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Diet and activity pattern of howler monkeys (Alouatta palliata) in Los Tuxtlas Mexico effects of habitat fragmentation and implications for conservation.

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American Journal of Primatology 69:1013–1029 (2007)
RESEARCH ARTICLE
Diet and Activity Pattern of Howler Monkeys
(Alouatta palliata) in Los Tuxtlas, Mexico:
Effects of Habitat Fragmentation and Implications
for Conservation
JURGI CRISTÓBAL-AZKARATE1 AND VÍCTOR ARROYO-RODRÍGUEZ2
1
Centre Special en Primats, Universitat de Barcelona, Barcelona, Spain
2
División de Postgrado, Instituto de Ecologı´a A. C., Km 2.5 Antigua Carretera a Coatepec
No. 351, Xalapa 91070, Veracruz, Mexico
Accelerated deforestation is causing the rapid loss and fragmentation of
primary habitat for primates. Although the genus Alouatta is one of the
most studied primate taxa under these circumstances, some results are
contradictory and responses of howlers to habitat fragmentation are not
yet clear. In this paper, we conduct a cross-study of the available
researches on mantled howlers (Alouatta palliata) in forest fragments in
Los Tuxtlas, Mexico, to (1) describe the diet and activity pattern of
howlers; (2) analyze the similarity in the diet across studies; and (3)
relate both fragment size and howler population density with different
characteristics of their diet, home range size, and activity pattern.
Howlers consumed 181 plant species belonging to 54 families. Ficus was
the most important taxa in the howlers’ diet, followed by primary species
such as Pterocarpus rohrii, Nectandra ambigens, Poulsenia armata, and
Brosimum alicastrum. Secondary and non-secondary light-demanding
plant species, which are representatives of disturbed habitat, contributed
with a high percentage of their feeding time. Only 23% of the species
consumed were the same across all the studies, suggesting that howlers
adapt their diet to the food availability of their respective habitats.
Population density is the best predictor of howlers’ ecological and
behavioral changes in response to forest fragmentation, probably owing
to its relationship with food availability. Howlers respond to the increase
in population densities by increasing the (1) diversity of food species in
the diet; (2) consumption of non-tree growth forms; and (3) consumption
of new plant items. Home range size is also predicted by population
density, but fragment size is a better predictor, probably owing to the fact
that howler groups can overlap their home ranges. Our results emphasize
the importance of conserving the larger fragments and increasing the size
Correspondence to: Jurgi Cristóbal-Azkarate, Centro de Investigaciones Tropicales Universidad
Veracruzana. Casco de la exhacienda Lucas MartÃn, privada de Araucarias. Sin numero. Col
Periodistas. C.P. 91019. Apartado Postal: 525. Xalapa, Veracruz, Mexico. E-mail: jurgic@yahoo.com
Current address: Centro de Investigaciones Tropicales Universidad Veracruzana, Xalapa, Veracruz,
Mexico.
Received 24 June 2006; revised 2 September 2006; revision accepted 23 November 2006
DOI 10.1002/ajp.20420
Published online 28 February 2007 in Wiley InterScience (www.interscience.wiley.com).
r 2007 Wiley-Liss, Inc.
1014 / Cristóbal-Azkarate and Arroyo-Rodrı́guez
of small and medium-sized ones. Am. J. Primatol. 69:1013–1029,
2007. c 2007 Wiley-Liss, Inc.
Key words: population density; food sources; fragment size; Neotropical
primates
INTRODUCTION
The principal threat for the conservation of primates is the loss, transformation
and fragmentation of their habitat [Cowlishaw & Dunbar, 2000]. Forest fragmentation is associated to an important reduction of suitable habitat for primates, a
decrease of habitat fragment size, an increase of fragment isolation, and a reduction
in habitat quality [Arroyo-Rodrı́guez et al., 2005; Arroyo-Rodrı́guez & Mandujano,
2006a; Fahrig, 2003; Marsh, 2003]. As a consequence, the persistence of primates in
highly fragmented landscapes depends on their ability to adapt their diets and
activity pattern to these new modified habitats [Bicca-Marques, 2003].
This situation has attracted the attention of many primatologists and a
significant effort is being made to understand primate responses to habitat
perturbation. The success of primates in coping with habitat fragmentation has
been related to their capacity to (1) feed from many different plant species and adapt
their diet to the species available in the habitat [Onderdonk & Chapman, 2000;
Crockett, 1998; Pinto et al., 2003; Rivera & Calmé, 2006; Silver & Marsh, 2003],
(2) increase the amount of leaves in their diet [Asensio et al., 2006; Juan et al., 2000;
Neves & Rylands, 1991; Rodrı́guez-Luna et al., 2003], (3) consume exotic and
secondary species frequent in disturbed habitats [Bicca-Marques & CalegaroMarques, 1994; Onderdonk & Chapman, 2000; Mbora & Meikle, 2004], (4) feed on
vines and climbing plants associated to secondary vegetation [Asensio et al., 2006;
Onderdonk & Chapman, 2000; Rodrı́guez-Luna et al., 2003], (5) use small home
ranges [Estrada & Coates-Estrada, 1996; Lovejoy et al., 1986; Neves & Rylands,
1991; Onderdonk & Chapman, 2000], and (6) minimize energy expenditure by
adjusting their activity patterns [Juan et al., 2000; Silver & Marsh, 2003].
