Am J Primatol. 2019;e23032. wileyonlinelibrary.com/journal/ajp © 2019 Wiley Periodicals, Inc. | 1 of 13

https://doi.org/10.1002/ajp.23032

Received: 27 November 2018 | Revised: 21 June 2019 | Accepted: 25 June 2019

DOI: 10.1002/ajp.23032

R E S EARCH AR T I C L E

Habitat preference in the critically endangered yellow‐tailedwoolly monkey (Lagothrix flavicauda) at La Esperanza, Peru

Sandra L. Almeyda Zambrano1,2 | Eben N. Broadbent2 | Sam Shanee1,3,4 |Noga Shanee1,4 | Anneke Deluycker5 | Michael Steinberg6 | Scott A. Ford7 |Alma Hernández Jaramillo3 | Robin Fernandez‐Hilario8 | Carolina Lagos Castillo1 |Angelica M. Almeyda Zambrano9

1Asociación Neotropical Primate

Conservation Perú, Amazonas, Peru

2School of Forest Resources and

Conservation, University of Florida,

Gainesville, Florida

3Asociación Neotropical Primate

Conservation Colombia, Bogotá, Colombia

4Neotropical Primate Conservation, Cornwall,

United Kingdom

5Smithsonian‐Mason School of Conservation,

Smithsonian Conservation Biology Institute,

Front Royal, Virginia

6Department of Geography, University of

Alabama, Tuscaloosa, Alabama

7Department of Geosciences and Natural

Resources Management, University of

Copenhagen, Copenhagen, Denmark

8Herbario Forestal MOL, Facultad de Ciencias

Forestales, Universidad Nacional Agraria La

Molina, Lima, Peru

9Department of Tourism, Recreation, and

Sport Management, University of Florida,

Gainesville, Florida

Correspondence

Sandra Lucia Almeyda Zambrano, Neotropical

Primate Conservation Peru, Grundtvigsvej

14A, ST TH, 1864 Frederiksberg C,

Copenhagen, Denmark.

Email: salmeydazambrano@ufl.edu

Funding information

Community Conservation; Care for the Wild;

Margot Marsh Biodiversity Foundation;

National Geographic Foundation; The

University of Alabama; Rufford Foundation;

Idea Wild; Neotropical Primate Conservation;

Lush

Abstract

Habitat loss is one of the main threats to wildlife. Therefore, knowledge of habitat use

and preference is essential for the design of conservation strategies and identification

of priority sites for the protection of endangered species. The yellow‐tailed woolly

monkey (Lagothrix flavicauda Humboldt, 1812), categorized as Critically Endangered

on the IUCN Red List, is endemic to montane forests in northern Peru where its

habitat is greatly threatened. We assessed how habitat use and preference in L.

flavicauda are linked to forest structure and composition. The study took place near

La Esperanza, in the Amazonas region, Peru. Our objective was to identify

characteristics of habitat most utilized by L. flavicauda to provide information that

will be useful for the selection of priority sites for conservation measures. Using

presence records collected from May 2013 to February 2014 for one group of

L. flavicauda, we classified the study site into three different use zones: low‐use,medium‐use, and high‐use. We assessed forest structure and composition for all use

zones using 0.1 ha Gentry vegetation transects. Results show high levels of variation

in plant species composition across the three use zones. Plants used as food

resources had considerably greater density, dominance, and ecological importance in

high‐use zones. High‐use zones presented similar structure to medium‐ and low‐usezones; thus it remains difficult to assess the influence of forest structure on habitat

preference. We recommend focusing conservation efforts on areas with a similar

floristic composition to the high‐use zones recorded in this study and suggest utilizing

key alimentation species for reforestation efforts.

K E YWORD S

conservation, forest composition, forest structure, montane forest, atelinae

1 | INTRODUCTION

The yellow‐tailed woolly monkey (Lagothrix flavicauda Humboldt,

1812) is endemic to the northern Peruvian Andes where it occupies

montane and pre‐montane forests between 1,500 and 2,700m.a.s.l.

(meters above sea level; Leo Luna, 1980; S. Shanee, 2014b). This

species is classified as Critically Endangered by the IUCN (Cornejo,

Rylands, Mittermeier, & Heymann, 2008) and Peruvian Law (Supreme

Decree No. 004–2014‐AG). Additionally, L. flavicauda was listed

three times among the world’s top 25 most threatened primate

species from 2000 until 2012 (Mittermeier et al., 2012). The species

is threatened by the complex interaction of several factors such as

increasing environmental temperature, changing rainfall patterns,

human population growth, unregulated land use, habitat fragmenta-

tion, deforestation, and poaching throughout its range (Butchart,

Barnes, Davies, Fernandez, & Seddon, 1995; N. Shanee, 2012;

N. Shanee & Shanee, 2014). However, among these many factors,

the main threat faced by L. flavicauda is habitat loss (DeLuycker,

2007; N. Shanee & Shanee, 2014). Buckingham and Shanee (2009)

estimated a minimum loss of 56% of its original habitat, and it is

estimated that L. flavicauda populations have decreased between

46% and 93% since 1981 (N. Shanee & Shanee, 2014). Habitat

protection and management programs are likely necessary to ensure

the species’ survival (DeLuycker, 2007).

