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Biogeographical and floristic predictors of the presence and abundance of mantled howlers (Alouatta palliata mexicana) in rainforest fragments at Los Tuxtlas Mexico.

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American Journal of Primatology 67:209–222 (2005)
RESEARCH ARTICLE
Biogeographical and Floristic Predictors of the
Presence and Abundance of Mantled Howlers
(Alouatta palliata mexicana) in Rainforest Fragments
at Los Tuxtlas, Mexico
JURGI CRISTÓBAL-AZKARATE1*, JOAQUIM J. VEÀ1, NORBERTO ASENSIO1, and
ERNESTO RODRÍGUEZ-LUNA2
1
Primats, Centre Especial de Recerca en Primats, Universitat de Barcelona, Barcelona,
Spain
2
Parque de la Flora y Fauna Silvestre Tropical, Instituto de Neuroetologı´a,
Universidad Veracruzana, Veracruz, México
This research focuses on identifying the principal habitat characteristics
that influence the presence and abundance of mantled howlers in forest
fragments. We provide information on the demography of several
fragmented Alouatta palliata mexicana subpopulations at Los Tuxtlas,
Mexico, and relate this to the biogeographical and floristic characteristics
of the forest fragments inhabited. The most important habitat characteristics related to the presence and abundance of howlers in the
fragments were fragment size and floristic diversity. On the other hand,
some evidence suggests that given the conditions under which howlers in
our study area live (i.e., small and degraded fragments with high
densities), secondary vegetation may be beneficial for the survival of the
howlers. Finally, we discuss the possibility that the very low immature-tofemale ratio (IFR) in the groups, and the lack of juveniles found in many
of the study groups may be due to high mortality rates in immatures. A
reduction in food availability because of the high population densities of
these groups may be responsible for this process. Am. J. Primatol.
67:209–222, 2005.
r 2005 Wiley-Liss, Inc.
Key words: Alouatta palliata; demographics; biogeographic characteristics; floristic characteristics; immature-to-female ratio;
Los Tuxtlas
Contract grant sponsor: Zientzi Politikarako Zuzendaritza, Basque Government; Contract grant
sponsor: Ministerio de Ciencia y Tecnologı́a, Spain; Contract grant numbers: PB98-127; BS0200203340.
*Correspondence to: Jurgi Cristóbal-Azkarate, Apartado Postal 199, C.P. 91001, Xalapa, Veracruz,
México. E-mail: jurgi@infomail.lacaixa.es
Received 31 May 2004; revised 12 February 2005; revision accepted 10 March 2005
DOI 10.1002/ajp.20178
Published online in Wiley InterScience (www.interscience.wiley.com).
r
2005 Wiley-Liss, Inc.
210 / Cristóbal-Azkarate et al.
INTRODUCTION
The Mexican mantled howler (Alouatta palliata mexicana), whose original
distribution was from southeast Mexico (excluding the Yucatan Peninsula) to
southern Guatemala, is at present restricted throughout this range to several
isolated reserves and nonprotected areas, all of which are greatly fragmented
[Rodrı́guez-Luna et al., 1996]. Hunting and the extensive deforestation of this
region during the last 60 years [Collins, 1990; FAO, 2003] are responsible for the
decline and isolation of A. p. mexicana populations [Rodrı́guez-Luna et al., 1996],
and this subspecies is now classified as critically endangered [Cuarón et al., 2003].
Although the literature pertaining to the mantled howlers’ capacity to live in
fragments is relatively abundant [Bicca-Marques, 2003; Clarke et al., 2002; Juan
et al., 2000; Lovejoy et al., 1986; Schwarzkoft & Rylands, 1989], only a few studies
have focused on the habitat characteristics (floristic and biogeographic) related to
the presence and demography of A. palliata in a fragmented landscape, and
contradictory results have been reported [DeGama-Blanchet & Fedigan, in press;
Estrada & Coates-Estrada, 1996; Rodrı́guez-Toledo et al., 2003; Sorensen &
Fedigan, 2000]. Such information is necessary for us to better understand how
howler monkeys respond to habitat fragmentation, and to formulate effective
management plans for the conservation of this species.
