indicated that the howlers spent
more time engaged in social interactions compared to both continuous focals and
group scans (table 2).

92 Folia Primatol 2013;84:87–101 Amato /Van Belle /Wilkinson

DOI: 10.1159/000348305
Table 2. Differences in pairwise data collection methods and corresponding one-sample t tests and p values

Group scans vs. Instantaneous vs. Continuous focals vs.

instantaneous focals continuous focals group scans
means ± SD t p means ± SD t p means ± SD t p

Activity
Feeding –0.031 ± 0.032 –3.48 0.005 –0.013 ± 0.045 –1.11 0.288 –0.036 ± 0.024 –5.48 0.000
Howling 0.005 ± 0.014 1.50 0.161 0.005 ± 0.022 –0.74 0.472 0.004 ± 0.012 1.09 0.298
Moving 0.077 ± 0.035 7.98 0.000 0.004 ± 0.018 –0.71 0.489 0.044 ± 0.026 6.05 0.000
Resting –0.030 ± 0.046 –2.36 0.036 0.011 ± 0.051 0.79 0.444 –0.016 ± 0.039 –1.48 0.165
Social interaction –0.022 ± 0.019 –4.29 0.001 0.011 ± 0.018 2.24 0.045 0.004 ± 0.008 1.72 0.112
Food type
Young leaves 0.048 ± 0.128 1.35 0.202 –0.084 ± 0.185 –1.63 0.128 –0.01 ± 0.094 –0.52 0.615
Mature leaves –0.007 ± 0.039 –0.68 0.508 –0.045 ± 0.076 –2.16 0.052 –0.04 ± 0.049 –2.95 0.012
Young fruits –0.008 ± 0.070 –0.42 0.684 0.006 ± 0.024 0.88 0.397 –0.01 ± 0.080 –0.40 0.698
Mature fruits 0.050 ± 0.068 2.65 0.021 –0.053 ± 0.110 –1.76 0.104 –0.01 ± 0.093 –0.30 0.766
Stems –0.013 ± 0.069 –0.67 0.516 0.027 ± 0.110 0.87 0.402 0.00 ± 0.047 0.01 0.994

n = 13 for each test. Bold p values indicate significant differences between two data collection methods (α = 0.050).

Despite some differences in the actual percentage of time spent in each activity
shown by each method, all methods indicated that the howlers spent the largest per-
centage of time resting, followed by feeding, and then moving, social interactions, and
howling. There were also no differences in activity patterns between adult sex classes
regardless of the method being used (all p > 0.05), and all methods showed differences
in activity budget according to age class (fig. 2). Both group scans and instantaneous
focals showed that juveniles spent more time moving and being social and less time
howling and resting than adults. Neither method showed age differences in the time
spent feeding.

Diet
Although the amount of time spent feeding was correlated among all observation
methods, the percentage of feeding time dedicated to different food types was not.
The average percentage of total feeding time dedicated to young fruits was not strong-
ly correlated between group scans and continuous focals or between group scans and
instantaneous focals (table 1). The average percentage of total feeding time spent con-
suming young and mature leaves and stems was not correlated between the two focal
observation methods (table 1). However, the differences between the values calcu-
lated using each observation method did not differ significantly from zero in most
cases (table 2). The two exceptions were that group scans indicated more time spent
consuming mature fruits than instantaneous focals and more time spent consuming
mature leaves than continuous focals.
When we examined feeding patterns using each method, both groups spent the
same amount of time feeding on most food types (all p > 0.05) except young leaves
(p = 0.004) and stems (p = 0.003). Data for both groups were analyzed together for all
categories except young leaves and stems. Comparisons of feeding patterns using

A Comparison of Howler Monkey Observation Folia Primatol 2013;84:87–101 93

Methods DOI: 10.1159/000348305
 Feeding Resting
0.30 1.00
a a a
0.25 a a 0.80 a a a
a a a
a b
Monthly rate

Monthly rate
0.20
a a 0.60 b
0.15
0.40
0.10
0.05 0.20

0 0
GRP SCN INST FCL CONT FCL GRP SCN INST FCL CONT FCL

Moving Howling
0.25 0.05 a a
b
0.20 0.04 a

Monthly rate
Monthly rate

0.15 0.03
a a b b
0.10 0.02
a a b
a a
0.05 0.01
c b b
0 0
GRP SCN INST FCL CONT FCL GRP SCN INST FCL CONT FCL