Although the genus Alouatta is one of the most studied primate taxa under
these circumstances and has shown to be one of the most adaptable to
fragmentation [e.g., Bicca-Marques, 2003; Chiarello, 2003; Lovejoy et al., 1986],
studies analyzing howlers’ behavioral and ecological changes in response to
habitat fragmentation are scarce. In addition, they are usually focused on only a
few groups of howlers. All this has favored that on some occasions results are
contradictory and that some response patterns to fragmentation are not yet clear
[see Bicca-Marques, 2003]. This information is of most importance to evaluate the
threats that howlers are facing in these modified environments and to, when
necessary, develop management strategies. With the aim of shedding some light
on these matters, Bicca-Marques [2003] performed a genus-based cross-study
comparison based on the research conducted in 27 Neotropical forests throughout
the Alouatta distribution, finding that most aspects of Alouatta ecology and
behavior were not predicted by fragment size.
Fragment size was the only fragmentation factor that Bicca-Marques [2003]
considered in his study, but another critical consequence of habitat fragmentation
observed for howlers is the increment in population density [Cristóbal-Azkarate
et al., 2005; Mandujano et al., 2006; Van Belle & Estrada, 2006]. Several studies
indicate that some of the adaptations of howlers to habitat fragmentation can be
caused by the increase in population density. For example, Rodrı́guez-Luna et al.
Am. J. Primatol. DOI 10.1002/ajp
Diet and Activity Pattern of Howler Monkeys / 1015
[2003] report that a group of howlers living on an island in Los Tuxtlas increased
time spent traveling and consuming leaves, vines, and climbing plants after the
population density increased from 1.2 to 6.9 individual per hectare. Similarly,
González-Picazo et al. [2001], also in Los Tuxtlas, observed an increase in folivory
and a reduction in the number of species consumed after the size of a fragment
was reduced from 3.2 to 2.2 ha and the population density increased from 1.6 to
3.2 individuals per hectare. Finally, Cristóbal-Azkarate et al. [2005] discuss that
the high population densities in Los Tuxtlas may be critically reducing the
availability of food for howlers and consequently increasing immature mortality.
Bicca-Marques [2003] concludes that there is an urgent need for comparative
studies analyzing the behavior of howlers under varying degrees of habitat
fragmentation. This should be done studying one species, to eliminate the interspecific differences in the response patterns [Bicca-Marques, 2003], and with
populations living in fragments that previously belonged to the same continuous
forest to reduce the influence of different floristic composition over the resulting
patterns [Bicca-Marques, 2003; Estrada et al., 1999].
This suggestion lead us to conduct a cross-study similar to Bicca-Marques’
but concentrating only on mantled howler (Alouatta palliata) populations living
in forest fragments and in the Agaltepec Island in Los Tuxtlas, Mexico. In this
paper, we describe the diet and activity pattern of howlers, analyze the similarity
in the diet across studies, and relate both fragment size and howler population
density with the (1) number of plant species consumed; (2) number of plant
species responsible for the bulk of the diet; (3) contribution of different plant
items and growth forms to the diet; (4) contribution of different plant ecological
groups (primary, secondary, and non-secondary light-demanding species) to the
diet; (5) home range size; and (6) activity pattern.
METHODS
Study Site
Los Tuxtlas represents the northernmost limit for the distribution of
A. palliata [Estrada & Coates-Estrada, 1988]. This region is located in the
southeast of the State of Veracruz, Mexico (18180 –181450 N, 941370 –951220 W). The
climate is warm and humid, with a mean annual temperature of 251C, an annual
rainfall between 3,000 and 4,600 mm [Soto & Gama, 1997], and contains altitudes
that range from 0 to 1,780 m. The original dominant vegetation type was tropical
rainforest, but this region has been severely fragmented during the last 60 years
[Guevara et al., 2004] and the remaining howler populations are isolated in
archipelagos of forest fragments that vary in size, isolation distances and habitat
quality [Arroyo-Rodrı́guez et al., 2005; Arroyo-Rodrı́guez & Mandujano, 2006a;
Cristóbal-Azkarate et al., 2005; Mandujano et al., 2006]. This is an appealing
region for the study of habitat fragmentation as it shows a clear pattern of
fragmentation, with forest fragments surrounded mainly by pasture lands, and
has a fairly well-known history of fragmentation [for further details see GonzálezSoriano et al., 1997; Guevara et al., 2004].