According to the island biogeographical theory (IBT) [McArthur & Wilson,
1967], the number of species and individuals will diminish with the reduction of
the area, and the degree of isolation of the fragments. Estrada and Coates-Estrada
[1996] found that the number of individuals of A. palliata inhabiting forest
fragments in one area of the Los Tuxtlas region in Mexico was positively related
to fragment size, and negatively to the isolation distance of the forest fragments.
In contrast, Rodrı́guez-Toledo et al. [2003] did not find any relationship between
fragment size and number of individuals in the fragments in another area in the
southern part of the same region. Furthermore, in a study in Costa Rica,
DeGama-Blanchet and Fedigan [in press] found no relationship among forest
fragment size, degree of isolation, and mantled howler density, which suggests
that the large size of forest fragments in the study area (up to 95 km2) were
responsible for the lack of relationship between the variables. Finally, in Costa
Rica, Clarke et al. [2002] observed that the construction of a canal that
fragmented and reduced the habitat did not reduce the population size of A.
palliata, although there was a reduction in group size.
In general, the transformation of the original vegetation resulting from forest
fragmentation has a negative impact on the number of mantled howlers. In a
certain area of the Los Tuxtlas region, Estrada and Coates-Estrada [1996] found
a positive relationship between floristic diversity and the number of howlers in
fragments, and associated the higher species diversity with large and undisturbed
fragments. In another area of the same region, Rodrı́guez-Toledo et al. [2003]
found larger group sizes in undisturbed fragments. In Costa Rica, Sorensen and
Fedigan [2000] and DeGama-Blanchet and Fedigan [in press] found higher
densities of A. palliata in older tropical dry forest than in younger regenerating
forests.
To enhance our understanding of how mantled howler monkeys respond to
habitat fragmentation, we provide information in this paper on the demography
of several fragmented A. p. mexicana subpopulations in the region of Los Tuxtlas,
Mexico, and relate this to the biogeographical and floristic characteristics of the
inhabited fragments. In addition, we discuss which habitat variables are most
likely related to the presence and size of howler populations in the fragments.
Howler Demography in Rainforest Fragment / 211
Finally, we analyze the demographic trends of these populations and discuss the
possible causes of these trends.
MATERIALS AND METHODS
Study Site
The study area (2,064,129 m, 2,049,182 m north and 272,772 m, 285,783 m
east, zone 15, Universal Transform Mercator; elevation 0–400 m above sea level)
is located in the northern part of the Los Tuxtlas Biosphere Reserve in southern
Veracruz, Mexico. The vegetation type is known as high evergreen rainforest
[Gómez-Pompa, 1973] with different degrees of transformation.
The original habitat of this region, as well as many others in Central and
South America, has been extensively transformed into pasture and agricultural
landscapes [Dirzo & Garcı́a, 1992]. In our study area only 13% of the original
75,000 ha of rainforest remains today in fragments of different sizes. For a
further description of the area, see Estrada and Coates-Estrada [1996].
Data Collection
Census of howlers.
We censused howlers from March to September 2000, and from March to
December 2001, in forest fragments surrounding the San Martı́n Tuxtla Volcano
in the northeastern portion of the Los Tuxtlas Biosphere Reserve. The censusing
party consisted of Cristóbal-Azkarate and one trained assistant. Our census
method involved the observers positioning themselves for several days (depending
on the size of the fragment) in strategic spots (inside or outside the fragments)
before sunrise, waiting for the monkeys to howl. This allowed us to determine the
number and location of the groups in the fragments. In addition, we interviewed
the local people who lived and worked in the proximity of the forest fragments
about the presence or absence of howlers in the fragments. If after several days no
howlers were heard in a fragment, and the local people reported that the
fragment was not occupied by howlers, it was considered empty. The fragments
were revisited on a opportunistic basis several times during the study period to
confirm howler occupancy.
Once we located the howlers, we recorded the number of adult males, adult
females, juveniles, and infants following Carpenter’s [1965] age classification, and
revisited the group if doubt existed after the first day. To avoid data repetition by
censusing the same individuals more than once, we identified group members by
drawing the distinguishing color patterns on their feet and tails that are
characteristic of this subspecies, and noting any other distinctive features.
