International Journal of Primatology, Vol. 27, No.

4, August 2006 (

C 2006)

DOI: 10.1007/s10764-006-9061-0

Forest Fragmentation Modifies Habitat Quality

for Alouatta palliata
Vı́ctor Arroyo-Rodrı́guez1,3 and Salvador Mandujano2
Received January 28, 2005; revised May 4, 2005; accepted May 17, 2005; Published Online
September 21, 2006

Fragmentation reduces habitat area, increases the number of habitat patches,

decreases their size, and increases patch isolation. For arboreal mammals
such as howlers (Alouatta palliata), canopy modifications from fragmen-
tation processes could also negatively affect habitat quality. We analyzed
changes in the composition and plant structure of 15 fragments (1–76 ha)
and compared them with vegetation from a continuous tropical rain forest
reserve (700 ha) in Los Tuxtlas, Mexico. At each site, we sampled 1000 m2 of
all trees, shrubs, and lianas with a diameter at breast height (DBH) ≥ 10 cm.
We obtained estimates of species richness, density, and basal area for dif-
ferent ecological groups, DBH ranges, and top food resources for howlers.
We used a stepwise multiple regression analysis to determine relationships
between fragment characteristics (size, shape index, and isolation) and plant
variables. Compared to continuous forest, fragments have altered composi-
tion and plant structure, with large trees absent from the canopy. The basal
area of top food resources is higher in continuous forest. Fragment size is the
best explanation for the differences in composition and plant structure. The
largest fragments had greater basal area of top food resources and more large
primary trees in the canopy. Overall, our results suggest that fragmentation
altered the habitat quality for howlers.
KEY WORDS: Alouatta palliata; conservation; fragmentation; habitat quality; Los Tuxtlas;
Mexico; vegetation.

1 División de Postgrado, Instituto de Ecologı́a A. C., Km 2.5 Ant. Carret. Coatepec No. 351,
Xalapa 91070, Ver., México.
2 Departamento. Biodiversidad y Ecologı́a Animal, Instituto de Ecologı́a A. C., Km 2.5 Ant.
Carret. Coatepec 351, Xalapa 91070, Ver., México.
3 To whom correspondence should be addressed; e-mail: victorarroyo rodriguez@hotmail.com.

1079
0164-0291/06/0800-1079/0

C 2006 Springer Science+Business Media, Inc.
1080 Arroyo-Rodrı́guez and Mandujano

INTRODUCTION

The greatest threat to the survival of nonhuman primates is habitat loss

and fragmentation (Mittermeier and Konstant, 2002). The fragmentation
process has 4 major effects: reduction in habitat amount, increase in the
number of habitat patches, decrease in habitat patch size, and increase in
patch isolation (Fahrig, 2003). In particular, studies with primates (Estrada
and Coates-Estrada, 1996; Medley, 1993; Wieczkowski, 2004) show that
abundance correlates positively with patch size. Further, application of
metapopulation models has shown that primate incidence depends on both
fragment size and connectivity (Chapman et al., 2003; Mandujano et al.,
2006; Swart and Lawes, 1996). In consequence, the spatial structure of a
landscape is of central importance in understanding the effects of fragmen-
tation on population viability (Fahrig, 2003).
For herbivorous primates that are principally tree-dwelling, however,
modifications in the tree canopy could also have a negative influence
on habitat quality. Botanical studies have suggested that on fragments,
the number of tree species drops and changes occur in plant composi-
tion and structure (Benitez-Malvido and Martinez-Ramos, 2003; Hill and
Curran, 2003; Laurance et al., 2002). The effect is most noteworthy
near fragment edges, where the recruitment rate of secondary species
is higher (Dislich and Pivello, 2002; Laurance et al., 1998a, b; Malcolm,
1994) and the tree mortality rate accelerates (Didham and Lawton, 1999;
Laurance et al., 1997, 2000), particularly in the case of shade-tolerant species
(Benitez-Malvido, 1998). Therefore, changes in plant composition, diver-
sity, and structure are more substantial on smaller, less uniformly shaped
fragments (Laurance and Yensen, 1991).
Howlers (Alouatta palliata) are an arboreal folivorous-frugivorous
species (Crockett and Eisenberg, 1987). Changes in the canopy can reduce
the quantity and quality of available habitat, limiting a fragment’s carrying
capacity (Estrada and Coates-Estrada, 1996; Medley, 1993; Wieczkowski,
2004). For instance, some studies have shown that the presence and abun-
dance of primates is related to vegetation attributes such as the rich-
ness, abundance, and basal area of top food resources (Balcomb et al.,
2000; Chapman and Chapman, 1999; Cristobal-Azkarate et al., 2005). In
a study of 30 sites across the Neotropics, Stevenson (2001) determined
that fruit production is a good predictor of primate biomass. In addition,
for many primates, the number and size of trees correlate positively with
primate abundance (Mbora and Meikle, 2004; Medley, 1993; Ross and
Srivastava, 1994; Skorupa, 1986; Wieczkowski, 2004). Consequently, to
elaborate management strategies for primate conservation, it is critical to
ascertain how fragment size, shape, and isolation affect both the quality and
Changes in Habitat Quality for Alouatta palliata 1081