Data Collection
For this paper, we considered all the available studies (published articles,
book chapters and theses) on the diet and activity pattern of A. palliata conducted
in Los Tuxtlas until June 2006 (Table I). With the corresponding authorization,
we also considered the results of two theses whose results have not been yet
Am. J. Primatol. DOI 10.1002/ajp
1016 / Cristóbal-Azkarate and Arroyo-Rodrı́guez
TABLE I. Studies Analyzed for Diet, Activity Pattern and Home Range of Howlers
(Alouatta palliata) in Los Tuxtlas, Mexico
Activity pattern (%)
Ref.a
1
2
3
4
5
5
5
6b
6
7
8
8
8
9b
9
10c
10c
11
12
12d
12
Site
Field Station
Santa Marta
Balzapote
Agaltepec Island
Balzapote
Medium
Large
Balzapote-t1
Balzapote-t2
Santa Marta
Agaltepec Island
Playa Escondida
Arroyo Liza
Agaltepec Island-t1
Agaltepec Island-t2
Montepı́o-Gr1
Montepı́o-Gr2
La Selva
Rancho Huber
Montepı́o-Gr3
Ruiz Cortinez
Forest
Home
Density
Months size (ha) range (ha) (ind/ha)
12
12
12
74
2
2
2
7
7
12
10
10
11
10
9
11
11
8
12
12
12
700.0
10.0
3.6
8.3
3.2
35.0
250
3.7
2.2
8.0
8.3
40.0
1.3
8.3
8.3
63.8
63.8
5.5
244.1
63.8
7.2
60.0
10.0
3.6
8.3
—
—
—
3.7
2.2
8.0
8.3
14.7
1.3
8.3
8.3
—
—
5.5
40.0
19.3
6.4
0.22
1.00
1.67
2.29
1.56
0.20
0.03
1.62
3.18
2.75
7.11
1.00
4.62
1.21
6.87
0.50
0.50
0.91
0.19
0.48
0.83
Rest
Feed
Travel
—
62.0
80.0
66.0
74.4
78.6
69.0
46.0
45.0
50.0
55.1
62.0
69.2
65.5
69.8
8.0
9.0
62.0
78.0
77.0
69.0
—
28.0
17.0
22.0
24.3
16.4
28.0
10.0
10.1
40.0
29.0
26.0
24.2
22.7
16.9
81.0
85.0
26.0
14.0
14.0
22.0
—
10.0
2.0
12.0
0.7
1.4
2.2
1.1
2.4
10.0
14.3
11.0
6.3
11.8
13.3
9.0
4.0
12.0
7.0
8.0
9.0
References: 1. Estrada [1982, 1984]; 2. Jiménez-Huertas [1992]; 3. Estrada et al. [1999]; 4. Serio-Silva [1992];
Serio-Silva et al. [2002]; 5. Juan et al. [2000]; 6. González-Picazo et al. [2001]; 7. Garcı́a-Orduña [2002]; 8. Asensio
[2003]; Asensio et al. [2006]; 9. Rodrı́guez-Luna et al. [2003]; 10. Bravo [2003]; 11. A. Shedden-González
[unpublished data]; 12. B. Hervier [unpublished data].
a
Only references 1–4 and 6–10 report the complete list of species used as food resource by howlers.
b
Studies the same group of howlers but in different times (t1 and t2).
c
Studies the two groups of howlers in the same forest fragment (Gr1 and Gr2).
d
Studies a different group than ref. 10–3-years later.
—, unavailable data.
published (A. Shedden-González & B. Hervier, unpublished data; Table I).
In addition to populations in forest fragments, we also considered for the analysis
a population of howlers living in the Agaltepec Island, in Catemaco, Los Tuxtlas.
Even if the Agaltepec Island is not a proper forest fragment, this population
does serve for the purpose of this study because (1) these howlers belong to the
same subspecies (A. palliata mexicana) as the rest of howlers in Los Tuxtlas,
(2) the floristic composition of the island is similar to the surrounding [CastilloCampos & Laborde, 2004; López-Galindo & Acosta-Pérez, 1998], and (3) all
the analyzed howler populations are studied under a no-migration scenario.
For further details on the history of the Agaltepec Island howlers, see Rodrı́guezLuna et al. [2003].
Similar to Bicca-Marques [2003], the variables that we considered for
analyses where, activity pattern (i.e., percentage of time resting, feeding and
travelling), home range size, number of species consumed, number of species
contributing with 50 and 80% of the diet, and percentage of total feeding time
(TFT) devoted to the consumption of different plant items (leaves, fruits, and
flowers). According to Rodrı́guez-Luna et al. [2003] and Asensio et al. [2006],
Am. J. Primatol. DOI 10.1002/ajp
Diet and Activity Pattern of Howler Monkeys / 1017
habitat fragmentation can ‘‘force’’ howlers to consume second choice plant items
(e.g., petioles and barks), as well as non-tree growth forms (lianas, vines, shrubs,
herbs, palms, hemiparasites; sensu Cornelissen et al. [2003]). Consequently, we
also considered the percentage of time spent feeding these plant items and growth
forms for the analysis. Finally, as howlers can respond to habitat fragmentation
increasing their consumption of secondary species frequent in disturbed habitats
[Bicca-Marques & Calegaro-Marques, 1994; Fuentes et al., 2003], we also
classified plant species used as food sources by howlers in three ecological groups
[Benı́tez-Malvido, 1998; Hill & Curran, 2003]: primary species, secondary species,
and non-secondary light-demanding (NSLD) species. Primary species establish
mainly under forest shade and persist in old-growth forests. Secondary species need
intense light during the first stage of growth, establishing only under canopy gaps
and at the forest edge and they do not persist in old-growth forest. Finally, NSLD
species grow under similar light requirement to secondary species, and during the
first growth stages they can be found together with secondary species, but they have
longer life cycles, and grow to become natural species of old-growth forest canopy. To
make this classification we consulted information from fascicles of Flora de Veracruz,
Flora Neotropica, XAL herbaria (Instituto de Ecologı́a, A.C.), and numerous plant
species lists [see further details in Arroyo-Rodrı́guez & Mandujano, 2006a,b].
Data Analysis
To analyze the similarity of the diets across study samples, we performed a
cluster analysis using the Sorensen’s coefficients (S): S 5 2C/A1B, where A is the
number of species used as food sources by howlers in the study i, B the number
of species used in the study j, and C the number of species used in both studies.
This analysis was performed using the MVSP program for Windows, version 3.0
[Kovach, 1998].
To establish if the variation in home range size, diet and activity patterns are
associated to fragment size and population density, we used the Spearman rank
correlation coefficient [Sokal & Rohlf, 1995].
To reduce the influence of seasonality on the results, all analyses were
performed considering only studies based on 49 study months [Bicca-Marques,
2003; see Table I]. All analyses were performed using the Statistica Program for
Windows, version 5.5 [Anonymous, 2000].