Since there is evidence that howlers in Los Tuxtlas may sometimes disperse
between fragments [Estrada & Coates-Estrada, 1996], we considered the sum of
all individuals living in a fragment as a subpopulation. We calculated several
demographic indexes (Table I). The subpopulation size, population density, and
number of groups were calculated for each subpopulation. The group size, sex
ratio, juvenile-to-female ratio (JFR), infant-to-female ratio (IFFR), and immature-to-female ratio (IFR) were calculated for each group, and the mean values
were calculated for each subpopulation.
Biogeography of the forest fragments.
We calculated the fragment size, the shortest distance to the nearest human
settlement, and two isolation variables, the shortest distance to the nearest
212 / Cristóbal-Azkarate et al.
TABLE I. Calculated Variables
Demographic indexes
Subopulation size: no. of individuals in each fragmenta
Population density: no. of individuals per hectarea
Number of groups: no. groups in the fragmenta
Group size: no. individuals per groupb
IFR: no. immatures (juveniles + infants) to no. adult female ratiob
JRF: no. juveniles to no. adult female ratiob
IFFR: no. infants to no. adult female ratiob
Sex ratio: no. adult females to no. adult male ratiob
Biogeographical variables
Fragment size: (ha)
SN: shortest distance to the nearest fragment (m)
SNM: shortest distance to the nearest fragment with monkeys (m)
DH: distance to the nearest human settlement (m)
Floristic variables
Tree species or family diversity: total no. of tree species or families
Relative tree species or families diversity: no. of tree species or families to total no. of trees
ratio
Shannon index: average degree of uncertainty-complexity (N–4)
Mean DBH: mean diameter at breast high (cm)
Tree density: no. of trees per hectare; S5: the sum of the importance values of the five most
consumed taxa by howler monkey at Los Tuxtlas according to Estrada [1984] (0–300).
a
b
These variables are calculated for each fragmented population.
These variables are calculated for each group.
fragment (SN) and the shortest distance to the nearest fragment with monkeys
(SNM) (Table I) by analyzing 1999 aerial photographs of the study area (1:20,000
scale) with ArcView GIS software (version 3.1) and the Patch Analyst 2.2
extension [Rempel & Elkie, 1999].
The analysis of aerial photographs from previous years demonstrated that by
1976 the deforestation in our study area was extensive, but that the actual
fragmentation of the forest took place between 1976 and 1986. Considering that
all forest fragments studied were approximately the same age, this variable was
not considered in the analysis.
Census of the vegetation.
For each fragment we censused a total area of 1,000 m2, distributed in 10
randomly located 50 2 m transects [Keel et al., 1993]. We registered all trees
with a diameter at breast height (DBH) Z10 cm, noting the species, family, DBH,
and position in the transect. We calculated several diversity indexes and floristic
variables (Table I).
One of the indexes we calculated to assess the floristic diversity of the forest
fragments was the Shannon index. This index is used by ecologists to describe the
average degree of uncertainty of predicting the species of an individual picked at
random from the community. The uncertainty of occurrence increases both as the
number of species increases and as the individuals are distributed more evenly
among the species already present. The values ranged from 0 (indicating low
community complexity) on up. The Shannon index was calculated with the use of
a base e logarithm.
Howler Demography in Rainforest Fragment / 213
According to Estrada [1984], five taxa (Ficus spp., Nectandra ambigens,
Poulsenia armata, Brosimum alicastrum, and Cecropia obtusifolia) account
for 80% of the total feeding time of one troop of A. palliata living in continuous
forest at Los Tuxtlas. The importance value refers to the relative contribution
of a plant species to the entire community, as it incorporates into a single measure
the relative density, the relative frequency, and the basal area of each
species. Therefore, the sum of the importance values of the five most consumed
taxa by howler monkeys at Los Tuxtlas (S5) is an approximation of the
availability of preferred food species in the fragment, and its value ranges
between 0 and 300.
Data Analysis
Statistics.
