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Ethology. 2019;125:593–602. wileyonlinelibrary.com/journal/eth
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593
© 2019 Blackwell Verlag GmbH
1 | INTRODUCTION
In group‐living animals, social relationships are mediated by a variety
of vocal signals. While many vocalizations are used by both sexes,
some are sex‐specific and used only by mature males (Bradbury &
Vehrencamp, 1998; Snowdon, 2004). A distinctive and ubiquitous
type of male‐specific vocalization is the loud call or long call, named
for the lon g distance (≥1 km for some s pecies) that the se vocaliza‐
tions carry (Delgado, 20 06; Wich & Nunn, 2002). Many animals pro‐
duce long calls, ranging from insects to amphibians to mammals (e.g.,
Received:9December2018
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Revised:18A pril2019
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Accepted:22April2 019
DOI : 10.1111 /eth .128 86
RESEARCH PAPER
Howling on the edge: Mantled howler monkey (Alouatta
palliata) howling behaviour and anthropogenic edge effects in a
fragmented tropical rainforest in Costa Rica
Laura M. Bolt1,2 | Amy L. Schreier2,3 | Dorian G. Russell2,4 | Zachary S. Jacobson2,5 |
Carrie Merrigan‐Johnson2,6 | Matthew C. Barton2,3 | Elizabeth M. C. Coggeshall2,7
1Depar tment of A nthrop ology, Uni versit y of
Toronto, Toronto, Ontario, Canada
2The Maderas Rainforest Conservancy,
Miami, Florida, USA
3Depar tment of Biology, Regis Univer sity,
Denver, Colorado, USA
4Department of Environmental
Science, American University, Washington,
District of Columbia, USA
5Department of Anthropology, Grand Valley
State University, Allendale, Michigan, USA
6Department of Anthropology, University
of Toronto at Mississauga, Mississauga,
Ontario, Canada
7Department of Anthropology, Central
Washington University, Ellensburg,
Washington, USA
Correspondence
Laura M. Bolt, Depar tment of A nthropology,
University of Toronto, Toronto, ON, Canada
M5S 2S2.
Email: laurabolt@gmail.com
Funding information
Cosmos Club Foundation, Grant/Award
Number: Cosmos Scholar Award; Explorer's
Club, Grant/Award Number: Exploration
and Fiel d Research Grant ; Regis Uni versit y,
Grant /Award Numbe r: URSC Faculty
Research and Scholarship Grant
Abstract
The function of long calling is a subject of interest across animal behaviour study, par‐
ticularly within primatology. Many primate species have male‐specific long‐distance
calls,includingplaty rr hineslikethefolivorou showlermonkey( Alouatta spp.). Howler
monkeysmayhowltodefendresourcessuchasfeedingtreesorareasofrichvegeta‐
tionfromothermonkeygroups.Thisstudyteststheecologicalresourcedefencehy‐
pothesisforhowlingbehaviourinthemantledhowlermonkey(Alouatta palliata) and
investigates how anthropogenic forest fragmentation may influence howling behav‐
iour. More specifically, this study examines how howling bout rate, duration, precur‐
sors and tree species richness, DBH, and canopy cover vary in 100 m anthropogenic
edge and interior forest zones at La Suerte Biological Research Station (LSBRS), a
fragmented tropical rainforest in Costa Rica. Results show that tree species richness
andcanopy cover are higher in forestinterior atthis site, suggesting that monkeys
should howl at greater rates in the interior to defend access to these higher‐qual‐
ity vegetation resources. Overall, our results supported the ecological resource de‐
fence hypothesis. The main howl precursor was howling from neighbouring groups.
Although howling rate did not differ between forest zones, howling bouts from for‐
est interior were longer, had a greater number of howls per bout and were preceded
by different precursors than howls from anthropogenic edge zones, including more
howls from neighbouring groups. Our findings provide some of the first evidence for
behavioural edge effects in primate vocal communication behaviour.
KEY WORDS
Alouatta, ecological resource defence hypothesis, forest fragmentation, long call, loud call,
roar
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BOLT eT aL.
deer, Clutto n‐Brock & Alb on, 1979; insect s and anuran am phibians,
reviewed in Prestwich, 1994; primates, reviewed in Wich & Nunn,
2002). Long calls are complex in form, repetitive and contagious, in
that hearing a call prompts other males to counter‐call in response
(Gautier & Gautier, 1977; reviewed in Delgado, 20 06). Long calls are
also energetically expensive and may honestly advertise male quality
(Bradbury & Vehrencamp, 1998; Prestwich, 1994; Zahavi, 1975), with
males who call at higher rates or for longer durations demonstrating
superior body condition (e.g., red deer [Cervus elaphus], McComb,
1991; chacma baboon [Papio ursinus], Kitchen, Seyfarth, Fischer, &
Cheney, 200 3) or genetic qualit y (e.g., anurans, G erhardt, 1994; Welch,
Semlitsch, & Gerhardt, 1998). Long calls are most commonly found
in animal species that live in forested areas, where long‐range visual
communication is not always possible, suggesting that the long call is
a signal adapted to carry through foliage, rather than through open
space (de Vore, 1979; Waser & Brown, 1986; Wich & Nunn, 2002).