RESULTS
Diet
Data on the species used as food sources by howlers in Los Tuxtlas are
available for 14 samples of nine studies (references 1–4 and 6–10; Table I).
In general, howlers in Los Tuxtlas consumed 181 plant species belonging to
54 families. Howlers consumed Ficus spp. nearly 50% of TFT in most studies.
Other plant species highly consumed by howlers were Pterocarpus rohrii,
Cecropia obtusifolia, Nectandra ambigens, Poulsenia armata, Trema micrantha,
and Brosimum alicastrum. It is noteworthy that the value of each of these species
in howler diet changed from one group to another (Table II).
Data on the contribution of plant items to the diet of howlers in Los Tuxtlas
are available for 17 samples of 10 studies (Table III). Leaves were the most
consumed plant item, with an average (7SD) of 55.2719.7% (range 5 26.6–
87.3%) of TFT, followed by fruits (35.0715.7%, range 5 12.7–59.0%), petioles and
barks (5.6710.2%, range 5 0–37.0%), and flowers (2.776.7%, range 5 0–26.0%).
Am. J. Primatol. DOI 10.1002/ajp
Moraceae
Moraceae
Cecropiaceae
Burseraceae
Anacardiaceae
Moraceae
Moraceae
Mimosaceae
Anacardiaceae
Caesalpinaceae
Fabaceae
Burseraceae
Fabaceae
Moraceae
Anacardiaceae
Anacardiaceae
Fabaceae
Fabaceae
Lauraceae
Sapotaceae
Vitaceae
Fabaceae
Mimosaceae
Myrtaceae
Combretaceae
Mimosaceae
Caesalpinaceae
Ebenaceae
Family
GF
Tree
Tree
Tree
Tree
Tree
Tree
Tree
Tree
Tree
Tree
Tree
Tree
Tree
Tree
Tree
Tree
Tree
Tree
Tree
Tree
Liana
Tree
Tree
Tree
Tree
Tree
Tree
Tree
Species
Ficus spp.
Brosimum alicastrum
Cecropia obtusifolia
Bursera simaruba
Spondias radlkoferi
Poulsenia armata
Pseudolmedia oxyphylaria
Albizia purpusii
Spondias mombin
Cynometra retusa
Andira galeotiana
Protium copal
Gliricidia sepium
Chlorophora tinctoria
Astronium graveolens
Tapirira mexicana
Lonchocarpus cruentus
Pterocarpus rohrii
Nectandra ambigens
Mastichodendron capiri
Vitis tilifolia
Dussia mexicana
Leucaena leucocephala
Eugenia acapulcensis
Terminalia amazonia
Inga acrocephala
Dialium guianense
Diospyros digyna
NSLD
Prim
Sec
NSLD
NSLD
Prim
Prim
Prim
NSLD
Prim
Prim
NSLD
Sec
NSLD
Prim
NSLD
Prim
Prim
Prim
Prim
Sec
Prim
Sec
NSLD
Prim
NSLD
Prim
Prim
EG
14
11
10
9
8
7
7
6
6
5
4
4
4
4
4
4
4
3
3
3
3
3
3
2
2
2
2
2
NS
46.1
5.5
9.2
3.4
2.2
8.8
2.1
1.8
1.4
2.3
4.7
3.2
1.9
1.8
1.7
1.4
0.8
21.2
7.8
5.8
3.9
2.8
0.9
5.7
5.2
4.7
4.5
3.9
(15.5)
(4.2)
(10.5)
(2.5)
(2.3)
(8.1)
(2.1)
(1.8)
(1.1)
(2.8)
(0.8)
(3.1)
(1.3)
(0.7)
(2.2)
(2.1)
(0.9)
(31.6)
(12.8)
(0.9)
(4.7)
(4.1)
(1.2)
(5.4)
(1.4)
(4.4)
(5.4)
(5.5)
% TFT
21.7–65.1
0.3–10.8
0.1–37.2
0.04–6.3
0.1–5.8
0.9–22.6
0.2–6.0
0.3–4.0
0.2–3.1
0.2–6.9
4.1–59.0
0.7–7.7
0.1–2.9
1–2.6
0.4–4.9
0.01–4.5
0.03–1.9
1.1–57.6
0.1–22.6
5–6.8
0.2–9.3
0.4–7.5
0.1–2.3
1.8–9.5
4.2–6.2
1.6–7.7
0.7–8.4
0.03–7.8
Range (%)
All
AGA, BAL, MON, PLA, SAN, STA
AGA, BAL, MON, PLA, SAN, STA
AGA, BAL, LIZ, MON, PLA, SAN
AGA, BAL, LIZ, PLA, SAN
BAL, LIZ, PLA, SAN, STA
BAL, LIZ, PLA, SAN, STA
AGA, LIZ, MON, PLA, SAN
AGA, SAN, STA
BAL, PLA, SAN
AGA
AGA
AGA
AGA
AGA
AGA, PLA, SAN
AGA
BAL, PLA, SAN
BAL, STA, SAN
AGA
AGA, LIZ, PLA
LIZ, SAN, STA
AGA
LIZ, PLA
SAN
LIZ, PLA
SAN, STA
AGA, PLA
Sitesa
TABLE II. Plant Species Contributing to 80% of Feeding Time of Nine Troops of Howlers Across 14 Samples in Los Tuxtlas (ref.
1–4 and 6–10 from Table I)
1018 / Cristóbal-Azkarate and Arroyo-Rodrı́guez
Am. J. Primatol. DOI 10.1002/ajp
Rollinia mucosa
Syngonium podophylum
Trema micrantha
Platymiscium sp.