We used six different statistical techniques for this study: 1) the
Mann-Whitney U-test to determine which variables were related to the presence
or absence of howler populations in the fragments; 2) a series of discriminant
analyses to determine which group of variables would better predict the
presence or absence of howler populations in a fragment; 3) stepwise multiple
regressions to determine which group of variables would better predict the
abundance of howlers in the fragments; 4) the Spearman-R correlation coefficient
and 5) simple regressions to determine the relationship between the floristic,
biogeographic, and demographic variables; and 6) Student’s t-test to determine
whether the demographic characteristics of our study population were statistically different from those reported by Estrada and Coates-Estrada [1996]
for another location in Los Tuxtlas, and those reported by Chapman and Balcomb
[1998] for this species. The accepted significance level for all of the analyses
was r.05.
RESULTS
Variables Related to the Presence of Howler Populations
We identified 55 forest fragments within our study area (7,500 ha). Of these
fragments, 21 were inhabited by at least one group of howlers (i.e., more than one
male or one female), and 15 were censused intensively (Table II). Two small
fragments were temporarily occupied by transient solitary males, but were
considered ‘‘empty’’ for the analysis. We studied the biogeography of all 55
fragments and the floristic characteristics of 31 fragments (18 occupied by
howlers (15 censused intensively) and 13 empty).
The mean size of the inhabited fragments was significantly larger than that
of the empty fragments (Table III), but we did not find any significant
relationship between the degree of isolation (SN and SNM) and the presence or
absence of howlers in the fragments.
We did not find any significant relationship between the presence or absence
of howler populations in the fragments and their proximity to human settlement.
Compared with the empty forest fragments, the inhabited fragments
exhibited a higher tree species and family diversity, Shannon index, and tree
density (Table III). These four variables are strongly correlated with each other
(Table IV).
The group of variables that best predicted the presence or absence of howler
populations in a fragment were the fragment size and Shannon index, with a
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
Fragment
5
10
9
5
1
3
1
1
2
1
1
1
1
1
1
No.
groups
5.4
10.5
6.44
8.4
12
4.3
5
4
7
6
2
5
6
3
3
Mean
group
size
0.12
0.71
0.58
0.67
1.66
2.46
0.54
0.55
0.43
0.34
0.29
1.38
2.85
4.35
3.07
Population
density
29
108
63
43
12
13
5
4
14
6
2
5
6
3
3
No.
individuals
15
32
27
17
4
3
2
2
5
2
1
2
1
1
1
No.
males
10
48
24
18
7
9
2
2
6
2
1
3
4
1
1
No.
females
TABLE II. Demographic Characteristics of the Censused Howler Populations
1
15
5
2
0
0
0
0
3
2
0
0
0
0
0
No.
juveniles
3
13
7
6
1
1
1
0
0
0
0
0
1
1
1
No.
infants
4
28
12
8
1
1
1
0
3
2
0
0
1
1
1
No.
immatures
0.67
1.50
0.89
1.06
1.75
3.00
1.00
1.00
1.20
1.00
1.00
1.50
4.00
1.00
1.00
Sex
ratio
0.10
0.31
0.21
0.11
0
0
0
0
0.50
1.00
0
0
0
0
0
JFR
0.30
0.27
0.29
0.33
0.14
0.11
0.50
0
0
0
0
0
0.25
1.00
1.00
IFFR
0.40
0.58
0.50
0.44
0.14
0.11
0.50
0
0.50
1.00
0
0
0.25
1.00
1.00
IFR
214 / Cristóbal-Azkarate et al.
Howler Demography in Rainforest Fragment / 215
TABLE III. Comparison Between the Habitat Characteristic of the Fragments Inhabited and
Not inhabited by Howler Monkeys (Mann-Whitney U test)
Inhabited
Mean
SD
Fragment size
38.57 61.14
Tree species diversity 36.26 13.24
Shannon index
3.25
0.22
Tree density
632.51 223.66
Tree family diversity
22.95
5.07
Not inhabited
Valid n Mean
21
19
19
19
19
SD
Valid n
U
Z
P
34
13
13
13
13
152.00
59.00
69.50
62.50
52.00
3.55
2.48
2.07
2.34
2.76
0.000
0.013
0.038
0.019
0.006
5.63 9.65
26
8.09
2.9
0.57
454.61 93.69
17.46 4.37
TABLE IV. Relationship Between Vegetation Variables
Tree species
diversity
Tree species diversity
Shannon index
Tree density
Tree families diversity
Shannon index
Tree density
Tree families
diversity
rs
p
rs
p
rs
p
rs
p
–
0.95
0.72
0.87
–
0.00
0.00
0.00
0.95
–
0.62
0.83
0.00
–
0.00
0.00
0.72
0.62
–
0.57
0.00
0.00
–
0.00
0.87
0.83
0.57
–
0.00
0.00
0.00
–
predictive value of 75% of the expected over the observed cases (l = 0.71,
F (2, 29), Po0.025).