Social interactions
0.10 c

0.08 b
Monthly rate

0.06

0.04
a a
0.02 a a a
b
0
GRP SCN INST FCL CONT FCL

Fig. 2. Monthly rates of feeding, moving, resting, howling, and engaging in social interactions by
adult males (dark gray bars), adult females (white bars), and juveniles (light gray bars) for data
collected via group scan (GRP SCN), instantaneous focals (INST FCL), and continuous focals
(CONT FCL). Statistically significant differences among the age classes within each data collec-
tion method are indicated by different letters (a, b, or c). n = 13 for each bar. Means ± SE.

these data revealed no significant differences in time spent consuming any food type
among age or adult sex classes for any method (fig. 3).

Proximity
In general, the correlations among methods for proximity data were weaker than
the correlations observed among methods for activity data, suggesting that the over-
all proximity patterns described by each method were less similar than the activity

94 Folia Primatol 2013;84:87–101 Amato /Van Belle /Wilkinson

DOI: 10.1159/000348305
 Mature leaves Young leaves
0.20 0.50
a a a
b a a
0.16 0.40 a
a a

Monthly rate
Monthly rate

0.12 0.30
a a
0.08 a 0.20
a a a
0.04 a 0.10

0 0
GRP SCN INST FCL CONT FCL GRP SCN INST FCL CONT FCL

Mature fruits Young fruits

0.35 0.14
a
0.30 a 0.12
a a
a
0.25 a 0.10
Monthly rate

Monthly rate
0.20 0.08 a
0.15 a a a 0.06 a a
a a
0.10 0.04 a
a
0.05 0.02
0 0
GRP SCN INST FCL CONT FCL GRP SCN INST FCL CONT FCL

Stems
0.20
a a
0.16
a a a
Monthly rate

0.12 a
a
a
0.08

0.04

0
GRP SCN INST FCL CONT FCL

Fig. 3. Monthly rates of feeding on mature and young leaves, mature and young fruits, and stems
by adult males (dark gray bars), adult females (white bars), and juveniles (light gray bars) for data
collected via group scan (GRP SCN), instantaneous focals (INST FCL), and continuous focals
(CONT FCL). Statistically significant differences among the age classes within each data collec-
tion method are indicated by different letters (a, b, or c). n = 13 for each bar. Means ± SE.

and diet patterns. However, correlations between group proximity scans and focal
proximity scans in both distance categories were higher than between focal nearest
neighbor samples and either group proximity scans or focal proximity scans (table 3).
In fact, only a few significant correlations were observed between focal nearest neigh-
bor samples and the other two methods. These correlations only occurred in the 0- to
1-meter category (table 3). Therefore, there was little agreement between focal nearest
neighbor samples and both other methods in terms of data patterns.

A Comparison of Howler Monkey Observation Folia Primatol 2013;84:87–101 95

Methods DOI: 10.1159/000348305
Table 3. Pearson correlations coefficients (r) and p values for pairwise comparisons among the three activ-
ity data collection procedures for proximity data

Dyad Instantaneous focals vs. Instantaneous vs. Continuous focals vs.

group scans continuous focals group scans
r p r p r p

0–1 m
AM-AM 0.005 0.988 –0.205 0.503 0.825 0.002
AF-AF 0.622 0.041 0.692 0.009 0.945 0.000
AM-AF 0.330 0.322 0.621 0.023 0.644 0.032
AF-J 0.646 0.032 0.781 0.002 0.864 0.001
AM-J 0.510 0.109 0.729 0.005 0.787 0.004
>1 – 5 m
AM-AM –0.372 0.260 –0.341 0.729 0.683 0.021
AF-AF 0.034 0.920 0.341 0.255 0.756 0.007
AM-AF –0.716 0.013 –0.439 0.133 0.873 0.000
AF-J 0.153 0.654 –0.215 0.480 0.678 0.022
AM-J –0.126 0.710 –0.057 0.854 0.781 0.005

n = 13 for each test. Bold p values indicate significant correlations between two data collection methods
after sequential Bonferroni corrections with the initial α set at 0.050. AM = Adult male; AF = adult female;
J = juvenile.