the quantity of resources for primates inhabiting fragmented landscapes

(see Marsh, 2003).
According to Estrada and Coates-Estrada (1996), in Los Tuxtlas,
Mexico, local people destroyed 75% of the original forest area for cattle
ranching and farming; actually 20% consists of forest fragments, and only
5% contains continuous forest at high elevations. Howler populations have
therefore become isolated on fragments of varying shapes, sizes, and de-
grees of isolation. Studies of the region have shown the effect of certain
fragment characteristics on howler distribution, abundance, and other bi-
ological factors (Estrada and Coates-Estrada, 1996; Gomez-Marin et al.,
2001; Juan et al., 2000; Rodriguez-Toledo et al., 2003; Silva-Lopez et al.,
1993). We analyzed changes in howler habitat resulting from tropical for-
est fragmentation. We define habitat quality as the degree of vegetation
disturbance—both in composition and structure—on fragments (1–76 ha)
compared to continuous forest vegetation (700 ha) across the core zone of
Los Tuxtlas Biosphere Reserve. In particular, we analyzed the availability
of basic plant families and species that serve as howler food resources in the
region.

METHODS

Study Area

The study area is located between the Santa Marta and San Martin
Pajapan Volcanoes in a buffer zone to the south of Los Tuxtlas Special
Biosphere Reserve (18◦ 26 N and 94◦ 55 W) in southern Veracruz, Mexico
(Fig. 1). The climate is humid warm to warm temperate with a mean
annual temperature of 24–26◦ C. Annual rainfall oscillates between 3000
and 4000 mm (Soto and Gama, 1997). The original dominant vegeta-
tion type was tropical rain forest. The study site covers 4986 ha, 11%
of which correspond to tropical forest distributed among 92 fragments
(1–76 ha) isolated by a matrix of pasture and cropland (Mandujano et al.,
2006). An increase in cattle-raising activity has led to isolation of some of
the fragments for the past 30 yr (Guevara et al., 2004)

Studied Fragments

Howlers inhabit 18 of the 92 existing fragments (Mandujano et al.,

2006). We randomly selected 15 (8 occupied by howlers and 7 unoccu-
pied) of varying sizes to cover the range represented within each category
1082 Arroyo-Rodrı́guez and Mandujano

Fig. 1. Location of the Los Tuxtlas Tropical Biology Station and the 15 forest fragments (in
black). Solid lines indicate routes that connect different towns; rivers and streams appear as
dotted lines.

(Table I). To locate fragments, we used the digitalized vegetation map of

Rodriguez-Toledo et al. (2003) and the 1:50,000 San Juan Volador (INEGI,
1999) topographical map. We calculated the size and perimeter of frag-
ments and the distance to continuous forest via GIS ArcView version 3.2.
Changes in Habitat Quality for Alouatta palliata 1083

We calculated √ fragment shape from a shape index (Forman and Godron,

1986): IF = P/2 Aπ, where in P and A are the fragment perimeter and area
measured in m, respectively. The index takes values = 1 when the frag-
ment is round and goes up to a maximum of 5 when the shape is highly
irregular.
As a control, we used continuous forest at Los Tuxtlas Tropical Bi-
ology Station, which has the same floristic association (Ibarra-Manriquez
et al., 1997), is located at the same altitude above sea level, and has a well-
preserved forest area (700 ha). A description of the flora, fauna, and forest
ecology of Los Tuxtlas is in Gonzalez-Soriano et al. (1997) and Guevara
et al. (2004).