Demographic Characteristics of the Fragmented Populations and
Related Biogeographical and Floristic Variables
We censused 316 howlers (104 resident adult males, 11 adult solitary males,
138 resident adult females, 28 juveniles, and 35 infants) in 43 groups living in 15
different forest fragments. The mean subpopulation size was 21.06 individuals
(SD = 29.68, range = 2–108, n = 15), the mean number of groups in a fragment
was 2.86 (SD = 3.04, range=1–10, n = 15), the mean group size was 7.09
(SD = 4.22, range = 2–18, n = 43), and the mean sex ratio was 1.47 (SD = 1.1,
range = 0.5–6, n = 43). The mean IFR was 0.45 (SD = 0.43, range = 0–2, n = 43),
the mean JFR was 0.18 (SD = 0.30, range = 0–1, n = 43), and the mean IFFR was
0.32 (SD = 0.41, range = 0–2, n = 43). Juveniles were present in only 40% of the
populations and 34.8% of the groups, while 66.6% of the populations and 55.8% of
the groups had infants.
Population density correlated in a negative and significant manner
with fragment size (rs = –0.69, P = 0.004, n = 15), and nonsignificantly with
population size. None of the populations with a density higher than 0.71 had
juveniles.
Fragment size (R2 = 0.45, P = 0.006, n = 15) and tree density (R2 = 0.27,
P = 0.045, n = 15) were significantly related to the number of howlers in the
fragments, but the best set of habitat variables that explained the number of
216 / Cristóbal-Azkarate et al.
howlers per fragment was the fragment size and the Shannon diversity index
(r2 = 0.675, P = 0.001, n = 15).
DISCUSSION
Comparison With Previous Studies at Los Tuxtlas
In a previous study, Estrada and Coates-Estrada [1996] conducted a broad
census of howler populations in 126 forest fragments in a different portion of Los
Tuxtlas Biosphere Reserve. Our study area was located at the northern part of
the reserve, and replicated only three of the fragments censused by the authors
(Coates, personal communication). Compared to the results of our study,
Estrada and Coates-Estrada [1996] found much lower howler population densities
(Table V) and population sizes (r15 individuals). It is interesting to note that
32% of their fragments were larger than 100 ha. Several factors may be related to
these differences, as discussed below.
The abundance of howlers is not uniform throughout the Los Tuxtlas
Biosphere Reserve, as shown by the small population densities and population
sizes observed in the southern part of the Reserve by Rodrı́guez-Toledo et al.
[2003]. On the other hand, since the area was decreed a Biosphere Reserve in
1998, hunting and illegal trafficking of howlers has practically disappeared. This
is consistent with our data demonstrating no relationship between the presence
and abundance of howlers in the fragments and their proximity to human
settlements. Interspecific competition could also account for these differences,
since in contrast to some of the fragments studied by Estrada and Coates-Estrada
[1996], none of the howler populations censused by us shared their habitat with
spider monkeys (Ateles geoffroyi). Finally, the differences between their study and
ours could be due to the different censusing techniques used in each case.
Whereas Estrada and Coates-Estrada [1996] censused howlers by walking
TABLE V. Comparison of the Demographic Characteristics of the Howler Populations
Censused at Our Study area with the Data Presented for the Species by Estrada & CoatesEstrada [1996] at Los Tuxtlas, and Chapman & Balcomb [1998] at Different Sites
Mean
Population density (ind./ha)
Our study at Los Tuxtlas
Estrada & Coates-Estrada [1996]
Chapman & Balcomb [1998]a
Group size
Our study at Los Tuxtlas
Estrada & Coates-Estrada [1996]
Chapman & Balcomb [1998]
Group immatures/female
Our study at Los Tuxtlas
Estrada & Coates-Estrada [1996]
Chapman & Balcomb [1998]
Group sex ratio
Our study at Los Tuxtlas
Estrada & Coates-Estrada [1996]
Chapman & Balcomb [1998]
a
at Los Tuxtlas
SD
n Student t
1.33 1.28 15
0.067 0.11 60
0.52
.309 18
P
d.f.
