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Behaviour (2019) DOI:10.1163/1568539X-00003582 brill.com/beh
Howling by the river: howler monkey (Alouatta palliata)
communication in an anthropogenically-altered
riparian forest in Costa Rica
Laura M. Bolt a,c,∗,Dorian G. Russell c,d,Elizabeth M.C. Coggeshall c,e,
Zachary S. Jacobson c,f,Carrie Merrigan-Johnson c,gand Amy L. Schreier b,c
aDepartment of Anthropology, University of Waterloo, Waterloo, ON, Canada N2L 3G1
bDepartment of Biology, Regis University, Denver, CO 80221, USA
cThe Maderas Rainforest Conservancy, P.O. Box 55-7519, Miami, FL 33255-7519, USA
dDepartment of Environmental Science, American University, Washington, DC, USA
eDepartment of Anthropology, Central Washington University, Ellensburg, WA, USA
fDepartment of Anthropology and Archaeology, University of Calgary, Calgary, AB,
Canada
gDepartment of Anthropology, University of Toronto at Mississauga, Mississauga, ON,
Canada
*Corresponding author’s e-mail address: laurabolt@gmail.com
Received 21 June 2019; initial decision 3 August 2019; revised 1 October 2019;
accepted 4 November 2019
Abstract
The ways that forest edges may affect animal vocalization behaviour are poorly understood. We
investigated the effects of various types of edge habitat on the loud calls (howls) of a folivorous-
frugivorous primate species, Alouatta palliata, with reference to the ecological resource defence
hypothesis, which predicts that males howl to defend vegetation resources. We tested this hypoth-
esis across four forest zones — interior, riparian, anthropogenic, and combined forest edges — in
a riparian forest fragment in Costa Rica. We predicted vegetation and howling would differ be-
tween forest zones, with riparian and interior zones showing the highest values and anthropogenic
edge the lowest. Our results indicated that vegetation was richer and howling longer in riparian
and interior zones compared to combined and anthropogenic edges, supporting the resource de-
fence hypothesis and providing some of the first evidence in animal communication scholarship
for differences in behavioural edge effects between natural riparian and anthropogenic edges.
Keywords
river edge, natural forest edge, edge effects, habitat quality, ecological resource defence
hypothesis, roar, long-distance call, loud call.
©Koninklijke Brill NV, Leiden, 2019 DOI 10.1163/1568539X-00003582
2Behaviour (2019) DOI:10.1163/1568539X-00003582
Resumen
Las formas en que los bordes del bosque pueden afectar el comportamiento vocal de los animales
son poco conocidas. Investigamos los efectos de varios tipos de hábitat de borde en los gritos (aulli-
dos) de una especie de primate folívoro-frugívora, Alouatta palliata, con referencia a la hipótesis
de la defensa de los recursos ecológicos, la cual predice que los machos aúllan para defender los
recursos vegetales. Probamos esta hipótesis en cuatro zonas forestales: interior, ribereña, antro-
pogénica y una combinación de bordes de bosque, en un fragmento de bosque ribereño en Costa
Rica. Predijimos que la vegetación y el aullido diferirían entre las zonas forestales, con zonas
ribereñas e interiores mostrando los valores más altos y el borde antropogénico los más bajos.
Nuestros resultados indicaron que la vegetación era más rica y el aullido prolongado en las zonas
ribereñas e interiores en comparación con los bordes combinados y antropogénicos, respaldando
la hipótesis de defensa de los recursos y proporcionando algunas de las primeras pruebas en la
investigación de la comunicación animal para diferencias en el comportamiento relacionadas con
los efectos de bordeentre los bordes naturales ribereños y los antropogénicos.
Palabras clave
borde del río, borde natural del bosque, efectos de borde, calidad del habitat, defensa de
recursos ecológicos hipótesis, rugido, llamada de larga distancia, llamada fuerte.
1. Introduction
When forest adjoins a different habitat type, the borders represent an edge
zone, where there is a transition in the biotic and abiotic properties of the
landscape (Laurance, 1991; Schwitzer et al., 2011). The amount of moisture,
solar energy, and wind in edge zones differs from forest interior (Lovejoy et
al., 1986; Harris, 1988; Cadenasso et al., 2003), leading to changes in the
vegetation, which may impact how wildlife use the space. Forest edges may
be human-caused and due to deforestation, but also occur naturally. Riparian
(river) edges, for example, represent one type of natural edge, marking the
transition from aquatic to terrestrial environments (Swanson et al., 1982).