Table 4. Pairwise differences of data collection methods and corresponding one-sample t tests and p values

Dyad Instantaneous focals vs. Instantaneous vs. Continuous focals vs.

group scans continuous focals group scans
means ± SD t p means ± SD t p means ± SD t p

0–1 m
AM-AM –0.014 ± 0.035 –1.31 0.218 –0.010 ± 0.050 –0.75 0.470 0.001 ± 0.028 –0.11 0.918
AF-AF –0.127 ± 0.097 –4.32 0.002 –0.107 ± 0.138 –2.80 0.016 0.000 ± 0.062 0.01 0.993
AM-AF –0.022 ± 0.030 –2.41 0.037 –0.020 ± 0.021 –3.44 0.005 –0.005 ± 0.021 –0.82 0.430
AM-J –0.023 ± 0.031 –2.45 0.034 –0.008 ± 0.020 –1.37 0.196 –0.016 ± 0.022 –2.45 0.034
AF-J –0.036 ± 0.052 –2.29 0.045 –0.051 ± 0.050 –3.66 0.003 0.019 ± 0.044 1.47 0.171
>1 – 5 m
AM-AM –0.146 ± 0.102 –4.74 0.001 –0.113 ± 0.090 –4.52 0.001 –0.022 ± 0.065 –1.10 0.296
AF-AF –0.147 ± 0.119 –4.08 0.002 –0.126 ± 0.100 –4.53 0.001 –0.006 ± 0.078 –0.27 0.792
AM-AF –0.157 ± 0.143 –3.65 0.004 –0.148 ± 0.133 –4.01 0.002 0.003 ± 0.045 0.21 0.837
AM-J –0.129 ± 0.105 –4.05 0.000 –0.128 ± 0.082 –5.64 0.001 0.009 ± 0.058 0.51 0.623
AF-J –0.144 ± 0.065 –7.36 0.002 –0.119 ± 0.094 –4.55 0.000 –0.012 ± 0.060 –0.68 0.509

n = 13 for each test. Bold p values indicate significant differences between two data collection methods (α = 0.050).
AM = Adult male; AF = adult female; J = juvenile.

96 Folia Primatol 2013;84:87–101 Amato /Van Belle /Wilkinson

DOI: 10.1159/000348305
 0–1 m
0.20 b
b b
b bc c
0.16 b
Mean ± SE monthly rate

bc
0.12

0.08 c b
ac c
a a ac
0.04 a a

0
a GRP SCN FCL SCN NRST NEIGHB

>1–5 m AM-AM
0.30 a a
a AF-AF
a a
0.25 AM-AF
Mean ± SE monthly rate

a a a AM-J
a a AF-J
0.20
a J-J
0.15 b b
0.10
a a
a
0.05 a

0
b GRP SCN FCL SCN NRST NEIGHB

Fig. 4. Monthly rates of time spent at 0–1 m (a) and at >1–5 m (b) for adult male (AM)-AM dy-
ads, adult female (AF)-AF dyads, AM-AF dyads, AM-juvenile (J) dyads, AF-J dyads, and J-J dy-
ads from data collected via group proximity scans (GRP SCN), focal proximity scan (FCL SCN),
and focal nearest neighbor sampling (NRST NEIGHB). Statistically significant differences among
the age classes within each data collection method are indicated by different letters (a, b, or c).
n = 13 for each bar. Means ± SE.

Similarly, the difference between average monthly values varied significantly

from zero for every age-sex dyad in the >1- to 5-meter category for all comparisons
involving focal nearest neighbor samples (table 3). Specifically, focal nearest neighbor
samples underestimated the time spent at this distance for almost every combination
of dyads. Fewer significant differences were observed in the 0- to 1-meter category.
In contrast, differences in the values reported by group proximity scans and focal
proximity scans did not diverge from zero in almost any case (table 4).
Additionally, group proximity scans and focal proximity scans provided the
same general proximity patterns across age and sex classes (fig. 4), while focal nearest
neighbor samples differed from both group proximity scans and focal proximity
scans in several cases. For example, only focal nearest neighbor samples indicated that
the amount of time spent at 0–1 m differed between adult male-juvenile dyads and

A Comparison of Howler Monkey Observation Folia Primatol 2013;84:87–101 97

Methods DOI: 10.1159/000348305
adult male-adult female dyads (fig. 4). Both scan methods reported that adult male-
adult female dyads spent less time at 0–1 m than adult female-adult female dyads,
adult female-juvenile dyads and juvenile-juvenile dyads, but focal nearest neighbor
samples did not detect these differences (fig. 4). Finally, focal nearest neighbor sam-
ples indicated that adult male-adult female dyads and adult female-juvenile dyads
spent more time at >1–5 m than other dyads while neither of the other methods
showed any difference in the amount of time spent by any dyad at this distance from
each other (fig. 4).