7.7
2.54
0.000
0.000
73
51
at Los Tuxtlas
7.09
7.03
14.62
4.22
3.34
4.51
43
60
39
0.08
7.81
0.9
101
0.000 80
at Los Tuxtlas
0.45
0.53
1.25
0.43
0.36
0.75
43
60
38
0.99
7.4
0.32 101
0.000 79
at Los Tuxtlas
1.47
1.85
2.34
1.11
0.74
0.63
43
60
38
209
4.22
0.039 101
0.000 79
Not considering Baldwin & Baldwin [1976].
Howler Demography in Rainforest Fragment / 217
through the fragments (40–2,500 m), we located the groups by their morning
howls and spent several days in each fragment, which enabled us to detect more
troops. This could explain why they did not detect more than one group per
fragment. The mean group size and IFR of the groups do not differ significantly
between the two studies; however, the mean sex ratio of the groups was larger in
Estrada and Coates-Estrada’s [1996] study (Table V).
Variables Associated With the Presence and Abundance of Howlers in
the Forest Fragments
Biogeographical variables.
Our results partially support the island biogeographical theory (IBT)
[McArthur & Wilson, 1967]. We found a strong positive relationship between
fragment size and the presence and abundance of howlers in the fragments, but
no significant relationship was observed regarding the degree of isolation. This
lack of relationship may be due to the general small degree of isolation found in
the fragments in our study area (50% of the fragments are less than 100 m apart).
Estrada and Coates-Estrada [1996] observed howlers traveling distances of up to
200 m on the ground, although they emphasized that this behavior is very
infrequent. Therefore, the short distances between fragments in our study area
may facilitate the occasional movement of individuals, and may diminish the
effects of isolation over howler populations.
Floristic characteristics.
Fragments that were occupied by howlers presented higher floristic diversity
(i.e., total number of tree species and families, and Shannon index) compared to
the empty fragments. Of these different floristic variables, the Shannon index in
conjunction with fragment size was the variable that best predicted the presence
and abundance of howlers in the fragments.
Howlers prefer seasonal foods (young leaves, fruits, and flowers) to perennial
foods [Juan et al., 2000; Milton, 1980; Rodrı́guez-Luna et al., 2003], since such
foods are generally of a higher nutritional quality [Milton, 1980]. To meet their
nutritional requirements, howlers feed from many different species. Most of these
different species are used as leaf sources, both overall and daily. According to
Milton [1980], the pressure to diversify leaf sources is higher because young
leaves have a lower content of ready energy and are usually less concentrated
than fruit sources. Furthermore, leaf species may also be diversified to avoid an
overload of toxic compounds, since leaves have a higher content of toxins.
Therefore, the presence of high floristic diversity may allow howlers to obtain an
optimal daily mix of food items (especially leaves) to fulfill their nutritional
requirements and avoid toxic secondary compounds.
Estrada and Coates-Estrada [1996] also reported a positive relationship
between floristic diversity and the number of howlers in the fragments, and
related high species diversity to large and undisturbed forest fragments. Different
studies support the idea that mature or undisturbed forests are better for howler
monkeys [DeGamma-Blanchet & Fedigan, in press; Estrada & Coates-Estrada,
1996; Rodrı́guez-Toledo et al., 2003; Sorensen & Fedigan, 2000]. Nevertheless,
this association was not clear in our study, since we found that high tree density
(a characteristic of secondary or pioneer vegetation [Bongers et al., 1988]) was
positively associated with the presence and abundance of howlers in the
fragments, and the floristic diversity of the forest fragments.
218 / Cristóbal-Azkarate et al.