Across species, long calls are used primarily in contexts of mate
defence, mate attraction and/or territorial defence (Delgado, 2006;
reviewed in Kitchen, da Cunha, Holzmann, & de Oliveira, 2015). In
non‐human primates, three non‐mutually exclusive hypotheses
have been proposed as explanations for their adaptive function:
the mate defence hypothesis, the mate attraction hypothesis and
the ecological resource defence hypothesis (Delgado, 2006; Wich
& Nunn, 20 02). The mate defence hypothesis predicts that males in
group‐living species use long calls to communicate with males from
other social groups to prevent these males from accessing resident
females, and has found suppor t from strepsirhines (e.g., ring‐tailed
lemur [Lemur catta], Bolt, 2013a), catarrhines (e.g., Thomas langur
[Presbytis thomasi] , Steenbeek, A ssink, & Wich, 1999; ch acma ba‐
boon, Kitchen, Cheney, & Seyfarth, 2004), platyrrhines (e.g., golden
lion tamarin [Leontopithecus rosalia], Halloy & Kleiman, 1994) and
apes (e.g., gibbon [Hylobates spp.], Cowlishaw, 1992). The mate at‐
traction hypothesis predicts that long calls may attract females
and entice them to copulate with calling males, and has found sup‐
port from strepsirhines (e.g., gray mouse lemur [Microcebus muri‐
nus], Zimmermann & Lerch, 1993), catarrhines (e.g., Thomas langur
[P. thomasi], Steenbeek et al., 1999) and apes (orangutan [Pongo
spp.], Delgado, 2006; common chimpanzee [Pan troglodytes], Mitani
& Nishida, 1993). Finally, the ecological resource defence hypoth‐
esis predicts that long calls are used to defend food and/or space
resources, and while it has found support from species in diverse
environments (e.g., catarrhines: mantled guereza [Colobus guereza],
Harris, 2006), platyrrhines: ursine howler monkey [Alouatta arc‐
toidea], Sekulic, 1982, apes: gibbon [Hylobates spp.], Cowlishaw,
1996), it has rarely been evaluated in relation to anthropogenically
altered forest landscapes.Anthropogenic activityiswell known to
impact vocalization in many animal species. Human‐caused noise,
for example, alters animal acoustic communication signals in both
terrestrial and aquatic environment s (e.g., insects, Lampe, Schmoll,
Franzke, & Rein hold, 2012; Morley, Jones , & Radford, 2014; am‐
phibians, Sun & Narins, 2005; Parris, Velik‐Lord, & North, 2009;
fish, Slabbekoorn etal.,2010;Radford, Kerridge,& Simpson,2014;
birds, Patricelli & Blickley,2006;Nemeth& Brumm, 2010; Francis,
Ortega,&Cruz,2011;cetaceans,Miller,Biassoni,Samuels,&Tyack,
2000;Nowacek,Thorne, Johnston, & Tyack,2007;rodents,Rabin,
Coss, & Owings, 2006). Anthropogenic noise causes animals to ad‐
just the spectralproperties of theirvocal signals, likely in order to
preser ve communication efficiency (Luther & Magnot ti, 2014). The
vocalizations of non‐human primates have changed in amplitude (i.e.,
call loudness) and duration (i.e., call length) in response to human‐
caused noise (macaque [Macaca nemestrina and Macaca fascicularis],
Sinnott, Stebbins, & Moody, 1975; common marmoset [Callithrix jac‐
chus], Brumm, Voss, Kollmer, & Todt, 2004; Roy, Miller, Gottsch, &
Wang, 2011; cotton‐top tamarin [Saguinus oedipus],Hotchkin,Parks,
& Weiss, 2015; gray mouse lemur, Schopf, Schmidt, & Zimmermann,
2016). The impact of other anthropogenic factors in natural environ‐
ments—such as human‐caused deforestation or proximity of vocal‐
izers to anthropogenic forest edge—has not been studied in relation
to primate vocalization characteristics.
With rampant deforestation occurring throughout tropical re‐
gions worldwide (Haddad et al., 2015), it is impor tant to better un‐
derstand how anthropogenic impact alters the natural behaviour of
animals. Although forest edges occur naturally (e.g., when a forest
borders a beach), anthropogenic deforestation greatly increases the
propor tion of forest edge relative to forest interior (Laurance, 1991).
Forest edges represent transitional landscape zones, where differ‐
ing amount s of sunlight, moisture and wind are present compared to
the forest interior, impacting the vegetation and animals found there
(Harris, 1988; Lovejoy et al., 1986). Edge ef fect s especially impact
indicatorspecieslikeprimates,andgenerallyhaveanegativeeffect
on biota, with both plant and animal biomass reduced in forest edge
zones (Arroyo‐Rodríguez & Mandujano, 20 06; Estrada, Anzures, &
Coates‐Estrada, 1999). Edges also tend to have poorer‐quality veg‐
etation for animal species such as primates (Arroyo‐Rodríguez &
Mandujano, 2006; Estrada et al., 1999; Ross & Srivastava, 1994). In
the present study, we considered tree species richness, tree diam‐
eter at breast height (DBH) and tree canopy cover as indicators of
vegetation quality for primates. We based this on previous findings
indicating that higher tree canopy cover means a higher‐quality hab‐
itat for monkeys (Arroyo‐Rodríguez & Mandujano, 2006), with the
numberandsizeoftreesinaforestarealinkedtoprimateabundance
(Mbora&Meikle,2004;Ross&Srivastava,1994).