Spatial distribution of primates is thought to be mainly influenced

by food availability, forest structure, and habitat connectivity (Boyle,

Lourenço, da Silva, & Smith, 2009; C. Chapman, 1988; Irwin, 2008).

Accordingly, habitat requirements are a major factor in determining

species survival and reproductive success (Warner, 2002). A clear

understanding of habitat preference is crucial to advance our

knowledge of primate ecology and represents valuable information

when designing conservation strategies for rare and threatened

species (Djègo‐Djossou et al., 2015).

The overarching goal of our study was to inform conservation

efforts of L. flavicauda by assessing its habitat preference. We tested

two main hypotheses: (a) habitat preference is influenced by food

availability and (b) habitat preference is influenced by forest

structure. We aimed to identify forest characteristics unique to

habitats preferred by L. flavicauda to highlight those which most

heavily influence habitat preference. Understanding these character-

istics would then allow us to make recommendations for habitat

protection and restoration.

2 | METHODS

2.1 | Study site and species

The study was conducted at La Esperanza, Yambrasbamba district,

Amazonas region, in northern Peru (S 05°39′, W 77°54′; Figure 1). The

area comprises primary forest and regenerating secondary forest

interspersed with pasture. Primary forests in the area show signs of

fine‐scale selective logging (e.g., single‐tree selection). The terrain is

dominated by high ridges and steep valleys with altitudes ranging from

1,800 to 2,400m.a.s.l. Average annual precipitation for the area is

F IGURE 1 Map of the study site and surroundings in the northern Peruvian Andes

2 of 13 | ALMEYDA ZAMBRANO ET AL.

1,500mm. The dry season occurs from May to October and wet season

from October to April. Average daytime temperature is 14°C±5.7°C

(S. Shanee & Shanee, 2011). The area is not officially protected, but

community‐based hunting and deforestation bans have resulted in a 35%

increase in L. flavicauda density, and lower deforestation rates than local

and regional averages (Sam & Shanee, 2016).

L. flavicauda is one of the largest primates endemic to Peru (Leo

Luna, 1980). Individuals are robustly built, with dense red‐brown

colored fur (Mittermeier, de Macedo‐Ruiz, Luscombe, & Cassidy,

1977). The most peculiar characteristics of the species include white‐colored hair around the mouth, yellow‐colored hair on the ventral

side of the final third of the tail, and a prominent yellow genital tuft in

adults and subadult males (Figure 2; Leo Luna, 1987; Mittermeier

et al., 1977). The study group comprised 17 individuals: seven adults

(3 males, 4 females), six juveniles, and four infants.

2.2 | Habitat use classification

To classify the area into use zones, we used data collected during focal

animal follows between May 2013 and February 2014. Food sources,

sleeping locations, and daily movement patterns were recorded and

georeferenced using a GPS unit (Garmin GPSMAP). Every tree with a

diameter at breast height (DBH; 1.3m above base) greater than 10 cm

where L. flavicaudawas observed eating or sleeping was georeferenced at

the base of the tree. A focal adult was followed from dawn to dusk with

the GPS set to optimal efficient data collection mode, where GPS fixes

are only collected as needed to describe the movement of the unit. This

results in fewer points during stationary times and more during times of

faster movement. Whenever the focal subject was lost, it was replaced

with another adult of the same sex. A total of 277 feeding trees, 36

sleeping trees, and 22,232 GPS fixes of the focal location were recorded

(Figure 3). The total tracking time was 401hr, during 54 days, distributed

over 10 months.

To calculate use density, we interpolated locations of the GPS fixes to

every 30 s or less. For example, if it took 60 s to move from point A to B,

then we would place an additional point halfway between them. The

temporal resolution of all collected GPS data was therefore 30 s or less,

which resulted in inter‐point movements of less than 10m. We then

F IGURE 2 Adult male of Lagothrix flavicauda in Amazonas region,Peru. Photo by Neotropical Primate Conservation

F IGURE 3 Geographic records of the study troop at the study site in Amazonas region, Peru

ALMEYDA ZAMBRANO ET AL. | 3 of 13

randomly subsampled one‐quarter of the GPS points 100 times, and for

each time calculated a density grid of 15m×15m across our entire study

area displaying total time spent in each grid cell (s/m2). We refer to the

mean of the 100 samples provided by this Monte‐Carlo resampling as use

density. This use map is inherently a daytime use intensity map, as we did

not include time spent in trees at night into the calculations (which would

have heavily weighted the maps to those trees). Rather, sleeping and fruit

trees naturally occur within this map due to most tracking periods

starting and ending at these locations. The continual values (seconds per

225m2 cell) in each cell were rasterized using the point density algorithm

on the duration data, using the ESRI Spatial Analyst extension (resolution

15m×15m, 30m search radius, s/m2 output), and this duration raster

was then binned into three use intensity classes (low, medium, and high)

using a modified Jenks natural breaks algorithm. The class threshold

values were low use (<0.1 s/m2), medium use (0.1≤0.4 s/m2), and high

use (>0.4 s/m2). Low use zones are calculated as any area within 50m of a

GPS fix that was not classified as medium or high use. To estimate

uncertainty, we calculated the standard error across our 100 Monte‐Carlo samples of seconds spent in each cell and used these values as

inputs to create uncertainty bounded use zone maps. Calculations were

performed in R (R Core Team, 2018) and in ArcGIS v.10.5 (ESRI, 2016).