In a previous study of howlers at Los Tuxtlas [Juan et al., 2000], their
residence in small forest fragments was related to a more folivorous diet,
presumably because of a reduction in fruit availability. Considering the
socioecological situation in which many of our study groups live (i.e., small
fragments (50% o10 ha) with small trees (mean DBH o30 cm in 75% of the
fragments, and never Z40 cm), and high population densities (Table V)), we
believe that leaves may comprise an important part of their diet. If this is the case,
the presence of secondary vegetation in the fragments may be beneficial for
howlers, for the following reasons: First, in comparison with mature forest,
secondary vegetation is characterized by a relatively higher and less seasonal
production of high-quality leaves (i.e., lower levels of chemical defenses and fiber,
and higher values of protein, digestible nutrients, and energy) [Chiarello, 2003;
Lovejoy et al., 1986]. Additionally, the pressures on howlers to diversify their food
species are stronger when they consume leaves than when they consume fruit
[Milton, 1980], and secondary vegetation appears to be positively related to
floristic diversity. Therefore, secondary vegetation may have a positive effect on
howler survival in fragments when fruit availability is reduced, as it offers a
higher diversity and better quality of young leaves. We believe this is a very
interesting possibility that deserves more attention, as it may change the way we
judge the conservation potential that these increasingly abundant transformed
habitats have for howler populations. Nevertheless, we consider that further
studies are necessary, especially studies that will focus on the feeding habits of
howlers in varying degrees of habitat transformation.
Finally, other factors that may be associated with the presence
and abundance of howlers in the fragments include poaching, which was
practiced in the past [Estrada & Coates-Estrada, 1996], and the sampling effect,
which means that the inclusion or exclusion of a group of howlers in a fragment at
the time of isolation may be entirely due to chance, and independent of the
suitability of the habitat [Rodrı́guez-Toledo et al., 2003; Schwarzkoft & Rylands,
1989].
Population Trends and Possible Causes
The mean IFR in the study groups was very low (0.45, which is less than half
the value reported for the species by Chapman and Balcomb [1998] (Table V); only
one group exhibited a higher value). It is noteworthy that there is no consensus on
the aging criteria across studies. In fact, Chapman and Balcomb’s [1998] estimate
for the species IFR was based on studies that used different aging criteria. For this
study we used Carpenter’s [1965] aging criteria, which is the most conservative
because it considers individuals of up to 50 months of age as immatures. In
contrast, Milton [1982] and Heltne et al. [1975] considered individuals no older
than 28 and 36 months, respectively, to be immatures. Therefore, the aging
criteria used in this study tend to increase the IFR compared to other studies,
which stresses the low value observed in our study groups.
The IFR has been used as a measure of a stable, decreasing, or increasing
population [Clarke et al., 2002; Heltne et al., 1975; Zucker & Clarke, 2003].
Zucker and Clarke [2003] argued that group size constrains this variable, and
that groups tend to show a cyclical pattern of increases and decreases in IFR.
Therefore, the determination of the IFR from a single measurement could present
an inaccurate view of the overall population dynamics. Nonetheless, 13 of our
study groups (79%) in forest fragments exhibited below-average IFR values for
the species [Chapman & Balcomb, 1998], which suggests that these low values
Howler Demography in Rainforest Fragment / 219
may be due to the general process of demographic decline rather than a cyclical
pattern of change.
Different factors working independently or in synchrony, such as a high and
early immature emigration rate, a reduced birth rate, and a high immature mortality
rate, could be responsible for the low IFR found in our study populations.
A. palliata is characterized by bisexual emigration of juveniles. Males and
females typically emigrate at ~22 months and ~33 months of age, respectively
[Glander, 1992], although this may occur much earlier (males at 1 year of age, and
females at 2 years of age) [Clarke, 1990]. After they analyzed scars and
mutilations, Cristóbal-Azkarate et al. [2004] suggested that the migration
patterns of howlers may be depressed in the Los Tuxtlas fragmented landscape.
Supporting this hypothesis, our current study did not find any solitary females,
and all 11 solitary males observed were adult individuals. On the other hand, the
sex ratios of our study groups are very low (Table V), which is consistent with
reduced rates of male emigration. These findings suggest that both females and
males may be abandoning their natal groups later and at lower rates than in other
localities, indicating that the low IFR value observed in our study groups is not
principally due to high emigration rates.