Because anthropogenic deforestation is one of the principal
threats reducing primate populations worldwide (Estrada et al.,
2017), it is vital to more thoroughly underst and how anthropogenic
edges affect primates and impact their behaviour, including their
communication behaviour. The present study investigates how pri‐
mate long calling may be impacted by edge effects in a fragmented
tropical forest landscape in Costa Rica, the La Suerte Biological
Research Station (L SBRS). LSBRS is a forest fr agment that repres ents
one of the increasingly few forested areas in a region of Costa Rica
that has been largely deforested since the 1970s, primarily due to
cattle ranching and large‐scale banana and pineapple production by
major corporations (Garber, Molina, & Molina, 2010; Molina, 2015).
Abrupt forest edges exist between many areas of LSBRS and the
neighbouringproperties,withbarbedwirefencesmarkingthesharp
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transitions between protected rainforest and cattle pasture or road
(Molina,2015).ThesedistinctforestedgesmakeLSBRSanidealsite
at which to investigate the relationship between anthropogenic edge
effects and howling behaviour. This study explores how anthropo‐
genic forest edges impact the long‐calling behaviour of a folivorous
primatespecies,themantledhowlermonkey(Alouatta palliata).
Howler monkeys( Alouatta spp.) are group‐living, large‐bodied
NewWorldmonkeysthatmainlyeatleaves,althoughtheyalsofeed
on fruit and flowers when available (Asensio, Cris tobal‐Azkarate,
Dias,Vea,&Rodríguez‐Luna,2007;diFiore,Link,&Campbell,2011;
Glander, 1982). They are extremely inactive primates who spend
most of the ir time rest ing, likely du e to the energ y restri ctions of
theirmostlyfolivorousdiet(Milton,1980).Theyareknownfortheir
long calls (“howls”), which have a loud, deep roaring sound, and are
produced only by adult males (Altmann, 1959). Adult males have
enlarged hyoid bones, which enable them to produce howls at high
amplitu de and that car ry more than 1 k m through som e environ‐
ments (Baldwin & Baldwin, 1976; da Cunha, de Oliveira, Holzmann,
& Kitchen, 2015).
The function of howling has been widely investigated in howler
monkeysatbothproximateandultimatelevels.Although proposed
functions include mate defence (ursine howler [A. arctoidea],Sekulic,
1982; brown howler [Alouatta guariba], black‐and‐gold howler
[Alouatta caraya], Holzmann, Agostini, & di Bitetti, 2012), group
cohesion (e.g., brown howler [A. guariba], Steinmetz, 2005), preda‐
tor deterrence (red‐handed howler [Alouatta belzebul], Camargo &
Ferrari, 2007) and advertisement of fighting ability to neighbour‐
ing groups ( black howler [Alouatta pigra], Kitchen, 2004; Kitchen,
Horwich,&James, 2004),howling ismost widelythought toserve
a group spacing function (ursine howler [A . arctoidea],Sekulic,1982;
brown howler [A. guariba], Chiarello, 1995;black‐and‐gold howler
[A. caraya], da Cunh a & Byrne, 200 6; black howler [ A. pigra], Van
Belle, Estrada, & Garber, 2013). Males howl to generally maintain
distance between groups and to avoid inter‐group encounters, but
evidence is preliminary as to whether males also howl to defend
specific areas or resources (reviewed in Kitchen et al., 2015). In the
ursinehowlermonkey,maleshowledandengagedininter‐groupen‐
counters at higher rates when near fig trees, which are preferred
food reso urces (Sekulic , 1982),an d in the brown howle r monkey,
inter‐group encounters occurred at higher rates near preferred
guapinol (Hymenaea courbaril) feeding a nd sleeping tr ees, likely in
order to defend access to them (Chiarello, 1995). Seasonality af‐
fectshowling patterns in other howlermonkey species, with more
howling during lower resource availability, potentially to defend
available resources (ursine howler, Sekulic, 1982; black howler,
Horwich & Gebhard, 1983; Guianan red howler, Drubbel & Gautier,
1993;brown howler,Chiarello,1995).Howlermonkeysalsovaryin
howling behaviour within home ranges, with some species howl‐
ing more of ten in core territor y areas (black‐and‐gold how ler, da
Cunha & Byrne, 2006) and other species howling more of ten in
borderareas(blackhowler,Horwich&Gebhard,1983;Guiananred
howler,Drubbel&Gautier,1993;brownhowler,daCunha&Jalles‐
Filho, 20 07). Themantledhowler monkey howled at greater rates
nearhomerangeborders(Altmann,1959);however,Hopkins(2013)
found that howling bout responses were best understood in the light
of inter‐group dominance interactions coupled with food availabilit y,
withmonkeysmoreoftenapproachingotherhowlinggroupsduring
times of food scarcity, presumably to gain access to their food‐rich
range area. Further, Whitehead (1989) found that mantled howler
monkeys howledmoreoften in frequently used homerange areas,
and thus may be broadcasting the location of primary food items
to other groups. These findings suggest that we may expect man‐
tledhowlermonkeys tohowlmorefrequentlyin areas ofricherre‐
sources. However, further research is needed to more fully elucidate
howhowlermonkeys maybeusinghowlswithinanthropogenically
altered forest habitats.