Riparian edges extend as far as 50 m from a riverbank (Grebner et al., 2013)
and are less windy with more moisture in the soil compared to other nearby
habitats (Swanson et al., 1982). Consequently, riparian zone vegetation usu-
ally has more water-tolerant plant and tree species (Richardson & Danehy,
2007) and higher biodiversity than other types of forest edge (Grebner et al.,
2013). Riparian edges are important corridors for wildlife, with undisturbed
vegetation along river edges allowing animals to travel through fragmented
forests and otherwise modified landscapes (Payne & Bryant, 1998). These
riparian corridors mitigate long-term negative impacts on species living in
fragmented landscapes through preventing isolation and inbreeding, and are
therefore important habitat features to preserve for conservation purposes
L.M. Bolt et al. / Behaviour (2019) 3
(Payne & Bryant, 1998). However, the large-scale destruction of tropical
forests worldwide (Haddad et al., 2015) has drastically increased the pro-
portion of anthropogenic forest edge. To meaningfully gauge the impact of
anthropogenic edges on wildlife, we need to better understand the effects of
naturally-occurring forest edge – such as riparian edge – on animal behaviour
(Murcia, 1995).
Non-human primates, as indicator species whose global welfare is threat-
ened by anthropogenic deforestation (Mace & Balmford, 2000; Estrada et
al., 2017), are ideal study subjects for investigating how edge effects im-
pact behaviour across both natural and anthropogenic edges. Primate long-
distance vocal communication behaviour differed between forest interior and
anthropogenic edge in previous study (Bolt et al., 2019), suggesting that
communication patterns should also be compared across natural riparian
edges. Long-distance calls (loud calls) are produced by a range of animal
taxa including primates, and can carry for more than 1 km through for-
est environments (Bradbury & Vehrencamp, 1998; Delgado, 2006). Loud
calls are typically uttered by adult males, exchanged between individuals
and groups, and thought to have a variety of adaptive functions including
the defence of resources (Bradbury & Vehrencamp, 1998; Wich & Nunn,
2002). The ecological resource defence hypothesis for loud calling posits
that males call to defend their group’s access to preferred food or space re-
sources, such as feeding trees and preferred territory areas (Wich & Nunn,
2002). While this hypothesis has support from a number of primate species
(e.g., red howler monkey (Alouatta seniculus), Sekulic, 1982; Thomas lan-
gur (Presbytis thomasi), van Schaik et al., 1992; black-and-white colobus
monkey (Colobus guereza), Fashing, 2001; gibbon (Hylobates spp.) Wich
et al., 2002), no studies to date have compared primate loud-calling be-
haviour across natural edges, anthropogenic edges, and forest interior within
the same forest landscape; doing so will lead to increased awareness of how
diverse types of edge effects may impact primates and will help clarify the
effects of anthropogenic habitat destruction.
This study examines the effects of riparian and anthropogenic edges on
monkey loud calling behaviour within a fragmented tropical rainforest in
Costa Rica, the La Suerte Biological Research Station (LSBRS). LSBRS is
located in the Caribbean lowland region of northeastern Costa Rica which
has been mostly deforested since the 1970’s due to ranching and corporate
agriculture (Garber et al., 2010; Molina, 2015). LSBRS has been reforested
4Behaviour (2019) DOI:10.1163/1568539X-00003582
since the 1990’s, and now has tall, secondary growth forest through much of
the site (Molina, 2015; Brandt & Singleton, 2018; Russell, 2018). It currently
represents one of the few relatively large (3 km2) forest fragments in the
broader region. At LSBRS, the forest interior consists of a dense, continuous
canopy of large trees (Pruetz & Leasor, 2002) while the anthropogenic forest
edge transitions sharply from continuous forest to roads, ranches and other
plantations (Molina, 2015). The La Suerte River flows through the interior of
LSBRS before joining the Tortuguero River and draining into the Caribbean
Ocean. The presence of natural riparian edges adjacent to the forest interior
as well as anthropogenic edges surrounding the fragment at LSBRS make
this an ideal site at which to examine differences in vocalization behaviour
across forest interior and various types of forest edge zones.
Previous investigation at this site (Bolt et al., 2019) compared the loud
calling (howling) behaviour of a platyrrhine primate species, the mantled
howler monkey (Alouatta palliata), across forest interior and 100 m an-
thropogenic edge zones, and found that howling bouts in the interior were
significantly longer and contained a greater number of howls than in an-
thropogenic edge. These results supported the ecological resource defence
hypothesis, with longer howling bouts found in areas of richer interior vege-
tation resources (Bolt et al., 2019). The present follow-up study divides the
forest at LSBRS into a greater number of landscape zones to further exam-
ine variation in howling behaviour and its potential causes, in order to more
accurately assess the effects of forest edge on monkeys inhabiting a forest
fragment.