Milton [1982] interpreted a high number of infants and a low number of
juveniles in the groups in Panama (BCI) as an indication of high mortality rates in
immatures, and not as a reproductive problem. In our study area, 55.9% of the
groups and 66.6% of the fragments had at least one infant, whereas only 34.8% of
the groups and 40% of the fragments had juveniles. On the other hand, the mean
IFFR of the study groups was 0.32, while the mean JFR was 0.18. Therefore,
considering that juvenile emigration may be reduced, we believe that the high
immature mortality rates may be the principal cause of the low IFR and JFR
values, as well as the reduced number of juveniles that we observed in our study
groups. Nevertheless, we cannot dismiss a reduction in female reproductive rates
as a possible cause of these reduced values.
Infanticide by immigrating males or subordinate males attempting to ‘‘take
over’’ from within the group is another possible cause of infant mortality [Clarke,
1983; Clarke et al., 1994]. However, although many studies of howlers at Los Tuxtlas
have been conducted, this behavior has never been reported, and there have been no
reports immatures showing signs of aggression. Therefore, we consider the possible
effects of infanticide on the demography of these populations to be negligible.
The regulatory effect that predators may have on the howler monkey
populations at Los Tuxtlas is not known, but presumably their numbers are small
in this area [Cristóbal-Azkarate et al., 2004]. Therefore, once again, we consider
this effect on the demography of howler monkeys at Los Tuxtlas to be negligible.
The population densities of our study fragments were very high–more
than twice the value reported for this species by Chapman and Balcomb [1998]
(Table V). It is noteworthy that these high densities were significantly related to
fragment size but not to the number of howlers. High population densities have
been related to a reduction in food availability [Fowler, 1987], which has been
argued to be one of the most important factors regulating howler population size
[Milton, 1982; Otis et al., 1981]. The reduction in food availability has been
associated with a reduction in group size [Chapman, 1989; Gaulin et al., 1980]
(Table V) and an increase in immature mortality [Fowler, 1987], which could
explain the small size and the very low IFR of the howler groups in our study area
(Table V). In our fragmented subpopulation’s density distribution there is a gap
between 0.71 and 1.37 ind./ha, and none of the groups that inhabited fragments
with a population density equal to or larger than 0.71 included juveniles. These
220 / Cristóbal-Azkarate et al.
results may suggest that surpassing a population density between these two
values is reflected as an increase in immature mortality, which is most likely
associated with a reduction in food availability. Finally, other causes of immature
mortality, such as disease, cannot be dismissed.
Finally, to reverse and avoid this process of population decline, we believe it
is essential to first of all protect the remaining forest fragments from the lowintensity logging that still occurs in the region despite the creation of the
Biosphere Reserve. Second, it is urgent to increase the amount of available
habitat for howlers, especially by connecting forest fragments (both empty and
inhabited). This could best be achieved by protecting and reforesting the
vegetation along the many streams that cross the landscape in different
fragments. These measures, in addition to increasing the amount of available
habitat, would break the isolation and facilitate the dispersal of individuals and
the genetic flux.
CONCLUSIONS
Fragment size and floristic diversity are the most important habitat
characteristics associated with the presence and abundance of howlers in our
study area.
The relationship between habitat disturbance and howler demographics in
our study area is not clear, but the evidence suggests that given the conditions
under which the howlers in our study area live (i.e., small and degraded
fragments with high population densities), secondary vegetation may play an
important role in howler survival.
The fragmented populations of howlers in our study may be in the process
of a demographic decline. We believe the reason for this crisis may be an increase
in immature mortality due to reduced food availability resulting from high
population densities.
To reverse this demographic trend, we believe it is imperative to protect the
remaining forest fragments and increase the amount of available forest for the
howlers by connecting the forest fragments.
ACKNOWLEDGMENTS
Jurgi Cristóbal Azkarate and Norberto Asensio were supported by a grant
from the Zientzi Politikarako Zuzendaritza of the Basque Government. We thank
Una Laffan for helping with the translation; Pulga, Lur, Hiru, Manolo, and Amets
for their constant company and support; and R. Coates and two anonymous
reviewers for their helpful comments and corrections regarding the manuscript.
Finally, we thank Domingo Canales Espinosa, director of the Instituto de
Neuroetologı́a, University of Veracruz, México, for his support.
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