Rynchosia minima
Sideroxylon capiri
Rivina humilis
Psiguria triphylla
Brosimum lactenses
Cissampelos pareira
Annonaceae
Araceae
Ulmaceae
Fabaceae
Fabaceae
Sapotaceae
Phytolaccaceae
Cucurbitaceae
Moraceae
Menispermaceae
Tree
vine
Tree
Tree
Liana
Tree
Shrub
Liana
Tree
Vine
LF
Prim
NSLD
Sec
Prim
Sec
Prim
NSLD
Prim
Prim
NSLD
EG
2
2
1
1
1
1
1
1
1
1
NS
1.5 (2.0)
1.2 (1.7)
12.1
5.7
4.7
4.3
3.3
3.0
2.8
2.1
% TFT
0.1–2.9
0.1–2.4
Range (%)
LIZ, PLA
AGA, LIZ
MON
MON
AGA
AGA
AGA
AGA
LIZ
AGA
Sitesa
We indicate the number of samples (NS), the percentage of total feeding time (% TFT), each plant species (mean7SD), the variation range (%), and the sites where each plant
species was used as food resource by howlers. GF, growth form. Ecological groups (EG): Prim, primary species, Sec, secondary species, NSLD, non-secondary light demanding
species.
a
Sites: AGA, Agaltepec Island; BAL, Balzapote; LIZ, Arroyo Liza; MON, Montepio; PLA, Playa Escondida; SAN, Santa Marta; STA, Field Station (see Table I).
Species
Family
Diet and Activity Pattern of Howler Monkeys / 1019
Am. J. Primatol. DOI 10.1002/ajp
1020 / Cristóbal-Azkarate and Arroyo-Rodrı́guez
TABLE III. Diet Composition of Howlers in Los Tuxtlas, Mexico
% Plant items in the diet
% Ecological groups
% Growth forms
Ref. No. Species Leaves Fruits Flowers Othera Prim
Sec
NSLD
Trees
Otherb
1
2
3
4
6
6
7
8
8
8
9
9
10
10
13
13
13
6.3
0.0
9.0
2.1
10.8
9.6
8.8
20.7
5.9
2.7
1.1
6.1
50.2
9.5
—
—
—
30.7
30.0
60.5
78.8
58.4
66.7
39.9
54.0
63.1
81.0
75.6
54.3
45.9
73.9
—
—
—
100.0
100.0
97.8
92.6
99.4
99.2
98.3
67.6
94.5
94.9
89.2
75.4
100.0
100.0
—
—
—
0
0
3.1
0.4
0.6
0.8
0.7
32.6
5.5
5.0
0.3
0.1
0
0
—
—
—
27
7
52
36
41
33
45
56
49
35
32
30
14
19
—
—
—
49.0
—
54.0
28.0
65.0
80.0
61.0
57.1
36.9
36.7
26.6
33.0
87.3
82.3
49.0
77.0
60.0
49.9
30.0
41.0
59.0
29.0
20.0
13.0
21.4
57.3
51.2
52.5
31.0
12.7
17.7
46.0
23.0
40.0
0.2
—
1.0
o1
0.4
0.1
26.0
5.2
0.2
2.1
0
0
0
0
5.0
0
0
0
0
4.0
0
0.6
0.1
0
16.3
6.2
10.0
20.1
37.0
0
0
0
0
0
63.0
63.8
36.1
12.2
30.9
23.8
50.3
25.4
30.9
16.3
12.8
15.1
4.0
17.4
—
—
—
Proportions are based on the time spent consuming each item. We indicate the number of plant species used, as
well as the contribution to the diet of (1) plant items, (2) ecological groups, and (3) growth forms. Ecological
groups: Prim, primary species, Sec, secondary species, NSDL, non-secondary light demanding species. Reference
numbers correspond to those in Table I.
a
Petioles and barks.
b
Lianas, vines, shubs, palms, herbs, epiphytes, and hemiparasites.
—, unavailable data.
Trees were the most consumed growth form (134 species, average of TFT
(7SD) 5 87.2724.9%), followed by vines and lianas (35 species, 2.877.3% of
TFT) and other growth forms such as shrubs, herbs, palms, epiphytes, and
hemiparasites (12 species, 7.1714.1% of TFT) (Table III).
According to ecological groups, most of the species consumed were primary
(77 of 181 species), but NSLD species were the most consumed species in terms
of feeding time (68 species; average of TFT (7SD) 5 54.2722.1%), followed by
primary species (28.5718.0% of TFT), and secondary species (31 species;
9.5712.5% of TFT) (Table III). Cecropia obtusifolia, Gliricidia sepium, Vitis
tilifolia, Leucaena leucocephala, Trema micrantha, and Rynchosia minima
were the most consumed secondary species by howlers (Table II). It is worth
mentioning that C. obtusifolia represented 9.2712.5% of TFT in ten of the
14 analyzed samples (range 5 0.1–37.2%).
When comparing the species used as food sources by howlers across study
samples we found that on average (7SD). Sorensen’s similarity index was
0.2370.14 (range 5 0.06–0.76). This means that only 23% of the species consumed
were the same across all the samples. The greatest similarities were between
samples from the same study groups observed at different times (Agaltepec and
Balzapote, Fig. 1).