1.1 | Hypothesis: Ecological resource defence
The ecological resource defence hypothesis predicts that howler
monkeys howl to defend access to preferred resources, such as
feeding trees and/or high‐quality habitats containing a large number
of preferred feeding tree species (reviewed in Kitchen et al., 2015).
We predicte d that the mantled h owler monkeys at LS BRS would
howl at higher rates in forest interior compared to anthropogenic
forest edge in order to defend their access to the interior's higher‐
qualityvegetationfromothermonkeygroups.Wefurtherpredicted
that howling bouts in forest interior would be longer in duration and
consist of a greater number of howls per bout than howling bouts
atforestedge,tofurtheradvertisemonkeypresenceandtodefend
access to higher‐quality tree resources. Finally, we predicted that
howling bouts would be preceded by different environmental pre‐
cursorsinforestedgecomparedtointerior.Ifmonkeysintheinterior
howl to aler t other groups that areas containing high‐quality feed‐
ing resources are already occupied, we predicted that more howling
bouts would be trig gered by howls from males in other social groups
in forest interior than in forest edge.
2 | METHODS
2.1 | Study species
ThemantledhowlermonkeyrangesthroughoutCentralAmerica
and lives in social groups containing 10–20 individuals, but up to
40 individuals, with adult s typically in a 1:4 male‐to‐female ratio
(di Fiore et al ., 2011;R yan, Star ks, Milton , & Getz, 20 08; Scot t,
Malmgren, & Glander, 1978). They live in single‐male or multi‐male
groups with polygynous mating systems (Glander, 1980) where
spatially clumped food resources may be defended by males,
making them an ideal species on which to testthe resource de‐
fence hypothesis for long calling (Wich & Nunn, 2002). Mantled
howlermonkeyshavealargevocalrepertoirewith9–20different
graded vocalizations fitting into 5–6 broad call families (Altmann,
1959; Baldwin & Baldwin, 1976; Carpenter, 1934), including the
male‐specific howl vocalization. Compared to other howler mon‐
key species, mantled howler monkeys have simple howls with
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short durations (reviewed in da Cunha et al., 2015). Their howls
also have high amplitudes, low frequencies (300–1,00 0 Hz) and a
noisy structure (see Baldwin & Baldwin, 1976, p. 88 for a spectro‐
gram) which facilitates long‐distance sound propagation. In previ‐
ous research, howls have also been called “roars” (Altmann, 1959;
Baldwin & Baldwin, 1976; Carpenter, 1934), “Type 1” vocalizations
(Carpenter, 1934) and “Type A” vocalizations (Altmann, 1959;
Baldwin & Baldwin, 1976). In the present study, although mantled
howlermonkeysmademanyvocalizationsfromvariouscallfami‐
lies across forest zones at LSBRS, we restricted our investigation
to the usage of the howl (type 1/type A/roar) vocalization. Other
vocalizations were not examined because of their differences
from the howl in form, amplitude and perceived adaptive function
(Baldwin & Baldwin, 1976).
2.2 | Study site
We conducted this study at the LSBRS in nor theastern Costa Rica
(10°26′N,83°46′W). LSBRSis atropicallowland rainforesttotaling
approximately 3 square kilometers (km2) of primary and second‐
ary forest (Garber et al., 2010; Pruetz & Leasor, 2002). The forest
fragment where we conducted research comprises two connected
forest patches, “Large Forest” (0.935 km2) to the north and “Small
Forest”(0.35km2) to the south, as well as a partially cleared area for
“camp”(0.071km2; Molina, 2015, Figure 1).
The mantledhowler monkey shares LSBRSwith two sympatric
monkey species: the white‐faced c apuchin monkey (Cebus capuc‐
inus) and the Central American spider monkey (Ateles geoffroyi).
Populationsurveyestimatesforthemantledhowlermonkeysuggest
FIGURE 1 Map of La Suerte Biological
Research Station showing howling bout
locationsandmonkeysamplinglocations
for each 30 min of sampling
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BOLT eT aL.
that the Small Forest contains 2–3 groups, while the L arge Forest
contains 6–8 groups (Garber et al., 2010; Pruetz & Leasor, 2002).
2.3 | Vegetation survey
We collected vegetation data at LSBRS from May to August 2015
and May to June 2017. These time periods all comprise the wet
season at L SBRS, and therefore, seasonal differences are not a con‐
founding factor in our analyses. The vegetation data we recorded are
not expec ted to var y considerably over a couple of years and there‐
fore can ef fectively be compared to howling data collected during
May–August 2017 and 2018.