Vegetation Sampling

We sampled vegetation following the Gentry (1982) protocol. In each

fragment and in continuous forest, we fixed 10 50 × 2-m transects randomly.
We recorded all tree, shrub, and liana species with diameter at breast height
(DBH) ≥ 10 cm. Based on fascicles from Flora of Veracruz and Neotropi-
cal Flora as well as on several studies (Benitez-Malvido 1998; Bongers et al.,
1988; Ibarra-Manriquez and Sinaca-Colin, 1995; Ibarra-Manriquez et al.,
1997; Martinez-Ramos and Alvarez-Buylla, 1995; Popma et al., 1988), we di-
vided species into 3 DBH ranges (10–30 cm, 31–60 cm, and >61 cm), which
also took into account their light needs for germination—primary or shade
tolerant, secondary or shade intolerant, and nonsecondary light demander
species (NSLD). Secondary species regenerate only in gaps and at the forest
edge. NSLD can survive in primary or secondary forest, but they need high
light during the first stage of growth. We collected species not identified in
the field for subsequent identification in MEXU herbaria (Institute of Biol-
ogy, Mexico, D.F.) and XAL (Institute of Ecology, Xalapa, Veracruz).

Data Analysis

On the basis of the sum of density (trees/unit of area), frequency (tran-

sects where each species appeared/total transects), and dominance (sum
of the total basal area for each species), we calculated the importance
value index (IVI) for each species grouping in the 8 occupied fragments,
7 unoccupied fragments, and in continuous forest (Moore and Chapman,
1986). The IVI permits us to obtain a more precise understanding of
 Table I. Vegetation and structural characteristics of 15 fragments and continuous forest at Los Tuxtlas, Mexico
1084

Fragment structural attributes Vegetation attributes/1000 m2

Fragments Isolationa (m) Size (ha) Shape indexb Forest interiorc (ha) No. families No. species No. plants Basal area (m2 )

Occupied fragments
F1 85 75.6 2.7 27.4 23 37 79 10.4
F2 17.8 57.2 2.9 13.6 25 43 89 9.0
F3 50.4 32.6 3.1 4 25 36 83 9.5
F4 195.7 29.9 4.3 0 29 48 79 7.5
F5 34.6 13.0 3.7 0 33 45 113 6.1
F6 115 11.8 1.5 0.2 42 42 80 3.9
F7 57.1 6.6 2.2 0 26 36 75 4.3
F8 19.9 2.7 1.5 0 26 35 61 6.8

Average 72.0 28.7 2.7 5.7 28.6 40.3 82.4 7.2

SD 59.9 26.0 1.0 10.0 6.2 4.9 14.7 2.4

Unoccupied fragments
F1 58.1 7.4 2.4 0 21 34 98 4.4
F2 115 6.7 1.7 0 20 33 58 3.1
F3 437.9 3.8 2.4 0 25 42 100 3.8
F4 199.5 3.0 1.3 0 20 28 58 4.2
F5 195.7 1.3 1.4 0 30 41 92 5.6
F6 70.5 1.1 1.7 0 36 52 102 9.6
F7 110 1.0 1.3 0 19 31 86 4.3

Average 169.7 3.5 1.7 0 24.4 37.3 84.9 5.0

SD 130.6 2.7 0.5 0 6.4 8.2 19.1 2.2

All fragments

Average 117.5 16.9 2.3 3.0 26.7 38.9 83.5 6.2

SD 107.9 22.6 0.9 7.6 6.4 6.6 16.3 2.5
Continuous – 700 1.0 – 20 34 63 14.1
forest

a Nearest neighbor distance.

b When shape index approaches 5, the fragment has a most irregular shape.
c Fragment size considering an edge of 100 m width (see Methods).
Arroyo-Rodrı́guez and Mandujano
Changes in Habitat Quality for Alouatta palliata 1085