Fragment size was only related to the number of species contributing to
howlers’ diet (rs 5 0.59, Po0.05) and to the percentage of time feeding from
non-tree growth forms (rs 5 0.64, Po0.05) (Fig 2). On the other hand, howler
population density was significant and negatively related to the percentage of
Am. J. Primatol. DOI 10.1002/ajp
Diet and Activity Pattern of Howler Monkeys / 1021
Santa Marta (2)
Agaltepec (4)
Agaltepec (9)
Agaltepec (9)
Agaltepec (8)
Montepio (10)
Montepio (10)
Balzapote (6)
Balzapote (6)
Balzapote (3)
Santa Marta (7)
Field Station (1)
Arroyo Liza (8)
Playa Escondida (8)
0.04
0.2
0.36
0.52
0.68
0.84
1
Sorensen's Coefficient
Fig. 1. Cluster analysis of the diet of howlers in Los Tuxtlas. Grouping of studies was performed
based on the similarities of the plant species consumed across studies (Sorensen’s similarity index).
No. food species
1)
rs = -0.59
n = 12
P < 0.05
60
50
40
30
20
10
0
0
2
4
6
rs = 0.60
n = 12
P < 0.05
60
50
40
30
20
10
0
0
8
2
4
8
6
Density of howlers (individuals/ha)
Fragment size (Ln)
% Time feeding non-trees
growth forms
2)
40
35
30
25
20
15
10
5
0
40
35
30
25
20
15
10
5
0
rs = -0.64
n = 12
P < 0.05
0
2
4
Fragment size (Ln)
6
8
rs = 0.68
n = 12
P < 0.05
0
2
4
6
8
Density of howlers (individuals/ha)
Fig. 2. Relationship between both fragment size and howler population density: (1) the number of
plant species used as food sources by howlers and (2) the percentage of total feeding time consuming
non-tree growth forms.
time feeding from trees (rs 5 0.53, Po0.01; Fig. 3), but positively related to
the (1) number of species in howlers’ diet (rs 5 0.60, Po0.05; Fig 2), (2) number of
species contributing with 50 and 80% of the TFT (rs 5 0.63, Po0.05 and rs 5 0.73,
Po0.01; Fig. 3), (3) consumption of non-tree growth forms (rs 5 0.68, Po0.01;
Fig. 2), and (4) consumption of new plant items (petioles and barks) (rs 5 0.67,
Po0.01) (Fig. 3). We did not find any significant relationship between both
howler population density and fragment size with the time spent feeding from
different ecological groups.
Am. J. Primatol. DOI 10.1002/ajp
1022 / Cristóbal-Azkarate and Arroyo-Rodrı́guez
2)
100
95
90
85
80
75
70
65
60
rs = -0.53
n = 12
P < 0.01
0
2
4
6
Density of howlers (individuals/ha)
8
40
35
30
25
20
15
10
5
0
rs = 0.41
n = 13
P < 0.01
0
2
4
6
Density of howlers (individuals/ha)
8
4)
8
7
6
5
4
3
2
1
0
rs = 0.63
n = 11
P < 0.05
0
2
4
No. species making up
80% of diet
No. species making up
50% of diet
3)
% Time feeding petioles
and barks
% Time feeding trees
1)
6
Density of howlers (individuals/ha)
8
rs = 0.41
n = 11
P < 0.01
20
18
16
14
12
10
8
6
4
2
0
0
2
4
6
8
Density of howlers (individuals/ha)
Fig. 3. Relationship between howler population density in Los Tuxtlas, Mexico: (1) percentage
of total feeding time (TFT) consuming trees; (2) percentage of TFT consuming petioles and barks;
(3) number of species that accounted for 50% of TFT; and (4) number of species that accounted for
the 80% of TFT.
Home Range Size
The home range size was reported in 16 of the 21 analyzed samples (Table I).
In 11 samples home range equaled fragment size owing to small size of habitat
fragments (Table I). Considering only cases in which home range differed from
fragment size (n 5 5), average home range size (7SD) was 28.1721.7 ha
(range 5 6.4–60 ha), and it was positively related with fragment size (rs 5 0.96,
P 5 0.01, Fig. 4). On the other hand, home range size was negatively related
to howler population density (rs 5 0.65, P 5 0.02) (Fig. 4).
Activity Pattern
The activity pattern was reported in 20 of the 21 analyzed samples (Table I).
Across studies, howlers on average (7SD) spent most of their time resting
63720% (range 5 8–97%), followed by feeding 24721% (range 5 0.3–85%) and
traveling 977% (range 5 0.03–26%) (Table I). We did not find any significant
relationship between either howler population density or fragment size with the
activity pattern.
DISCUSSION
In a cross-study comparison of the responses of Alouatta to habitat
fragmentation, Bicca-Marques [2003] found that most of the aspects of howler
ecology and behavior were not predicted by fragment size. In a similar fashion, we
found that fragment size is not a good predictor of howlers’ response to forest
fragmentation but that population density is. The increase in population density
in fragments was positively related with the total number of species used as food
sources, the number of species making up most of the diet, the consumption of
Am. J. Primatol. DOI 10.1002/ajp
Diet and Activity Pattern of Howler Monkeys / 1023
Home range (ha)
60
rs = 0.96
50
n=5
P < 0.01
40
30
20
10
0
0
2
4
6
8
Fragment size (Ln)
Home range (ha)
60
50
rs = -0.65
40
n = 13
P < 0.05
30
20
10
0
0
2
4
6
8
Density of howlers (individuals/ha)
Fig. 4. Relationship between both fragment size and howler population density, with the home
range size of howlers in Los Tuxtlas, Mexico.
non-tree growth forms, and the consumption of plant items other than fruits,
leaves and flowers.