We conducted vegetation surveys along forest edge (within
100 m of anthropogenic forest edge) and interior transec ts (more
than 100 m from forest edge). Each survey transect was 50 × 5 m;
we aimed to distribute them evenly throughout the Large and Small
Forests and camp. Overall, we conducted 17 edge and 12 interior
transects (described in detail in Bolt et al., 2018). Along each tran‐
sect and within 2.5 m on either side of the transect line, we recorded
all trees with circumferences at breast height >10 cm and identified
tree species when possible. We then calculated mean DBH for each
transect. We estimated tree cover using a point sampling method. At
each1‐minterval,weestimatedtreecoverbylookingstraightabove
and assigning a score of 1–4 (1 = 0%–25% coverage, 2 = 26%–25%
coverage, 3 = 51%–75% coverage and 4 = 76%–100% coverage). We
also determined tree species richness for transects located in the
Large Forest.
2.4 | Howling data collection
Data on mantled howler monkey howling behaviour were col‐
lected from May to August 2017 and 2018 from approximately
11groupsofmonkeys—eightgroupsprimarilyintheLargeForest
and three groups primarily in the Small Forest. We collected data
over 70 days in 2017 (n = 208 hr,
x
= 3.0 hr/day) and 77 days in
2018 (n = 361 hr,
x
= 4.7 hr/day). Researchers actively searched
forandsampledmonkeysdailybetween500and1800hr,collect‐
ing data approximately evenly throughout the day, but especially
from 730 to 120 0 hr and 1230 to 1600 hr. We aimed to collect
approximately equal amounts of data across anthropogenic edge
(n = 336 hr) and interior (n = 233 hr) forest zones. Because in‐
dividualmonkey identities wereunknowninthis population and
group membership likely changed between summer 2017 and
2018 due to births, deaths and dispersals, we cannot be com‐
pletely certain of individual group identities and compositions;
based on ou r data, however, mean gro up size was 9.1mo nkeys
(SD = 3.2), mean male:female sex ratio was 1:1.6, and groups of
monkeysranged from threeindividualstoupto20individualsof
both sexes ( Table 1). We followed groups as they traveled across
various habitat zones, and all occurrences of howling data were
collected for continuous durations of time ranging from 30 min
to5 hr.Due to the high canopy,thick foliage and poor visibility
at LSBRS, datacollectors stayed as close as possible to monkey
groups during sampling to ensure that monkey groups remained
visible.Allmonkeygroupswerewell‐habituatedanddidnotreact
to researchers.
Dur ingallti mespe ntw ithamantledhowle rmonkeygrou p,a ll‐
occurrences sampling (Altmann, 1974) was conducted for group‐
wide howlingbehaviour (followingBolt, 2013a, 2013b; Hopkins,
2013). 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 close st trail mar ker to him and ta king a single GP S point as
close to him as possible using a Garmin GPSMAP 62s Handheld
GPS Navigator) and any potential precursor(s) in the seconds pre‐
cedingthehowl.Theseknownhowlingprecursorswererecorded
qualitatively, then placed into one of six categories for analysis: (a)
no observed precursor, (b) other group howling, (c) environmental
factor (e.g., rain, wind, thunder), (d) intra‐group social behaviour
(e.g., agonism, travel, non‐howl vocalization), (e) inter‐species
interaction (e.g.,dog, birdor other monkey species was seenby
researc hers and obs erved inter acting wi th focal howl er monkey
group) and (f) anthropogenic noise (e.g., lawn mower, chainsaw,
airplane) (Baldwin & Baldwin, 1976; Van Belle et al., 2013; re‐
viewed in Kitchen et al., 2015).
Howls were defined as male‐specific, high‐amplitude Type 1/A
loud calls (Altmann, 1959; Baldwin & Baldwin, 1976; Carpenter,
1934) 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 separated by <2 s, they were
considered part of the same howl vocalization. Howls were con‐
tained within howling bouts.
A howling bout comprised howls occurring <60 s apart (follow‐
ingSekulic,1982).Howlingboutscouldthereforebesecondslong
and consist of a single howl vocalization by one male, or many min‐
utes 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 howlingbouts, a GPS pointwastaken
at the location of ever y 30‐min period we spent in the presence of
a monkey grou p, regardless of w hether howlin g occurred duri ng
thesample.TheseGPSsamplingpointsweretakenintheapproxi‐
matecentreofthemonkeygroupandallowedustodeterminebe‐
havioural sampling frequency across various forest zones at LSBRS
(Figure 1).
TABLE 1 Mantledhowlermonkey(Alouatta palliata) group
membership at La Suerte Biological Research Station
Group membership
Mean number per
group Range per group
Adult males 2.4 1–6
Adult females 3.8 1–8
Juveniles 1.4 0–3
Infants 0.7 0–6
Tot al 9.1 3–20
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BOLT eT aL.
2.5 | Data analysis
We compared mean tree species richness and mean tree DBH
across edge and interior vegetation transects at L SBRS using Mann–
Whitney Utests.Wealsocomparedmeanhowlermonkeyhowling
rate, mean length of howling bouts and mean number of howls in
howling bouts in forest edge vs. interior zones using Mann–Whitney
U tests. To compare whether howling precursors showed different
distributions than expected by chance across forest zones, we used
a Pearson chi‐squared test. A s a post hoc test to determine which
precursors showed differences across forest zones, we examined
adjusted residuals and identified those with z‐scores greater than
±1.97 as showing differences across forest zones. We used SPSS
version 25 (IBM SPSS Statistics; IBM Corporation, 2013) for all sta‐
tistical tests and set the alpha level to 0.05.