1.1. Hypothesis 1: vegetation will differ in riparian vs. anthropogenic edges
Based on variation in vegetation across riparian and anthropogenic forest
zones (Richardson & Danehy, 2007; Grebner et al., 2013), we expected that
riparian edge would differ in vegetation characteristics compared to forest
interior and anthropogenic edge. Previous research at LSBRS on a separate
dataset of a smaller number of vegetation transects found lower tree canopy
cover and tree species richness in anthropogenic edge compared to forest in-
terior (Bolt et al., 2018, 2019), but did not examine vegetation differences
between riparian edge and other habitat types. Given these findings (Bolt et
al., 2018, 2019), we predicted that percentage of canopy cover, mean tree
diameter at breast height (DBH), and mean tree height would vary between
forest zones, with forest interior showing the highest vegetation values, ripar-
ian edge showing intermediate values, and anthropogenic edge showing the
L.M. Bolt et al. / Behaviour (2019) 5
lowest vegetation values. We considered the vegetation measures included
in this study to indicate high-quality vegetation for primates as previous re-
search has indicated that the size and abundance of trees in a forest area pre-
dict primate abundance (Ross & Srivastava, 1994; Mbora & Meikle, 2004),
while higher levels of canopy cover signify a better-quality primate habitat
(Arroyo-Rodríguez & Mandujano, 2006).
1.2. Hypothesis 2: howling for ecological resource defence
If, as previously suggested, howler monkeys at LSBRS howl to defend eco-
logical resources (Bolt et al., 2019), we would expect howling to occur more
often in areas of rich vegetation, which are likely to contain more preferred
resources for howler monkeys. Given previous findings at LSBRS showing
longer howling bouts containing a greater number of howls in forest interior
compared to anthropogenic edge (Bolt et al., 2019), we similarly predicted
that monkeys would howl at the highest rates, have the longest howling
bouts, and produce more howls per howling bout when in forest interior
regions and riparian edge regions, in order to defend the high-quality veg-
etation resources likely to be located there. Building on previous findings,
we also expected howling rate would be higher and howling bouts would be
longer with more howls in riparian edge compared to anthropogenic edge,
given the higher plant species richness found in natural edges compared to
anthropogenic edges (Ramos & Santos, 2006; Skrinyer, 2016).
2. Methods
2.1. Study site
We conducted this study at the La Suerte Biological Research Station (LS-
BRS) in northeastern Costa Rica (10°26N, 83°46W). This site is a tropical
lowland rainforest comprising approximately 3 km2of primary forest, sec-
ondary forest, and regenerating pastures (Pruetz & Leasor, 2002; Garber et
al., 2010). The main forest fragment where we conducted this study is com-
posed of two connected forest patches (‘Large Forest’ =0.94 km2to the
north end of the site and ‘Small Forest’ =0.35 km2to the south end of the
site) and a small deforested area for ‘camp’ (0.07 km2in the centre of the
site) (Molina, 2015; Bolt et al., 2018, 2019; Figure 1).
The mantled howler monkey is a group-living, folivorous-frugivorous
platyrrhine primate that is well known for its howl vocalizations (di Fiore
6Behaviour (2019) DOI:10.1163/1568539X-00003582
Figure 1. Map of La Suerte Biological Research Station (LSBRS) showing 50 m edge zones
and vegetation survey plots.
et al., 2011; reviewed in Kitchen et al., 2015; described in detail in Bolt
et al., 2019). This species shares LSBRS with the Central American spider
monkey (Ateles geoffroyi) and the white-faced capuchin monkey (Cebus ca-
pucinus). Population survey estimates suggest that the Large Forest contains
L.M. Bolt et al. / Behaviour (2019) 7
6–8 groups of howler monkeys, while the Small Forest contains 2–3 groups
(Pruetz & Leasor, 2002; Garber et al., 2010). During the course of this study,
we observed and collected data from approximately 11 groups of mantled
howler monkeys (Bolt et al., 2019).
2.2. Vegetation data collection
Although previous investigations at LSBRS defined anthropogenic forest
edge as 100 m (Bolt et al., 2018, 2019), for the current study we defined
forest edge as 50 m from any natural or anthropogenic forest boundary, fol-
lowing previous research evaluating the depth of edge influence on plants, in-
sects, and birds in both natural and disturbed forest landscapes (e.g., Harper
& Macdonald, 2001; Magura, 2002; Harper et al., 2005; Roume et al., 2011;
Stone et al., 2018). This 50 m edge definition for riparian edge is better sup-
ported by existing literature (Laurance et al., 2009; Pohlman et al., 2009;
Grebner et al., 2013). We divided the forest at LSBRS into four different
zones for analysis: riparian forest edge (within 50 m of the La Suerte River),
forest interior (more than 50 m from any type of forest edge), anthropogenic
forest edge (within 50 m of deforested area including camp, roads, and neigh-
bouring cattle ranches and coconut plantations), and combined riparian and
anthropogenic forest edge (the edge area within 50 m of both the river and
anthropogenically deforested area that contains both (i.e., overlapping) types
of forest edge; referred to as combined edge; Figure 1).