High population densities have been related to the reduction in food
availability for several species [see Fowler, 1987], and in the case of Los Tuxtlas,
this may be negatively affecting immature howlers’ survival [Cristóbal-Azkarate
et al., 2005]. Our results are in line with these studies, and suggest that the
increase in population densities is the principal cause for the reduction in food
availability that results in the observed changes in howlers’ behavior and ecology.
According to our results, howlers in Los Tuxtlas respond to the increase
in population densities by diversifying their diet (i.e., increasing the number of
species used as food source, as well as the number of species contributing with
50 and 80% of the feeding time). This is not surprising as different studies have
pointed out that two of the most important features of howlers’ success in coping
with forest fragmentation are their capacity to feed from many different plant
species, and their ability to adapt their diet to the plant species available in
different habitats [Asensio et al., 2006; Bicca-Marques & Calegaro-Marques,
1994; Crockett, 1998; Pinto et al., 2003; Rivera & Calmé, 2006; Rodrı́guez-Luna
et al., 2003; Silver & Marsh, 2003]. In this sense, howlers in Los Tuxtlas
consumed a great amount of different plant species (181 species belonging to
54 families) and their diet’s composition only coincided with one another in 23%
of the species (Fig. 1). As studies in Los Tuxtlas showed that plant composition
and structure varies significantly between forest fragments [Arroyo-Rodrı́guez
et al., 2005; Arroyo-Rodrı́guez & Mandujano, 2006a,b], these results suggest that
howlers are adapting their diet to the dietary availability of their respective
habitats.
Am. J. Primatol. DOI 10.1002/ajp
1024 / Cristóbal-Azkarate and Arroyo-Rodrı́guez
Despite the capacity to feed from many different species, howlers in Los
Tuxtlas spent on average 46% (range 5 22–65%) of the TFT feeding from Ficus
spp. This marked preference for Ficus is a feature also observed in other studies
[reviewed by Bicca-Marques, 2003]. This is most probably related to the high
abundance of figs in fragments in Los Tuxtlas [Arroyo-Rodrı́guez & Mandujano,
2006a, b] and their large fruit production and asynchronous phenological cycles
[Ibarra-Manrı́quez & Wendt, 1992; Shanahan et al., 2001]. Nevertheless, this
study shows that howlers can also feed heavily from other available species,
e.g., Andira galeotiana (59% of TFT); Pterocarpus rohrii (57.6% of TFT); Cecropia
obtusifolia (37.2% of TFT); Poulsenia armata (22.6% of TFT); Nectandra
ambigens (22.6% of TFT).
Howlers responded to the increase in population density by increasing the
consumption of non-tree growth forms (vines, lianas, epiphytes, hemiparasites,
shrubs, herbs, and palms). Similarly, Onderdonk and Chapman [2000] reported
that a group of Colobus guereza living in a forest fragments consumed more vines
and shrubs than a group in continuous forest. These food items appear to be
second choice food sources as their consumption seems to be ‘‘forced’’ by the
reduction in food availability. Nevertheless, the case of Agaltepec Island (33%
of TFT) demonstrates that they can become important food sources for howlers
when food items from preferred trees become scarce [Asensio, 2003; Asensio et al.,
2006; Rodrı́guez-Luna et al., 2003].
Neither population density or fragment size are good predictors of the time
howlers spent eating leaves, fruits or flowers in Los Tuxtlas. Our results are
similar to those of Bicca-Marques [2003]. It is not clear why howlers do not
increase the amount of leaves in their diet in response to higher population
densities or smaller fragment sizes, but it seems this change is not a
straightforward response to the reduction of food availability and that other
factors may be involved. Unfortunately, this question will need to be further
explored. However, population density was a good predictor of the time howlers
spent eating barks and petioles. It is noteworthy that they were not consumed in
most studies, but whenever consumed, they were consumed heavily (Table III)
which suggests that they can be important food sources when first choice plant
items become scarce.
This study supports the idea that secondary vegetation may be an important
food source for folivorous primates [Chiarello, 2003; Cristóbal-Azkarate et al.,
2005; Lovejoy et al., 1986; Mbora & Meikle, 2004; Onderdonk & Chapman, 2000].
Howlers in Los Tuxtlas fed from 31 different secondary species, which on average
accounted for 9.5% of TFT, and its consumption reached 50.2% of TFT in one
study. Three observations support that secondary species are not necessarily
second choice food sources: (1) its consumption did not change with the increase
in population densities or the reduction in fragment size; (2) Estrada [1984]
reported Cecropia obstusifoia, a typical secondary vegetation species, as one of
the most consumed species in continuous forest; and (3) Cecropia obsusifolia was
one of the most consumed species (9.2% of TFT) in Los Tuxtlas, and in one study
it was the most consumed species (37.2% of TFT). Other secondary vegetation
species important for howlers’ diet in Los Tuxtlas were Trema micrantha, Vitis
tilifolia, Rynchosia minima, Gliricidia sepium, and Leucaena leucocephala
(Table II).
On average, NSLD species accounted for most of the feeding time (54% of
TFT). Note that Ficus is a NSLD genus. It is most likely that in the short and
medium term most of the fragments in Los Tuxtlas will continue to be isolated.
Therefore, the capacity of NSLD species to establish and grow in ‘‘modified’’
Am. J. Primatol. DOI 10.1002/ajp
Diet and Activity Pattern of Howler Monkeys / 1025
conditions found in fragments [see Arroyo-Rodrı́guez & Mandujano, 2006b;
Hill & Curran, 2003] is very important for howlers. As long as processes like
pollinization and seed dispersion are maintained, which seems to be the case in
Los Tuxtlas fragments (Javier Laborde, unpublished data), the replacement of
these feeding species will not be compromised in the forest fragments.