3 | RESULTS
Mean tree species richness was significantly higher in the forest in‐
terior (
x
= 6.1 trees, SD = 2.1) than the anthropogenic edge (
x
= 3.8
trees; SD = 1.8; U = 22.5, p = 0.038) at LSBRS. Mean tree cover was
also higher in the interior than the edge, with 92.0% of 1‐m intervals
in the interior having between 51% and 100% cover compared with
73.6% of 1‐m intervals in the edge. Mean tree DBH in interior tran‐
sects (34.1 cm, SD = 29.6) was higher than mean DBH in the edge
(22.4 cm, SD = 11.6), but this difference was not statistically signifi‐
cant (U = 75.0, p = 0.245).
Across habitat zones, mean howler monkey howling rate
was 1.13 bouts/hr (range = 0–18 bouts/hr, n = 569 hr), while
mean howling bout length was 122.4 s/bout (range = 1–2,882 s/
bout, n = 641 bouts), and mean number of howls in a bout was
5.4 howls/bout (range = 1–176 howls/bout, n = 433 bouts). There
was no difference in overall howling rate between anthropo‐
genic edge and forest interior (
x
= 1.0 bouts/hr in forest interior
[range = 0–18 bouts/hr, n = 233 hr] vs. 1. 2 bouts/hr in anthro‐
pogenic edge [range = 0–14 bouts/hr, n = 336 hr]; U = 1 51,731.0 ,
z = −1.114, r = −0.033, p = 0.265). Howling bouts were signifi‐
cantly longer in forest interior than in anthropogenic edge
(
x
= 149.4 s in forest interior [range = 1–2,882 s, n = 242 bout s]
vs. 106.1 s in forest edge [range = 1–1,641 s, n = 399 bouts];
U = 43,382.5, z=−2 .15 8,r=− 0. 0852 ,p = 0.031, n = 641; Figure 2).
There were also significantly more howls per bout in forest in‐
terior than in anthropogenic edge (
x
= 7.91 howls/bout in inte‐
rior [range = 1–176 howls/bout, n = 143 bouts] vs. 4.09 howls/
bout in forest edge [range = 1–78 howls/bout, n = 290 bouts];
U = 18,216.0, z=−2.179,r=−0.1047,p = 0.029, n = 433; Figure 3).
When examining the association between howling bout precursor
and howling location (anthropogenic edge vs. interior), howling
bouts in different forest zones had significantly different precur‐
sors (x2(5) = 31.489, p = 0.000, n = 624). The streng th of associ‐
ation between variables was strong (Cramer's V test: φc = 0.225,
p = 0.00 0), and post hoc examination of adjusted residuals
indicated that when adjusted for sample size, monkey howling
bouts in the forest interior zone were more frequently preceded
by howls from other groups and inter‐species interactions than
expected, while they were less frequently preceded by no precur‐
sor and environmental factors than expected (z > ±1.97, Table 2).
The reverse pattern was seen for howling bouts sampled in forest
edge zones. Observed values such as intra‐group interaction and
anthropogenic noise did not differ from expected values across
forest zones (z < ±1.97, Table 2).
4 | DISCUSSION
Our results partially supported the predictions of the ecological re‐
source defence hypothesis for howler monkey howling behaviour.
Vegetation transects confirmed higher resource quality in forest
interior, and while overall howling rate did not differ between for‐
est zones, howling bouts were significantly longer and consisted of
a greater number of howls per bout in forest interior compared to
FIGURE 2 Mean howling bout leng th in forest interior vs.
anthropogenic edge at L a Suer te Biological Research Station
(p = 0.031). Boxes represent inter‐quartile ranges, lines represent
medianvalues,andwhiskersrepresentmaximumandminimum
values. Outliers were removed for graphical purposes
)RUHVW]RQH
,QWHULRU$QWKURSRJHQLFHGJH
0HDQKRZOERXWOHQJWKVHFRQGV
FIGURE 3 Mean number of howls per howling bout in
anthropogenic edge vs. forest interior at La Suerte Biological
Research Station (p = 0.029). Boxes represent inter‐quartile ranges,
linesrepresentmedianvalues,andwhiskersrepresentmaximum
and minimum values. Outliers were removed for graphical purposes
)RUHVW]RQH
,QWHULRU$QWKURSRJHQLFHGJH
0HDQQXPEHURIKRZOVLQERXW
|
599
BOLT eT aL.
anthropogenic edge. Howling precursors also differed across for‐
est zones as predicted, with more focal group howls preceded by
howlsfromothergroupsinforestinteriorthaninforestedge.Taken
together, these results support our prediction that mantled howler
monkeys may be h owling more when in f orest interior, potenti ally
to advertise to other groups that their high‐quality habitat is already
occupied.