the importance of different plant species on fragments and in continuous

forest.
To select top food families and species, we reviewed research on food
resource use by howlers living on different-sized fragments (Juan et al.,
2000; Silva-Lopez et al., 1993) on the 8.3-ha Agaltepec Island (Rodriguez-
Luna et al., 2003; Serio-Silva, 1995) and in continuous forest (Estrada, 1984)
in Los Tuxtlas. Based on the percentage of time the primates spent con-
suming each species, we selected the top 10 families and 20 species howlers
consumed most.
Considering both fragments and continuous forest, we quantified
species richness, density, and basal area (m2 ) for (1) all plant species in
1000 m2 , (2) each ecological group, (3) each DBH range, (4) sum of top 10
food families, and (5) sum of top 20 food species, summarizing a total of 27
variables. To analyze the values obtained for the 2 environments, we used a
Student’s t-test that compared a single observation, i.e., continuous forest,
with the mean from the fragments sampled (Sokal and Rohlf, 1995).
To determine the influence of fragment size, shape, and isolation on
the vegetation variables studied, we performed forward stepwise multiple
regression analysis, considering continuous forest as the largest (700 ha),
most regular fragment (shape index = 1), with zero isolation. We first log-
transformed the patch area to meet normality assumptions (Kolmogorov-
Smirnof; p>0.05). We used all 27 vegetation variables described previ-
ously. The multiple regression permits us to determine the explanatory
value of each independent variable included in the model, emphasiz-
ing the order of importance of the independent variables through the β
value.
Because the edge effect exercises the greatest influence ≤ 100 m of
the forest edge (Laurance and Yensen, 1991; Laurance et al., 1998b, 2002),
to ascertain its consequences in terms of fragment vegetation, we used
ArcView version 3.2 to calculate fragment size by eliminating 100 m of edge.
The size is henceforth considered the fragment interior (Table I). We per-
formed all analyses via the STATISTICA for Windows, version 5.5 (Stat-
Soft, 2000).

RESULTS

Differences Between Fragments and Continuous Forest

From the 16,000 m2 of sampled surface, we recorded 1316 plants

in 50 families and 147 species. The families with the highest number
of individuals are Euphorbiaceae (9.3% of records), Moraceae (8.3%),
1086 Arroyo-Rodrı́guez and Mandujano

Anacardiaceae (6.6%), Vochysiaceae (5.8%), and Monimiaceae (4.2%).

Considering the 10 species with the IVI, in continuous forest 9 are primary,
while in fragments, half of the 10 most important are secondary species and
NSDL (Table II). Of the 10 most important species in continuous forest,
only 4 (Pseudolmedia oxyphyllaria, Brosimum alicastrum, Guarea glabra
raza bijuga, and Dialium guianense) are important in occupied fragments,
and only 2 (Cynometra retusa and Vatairea lundelli) in unoccupied frag-
ments.
The occupied fragments are significantly larger (t = 2.54, df = 13,
p = 0.03) with more irregular shape (t = 2.41, df = 13, p = 0.03) than un-
occupied ones (Table I). Nevertheless, neither total plant abundance nor
the number of families and species differed between occupied and unoccu-
pied fragments, or between all fragments and continuous forest (Student’s
t-test, p>0.05). Total basal area, however, is significantly greater in con-
tinuous forest than in fragments (t = 3.33, df = 14, p = 0.005), and almost
significantly greater in occupied fragments compared with unoccupied frag-
ments (t = 1.85; df = 13, p = 0.09) (Table I). Per stratum, fragments had sig-
nificantly greater abundance and basal area of plants with DBH between
10 and 30 cm (Fig. 2). In contrast, continuous forest had greater richness,
abundance, and basal area of large trees (DBH > 60 cm). Consideration of
different ecological groups shows that only the basal area of primary species
is significantly higher in continuous forest (Fig. 2).

Analysis of Top Food Families and Species

Analyzing the 10 most important species of each community (Table II),

we found a higher percentage of species howlers potentially used in continu-
ous forest (90%) than on occupied (80%) and unoccupied (50%) fragments
(Table II). In continuous forest, 40% of the species belong to Moraceae or
Lauraceae, while in unoccupied fragments, they were not among the com-
munity’s most important species.
Considering the sum of the top 10 food families and top 20 food species
for Alouatta palliata, the basal area of the taxa is significantly higher in
continuous forest than in fragments (Fig. 2). Continuous forest has greater
representation of the Moraceae, Fabaceae, Lauraceae, and Boraginaceae
(Table III), the primary species Brosimum alicastrum, Poulsenia armata,
Nectandra ambigens, Pseudolmendia oxyphyllaria, Dialium guianense, and
Dussia mexicana, and the NSLD species Ficus sp. and Lonchocarpus cruen-
tus (Table IV). The remaining families and species were more representa-
tive in fragments (Tables III and IV).
 Table II. The 10 plant species with higher importance values index (IVI) in continuous forest and 15 forest fragments
Species Family Ecological groupa IVI Potential food for howlers