Our movement data was overlaid on RapidEye satellite visual imagery

(6m×6m) collected during our study period (7 September 2014) to aid

in interpretation.

2.3 | Data collection

2.3.1 | Forest composition and structure

Assessing habitat preference can pose a considerable challenge in the

Tropical Andes where even small areas can show a complex and

highly variable array of habitat types (Hill & Foody, 1994). Thus, we

utilized transects to assess forest composition and structure as they

provide the most appropriate, complete, and representative descrip-

tion for heterogeneous ecosystems (Ganzhorn, 2011). All zones used

by L. flavicauda (low, medium, and high use) were sampled following

the Gentry vegetation transect method (Gentry, 1982) from June to

July 2015. We established two 0.1 ha transects (2 m × 500m),

composed of ten subplots (2 m × 50m) in each use zone (Table 1

and Figure 4). Starting points and azimuths of transects were

determined with ArcMap v.10.2 to ensure that transects were

located within the appropriate use zones. Azimuths were adjusted in

the field when impassible cliffs and use‐zone boundaries were

encountered to limit potential edge effect.

To assess the adequacy of our floristic sampling effort, we calculated

the Chao 1 estimator for each use zone (Colwell, 2009). According to the

estimator, we recorded >85% of expected species for high‐ and medium‐use zones indicating adequate sampling (Villarreal et al., 2004). Although

the low‐use zone did not pass the 85% threshold (72.4%), species

accumulation curves were asymptotic for singleton and unique species

which also implies good sampling (Cava, Coscarón, & Corronca, 2015;

Villarreal et al., 2004; see Supporting Information for species accumula-

tion curves). Thus, our sampling effort was robust to accurately describe

the overarching species composition in each zone. Furthermore, rare

plant species are not likely to be an important factor in controlling habitat

use of L. flavicauda.

Species, DBH, crown spread, total height, bole height, crown solar

exposure, crown position, phenological state, vine infestation, moss cover,

and vascular epiphyte load were recorded for all stems (dead or alive)

with a DBH, ≥2.5 cm when 50% or more of the visible root system was

inside the transect. In addition, altitude, slope, aspect, and canopy cover

were measured for all subplots. See Supporting Information for a full

description of forest composition and structure methods.

2.4 | Data analysis

2.4.1 | Forest composition

All species were identified to the lowest taxonomic level possible.

Density (stems/ha), relative density (contribution to total stems),

TABLE 1 Descriptive characteristics of the vegetation transects

Transect Use zoneGeographicCoordinates

Elevationa

(m.a.s.l) Slopea (%)

Basal area

(m2/ha)Density(stems/ha)

Canopy

coverb (%)Richness(spp 0.1/ha)

Diversity(H′)

H1 High S 5°39′27″W 77°49′24″

1918–2008 1–48 40 3540 90 64 3.66

H2 High S 5°39′55″W 77°54′ 36″

2083–2156 0–51 52.1 3510 91 62 3.47

M1 Medium S 5°39′20"W 77°54′40″

1948–2529 0–60 65.3 2430 87 66 3.63

M2 Medium S 5°39′42″W 77°54′42″

2045–2133 2–49 52 3700 92 74 3.73

L1 Low S 5°39′17″W 77°54′33″

2010–2128 1–60 30.9 2390 94 67 3.49

L2 Low S 5°39′49″W 77°54′53″

1975–2140 0–39 46 3800 94 78 3.91

Abbreviation: m.a.s.l, meters above sea level.a Elevation and slope values shown are the lowest and highest registered at each transect.b Average canopy cover per transect is reported.

4 of 13 | ALMEYDA ZAMBRANO ET AL.

dominance (basal area, m2/ha), relative dominance (contribution to

total basal area), and relative importance (mean of relative density

and relative dominance; J. T. Curtis & McIntosh, 1951) for all tree

species were calculated for each transect (Table 2).

A detrended correspondence analysis (DCA) was performed to

compare floristic composition across transects in the three use zones

using the community ecology package VEGAN v.2.3‐4 (Oksanen

et al., 2016) in R v.3.2.4 allowing visualization of similarities in species

composition across multiple sites (Honorio Coronado et al., 2009;

Pyke, Condit, Aguilar, & Lao, 2001; ter Steege et al., 2006; ter Steege

et al., 2000; Terborgh & Andresen, 1998). The Shannon index (H′)was calculated to measure species diversity and compare diversity

among all transects.

2.4.2 | Forest structure

One‐way analysis of variance (ANOVA), Kruskal–Wallis, and Inde-

pendent samples median tests were performed using IBM SPSS

Statistics v.22 to compare means and medians across all six transects

(N = 10 subplots per transect) for the following variables: quadratic

mean diameter (R. O. Curtis & Marshall, 2000), live stems density,

live stems total basal area, dead stems density, dead stems total basal

area, density of vines in transect, total height, bole height, crown

position, crown illumination, load of vascular epiphytes, moss cover,

and vine infestation on stems. A Scheffe, repetitive Kruskal–Wallis,

or Dunnett T3 post hoc test was performed when significant

differences were detected (p < .05).