Howls,likethelongcallsmadebyotheranimaltaxa, arethought
to be energetically expensive to produce (Bradbur y & Vehrencamp,
1998; da Cunha et al., 2015; Prestwich, 1994; Wich & Nunn, 2002),
with longer howling bouts requiring more energy. Males will howl for
longer durations of time in certain habitat zones if doing so provides
them with some fitness advantage, such as maintaining their access
tothehigher‐qualit ytreesintheforestinterior.Howlermonkeysare
known to be li mited by food sup ply (Jones , 1980) and to be sele c‐
tive feeders that mostly eat from trees (Estrada, 1984, but see Dunn,
Asensio, Arroyo‐Rodríguez, Schnitzer, & Cristóbal‐Azkarate, 2012;
Arroyo‐Rodríguez, Asensio, Dunn, Cristóbal‐Azkarate, & Gonzalez‐
Zamora,2015).Forexample, howlermonkeysatefrom 27treespe‐
cies from 15 families at a rainforest site in Mexico (Estrada, 1984).
At LSBR S, prelimin ary inves tigation of how ler monkey fee ding tree
species use in forest interior compared to 50 m anthropogenic edge
atLSBRS(Russell,2018)showedthatmonkeysfedfromatleastnine
different tree species in forest interior compared to only four species
in forest edge. With both number of observed feeding tree species
(Russell, 2018) and overall tree species richness (this study) higher
in forest interior at LSBRS, it may be adaptive for mantled howler
monkeystohowlforlongerdurationsof timewhileintheinteriorto
prolong access to this higher‐quality food resource zone. Our results
findsuppor tfromotherhowler monkey speciesincludingthe ursine
howler(Sekulic,1982)andthebrownhowler(Chiarello,1995),bothof
which howled at higher r ates in areas of higher‐quali ty food resource s.
The differences in howl bout length at L SBRS may additionally be
due to differences in long call sound propagation properties across
forest zones. Given that the sound reverberation (i.e., sound being re‐
flected by static objects and dispersed during propagation, see Naguib
& Wiley, 2001; da Cunha et al., 2015) of long calls is typically stronger
in dense forest habitats than in open areas (Waser & Brown, 1986), this
limits the long‐distance communication potential of howls in forest in‐
terior.Ifmantledhowlermonkeysare howling to communicatetheir
location to other conspecific groups for any reason, they may increase
the length and number of howls contained in their howling bouts when
in forest interior in order to ensure that other groups can effectively
receive and locate their signal. It is adaptive for males to spend more
energy producing longer howling bout s in interior locations if doing so
minimizes their number of face‐to‐face inter‐group encounters, which
are often violent and can lead to severe injur y or death for mature
males (Chi arello, 1995; Sekulic , 1982).A lthough h owls carr y for long
enoughdistancesthattheycanlikelybeheardbyneighbouringgroups
across forest zones, regardless of whether howls are uttered in forest
edge or interior, males may howl for longer durations of time while in
the interior to compensate for sound reverberation. Reverberation and
other acoustic properties of howls have not been measured in forest
edge and interior zones at LSBRS; future study will more fully assess
the range of environmental fac tors that could be driving differences in
howl bout length across forest zones.
Males may have also howled for longer durations of time in
forest interior compared to forest edge due to differing predation
pressures across forest zones. Monkeys in anthropogenic edge
areas had shorter howling bouts with fewer howls per bout, poten‐
tially to avoid being detected by predators in this area of less dense
canopy cover. In this study, male howling in both forest edge and
interior was preceded by interac tions with other species including
dogs (Canis familiaris),capuchinandspidermonkeys,turkeyvultures
(Cathartes aura) and the green ibis (Mesembrinibis cayennensis). Of
these, dogs aretheonlyknownhowler monkey predators(Baldwin
& Baldwin, 1976; Carpenter, 1934; Raguet‐Schofield, 2008), but the
presence of unfamiliar or unexpected animals also appears to trigger
howlinginhowlermonkeysatothersites(Baldwin&Baldwin,1976;
Carpe nter,1934; S ekulic, 1982). Ca lling animals a re more likely to
attract the attention of potential predators (reviewed in Bolt, 2016),
as are animals that call for longer periods of time. Thus, in areas of
increas ed threat, it may be a daptive for howle r monkey males to
howl for shorter lengths of time, as they did on the edge at L SBRS.
Howling in forest interior at LSBRS, however, was preceded by in‐
teractions with other species more often than would be expected by
chance.Theresponseofmonkeysmaybemoremarked(i.e.,longer
howling bouts, greater number of howls per bout and greater num‐
ber of howls preceded by inter‐species interaction) in forest interior
duetogreatertreecoverhelpingtoconcealmonkeysfrompredators
and increased sound reverberation helping to obscure the locations
of howling males from other animals (Naguib & Wiley, 2001; Waser
&Brown,1986).Becausecallingmonkeysarelikelymoredifficultfor
predators to localize and target in dense forest interior than in open
edge areas, they may howl for longer durations of time in the interior
withoutsubstantiallyincreasingtheirriskofpredation.
TABLE 2 Mantledhowlermonkey(Alouatta palliata) howling precursors at La Suerte Biological Research Station 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
Interior Forest Zone −2. 8*4.1*−2. 1*−1.8 2.8*−1. 2
Edge Forest Zone 2.8*−4.1*2.1*1.8 −2 .8*1.2
*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 expec ted by chance.