Continuous forest
Poulsenia armata Moraceae Pri 0.29 Yes
Pseudolmedia oxyphyllaria Moraceae Pri 0.25 Yes
Brosimum alicastrum Moraceae Pri 0.23 Yes
Nectandra ambigens Lauraceae Pri 0.22 Yes
Guarea glabra raza bijuga Meliaceae Pri 0.19 Yes
Dussia mexicana Fabaceae Pri 0.19 Yes
Cordia megalantha Boraginaceae Sec 0.17 Yes
Cynometra retusa Caesalpinaceae Pri 0.15 Yes
Dialium guianense Caesalpinaceae Pri 0.14 Yes
Vatairea lundelli Fabaceae Pri 0.10
Occupied fragments
Terminalia amazonia Combretaceae Pri 0.26 Yes
Tapirira mexicana Anacardiaceae NSLDs 0.16 Yes
Siparuna andina Monimiaceae Sec 0.12
P. oxyphyllaria Moraceae Pri 0.11 Yes
Dendropanax arboreus Araliaceae NSLDs 0.10 Yes
Changes in Habitat Quality for Alouatta palliata

G. g. r. bijuga Meliaceae Pri 0.09 Yes

Bursera simaruba Burseraceae NSLDs 0.08 Yes
B. alicastrum Moraceae Pri 0.07 Yes
D. guianense Caesalpinaceae Pri 0.07 Yes
Vochysia guatemalensis Vochysiaceae NSLDs 0.07
Unoccupied fragments
V. guatemalensis Vochysiaceae NSLDs 0.33
T. amazonia Combretaceae Pri 0.14 Yes
T. mexicana Anacardiaceae NSLDs 0.13 Yes
Croton schiedeanus Euphorbiaceae Sec 0.13 Yes
Dendropanax arboreus Araliaceae Pri 0.11 Yes
Siparuna andina Monimiaceae Sec 0.07
C. retusa Caesalpinaceae Pri 0.06 Yes
Hirtella triandra Chrysobalanaceae Pri 0.06
V. lundelli Fabaceae Pri 0.06
Saurauia yasicae Actinidiaceae Sec 0.06

a Primary (Pri), secondary (Sec), and nonsecondary light demander (NSLD) species.
1087
 1088

Fig. 2. Species richness, number of plants, and basal area by ecological groups, DBH ranges, and food resources of howlers, sampled in
1000 m2 of 15 fragments (average ± SD) and a continuous forest. Significant differences between fragments and continuous forest: ∗ p < 0.05,
∗∗ p<0.01; Student’s t-test, df = 14 for all cases.
Arroyo-Rodrı́guez and Mandujano
Changes in Habitat Quality for Alouatta palliata 1089

Table III. Species richness, density (plants/1000 m2 ), and basal area (m2 ) of the top 10 food
families for howlers at Los Tuxtlas
Number of species Density Basal area
Family Fragmentsa CFb Fragments CF Fragments CF

Moraceae 3.13 (2.4–3.9) 5 + 5.9 (4.3–7.5) 18 + 0.7 (0.3–1.1) 4.7 +

Lauraceae 1.9 (1.4–2.5) 1 − 2.3 (1.5–3.1) 3 + 0.1 (0.02–0.3) 1.6 +
Fabaceae 2.1 (1.5–2.8) 4 + 2.7 (1.4–3.9) 4 + 0.4 (0.2–0.6) 3.3 +
Boraginaceae 0.3 (0–0.7) 2 + 0.5 (0.03–1.0) 3 + 0.02 (0–0.04) 1.6 +
Sapotaceae 2.1 (1.6–2.6) 1 − 3.3 (2.1–4.5) 3 ns 0.3 (0.1–0.5) 0.2 ns
Euphorbiaceae 2.7 (2–3.5) 1 − 8.0 (5.8–10.2) 1 − 0.31 (0.2–0.4) 0.01 −
Annonaceae 1.1 (0.7–1.5) – 1.9 (1.0–2.8) – 0.1 (0.1–0.2) –
Anacardiaceae 1.9 (1.6–2.3) – 5.7 (3.9–7.5) – 0.5 (0.3–0.7) –
Burseraceae 1.0 – 1.9 (0.5-3.2) – 0.1 (0.02–0.1) –
Cecropiaceae 1.0 – 1.6 (0.6-2.6) – 0.03 (0.01–0.04) –
a Forest fragments: average (95% confidence interval).
b CF, Continuous forest: above the 95% CI ( + ); below the 95% CI ( − ); within 95% CI (ns).