Normality and homoscedasticity were tested using the Kolmo-

gorov–Smirnov and Shapiro–Wilk tests, respectively. When the data

did not show a normal distribution, the nonparametric Kruskal–Wal-

lis test was performed instead of an ANOVA. When homoscedasticity

was not met, the Dunnett T3 post hoc test was used instead of the

Scheffe post hoc test. When comparing ordinal variables, such as

indexes and medians, the nonparametric independent samples

median test was performed. Additionally, the diametric distribution

of stems, defined as the density of stems per 0.1 ha in 5 cm diameter

classes (Nyland, 2002), was calculated for each transect and

separately for Hieronyma macrocarpa Müll. Arg., Ficus spp., Ocotea

sp., Styloceras columnare Müll. Arg., Myriocarpa sp., Hedyosmum

cuatrecazanum Occhioni, Heliocarpus americanus L., Heteropterys sp.,

and Cecropia spp., which were considered plant food species for

L. flavicauda (Hernandez Jaramillo, 2013; Leo Luna, 1980; S. Shanee,

2014a).

2.5 | Legal and ethical guidelines

The research presented in this paper adhered to the legal

requirements of the Peruvian Government Forest service (research

F IGURE 4 Mean use zones identified for Lagothrix flavicauda, and vegetation transects (H1, H2, M1, M2, L1, L2) at the study site in

Amazonas region, Peru. The gray outline represents the low‐use area (and study site boundary). A satellite image is a RapidEye visualorthomosaic acquired on 7 September 2014

ALMEYDA ZAMBRANO ET AL. | 5 of 13

TABLE2

Den

sity

(stems/hectare),dominan

ce(m

2/ha),andrelative

ecologicalimportan

ceva

lue(m

eanofrelative

den

sity

andrelative

dominan

ce)forplantspecies(livestem

s,≥2.5cm

,diameter

atbreastheigh

t)docu

men

tedacross

thethreeuse

zones

(six

vege

tationtran

sects)

locatedin

Amazonas

region,P

eru

Spec

ies

Den

sity

(stems/ha)

(relativeden

sity

[%])

Dominan

ce(m

2/ha)

(relativedominan

ce[%

])Eco

logicalIm

portan

ceValue

Highuse

Med

ium

use

Low

use

Highuse

Med

ium

use

Low

use

Highuse

Med

ium

use

Low

use

H1

H2

M1

M2

L1L2

H1

H2

M1

M2

L1L2

H1

H2

M1

M2

L1L2

Cecropiaaff.telenitida

Cuatrec

0(0)

40(1)

20(1)

30(1)

0(0)

10(0)

0(0)

0(3)

0(4)

0(2)

0(0)

0(3)

02.1

2.7

1.6

01.8

Cecropiaan

gustifolia

Trécu

l

0(0)

20(1)

0(0)

50(1)

0(0)

20(1)

0(0)

0(2)

0(0)

0(2)

0(0)

0(1)

01.4

01.8

00.6

Styloceras

columna

reMüll.

Arg.

410(12)

300(9)

310(13)

190(5)

470(20)

50(1)

3(7)

0(3)

0(5)

0(3)

0(13)

0(1)

9.2

5.9

8.7

3.9

16.1

1

Heterop

teryssp.1

20(1)

60(2)

50(2)

20(1)

10(0)

0(0)

0(0)

0(1)

0(1)

0(1)

0(0)

0(0)

0.3

1.3

1.4

0.7

0.3

0

Myriocarpastipitata

Ben

th.

40(1)

10(0)

10(0)

10(0)

0(0)

10(0)

0(1)

0(0)

0(1)

0(0)

0(0)

0(1)

1.1

0.2

0.5

0.3

00.5

Heliocarpus

american

usL.

20(1)

50(1)

20(1)

10(0)

20(1)

20(1)

0(0)

0(3)

0(1)

0(1)

0(2)

0(0)

0.4

2.3

0.8

0.7

1.3

0.4

Ocoteasp.1

110(3)

170(5)

30(1)

0(0)

0(0)

0(0)

1(3)

0(4)

0(2)

0(0)

0(0)

0(0)

3.1

4.4

1.7

00

0

Ficussp.2

0(0)

10(0)

10(0)

0(0)

10(0)

0(0)

0(0)

0(2)

1(13)

0(0)

0(0)

0(0)

01.3

6.8

00.2

0

Ficussp.1

10(0)

40(1)

20(1)

0(0)

20(1)

10(0)

1(3)

0(6)

1(13)

0(0)

0(3)

0(0)

1.8

3.7

6.7

02.1

0.1

Hed

yosm

umcuatrecazanu

mOcchioni

160(5)

140(4)

20(1)

170(5)

10(0)

130(3)

3(7)

10(14)

0(0)

1(11)

0(4)

0(1)

5.7

90.5

82.1

2.3

Hierony

ma

macrocarpaMüll.Arg

120(3)

40(1)

10(0)

40(1)

0(0)

60(2)

5(13)

0(0)

0(0)

0(0)

0(0)

0(0)

8.1

0.7

0.3

0.6

01

Nectand

ramem

bran

acea

(Sw.)

Griseb.

260(7)

180(5)

150(6)

210(6)

60(3)

70(2)

4(10)

0(3)

0(5)

0(3)

0(4)

0(1)

8.5

3.8

5.6

4.6

3.2

1.3

Aioue

amon

tana

(Sw.)