Discussion

As expected with a primate species that exhibits high group cohesiveness, group
scans, continuous focals, and instantaneous focals generally provided similar infor-
mation about howler monkey activity and diet. The majority of activity and diet data
were correlated across methods, suggesting that all methods documented similar pat-
terns in behavior. For example, if group scans indicated the howlers spent a larger
percentage of time feeding in month A compared to month B, so did continuous fo-
cals and instantaneous focals. The observed discrepancies emerged mostly for catego-
ries that occurred with less frequency during the study period (e.g. howling, moving,
or feeding on young fruits). In these cases, it seems likely that the mismatches were a
product of scatter in the data from small sample sizes and not necessarily a reflection
of the quality of the method itself [Edwards et al., 2010]. Indeed, when the actual per-
centage of time spent in these weakly correlated activities was compared using t tests,
few differences were detected among methods.
However, despite the similarities in patterns among datasets, important differ-
ences did exist in the percentage of time each method showed the howlers spending
in each activity. To begin with, t tests suggested that group scans underestimate time
spent feeding and overestimate time spent moving. A bias toward moving in scan
samples has been detected in other studies [Rose, 2000; Stevenson and Quinones,
2004], and although the cohesive nature of howler monkey social groups leads to a
low interindividual variation in activity that might counteract this effect, howler
groups are naturally less cohesive during travel bouts [pers. observation]. At these
times, howler monkeys moving within or between trees are more likely to stand out.
Therefore, when observers are challenged to locate and score the activity of all indi-
viduals in a social group in a short time period during group scans, there may be a
bias toward locating moving individuals. Similarly, if individuals are moving during
a feeding bout (i.e. foraging) an observer bias toward moving could result in a bias
against feeding. Although the protocol for group scans that was employed in this
study was designed to eliminate the bias toward moving by implementing a 5-second
minimum duration for an activity to be recorded [Fragaszy et al., 1992; Kortsjens et
al., 2005], our t test results suggest that this effort was not entirely successful. There-
fore, another measure must be taken to counteract the group scan bias toward mov-
ing if studies collecting group scan data are to be compared with focal data, especial-
ly in primates with larger interindividual distances.
Our comparisons also provided evidence that instantaneous focals overestimate
social behavior when compared to the other two data collection procedures. Instan-
taneous focals assume the recorded proportions of the behaviors performed by the

98 Folia Primatol 2013;84:87–101 Amato /Van Belle /Wilkinson

DOI: 10.1159/000348305
Table 5. Summary of pros and cons for each observational method as utilized for describing
howler monkey activity, diet and proximity among individuals

Group scans Instantaneous focals Continuous focals

Activity Accurate overall patterns Accurate overall patterns Accurate overall

patterns
Overestimates moving Overestimates sociality No bias detected
Underestimates feeding
Diet Accurate overall patterns Accurate overall patterns Accurate overall
patterns
Overestimates mature fruit feeding No bias detected No bias detected
Overestimates mature leaf feeding

Group proximity scans Focal nearest neighbor sample Focal proximity scans

Proximity Accurate overall patterns Inaccurate overall patterns Accurate overall

patterns
No bias detected Underestimates time at 0 – 1 m No bias detected
Underestimates time at >1 – 5 m