Effects of Fragment Size, Shape, and Isolation

The stepwise multiple regression model is significant for 14 of the

27 variables analyzed (Table V). Fragment size is the best explanation
for the differences in plant composition and structure, with fragment iso-
lation as the variable with the lowest β values. Specifically, as fragment
size increased, total basal area also increased, especially that of primary
species, while secondary species density decreased. Fragment size also
correlates positively with the species richness, density, and basal area of
large trees (>60 cm DBH) but negatively with the species richness, den-
sity, and basal area of thin plants (>10–30 cm DBH). It is noteworthy
that as fragment size increased, so did the basal area of the most impor-
tant families and species for howlers, showing the highest determination
coefficients.
Conversely, fragment shape and isolation had lower β values in regres-
sions. It is interesting that primary species richness decreased and NSLD
richness increased with greater fragment isolation (Table V). Further, with
more fragment irregularity, the abundance of small species increased (>10–
30 cm DBH).

DISCUSSION

Does forest fragmentation modify habitat quality for howlers? Our re-
sults suggest that fragmentation not only modifies habitat amount, num-
ber of habitat patches, habitat patch size, and patch isolation (Fahrig,
1090 Arroyo-Rodrı́guez and Mandujano

Table IV. Density and basal area (m2 ) of the 20 top food species for howlers at Los Tuxtlas
Density Basal area
Species Fragmentsa CFb Fragments CF

Primary species
Brosimum alicastrum 0.7 (0.2–1.3) 3 + 0.2 (0–0.4) 2.10 +
Poulsenia armata 0.8 (0.01–1.6) 4 + 0.04 (0–0.07) 2.20 +
Pouteria campechiana 0.6 (0.1–1.1) 0.1 (0–0.2)
Pseudolmedia oxyphyllaria 2.5 (1.3–3.8) 9 + 0.13 (0.04–0.2) 0.40 +
Nectandra ambigens 0.2 (0–0.5) 3 + 0.05 (0–0.2) 1.60 +
Dialium guianense 1.6 (0.7–2.5) 3 + 0.1 (0.04–0.2) 0.48 +
Dussia mexicana 0.4 (0.1–0.8) 1 + 0.16 (0–0.3) 2.14 +
Secondary species
Cecropia obtusifolia 1.6 (0.6–2.6) 0.03 (0.01–0.04)
Non secondary-light demanders species
Bursera simaruba 1.9 (0.5–3.2) 0.08 (0.02–0.14)
Cordia dodecandra 0.3 (0–0.7)
Dendropanax arboreus 3 (1.9–4.1) 1 − 0.18 (0.05–0.3) 0.02 −
Ficus oerstediana 0.13 (0–0.3) 0.03 (0–0.07)
Ficus petenensis 0.06 (0–0.2) 0.003 (0–0.01)
Ficus sp 0.2 (0–0.4) 1 + 0.09 (0–0.3) 0.10 ns
Ficus tecolutensis 0.07 (0–0.2) 0.001 (0–0.004)
Ficus yoponensis 0.9 (0.4–1.4) 0.2 (0–0.4)
Lonchocarpus cruentus 0.2 (0–0.4) 1 + 0.003 (0–0.01) 0.21 +
Spondias mombin 0.7 (0–1.7) 0.05 (0–0.1)
Spondias radlkoferi 0.3 (0–0.8) 0.01 (0–0.01)
Tapirira mexicana 3.2 (1.9–4.5) 0.4 (0.2–0.6)
a Forest fragments: average (95% confidence interval).
b Continuous forest: above the 95% CI ( + ); below the 95% CI ( − ); within 95% CI (ns).