We collected vegetation data from May–August 2017 and May–July 2018,
with a total of 44 vegetation plots conducted throughout the LSBRS for-
est fragment: 6 plots in riparian edge, 25 plots in forest interior, 9 plots in
anthropogenic edge, and 4 plots in combined edge (Figure 1). Vegetation
plots measured 5 ×10 m and were spread throughout LSBRS across ri-
parian edge, forest interior, anthropogenic edge, and combined edge zones
(Figure 1). Using a central transect line within each plot, at each one-meter
interval we estimated canopy cover with a cardboard scope on a scale of 1–4
(1 =0–25% cover, 2 =26–50%, 3 =51–75% and 4 =76–100%). Within
each vegetation plot, we measured all trees over 10 cm in circumference with
a standard forestry tape reel, then calculated tree diameter at breast height
(DBH). Within each plot we also measured tree height using a hypsometer
for all trees 10 m tall or higher. We only collected tree height data in 2018
(N=22 of 44 vegetation plots).
8Behaviour (2019) DOI:10.1163/1568539X-00003582
2.3. Howling data collection
We collected data on mantled howler monkey howling behaviour from May–
August 2017 and 2018 (see Bolt et al., 2019 for a map of the site showing
behavioural sampling points). Researchers actively searched for and sampled
monkeys daily between 500 and 1800 hours. We followed groups as they
travelled across various edge and interior habitat zones, and all-occurrences
of howling data were collected for continuous durations of time ranging from
30 min to 5 h. Due to the dense foliage, high forest canopy, and poor visibility
at LSBRS, data collectors stayed as close as possible to monkey groups dur-
ing sampling to ensure that monkeys remained visible. All monkey groups
were well-habituated and did not react to researchers.
During all time spent with a mantled howler monkey group, we con-
ducted all-occurrences sampling (Altmann, 1974) for group-wide howling
behaviour (following Bolt, 2013a, b; Hopkins, 2013; Bolt et al., 2019).
Groups of monkeys ranged from three to 20 individuals of both sexes (Bolt
et al., 2019). When howling from one or more members of the focal group
was heard, we recorded the start time and end time of the howling bout,
the number of howls in the bout, the location of the howling bout (recorded
the location of the howling male by noting the closest trail marker to him
and taking a single GPS point as close to him as possible using a Garmin
GPSMAP 62s Handheld GPS Navigator), and any potential precursor(s) in
the seconds preceding the howl (Bolt et al., 2019). These known howling
triggers were recorded qualitatively, then grouped into one of six categories
for analysis: (1) no observed precursor, (2) other group howling, (3) envi-
ronmental factor (e.g., rain, wind, thunder), (4) intra-group social behaviour
(e.g., agonism, group travel, high arousal non-howl vocalization), (5) inter-
species interaction (e.g., dog, bird, or other monkey species was seen by
researchers and observed interacting with focal howler monkey group) and
(6) anthropogenic noise (e.g., lawn mower, chainsaw, airplane) (Baldwin &
Baldwin, 1976; Van Belle et al., 2013; reviewed in Kitchen et al., 2015; Bolt
et al., 2019).
Howls were defined as male-specific, high-amplitude Type 1/A loud calls
(Carpenter, 1934; Altmann, 1959; Baldwin & Baldwin, 1976) separated from
other long-distance vocalizations made by the caller or members of the same
group by at least 2 s. If individual vocal utterances were continuous or sepa-
rated by less than two seconds, they were considered part of the same howl
vocalization (Bolt et al., 2019). Howls were contained within howling bouts.
L.M. Bolt et al. / Behaviour (2019) 9
A howling bout comprised howls occurring less than 60 seconds apart
(following Sekulic, 1982; Bolt et al., 2019). Howling bouts could therefore
be seconds long and consist of a single howl vocalization by one male, or
many minutes long and consist of a large number of howl vocalizations by
multiple males from the same group. In addition to recording GPS points
to note locations of howling bouts, a GPS point was taken at the location
of every 30-minute period we spent in the presence of a monkey group,
regardless of whether howling occurred during the sample (Bolt et al., 2019).
These GPS sampling points were taken in the approximate centre of the
monkey group and allowed us to determine behavioural sampling frequency
across various forest zones at LSBRS.
2.4. Data analysis
To determine differences in vegetation and howling characteristics across
the four forest zones, we compared percentage of canopy cover, mean tree
DBH, mean tree height, mean length of howler monkey howling bouts, mean
number of howls in howling bouts, and mean howling rate using Kruskal–
Wallis H-tests. For significant values, we performed pairwise asymptotic
(2-sided) post-hoc tests with significance adjusted by the Bonferroni correc-
tion for multiple tests to determine which forest zones differed in vegetation
and howling characteristics. To compare whether howling precursors showed
different distributions than expected by chance across the four forest zones,
we used a Pearson chi-squared test. As a post-hoc test to determine which
precursors varied across forest zones, we examined adjusted residuals and
identified those with z-scores greater than ±1.97 as indicating differences
across forest zones. We used SPSS version 25 (IBM SPSS Statistics, IBM,
Armonk, NY, USA) for all statistical tests, and set the alpha level to 0.05.
3. Results
At LSBRS, overall mean level of canopy cover was 3.00 (approx. 51–75%
coverage; SD =0.98, range =0–100% coverage, N=494), mean tree DBH
was 16.85 cm (SD =28.49, range =3.18–256.24 cm, N=537 trees), and
mean tree height was 15.59 m (SD =5.06, range =10.2–30.2 m, N=70
trees).