R.R

ohde

110(3)

200(6)

40(2)

140(4)

70(3)

120(3)

1(2)

0(4)

0(4)

0(4)

0(12)

0(4)

2.4

4.8

2.9

47.7

3.8

Psychotriaaff.

tinctoria(Aubl.)

Rae

usch.

250(7)

470(13)

20(1)

460(12)

30(1)

50(1)

0(1)

0(3)

0(0)

0(2)

0(0)

0(0)

4.1

8.1

0.5

7.2

0.7

0.7

Merianiahe

xamera

Spragu

e

110(3)

170(5)

20(1)

20(1)

210(9)

20(1)

1(1)

0(6)

0(0)

0(0)

0(3)

0(0)

2.2

5.6

0.5

0.3

5.8

0.5

Faramea

micon

ioides

Stan

dl.

100(3)

60(2)

50(2)

130(4)

30(1)

90(2)

1(2)

0(1)

0(0)

0(1)

0(1)

0(1)

2.2

1.2

1.2

2.2

0.9

1.7

Psychotria

cartha

gene

nsisJacq

.

110(3)

10(0)

30(1)

130(4)

50(2)

90(2)

1(2)

0(0)

0(1)

0(1)

0(1)

0(1)

2.4

0.2

1.2

21.8

1.6

(Continues)

6 of 13 | ALMEYDA ZAMBRANO ET AL.

TABLE

2(Continued

)

Spec

ies

Den

sity

(stems/ha)

(relativeden

sity

[%])

Dominan

ce(m

2/ha)

(relativedominan

ce[%

])Eco

logicalIm

portan

ceValue

Highuse

Med

ium

use

Low

use

Highuse

Med

ium

use

Low

use

Highuse

Med

ium

use

Low

use

H1

H2

M1

M2

L1L2

H1

H2

M1

M2

L1L2

H1

H2

M1

M2

L1L2

Palicou

reasp.1

70(2)

70(2)

20(1)

10(0)

10(0)

100(3)

1(2)

0(2)

0(3)

0(0)

0(0)

0(3)

1.9

21.9

0.1

0.2

3

Palicou

reasp.2

70(2)

10(0)

70(3)

80(2)

10(0)

50(1)

1(2)

0(0)

0(1)

0(1)

0(0)

0(2)

1.9

0.1

21.5

0.3

1.4

Magno

liaaff.gentryiA

.

Vázquez

70(2)

10(0)

10(0)

10(0)

0(0)

10(0)

3(7)

0(1)

0(0)

0(0)

0(0)

0(1)

4.6

0.7

0.4

0.3

00.6

Cyathea

bipinn

atifida

(Bak

er)Domin

50(1)

90(3)

10(0)

20(1)

10(0)

20(1)

1(3)

0(2)

0(0)

0(0)

0(0)

0(0)

22.2

0.4

0.3

0.3

0.4

Elaeagia

sp.1

80(2)

0(0)

0(0)

60(2)

0(0)

0(0)

1(4)

0(0)

0(0)

0(0)

0(0)

0(0)

2.9

00

0.9

00

Saurau

iape

ruvian

a

Buscal.

110(3)

60(2)

30(1)

0(0)

0(0)

0(0)

0(1)

0(0)

0(0)

0(0)

0(0)

0(0)

1.9

10.6

00

0

Ced

rela

mon

tana

Moritz

exTurcz.

20(1)

20(1)

20(1)

0(0)

10(0)

0(0)

1(3)

0(0)

0(2)

0(0)

0(0)

0(0)

1.7

0.3

1.2

00.2

0

Eugeniasp.2

20(1)

0(0)

0(0)

0(0)

10(0)

0(0)

2(5)

0(0)

0(0)

0(0)

0(0)

0(0)

30

00

0.3

0

Others

1,220(34)

1,280(36)

1,460(60)

1,910(52)

1,350(56)

2,870(76)

9(23)

20(39)

3(43)

3(66)

2(56)

4(79)

28.6

37.7

51.7

58.8

56.3

77

Total

3,540

(100)

3,510

(100)

2,430

(100)

3,700

(100)

2,390

(100)

3,800

(100)

40

(100)

50

(100)

7 (100)

5 (100)

3 (100)

5 (100)

100

100

100

100

100

100

Note:

Relativeva

lues

expressed

inpercentage

sareplacedin

paren

thesisnex

tto

absolute

values.F

oodspeciesarelistedin

bold

andpresentedfirst,follo

wingspeciesareranke

dbyove

rallecologicalimportan

ce.

ALMEYDA ZAMBRANO ET AL. | 7 of 13

permits 125‐2014‐MINAGRI‐DGFFS/DGEFFS, 056‐2013‐AG‐DGFFS‐DGEFFS, and 225‐2015‐SERFOR‐DGGSPFFS). All research followed

the protocols for the ethical treatment of primates outlined by the

American Society of Primatologists (ASP).

3 | RESULTS

3.1 | Habitat use

The total area within 50m of a GPS fix was 235.6 ha (e.g., study site).