2003), but in Los Tuxtlas it also causes a reduction in habitat quality for
howlers. Consistent with several studies on fragmented tropical forest, ours
showed that the fragments had an altered vegetation composition and struc-
ture (Benitez-Malvido and Martinez-Ramos, 2003; Hill and Curran, 2003
Laurance et al., 2002), with lower quantity and quality of howler food re-
sources (Juan et al., 2000; Medley, 1993). Compared to continuous forest,
dominant plants on fragments are secondary species and NSLD that have
adapted to disturbed environments. Total basal area was higher in contin-
uous forest because of a greater abundance of large trees (DBH >60 cm),
especially primary species. Compared to continuous forest, fragments are
smaller and have a greater proportion of edge than interior areas have.
In fact, on removal of 100 m of edge, only 4 fragments have an interior
(Table I), which may accelerate the tree mortality rate (Laurance et al.,
2000), promoting clearings that favor the growth of secondary species and
NSLD (Benitez-Malvido, 1998; Hill and Curran, 2003). We found that the
mean basal area of the occupied fragments is larger than of the unoccu-
pied ones, but the difference is not significant. Moreover, considering the 10
Changes in Habitat Quality for Alouatta palliata 1091

Table V. Significant results of the stepwise multiple regression analysis

Beta valuesa
Vegetation variables R2 Log (area) Isolation Shape

Total richness 0.21∗ −0.38 n.s – 0.54∗∗

Total basal area 0.45∗∗∗ 0.62∗∗∗ −0.24 n.s –
Richness of primary species 0.28∗∗ – −0.57∗∗ 0.29 n.s
Basal area of primary species 0.53∗∗∗ 0.72∗∗∗ −0.24 n.s −0.24 n.s
Richness of NSLD species 0.27∗∗ – 0.57∗∗ –
Density of secondary species 0.22∗ −0.51∗ – 0.45∗
Richness >10–30 cm DBH species 0.26∗ −0.42∗ – 0.57∗∗
Density >10–30 cm DBH individuals 0.40∗∗ −0.56∗∗ – 0.61∗∗
Basal area >10–30 cm DBH ind 0.38∗∗ −0.48∗∗ – 0.65∗∗∗
Richness >60 cm DBH species 0.36∗∗ 0.56∗∗ −0.25 n.s –
Density >60 cm DBH ind 0.37∗∗ 0.57∗∗ −0.24 n.s –
Basal area >60 cm DBH ind 0.47∗∗∗ 0.65∗∗∗ −0.21 n.s –
Sum of Top food families‘ basal area 0.60∗∗∗∗ 0.83∗∗∗∗ – −0.40∗∗
Sum of Top food species‘ basal area 0.50∗∗∗ 0.79∗∗∗∗ – −0.31 n.s
a Beta values of the independent variables included in the multiple model.
∗ 0.1>p>0.05; ∗∗ 0.05 ≥ p>0.01; ∗∗∗ 0.01 ≥ p>0.001; ∗∗∗∗ p ≤ 0.001; (—) variable not included by
the multiple model.

species with greater IVI, the occupied fragments presented a composition

most similar to continuous forest. The results suggest that the composition
and structure of the vegetation of the occupied fragments is more similar to
the vegetation of the continuous forest than of the vegetation of the unoc-
cupied fragments, but further studies are necessary.
The lack of large trees had a particularly severe effect on the top
howler food resources at Los Tuxtlas. On the basis of the sum of the top
10 food families and top 20 food species, we found significantly lower basal
area in fragments. Moraceae, Fabaceae, Lauraceae, and Boraginaceae, and
particularly Nectandra ambigens, Poulsenia armata, Brosimum alicastrum,
Pseudolmedia oxyphyllaria, Dialium guianense, and Dussia mexicana, all
reported as important food sources for howlers living in the forest reserve
of Los Tuxtlas (Estrada, 1984), have lower density and basal area in frag-
ments. This has important implications for Alouatta palliata, as the largest
trees produce greater amounts of fruits (Chapman et al., 1992).
Our results indicate a greater abundance of secondary species in frag-
ments. While research suggests that secondary species have high concen-
trations of toxic compounds, which could jeopardize the health of howlers
on smaller fragments (Fuentes et al., 2003; Juan et al., 2000; Milton, 1980),
the species also produce large numbers of young leaves that typically have
fewer chemical defenses, are more digestible, and have higher nutrition
value for primates (Coley and Barone, 1996). Moreover, secondary species
such as Cecropia obtusifolia are important food resources for Alouatta
1092 Arroyo-Rodrı́guez and Mandujano