Mean level of canopy cover differed significantly across forest zones
at LSBRS (Kruskal–Wallis H3=21.947, p=0.000, N=494; Figure 2).
10 Behaviour (2019) DOI:10.1163/1568539X-00003582
Figure 2. Level of canopy cover across forest zones at LSBRS (p=0.000). Boxes repre-
sent inter-quartile ranges, lines represent median values, whiskers represent maximum and
minimum values and dots represent outliers. Similar asterisks indicate significant differences
between paired forest zones (riparian vs. combined edge, p=0.001; forest interior vs. com-
bined edge, p=0.000).
Canopy cover was significantly higher in riparian edge (3.13 (51–75%
canopy cover), SD =0.89, range =1–4 (0–100% canopy cover), N=76)
than combined edge (2.39 (26–50% canopy cover), SD =1.02, range =
1–4 (0–100% canopy cover, N=44); p=0.001), as was forest interior
(3.11 (51–75% canopy cover), SD =0.95, range =1–4 (0–100% canopy
cover), N=275; p=0.000; Figure 2). Mean level of canopy cover in an-
thropogenic edge (2.88 (26–50% canopy cover), SD =1.00, range =1–4
(0–100% canopy cover), N=99) did not differ significantly from any forest
zones, but showed the non-significant tendency to be higher than combined
edge and lower than riparian edge and forest interior.
Mean tree DBH also varied significantly across forest zones at LSBRS
(Kruskal–Wallis H3=7.894, p=0.048, N=537 trees; Figure 3). Mean
tree DBH was significantly higher in riparian edge (20.49 cm, SD =30.08,
range =3.18–156.55 cm, N=61 trees) than combined edge (12.64 cm,
SD =18.16, range =3.18–83.4 cm, N=49 trees; p=0.042). Mean tree
DBH in forest interior (16.86 cm, SD =26.95, range =3.18–256.24 cm,
N=309 trees) and anthropogenic edge (16.68 cm, SD =34.55, range =
3.18–254.65 cm, N=118 trees) did not differ significantly from other forest
L.M. Bolt et al. / Behaviour (2019) 11
Figure 3. Mean tree DBH across forest zones at LSBRS (p=0.048). Boxes represent
inter-quartile ranges, lines represent median values and whiskers represent maximum and
minimum values. Outliers were removed for graphical purposes. Asterisks indicate signifi-
cant differences between paired forest zones (riparian vs. combined edge, p=0.042).
zones, but showed the tendency of being lower than riparian edge and higher
than combined edge.
Finally, tree height did not differ significantly across forest zones
(Kruskal–Wallis H2=1.15, p=0.563, N=70 trees). Mean tree height
was highest in riparian edge (17.92 m, SD =6.99, range =10.3–29.2 m,
N=9 trees), lower in forest interior (15.30 m, SD =4.98, range =10.2–
30.2 m, N=48 trees), and lowest in anthropogenic edge (15.05 m, SD =
3.53, range =10.2–20.2 m, N=13 trees). There were no trees 10 m in
combined edge.
Howling bout length differed significantly across forest zones (Kruskal–
Wallis H3=14.355, p=0.002, N=641, Figure 4). Pairwise post-hoc
tests showed significant differences in mean howl bout length between ri-
parian edge (165.52 s, SD =388.98, range =1–2882 s, N=156) and
anthropogenic edge (104.62 s, SD =210.32, range =1–1641 s, N=197;
p=0.007) and between riparian edge and combined edge (117.38 s, SD =
251.27, range =1–1133 s, N=63; p=0.042), with longer howl bout
lengths at riparian edge than at combined and anthropogenic edges. Mean
howling bout length in forest interior (mean bout length =109.54 s, SD =
174.69, range =1–1260 s; N=225) did not differ significantly from any
12 Behaviour (2019) DOI:10.1163/1568539X-00003582
Figure 4. Mean howl bout length in seconds across forest zones at LSBRS (p=0.002).
Boxes represent inter-quartile ranges, lines represent median values and whiskers represent
maximum and minimum values. Outliers were removed for graphical purposes. Similar aster-
isks indicate significant differences between paired forest zones (riparian vs. anthropogenic
edge, p=0.007; riparian vs. combined edge, p=0.042).
forest zones, but tended to be shorter than in riparian and combined edges
and slightly longer than in anthropogenic edge.
Mean number of howls per bout also varied significantly across forest
zones (Kruskal–Wallis H3=11.381, p=0.010, N=433, Figure 5). Pair-
wise post-hoc tests indicated significant differences in mean number of howls
per bout between forest interior (5.66 howls/bout, SD =8.90, range =1–60
howls/bout, N=147) and anthropogenic edge (3.77 howls/bout, SD =6.95,
range =1–53 howls/bout, N=158; p=0.035), but other forest zones did
not differ significantly in howling bout length when adjusted values were
compared pairwise. Mean number of howls per bout was highest in riparian
edge (7.86 howls/bout, SD =26.98, range =1–176 howls/bout, N=79),
second-highest in forest interior, smaller in combined edge (5.49 howls/bout,
SD =14.19, range =1–78 howls/bout, N=49) and lowest in anthropogenic
edge.