High‐use zones covered 9.2 min–max 7.7–10.5% (21.6min–max,

18.2–24.7 ha) of the study area within three main separate polygons

ranging from 5.1 to 8.8 ha (Figure 4). Medium‐use zones covered

22.3 min–max 21.7–23.1% (52.6min–max, 51.1‐54.5 ha) of the study

site divided into two main separate areas comprising 12.6 and

19.0 ha. Low‐use zones constituted 68.5 min–max 66.4–68.5%

(161.0 min–max, 156.4–166.2 ha) of the study area. Differences in

total area and spatial distribution of use zones did not differ greatly

between mean and uncertainty bounded use maps and are therefore

not presented.

3.2 | Forest composition

A total of 157 plant species (134 species and 23 morphospecies)

were recorded across the six vegetation transects (0.6 ha). A

maximum richness of 78 species was found in transect H1 (high‐use zone), and a minimum richness of 62 species was found in

transect H2 (high‐use zone, Table 1). The Shannon diversity index

ranged from 3.47 (transect H2) to 3.9 (transect L2, low‐use zone).

The DCA showed considerable variation in species composition

across the three use zones except for high‐use transects, which

shared a very similar floristic composition (Figure 5). Transect M2

(medium‐use zone) had the highest similarity in species composition

to the high‐use zones of all transects in medium‐ and low‐use zones.

Species considered as food sources for L. flavicauda had higher

density, dominance, and ecological importance values (EIV) in

transects in high‐use zones (Figure 6). As a group, food species had

a relative density, relative dominance, and relative importance of

25.1%, 36.0%, and 31.0% respectively in high‐use zones, compared to

13.7%, 14.5%, and 14.9% in low‐use zones. In transect H1, the most

important species were Styloceras columnare (EIV: 9.2), Nectandra

membranacea (Sw.) Griseb. (EIV: 8.5), Hieronyma macrocarpa (EIV:

8.1), and Hedyosmum cuatrecazanum (EIV: 5.7). In transect H2, the

most important species were H. cuatrecazanum (EIV: 9.0), Psychotria

aff. tinctoria (Aubl.) Raeusch. (EIV: 8.1), Pourouma montana C.C. Berg

(EIV: 7.4), and S. columnare (EIV: 5.9). Styloceras columnare had high

ecological importance in all use zones. The remaining food plant

species were found to be either absent or in low density or

dominance in the medium‐ and low‐use zones (Figure 6 and Table 2).

Hieronyma macrocarpa and Hedyosmum cuatrecazanum, two

sources of fruits and flowers for L. flavicauda (Hernandez Jaramillo,

2013) had greater ecological importance in high‐ and medium‐usetransects. Hieronyma macrocarpa had a relative dominance of 13% in

transect H1, but its relative dominance fell below 0.5% in all other

transects. Similarly, H. cuatrecazanum had a relative dominance of

14%, 11%, and 7% in transects H2 (high‐use), M2 (medium‐use), andH1 (high‐use zone), respectively, whereas its lowest relative

dominance values of 4%, 0.1%, and 1% were seen in transects L1,

L2 (low‐use), and M1 (medium‐use), respectively.Nectandra membranacea and Magnolia aff. gentryi A. Vásquez also

showed particularly high relative dominance in transect H1 com-

pared to medium‐ and low‐use zones. Magnolia aff. gentryi had a

relative dominance of 7% in transect H1, whereas its relative

dominance was less than 1% in the medium‐ and low‐use zones.

N. membranacea had relative dominance of 10% in transect H1,

whereas it accounted for 5% or less of the total basal area in

medium‐ and low‐use zones. Species found to have high ecological

importance (EIV, >8) only in high‐ and medium‐use zones were

H. macrocarpa, H. cuatrecazanum, N. membranacea, Nectandra sp.,

Magnolia aff gentryi, P. aff tinctoria, and Ficus spp. (Table 2).

3.3 | Forest structure

Forest structure analysis revealed significant differences (p < .05)

across transects for stem density (F = 7.16, df = 59, p < .001), vine

density (χ2 = 13.54, df = 5, p = .019), total height (χ2 = 11.35, df = 5,

p = .045), crown spread (F = 3.60, df = 59, p = .007), moss cover

(χ2 = 12.80, df = 5, p = .025), crown illumination (χ2 = 12.80, df = 5,

p = .25), and vine infestation (χ2 = 20.80, df = 5, p = .01; Table 3).

F IGURE 5 Detrended correspondence analysis (DCA) displaying

the similarity/dissimilarity in plant species composition acrosstransects in the three use zones: low‐use (L1, L2), medium‐use(M1, M2), and high‐use (H1, H2). Distances on the graph reflect the

similarity in species composition

8 of 13 | ALMEYDA ZAMBRANO ET AL.

However, post hoc tests showed that transects located in high‐usezones had similar characteristics to medium‐ and/or low‐usetransects for all variables. Thus, we did not find a clear relationship

between high‐use zones and any of the structural variables

evaluated.

Collectively, stems from all species showed a reverse J‐shapediameter distribution across all transects. This trend indicates

continuous regeneration and recruitment into larger diameter classes

throughout the study area. However, when looking at the diameter

distribution of the nine species identified as food plants for

L. flavicauda separately, we observed variation in diameter distribu-

tions across transects and species (Figure 7).

Transects located in the high‐use zones had an overall higher

presence of food plants across diameter classes than transects in the

medium‐ and low‐use zones. Transects H1 and H2 (high‐use zones)

had a total of 910 and 870 stems of feeding species/ha respectively,

whereas densities in low‐ and medium‐use transects ranged between

360 and 610 stems of feeding species/ha.