palliata inhabiting a continuous forest of 700 ha (Estrada, 1984). Therefore,

according to Cristobal-Azkarate et al. (2005) and Mbora and Meikle (2004),
the secondary vegetation may have a positive effect on primate survival in
fragments when fruit availability is reduced, as it offers a higher diversity
and better quality of young leaves. In addition, our results indicate a greater
abundance of Ficus spp. in fragments, suggesting that in remnant habitats,
howlers can still find vital resources (Serio-Silva et al., 2002). Nevertheless,
the lack of large trees species in fragments, particularly of the top food re-
sources for howlers, suggest that fragments offer less quality and quantity
of howler food sources.
Fragment size was the variable that best explained differences in vege-
tation composition and structure, which coincides with the findings of other
authors (Hill and Curran, 2003; Laurance et al., 2002). The largest frag-
ments had a greater abundance of large, primary trees, lower density of
small secondary species, and more basal area of species and families crucial
for howlers. Numerous botanical studies corroborate the results (Benitez-
Malvido and Martinez-Ramos, 2003; Hill and Curran, 2003; Laurance et al.,
2002). In addition, primatological research shows positive correlations be-
tween fragment size and primate abundance caused by an increase in the
carrying capacity of large fragments (Estrada and Coates-Estrada, 1996;
Medley, 1993; Wieczkowski, 2004). Thus, fragmentation, especially that
caused by a reduction in habitat amount, compromises habitat quality for
howlers.
Though to a lesser degree, fragment shape and isolation also explain
part of the variability in the vegetation attributes studied. In particular, we
found that on the most irregular fragments, there was a greater proliferation
of secondary species, with greater density and basal area of plants on the
lower stratum, as irregular shape increases edge effects (Benitez-Malvido,
1998; Saunders et al., 1991). More isolated fragments, in contrast, had lower
richness and basal area of primary species, with less richness, density, and
basal area of plants on the upper stratum. Isolation may be modifying the
dispersal and predation of the seeds produced by many primary species, as
the species commonly have larger fruits that herbivores detect more easily
(J. Benitez-Malvido, personal communication). In consequence, along with
the selective felling already practiced at the site (Silva-Lopez and Portilla-
Ochoa, 2002), the factors may explain changes in forest composition and
structure. Experimental research is needed to clarify the mechanisms be-
hind the decrease in habitat quality.
How might the reduction in habitat quality affect the viability of howler
populations in the long run? A decline in the quality and quantity of food
sources may reduce fragment carrying capacity. For the same landscape,
Rodriguez-Toledo et al. (2003) noted that the percentage of fragments
Changes in Habitat Quality for Alouatta palliata 1093

howlers occupy is negatively related to fragment size. In particular, when

fragments have an area of <10 ha and an isolation distance of >200 m, oc-
cupation drops to <10% of total fragments (Mandujano et al., 2006). Our
results suggest that for howlers, habitat quality is strongly linked to frag-
ment size, in which case size and isolation thresholds would be influenced
by habitat quality loss on the smallest and most isolated fragments. How-
ever, Bicca-Marques (2003) documented that Alouatta palliata have high
plasticity in terms of adapting to altered conditions (Bicca-Marques, 2003),
as it is very flexible in its food selection (Milton, 1980), even feeding on sec-
ondary and introduced plants (Fuentes et al., 2003; Rodriguez-Luna et al.,
2003). Further, its growth rate permits a relatively swift response to condi-
tions that fragmentation creates (Clarke et al., 2002; Crockett, 1998).
In conclusion, though in fragments we still found several of the plant
species and families described as heavily used by howler monkeys in the
region, the most important primary species in the diet were less abundant
and smaller. However, no in-depth research has addressed the question of
whether or not the selection of alternative food satisfies its needs, and if
there is long-term impact on female fecundity and the survival of infants and
juveniles. Though in the short run howlers appear to respond adequately to
the conditions that arise from fragmentation, in the long run population vi-
ability is not ensured in small fragments (Bicca-Marques, 2003; Escobedo-
Morales, 2005). Future research incorporating habitat quality into popula-
tion viability analysis will allow us to determine how sensitive howler mon-
key populations are to such changes.

ACKNOWLEDGMENTS

We thank Mateo-Gutierrez’s family for their hospitality and invaluable

help. We also thank F. Garcia-Orduña and D. Canales of the University
of Veracruz’ Institute of Neuroethology. The comments and suggestions
of J. Benitez-Malvido, G. Castillo-Campos, and D. Piñero helped improve
the article. We also thank R. Palacios-Silva, A. Gonzalez-Zamora, L. A.
Escobedo-Morales, and J. Cristóbal-Azkarate. The Institute of Ecology’s
Department of Biodiversity and Animal Ecology provided the support nec-
essary for the completion of the research.

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