Howling rate between forest zones did not differ significantly (Kruskal–
Wallis H3=7.639, p=0.054, N=568.5 hours), although differences
closely approached significance. Mean howling rate was highest in ripar-
ian edge (1.36 howls/h, SD =2.43, range =0–12 howls/h, N=111.5h),
L.M. Bolt et al. / Behaviour (2019) 13
Figure 5. Mean number of howls per bout across forest zones at LSBRS (p=0.01). Boxes
represent inter-quartile ranges, lines represent median values and whiskers represent maxi-
mum and minimum values. Outliers were removed for graphical purposes. Asterisks indicate
significant differences between paired forest zones (forest interior vs. anthropogenic edge,
p=0.035).
second-highest in anthropogenic edge (1.29 howls/h, SD =2.57, range =
0–14 howls/h, N=159.5 h), lower in combined edge (1.23 howls/h, SD =
2.17, range =0–10 howls/h, N=50.5 h) and lowest in forest interior (0.895
howls/h, SD =2.02, range =0–18 howls/h, N=247 h).
Finally, there were significant differences in howling precursors across
forest zones (x2(15)=65.783, p=0.000, N=624). The strength of as-
sociation between variables was strong (Cramer’s V-test: ϕc=0.187, p=
0.000), and post-hoc examination of adjusted residuals indicated that when
adjusted for sample size, monkey howling bouts in riparian edge were pre-
ceded by no precursors more frequently than expected and preceded by
environmental factors and intra-group interactions less frequently than ex-
pected by chance (z>±1.97, Table 1). In forest interior, howling bouts were
preceded by inter-species interactions more frequently than expected and by
no precursors less frequently than expected by chance (z>±1.97, Table 1).
In anthropogenic edge, howling bouts were preceded by howls from other
groups and inter-species interactions less frequently than expected, and pre-
ceded by intra-group interactions, environmental factors, and anthropogenic
noise more frequently than expected (z>±1.97, Table 1). In combined
14 Behaviour (2019) DOI:10.1163/1568539X-00003582
Table 1.
Mantled howler monkey (Alouatta palliata) howling precursors at LSBRS showing z-scores for adjusted residual values.
No howling
precursor
Howl from
other group
Environmental
factor
Intra-group
social behaviour
Inter-species
interaction
Anthropogenic
noise
Riparian edge 3.5∗1.2−3.1∗−2.0∗−1.8−1.7
Forest interior −2.8∗1.5−0.8−0.63.9∗0.2
Anthropogenic edge 1.2−3.4∗2.3∗3.4∗−2.7∗2.0∗
Combined edge −2.0∗1.01.8−1.40.3−1.2
Asterisks show significant differences between zones (values >±1.97). Negative results indicate that howling occurrence following a
precursor was lower than expected by chance, while positive results indicate that howling occurrence following a precursor was higher than
expected by chance.
L.M. Bolt et al. / Behaviour (2019) 15
edge, howling was preceded by no precursor less frequently than expected
(z>±1.97, Table 1). Other observed values for howling precursors did not
differ from expected values across forest zones (z<±1.97, Table 1).
4. Discussion
Our results provided some support for the ecological resource defence hy-
pothesis, although alternate explanations are also feasible. Mean level of
canopy cover was higher at riparian edge and forest interior than in com-
bined edge, and mean tree DBH was higher at riparian edge than combined
edge. Tree height also showed a consistent though non-significant trend of
being highest at riparian edge and lowest at anthropogenic edge, indicating
that riparian zones tend to contain taller, larger trees than anthropogenic and
combined edge zones. Monkey howling behaviour also varied across habitat
zones, suggesting that differences in vegetation characteristics may be linked
to observed differences in monkey howling behaviour.
Monkey howl bout length, number of howls per bout, and howling rate
were all highest at riparian edge and bout length and number of howls per
bout were also high in forest interior, suggesting that monkeys may be howl-
ing to defend higher quality vegetation resources in these zones or some other
type of habitat feature, such as denser habitat. These results support previous
findings at LSBRS that mantled howler monkeys have longer howling bouts
containing a greater number of howls in forest interior areas with richer veg-
etation compared to anthropogenic edge areas with poorer vegetation (Bolt
et al., 2019).