Natural regeneration (DBH, <10 cm) of feeding plants occurred at

higher densities in high‐use transects. In transect H1, all food species

identified for L. flavicauda, were present in diameter classes lower

than 10 cm and totaled 640 stems/ha. In transect H2, 550 stems/ha

had a DBH <10 cm including all identified food species. In all other

transects, natural regeneration occurred at lower densities and did

not include all food species. For example, transect L1 had a total of

450 regenerating stems/ha, 82% (370) of which were S. columnare.

Similarly, in DBH classes greater than 20 cm, transects in the

high‐use zones presented the highest density of feeding plants, with

120 stems/ha in transect H1 and 150 in transect H2. Transects in the

medium‐use zone had 120 and 110 stems/ha of feeding species.

F IGURE 6 Relative density, dominance, and importance of feeding plants for Lagothrix flavicauda across use zones evaluated at the study sitein Amazonas region, Peru

TABLE 3 Structural parameters across transects

Parameter

High use Medium use Low use

H1 H2 M1 M2 L1 L2

Density (stems 0.01/ha) 35.4 ± 2.16 a,b 35.1 ± 2.81 a,b 24.3 ± 2.10 a 37 ± 2.40 b 23.9 ± 1.69 a 38 ± 3.3 b

Density (stems/ha) 3540 3510 2430 3700 2390 3800

Vine density in transect 0.9 ± 0.38 a,b 0.5 ± 0.22 a 1.7 ± 0.56 a,b 0.9 ± 0.38 a,b 3.3 ± 0.8 b 1 ± 0.49 a,b

Total height (m) 6.62 ± 0.39 a 7.44 ± 0.31 a,b 8.89 ± 0.7 b 7.05 ± 0.28 a,b 7.48 ± 0.52 a,b 7.28 ± 0.33 a,b

Crown spread (cm) 2.07 ± 0.1 a 2.8 ± 0.13 b 3.18 ± 0.277 b 2.57 ± 0.13 a,b 2.74 ± 0.19 a,b 2.75 ± 0.25 a,b

Moss cover 1.88 a 2.16 a 2.41 a,b 2.49 a,b 2.64 b 1.84 a

Crown illumination index 1.88 2.16 2.47 2.49 2.64 1.84

Vine infestation index 0.82 a,b 1.81 a 1.29 a,b 1.42 a,b 1.35 a,b 1 b

Note: Values given are means ± standard deviation (SD). Letters (a, b) indicate significant differences at p < .05.

ALMEYDA ZAMBRANO ET AL. | 9 of 13

Low‐use transects presented the lowest density of feeding species in

this diameter class with 90 and 30 stems/ha.

4 | DISCUSSION

4.1 | Habitat preference

Foraging and feeding occupy a large portion of the time budget of

many primate species (Defler, 1995; Di Fiore & Campbell, 2010; Di

Fiore & Rodman, 2001; Hanya, 2004). Therefore, the spatial

distribution and density of food sources can influence the intensity

of habitat use. L. flavicauda spends on average 30% of their time

feeding and 13–18% foraging (Hernandez Jaramillo, 2013; S. Shanee

& Shanee, 2011). Accordingly, our results showed that differences in

forest composition and especially the dominance of mature food

trees appear to be important factors in determining habitat use by

L. flavicauda. At least nine species reported in the literature as food

sources for L. flavicauda (Hernandez Jaramillo, 2013; Leo Luna, 1980;

S. Shanee, 2014a) had greater ecological importance (density +

dominance) in high‐use zones (Figure 6) and presented continuous

regeneration and recruitment into larger diameter classes. In

contrast, food plants in medium‐ and low‐use zones had less

ecological importance or were absent.

Hieronyma macrocarpa and Hedyosmum cuatrecazanum are

sources of fruits and flowers for L. flavicauda (Hernandez Jaramillo,

2013). We found that individuals of H. macrocarpa in transect H1 had

greater diameters (higher dominance) than those present in medium‐and low‐use zones. As tree diameter is an accurate indicator of

canopy volume, which is positively correlated with fruit yield

(C. A. Chapman et al., 1992; Miller & Dietz, 2004), this could indicate

that L. flavicauda prefers habitats with food trees of greater

diameters and therefore greater fruit and flower productivity.

There is no clear influence of forest structure on L. flavicauda

habitat use, as structural measures were relatively similar between

high‐ and low‐use zones. None of the 14 structural characteristics

evaluated were significantly different in high‐use zones compared to

F IGURE 7 Diameter distribution. Density of stems/ha in 5‐cm diameter classes across the three use zones evaluated at the study site in

Amazonas region, Peru

10 of 13 | ALMEYDA ZAMBRANO ET AL.

both medium‐ and low‐use zones. Transects from high‐use zones

showed a higher density of fruiting and flowering trees compared to

the low‐use zone and transect M1. However, these differences were

not significant, and long‐term phenological data from all use zones

would be necessary to better understand differences in fruiting and

flowering patterns.