600
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BOLT eT aL.
Anotherpossibility,that differences inmantled howler monkey
population densit y across forest zones may be motivating differ‐
ences in howling behaviour, has little support. Mantled howler mon‐
keydensityhasbeen suggested to relatetointer‐group aggression
in some populations, with higher monkey density in some areas
leading to increased aggression (Kitchen et al., 2015) and howling
rate.However,atLSBRS,howlermonkeygroupswereencountered
equally in anthropogenic edge and interior (Bolt et al., 2018), sug‐
ge sti ngnod iff ere nce in mon ke ygrou pde nsi tyb etw een for est zo nes .
We collected howling data from May to August, during the wet
season in northeastern Costa Rica. Howl sampling conducted at
other times of year, including during the dry season, may yield dif‐
ferent results for howling rate and bout characteristics at LSBRS.
However, because seasonal variatio n is not expected to impact range
useorfooditemselectioninthemantledhowlermonkey(Boltetal.,
2018; Chapman, 1988), we would not necessarily expect it to influ‐
ence the edge vs. interior spatial patterns of howling in our study.
We tested the ecological resource defence hypothesis in relation
to overall tree species richness, DBH and c anopy cover, but did not
test how other forms of resource defence, such as feeding/resting
tree species richness or abundance, may relate to howling behaviour.
We also did not investigate potential variation in vegetation quality
in areas within edge and interior forest zones. Some forest interiors
at other tropical sites have core areas containing higher‐quality veg‐
etation(e.g.,daSilvaJúnioretal.,2009;Asensio,Lusseau,Schaffner,
&Aurel,2012),anditisunknown whetherinteriorforest atLSBRS
showssi mi la rfeatures.Wealsodidn ot evaluatehow lerm on keypre‐
ferred feeding tree abundance or usage between edge and interior.
Future study should examine a broader range of ecological factors
thatmayinfluencehabitatuseinthemantledhowlermonkey.
Our results have conservation implications. Howling bout prop‐
erties and characteristics differed between anthropogenic edge
and forest interior, which in turn indicates that proximit y to anthro‐
pogenic ed ge is likely alterin g mantled howler m onkey behaviour.
Althoughit is unclear how thismay affect howlermonkey fitness,
our findings suggest that long‐term initiatives for mantled howler
monkey conservation shouldprioritize both preservation of forest
interior zones and regeneration of forest edges exposed to anthro‐
pogenic ac tivit y. Forest destruction should be minimized to mitigate
anyalterationstomantledhowlermonkeycommunicationbehaviour
caused by human impact.
Finally, it is important to note that howl bout length in mantled
ho w ler m onk eysm ayv a r yac r oss e dge andi nte r iorh abi t a tzo nesd ue
to a range of factors which are not mutually exclusive. As Kitchen
etal.(2015) obser ve,howlermonkeylongcallshavelikelyevolved
in response to a variet y of competing selec tive pressures. Mantled
how lermonkeys mayut terhowlboutswi thdiffere nttem po ra lchar‐
acteristics across habitat zones due to a variety of adaptive func‐
tions, in cluding—but not limited to—resource defence, group spaci ng
and predator avoidance. Our findings may be interpreted in the light
of other functions, but when our results for tree characteristic s in
edge and interior zones at LSBRS are considered, our howling be‐
haviour results support the ecological resource defence function of
howling among other possibilities. Our findings thus contribute to
the existing literature addressing the potential function(s) of howler
monkeylongcalls(reviewedinKitchenetal.,2015)andprovideone
of the first focused investigations of how primate communication
behaviour is impacted by anthropogenic edge effects.
ACKNOWLEDGEMENTS
We are grateful to Renee Molina and the Maderas Rainforest
Conser vancy for their support and facilitation of our research at the
La Suer te Biologi cal Researc h Station, Co sta Rica . Wet hank Philip
Quinn, Sophie Lieber,Mic ah Adams, Stacy Hill and MareikeJaniak
fordata collection. We also thankNancy Barrickman, Ryan Janzen
and Tristan R hys Williams. Fin ally, we thank Luis Ebe nsperger and
anonymous reviewers for their comments, which have improved our
manuscript. Our research complies with the guidelines for the use
of animals in research as set by the Animal Behaviour Society. This
research protocol was approved by the Regis University Animal Care
Committee and was conducted with the permission of the Molina
family. Our research was supported by a University Research and
Scholarship Council (URSC) Faculty Research and Scholarship Grant
(Regis Unive rsity), a Cosmos S cholar Award (Cosm os Club Foundatio n)
and an Explorer's Club Exploration and Field Research Grant.
ORCID
Laura M. Bolt https://orcid.org/0000‐0002‐8275‐6543
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How to cite this article: Bolt LM, Schreier AL, Russell DG,
etal.Howlingontheedge:Mantledhowlermonkey( Alouatta
palliata) howling behaviour and anthropogenic edge effects in
a fragmented tropical rainforest in Costa Rica. Ethology.
2019;125:593–602. htt ps ://doi.org/10 .1111/et h.1 2886