Howler monkeys may howl for longer durations of time and utter bouts
containing a greater number of howls when in riparian edge zone due to
the greater proportion of primary forest containing mature feeding tree
species along the river in the largely secondary-growth forest at LSBRS
(Molina, 2015; Russell, 2018). Our vegetation surveys assessed overall tree
and canopy characteristics, but did not identify primary vs. secondary forest
areas, preferred howler monkey feeding tree species, or relative feeding tree
size across forest zones. Mantled howler monkeys preferentially eat from
trees and are selective about the tree species from which they feed (Estrada,
1984). It may be that the riparian zone contains larger, more mature preferred
feeding tree species than all other zones due to its comparative protection
from deforestation during LSBRS’s history as a cattle plantation prior to the
16 Behaviour (2019) DOI:10.1163/1568539X-00003582
1990’s (Garber et al., 2010; Molina, 2015). In tropical regions, riparian zone
trees are more frequently left intact to prevent erosion and nutrient leach-
ing from the soil, even when a site’s other trees may be cut to enable use
of the land for cattle pasture or agriculture (Lees & Peres, 2008). LSBRS
followed this trend of leaving many riparian zone trees — particularly those
closest to the river — when clearing parts of the site for use as a ranch in
the 1960’s (Renee Molina, personal communication). Thus, riparian zones
at LSBRS likely contain a greater proportion of primary forest than other
edge and interior forest zones at LSBRS, which may be driving the observed
differences in howling behaviour. Howler monkeys spend more time in trees
that are larger than average within forests (Munoz et al., 2006) and at LS-
BRS fed from trees that were taller and had higher mean DBH than average
across each habitat zone (Russell, 2018; Schreier & Bolt, unpublished data),
thus exhibiting preference for large trees as food sources. The higher canopy
cover in riparian and interior forest zones at LSBRS suggests that there are
more of these large trees growing closely together in these habitats. However,
further research focused on howler monkey feeding tree usage at LSBRS is
needed.
Howler monkeys may also howl for longer durations in riparian edge and
forest interior for reasons unrelated to vegetation quality. Instead, observed
differences could be due to the acoustics of how this long-range vocalization
carries through vegetation in diverse forest zones. Howls typically carry for
longer distances through thick forest vegetation than through open space (de
Vore, 1979; Waser & Brown, 1986), but are more difficult to localize in these
areas due to differences in sound reverberation (i.e., sound dispersal through
propagation as a result of being reflected by objects; Naguib & Wiley, 2001;
da Cunha et al., 2015), meaning that howler monkeys may need to howl for
longer periods of time when in dense foliage to ensure they can be heard
and located by neighbouring groups. Loud calling is generally energetically
expensive for organisms, and costs are higher when vocalizations are longer
and/or repeated at higher rates (Zahavi, 1975; Prestwich, 1994; Bradbury
& Vehrencamp, 1998). It is adaptive for howler monkeys to utter longer
howling bouts containing a greater number of howls if doing so minimizes
close-range interactions with males from other groups, given that inter-group
encounters often harm mature males (Sekulic, 1982; Chiarello, 1995).
Howler monkeys at LSBRS howl for the longest durations in riparian edge
and forest interior, and may do so to enable better sound localization through
L.M. Bolt et al. / Behaviour (2019) 17
the higher level of canopy cover and thicker vegetation found in these zones,
thus making sure that other monkey groups know where they are. With the ri-
parian edge bordering the river and therefore containing more open space in
the adjacent environment than in forest interior, however, the more open river
environment would seem to contradict longer howls being necessary as com-
pensation for sound reverberation (Waser & Brown, 1986; Naguib & Wiley,
2001). In the present study, howler monkeys in riparian edge howled sponta-
neously (i.e., in response to no known precursor) more often than expected
by chance, while they howled in response to environmental noise less often
than expected. In contrast, monkeys in forest interior howled spontaneously
less often than expected, but howled in response to environmental noise no
more or less often than predicted. These differences between riparian and
interior forest zones may be due to the background noise provided by the La
Suerte River, which could act as a sound source that masks other types of en-
vironmental sound in the riparian edge (e.g., thunder or rain) and/or falsely
triggers howling due to monkeys not being able to clearly identify other types
of sound in their environment. The La Suerte River is fast-flowing, and while
not high in amplitude, is audible in many parts of the riparian edge zone at
LSBRS. This higher level of background noise in the riparian zone could
be stimulating monkeys to both howl spontaneously and utter longer howl-
ing bouts as a way of ensuring other monkey groups do not approach. This
phenomenon could also account for the trend towards higher howling rate
in riparian edge zone. Monkeys would thus howl more by the river than in
other forest zones as a precautionary measure, to discourage the approach of
other monkey groups which they would be less able to accurately detect in
the riparian zone due to a higher level of background noise.
Howl bout length and number of howls per bout may also differ across for-
est zones due to differences in predation pressure at LSBRS. Animals who
call more often and/or for longer periods of time are easier for predators to
locate (Bolt, 2016), which means that it is adaptive for potential prey species
to vocalize less in areas of higher risk. A variety of predators exist at LSBRS,
including ocelots (Leopardus pardalis), tayra (Eira barbara) and venomous
snakes (e.g., Bothrops asper) (Molina, 2015), so it is likely advantageous
for monkeys to be cautious of unfamiliar animals in this species-rich envi-
ronment. While predator abundance across habitat zones has not yet been
determined at LSBRS, increased sound reverberation in the forest interior as
well as the background noise caused by the river in riparian zones may help
18 Behaviour (2019) DOI:10.1163/1568539X-00003582
conceal the location of calling animals from potential predators (Naguib &
Wiley, 2001; da Cunha et al., 2015), meaning that animals may call for longer
durations in these zones without increasing their risk of detection. Further
study is needed to examine the interaction between predator abundance and
howling behaviour across forest zones.