focal are related to the real-time durations of those behaviors when the interval be-
tween the records is short enough. For most howler monkey behaviors, our chosen
interval of 2 min appears to be short enough since the howlers engage in those behav-
iors for at least 2 min at a time. However, with the exception of juvenile play, social
behavior in howler monkeys rarely lasts more than a few seconds. Therefore, for a
social behavior recorded for a focal individual at any given time point the proportion
of time spent in that behavior as described by instantaneous focal data will overesti-
mate the amount of real time spent in that behavior. In a species that engages in social
behavior more frequently and/or in which social bout duration is longer, this error
may be less dramatic [Rose, 2000].
Because group scans record behavior at longer intervals, we would expect it to
overestimate social behavior as well. However, there is a lower probability of social
behavior occurring on a 15-min time point than on a 2-min time point, and subtle
social behaviors may be easily overlooked by observers during scan sampling. Fur-
thermore, group scans record the behaviors of all group members at each time point
instead of that of a single focal individual. For howler monkeys, it is uncommon for
all group members to engage in social behavior at once. As a result, the social behav-
ior of a individual at a single group scan time point is balanced by the activities of all
other individuals at that time point. Additionally, because group scans provide data
for all individuals for the duration of the day instead of for the activity of a single in-
dividual during one or two focal periods (over the course of a day), it may counteract
biases toward infrequent activities that occur during a single scan.
Finally, dramatic differences occurred among methods for describing spatial as-
sociations among group members. While proximity data from scan samples of the
entire group and relative to the focal individual corresponded well, focal nearest
neighbor samples consistently provided distinct patterns and values, suggesting that
focal nearest neighbor samples are ineffective for estimating the amount of time pairs

A Comparison of Howler Monkey Observation Folia Primatol 2013;84:87–101 99

Methods DOI: 10.1159/000348305
of individuals spent at different distances from each other. Nearest neighbor sam-
pling is designed to identify a focal individual’s nearest neighbor, often for the pur-
pose of determining the influence of that neighbor on the focal individual’s behavior.
It is not designed to estimate the position of the focal individual in relation to all
other individuals or the position of all individuals in relation to each other, as the scan
methods do. In a species with less spatial association among group members, nearest
neighbor data are likely to provide a fairly accurate representation of proximity pat-
terns at distances within 5 m. However, for howler monkeys, using focal nearest
neighbor data for this purpose is inappropriate since individuals are frequently in
close proximity (<5 m) to more than 1 individual at a time. Recording 1 individual as
the nearest neighbor in this situation leads to oversimplification.
The differences we detected among both behavioral and proximity data collec-
tion methods in this study demonstrate that not all behavioral observation methods
are easily interchangeable, even in primates with cohesive social groups and infre-
quent behavior shifts. Careful thought must be given to the types of questions one
wishes to answer before choosing an observation method, and after a method is cho-
sen, it must be validated. We found that, for howler monkeys, group scans and con-
tinuous and instantaneous focals are effective tools for determining general activity
budgets (table 5). However, studies focused on social behavior should avoid the use
of instantaneous focals (table 5). Likewise, group proximity scans and focal proxim-
ity scans provide similar data regarding the time group members spent in proximity
to each other while focal nearest neighbor samples are more appropriate for deter-
mining the influence of one individual on another at any given moment (table 5).
These patterns are likely to vary in other primate species with distinct behavioral pat-
terns and social systems.
While most researchers consider which observation methods are best when de-
signing a study, few of us actually test them. With concurrent projects happening at
many field sites, comparisons of data collection methods are becoming easier. We
recommend that additional studies collect comparative data to compare the effects of
sampling methods on patterns in behavioral and proximity data. Only by under-
standing the strengths and weaknesses of observation methods for a variety of pri-
mate species across a variety of sites can we truly evaluate similarities and differences
in primate behavior among studies.

Acknowledgments

We thank the Mexican government environmental agency for research permission to work
in Palenque National Park, granted to Dr. Alejandro Estrada. We thank the Universidad Nacional
Autónoma de México for logistical and financial support. K.R.A. was funded by a National Geo-
graphic Waitt Grant and University of Illinois Dissertation Travel Grant, and is also supported
by an National Science Foundation Graduate Research Fellowship. S.V.B. was supported by a
postdoctoral fellowship from Universidad Nacional Autónoma de México. K.R.A. is grateful
to S. Wengert, and S.V.B. is grateful to E. Pain, B. Thomas, E. Thom, P. Boone, L. Cervera, T.
Roberts, S. Schindel, and M. Groenenberg who provided support in the field. We also thank 3
anonymous reviewers for their comments.

100 Folia Primatol 2013;84:87–101 Amato /Van Belle /Wilkinson

DOI: 10.1159/000348305
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