Tree height has been reported to play a role in habitat preference

with some primate species preferring taller trees as an antipredation

strategy (Enstam & Isbell, 2004) and other species preferring lower forest

strata for the same reason, either in foraging or sleeping uses (Chagas &

Ferrari, 2011; Kupsch, Waltert, & Heymann, 2014; Pyritz, Büntge,

Herzog, & Kessler, 2010). The use of forest strata can be influenced by

ecological constraints (i.e., niche partitioning; Md‐Zain & Ch’ng, 2011;

Schreier, Harcourt, Coppeto, & Somi, 2009). L. flavicauda predominantly

uses higher forest strata, using the mid‐canopy for traveling and the

upper canopy for resting and feeding (S. Shanee, 2014b). We did not find

the high‐use zones to have significantly different average tree height.

Nevertheless, visual estimates of height are subject to error, and this

result should be taken with caution. To further assess the influence of

forest structure on L. flavicauda habitat use, future studies will need to

focus on areas with more structural variability. Additionally, our study

does not draw conclusions on how competition (intraspecific or

interspecific) and predation may be driving habitat use, and should thus

be subject to future studies as well.

4.2 | Ecological and conservation implications

Primates are one of the primary consumers of fruits in tropical forests

(Terborgh, 1983), and therefore among the main seed dispersers

(Stevenson, 2000; Stevenson, Castellanos, Pizarro, & Garavito, 2002). In

addition, forest demography and structure are profoundly influenced by

seed dispersal (Nathan & Muller‐Landau, 2000; Schupp & Fuentes,

1995; Wang & Smith, 2002). In our study, the importance of the

ecological role of L. flavicauda as a seed disperser is suggested by the

spatial distribution of plant species and natural regeneration. Spatial

distribution of seeds dispersed by Ateline primates within their home

range is highly correlated with habitat use (Stevenson, 2004). In our

study, transects in the high‐use zones (separated by 0.6 km) showed the

highest regeneration of feeding plants. In addition, we found that high‐use zones have the highest similarity in floristic composition. Indeed,

Hieronyma macrocarpa, S. columnare, H. cuatrecazanum, Ficus spp., and

most other feeding plants known to be utilized by L. flavicauda have

colorful fleshy fruits with seeds dispersed mainly by endozoochory (C. A.

Chapman, 2005). Species that L. flavicauda feed upon which are

primarily wind dispersed and shade‐intolerant (i.e., H. americanus) did

not show high densities of regeneration at the study site. Future studies

are necessary to better understand the influence of seed dispersal by L.

flavicauda on forest composition and structure. Other primate seed

dispersers such as Cebus yuracus, Aotus miconax, and Ateles belzebuth

occur in the region and may be important drivers of forest composition

and structure as well.

The observed natural regeneration represents an excellent opportu-

nity for future habitat improvement. Sites, where regeneration occurs

naturally, are of particular importance as conservation efforts in these

areas can be more effective and less costly by avoiding deforestation and

protecting seed dispersers. Additionally, we recommend targeting

reforestation and enrichment planting with key food species where

natural regeneration is not possible. For example, Styloceras columnare

and Ocotea sp. have successfully been produced in nurseries run by local

communities around the study site (N. Shanee & Shanee, 2010). Such

efforts could be replicated with other species and expanded to other

areas. Furthermore, identification and protection of sites with similar

floristic composition to the high‐use zones may ensure habitat availability

for L. flavicauda. We recognize that the applicability of our findings to

broader conservation efforts may be limited, as this study examined one

group for a 10‐month period. Variability may exist between the factors

driving habitat use for different groups of L. flavicauda, thus, our results

should be viewed with caution until they are supplemented by further

studies focused on other groups. Habitat preference by

L. flavicauda can be better understood by evaluating seasonal movements,

feeding behavior, and plant phenology over a longer period. We hope

that the findings presented in our study will be synthesized with future

findings to further understand habitat use by L. flavicauda throughout its

range and optimize conservation guidelines.

ACKNOWLEDGMENTS

This study was made possible thanks to funding from Neotropical

Primate Conservation, Community Conservation through grants from the

Margot Marsh Biodiversity Foundation, Care for the Wild, National

Geographic Foundation, Idea Wild, Lush, and the Rufford Foundation;

The College of Arts and Sciences, The Graduate School, and The

Department of Geography at The University of Alabama. We thank Ítalo

Revilla, Luis Pillaca, and the Forestry Herbarium MOL of the Forest

Sciences Department at Universidad Nacional Agraria La Molina for

support during plant species identification, and SUMPA S.A.C for lending

us equipment for botanic surveys. We are grateful to Godofredo, Pascual,

and Floriano Diaz, and to Mike and Renee Young for their assistance

during fieldwork.

ORCID

Sandra L. Almeyda Zambrano http://orcid.org/0000-0001-5731-

9248

Eben N. Broadbent http://orcid.org/0000-0002-4488-4237

Sam Shanee http://orcid.org/0000-0001-5573-6208

Scott A. Ford http://orcid.org/0000-0002-7881-8270

Angelica M. Almeyda Zambrano http://orcid.org/0000-0001-5081-

9936

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SUPPORTING INFORMATION

Additional supporting information may be found online in the

Supporting Information section.

How to cite this article: Almeyda Zambrano SL,

Broadbent EN, Shanee S, et al. Habitat preference in the

critically endangered yellow‐tailed woolly monkey (Lagothrix

flavicauda) at La Esperanza, Peru. Am J Primatol. 2019;e23032.

https://doi.org/10.1002/ajp.23032

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