Another possibility is that monkey groups could be howling to defend
specific territory areas at La Suerte. While it is still unknown whether or not
the mantled howler monkey is a territorial species, mantled howler monkey
researchers at some other sites have observed territorial behaviour (e.g., Car-
penter, 1934; Chivers, 1969, but see Mitani & Rodman, 1979; Milton, 1980;
Crockett & Eisenberg, 1987), suggesting that howling behaviour could vary
at La Suerte based on variation in vegetation characteristics between group
territories. Of the 11 monkey groups we studied, we noticed that individual
groups did tend to range within the same general areas, with some overlap
among groups. However, since we were not able to reliably identify groups
during the study period, we were unable to systematically test if the howler
monkeys at La Suerte demonstrated territoriality and the potential connec-
tion between group-level howling behaviour and vegetation quality within a
group’s range. Future study should address these possibilities.
Finally, it is possible that the longer howling bouts in the riparian re-
gion may not relate directly to any one factor, but instead could be due to a
range of variables which are not mutually exclusive. These include a greater
concentration of rich feeding resources with a higher proportion of mature
feeding trees in the riparian zone, acoustic propagation factors due to land-
scape features causing howl bouts to be longer by the river and in forest
interior, and/or lower predator vigilance in the riparian zone.
We collected both howling and vegetation data in May–August over a
two-year period during the Costa Rican wet season. Data collected at other
times of year may yield different results. However, seasonality is not known
to influence feeding behaviour or habitat use in the mantled howler monkey
(Chapman, 1988; Bolt et al., 2018), suggesting that it should not impact
howling behaviour across forest zones (Bolt et al., 2019). We compared
group-level howling differences across habitat zones, but were not able to test
individual male or social group differences in howling behaviour at LSBRS.
We tested the ecological resource defence hypothesis in relation to overall
vegetation quality, but did not test how other forms of resource defence,
such as feeding or resting tree species richness or abundance, may relate
L.M. Bolt et al. / Behaviour (2019) 19
to howling behaviour. Future study should examine individual differences in
howling behaviour, as well as a broader range of ecological factors that may
influence habitat use in the mantled howler monkey.
Our results have important conservation considerations. Mantled howler
monkey howling differed significantly between natural riparian and anthro-
pogenic edge, suggesting that it is proximity to human-caused edge, rather
than to forest edge itself, that is altering monkey communication behaviour
at LSBRS (Bolt et al., 2019). While it is yet unknown what implications
these behavioural changes across different edge zones may have for monkey
fitness, any human-caused alteration of primate behaviour should be avoided
as a general animal welfare goal. Our results suggest that Central American
conservation initiatives should prioritize riparian edge and forest interior for
protection within forests, while anthropogenic edge should be reforested to
ensure the long-term well-being of the mantled howler monkey.
Overall, we found that mantled howler monkey howling properties var-
ied across forest zones at LSBRS. While our results may be interpreted in
several non-mutually exclusive ways, they provide some support for the eco-
logical resource defence hypothesis. In addition to contributing to the body
of scholarship on howler monkey howling function (reviewed in Kitchen et
al., 2015), we provide the first evidence of differences in animal loud calling
behaviour between natural riparian and anthropogenic forest edges.
Acknowledgements
We are grateful to Renee Molina and the Maderas Rainforest Conservancy
for their support and facilitation of our research at the La Suerte Biological
Research Station, Costa Rica. We thank Philip Quinn, Sophie Lieber, Micah
Adams, Stacy Hill and Mareike Janiak for howling data collection. We also
thank Aspen Russell and Stacy Hill for aid in conducting vegetation sur-
veys, and acknowledge Micah Adams, Carson Black, Seriana Gamble, Emily
Glotfelty, Montana Goldsmith, Heather Hicks, Alyssa MacAusland, Renee
Russell and Katie Travis for providing assistance. We acknowledge Ryan
Janzen and Michael Ennis for project support, Eugenia Tsao for technolog-
ical assistance, and Tristan Rhys Williams for inspiration. We also thank
María José Sandí for Spanish abstract translation. This research protocol
was approved by the Regis University Animal Care Committee and was con-
ducted with the permission of the Molina family. Our research was supported
20 Behaviour (2019) DOI:10.1163/1568539X-00003582
by a University Research and Scholarship Council (URSC) Faculty Research
and Scholarship Grant (Regis University), a Cosmos Scholar Award (Cosmos
Club Foundation), an Explorer’s Club Exploration and Field Research Grant,
and the American University Mellon Fund for Graduate Student Research.
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