Primates’ success to persist in fragments has been related to their capacity to
adapt home range size to habitat availability [Estrada & Coates-Estrada, 1996;
Lovejoy et al., 1986; Onderdonk & Chapman, 2000]. Similarly, in Los Tuxtlas
howlers responded to the reduction in fragment size and the increase in
population density by reducing the size of their home ranges. Fragment size is a
better predictor of home range size than population density. We believe that this
is related to the fact that howler groups usually overlap their home ranges
[Crockett & Eisenberg, 1987], so the most important factor affecting their home
range size is the total availability of habitat. This result suggests that howlers can
adapt their home range size to habitat availability, which is probably
accomplished through dietary adaptations discussed in this paper.
Similar to Bicca-Marques [2003], we did not find any relationship between
fragment size or population density with the activity patterns. Bicca-Marques
[2003] argues that howlers’ energy-saving behavioral adaptation for their
folivorous diet compromises their activity pattern. Contrarily, Pavelka & Knopff
[2004] argue that howlers inactive behavior may be more phylogenetically
constrained and not linked to the digestion of large quantities of leaves. Further
studies will be necessary to identify the factors determining the activity patterns
of howlers.
In general, this study emphasizes the importance of conserving the larger
fragments, and increasing the size of small and medium sized ones. This should
be done by first planting secondary species such as Cecropia obtusifolia, and Vitis
tilifolia, and NSLD such as Ficus spp. Secondary species grow fast and can
provide food for howlers in the short term, whereas NSLD will provide food in
the medium and long term. In addition, the growth of this vegetation will create
the microclimatic conditions that will permit the germination of growth of
primary species such as Pterocarpus rohrii, Nectandra ambigens, Poulsenia
armata, and Brosimum alicastrum, important food sources for howlers in the long
term. These actions will favor the persistence of this endangered primate in
fragmented landscapes [Mandujano et al., 2006], as fragment size is negatively
related to population density [Cristóbal-Azkarate et al., 2005; Mandujano
et al., 2006], positively associated with the quantity and quality of food sources
[Arroyo-Rodrı́guez et al., 2005; Arroyo-Rodrı́guez & Mandujano, 2006a; CristóbalAzkarate et al., 2005; Juan et al., 2000], and negatively related to howler
parasitism [Santa Cruz et al., 2000] and hunting pressure [Chiarello & de Melo,
2001; Peres, 2001].
Finally, as forest fragmentation is not only related to the reduction of
available habitat, but also to changes in its floristic characteristics [e.g., ArroyoRodrı́guez & Mandujano, 2006b; Benı́tez-Malvido, 1998; Hill & Curran, 2003;
Laurance et al., 1997, 2000], we would like to stress the need for sound studies
relating the floristic characteristics of the forest fragments and howlers’ ecology,
behavior and food choice.
Furthermore, processes other than the reduction in food availability may
affect primates in forest fragments. For example, the extinction of big predators
[Cristóbal-Azkarate et al., 2005] and food competitor such as spider monkeys
(Ateles geoffroyi) [Estrada & Coates-Estrada, 1996] in most forest fragments,
in addition to the reduction in hunting pressure, could account for the high
Am. J. Primatol. DOI 10.1002/ajp
1026 / Cristóbal-Azkarate and Arroyo-Rodrı́guez
population densities observed in Los Tuxtlas [Cristóbal-Azkarate et al., 2005].
Higher densities of solitary howler males associated to changes in the population
dynamics in forest fragments have been related to higher levels of cortisol and
testosterone [Cristóbal-Azkarate et al., 2006, in press]. This may have negative
effects on their health and fitness. Furthermore, the high population densities,
forest disturbance and forest fragmentation may facilitate contact between
primates and between primates and humans [Gillespie, 2004; Gillespie &
Chapman, 2006; Nunn et al., 2003; Scott, 1998; Stuart & Strier, 1995]. Without
the understanding of how these processes are affected by forest fragmentation
and how they interact with each other, we will not be able to understand fully the
pressures imposed by fragmentation over howlers and their response to them.
CONCLUSIONS
Howlers in Los Tuxtlas consumed a huge range of plant species and
demonstrated low dietary overlap among sites.
Population density, and not fragment size, is the best predictor of howlers’
ecological and behavioral changes in response to forest fragmentation in Los
Tuxtlas. This is probably owing to its relationship with food availability.
Fragment size seems to be the most important factor affecting howlers’ home
range size.
Howlers cope with higher population densities associated with habitat
fragmentation by increasing (1) the diversity of food species consumed; (2) the
consumption of non-tree growth forms; and (3) the consumption of new plant
items. These adaptations may explain howler success in disturbed habitats.
Most of the howlers’ diet is based on secondary and non-secondary lightdemanding species such as Cecropia obtusifolia. and Ficus spp. As these feeding
species do well in modified environments, their availability in forest fragments
may be secured. This would favor the persistence of howlers in fragmented
landscapes.
Finally, our results emphasize the importance of conserving the larger
fragments, and increasing the size of small and medium sized ones. This should
be done by first planting secondary and NSLD species, which could create the
condition for the establishment and growth of primary species.
ACKNOWLEDGMENTS
We thank Blanca Hervier and Aralisa Shedden for providing the results of
their yet unpublished theses; Pedro Dias and Jake Dunn for the very helpful
comments and corrections on the manuscript, and finally Una Laffan and Yashua
Silem for their support. J. C. Serio-Silva provided valuable information.
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