BIOTROPICA 38(1): 57–63 2006
10.1111/j.1744-7429.2006.00100.x
Comparative Seed Dispersal Effectiveness of Sympatric Alouatta guariba
and Brachyteles arachnoides in Southeastern Brazil1
Milene Moura Martins2
Dept. de Zoologia, Instituto de Biociências, Universidade de São Paulo (USP), Cx. P. 11461, CEP 05422-970, São Paulo, Brazil
ABSTRACT
I compared the effectiveness of sympatric brown howlers (Alouatta guariba) and muriquis (Brachyteles arachnoides) as seed dispersers in terms of quantitative and
qualitative attributes. I hypothesized that differences in feeding and behavioral patterns between these large-bodied folivorous/frugivorous primates would lead to
dissimilarities in their effectiveness as endozoochoric seed dispersal agents. The study was carried out in a semideciduous forest fragment of Fazenda Barreiro Rico,
southeastern Brazil. Through behavioral sampling of frugivory and defecation events as well as analyses of fecal samples, I determined that A. guariba dispersed fewer
species and produced a lower proportion of dung with intact seeds than B. arachnoides. There was no difference between the number of seeds in fecal samples of A.
guariba and B. arachnoides. These primates affected to a similar degree both germination percentage and latency to germination of seeds they ingested or removed the
pulp from. Howlers and muriquis were also similar in carrying seeds away from the parent trees. Contrary to muriquis, howlers defecated seeds under the canopy of
conspecific lianas, where seeds are expected to suffer high mortality rates, and voided seeds predominantly in a clumped pattern. B. arachnoides was a more effective
seed disperser when compared to A. guariba in some attributes evaluated, but not in others. Given the interspecific variation in recruitment patterns of tropical plants
and the loss of frugivorous bird species at the study site, the differences between howlers and muriquis in their abilities as seed dispersers may crucially influence the
composition and maintenance of seedling diversity.
RESUMO
A eficácia de bugios ruivos (Alouatta guariba) e muriquis (Brachyteles arachnoides) como dispersores de sementes foi comparada através de atributos quantitativos e
qualitativos. A hipótese testada foi de que diferenças nos padrões alimentares e comportamentais destes primatas de hábito folı́voro/frugı́voro conduz a divergências
na eficicácia da dispersão endozoocórica de sementes. O estudo foi conduzido em um fragmento de floresta semidecı́dua da Fazenda Barreiro Rico, no sudeste do
Brasil. Através da amostragem de eventos de frugivoria e defecação, assim como da análise de amostras fecais, determinei que A. guariba dispersou um número menor
de espécies e produziu uma proporção menor de amostras fecais com sementes intactas do que B. arachnoides. Não houve diferença entre o número de sementes em
amostras fecais de A. guariba e B. arachnoides. Estes primatas afetararam em grau semelhante a porcentagem de germinação e a latência de germinação das sementes
que ingeriram ou das quais removeram a polpa. Bugios e muriquis também foram semelhantes no transporte de sementes à partir da árvore-mãe. Ao contrário dos
muriquis, os bugios defecaram sementes sob a copa de lianas co-especı́ficas, onde altas taxas de mortalidade de sementes são esperadas, e depositaram sementes de
forma predominantemente agregada. Brachyteles arachnoides foi um dispersor de sementes mais eficaz do que A. guariba em alguns dos atributos avaliados, mas não
em outros. Em função da variação interespecı́fica nos padrões de recrutamento de plantas tropicais e da perda de espécies da avifauna frugı́vora na área de estudo,
as diferenças na habilidade de bugios e muriquis quanto à dispersão de sementes podem influenciar de forma crucial a composição e manutenção da diversidade de
plântulas.
Key words: Alouatta guariba; Brachyteles arachnoides; seed dispersal effectiveness; semideciduous forest; southeastern Brazil.
FRUIT EATERS ARE EFFECTIVE AS SEED DISPERSERS whenever their
foraging behavior contributes to the reproductive success of plants.
Based on the approach outlined by Schupp (1993), in which seed
dispersal effectiveness is the product of quantitative and qualitative components, comparative investigations on the performance
of sympatric seed dispersers have increased recently (Graham et al.
1995, Zhang & Wang 1995, Sun et al. 1997, Andresen 1999,
Yumoto et al. 1999, Pizo & Simão 2001, Knogge et al. 2003).
Quantitative (i.e., number of visits or number of dispersed seeds)
and qualitative (i.e., increasing dispersal distance, enhancement of
seed germination success, and delivery of seeds at sites whose characteristics may favor seed and seedling survival) attributes of dispersal
vary in effectiveness among species or functional groups.
The importance of primates as seed dispersers in Neotropical
forests has been widely recognized (e.g., Estrada & Coates-Estrada
1
Received 19 May 2004; revision accepted 3 April 2005.
Current address: Dept. de Zoologia, Instituto de Biociências, University of
Campinas, Cx.P. 6109, CEP 13.083-970, Campinas, Sao Paulo, Brazil; e-mail:
milenemartins@terra.com.br
2
1984, 1986; Chapman 1989; Julliot 1996, 1997; Lambert & Garber
1998). Yet, some species remain poorly investigated. For instance,
most studies on howler monkeys (genus Alouatta) have focused on
the northern species (Alouatta palliata: Estrada & Coates-Estrada
1984, 1986, 1991; Chapman 1989; Serio-Silva & Rico-Gray 2002;
Alouatta pigra: Marsh & Loiselle 2003; Alouatta seniculus: Julliot
1996, 1997; Andresen 1999, 2002; Feer 1999; Yumoto et al. 1999;
Feer & Forget 2002), whereas the southern brown howler monkey
(Alouatta guariba, Cabrera 1940) has received little attention.
Endemic to the highly fragmented Atlantic Forest, the brown
howler and the muriquis are the largest (A. guariba up to ca
6 kg, Brachyteles arachnoides up to ca 8 kg; Kinzey 1997) arboreal
folivores/frugivores that occur sympatrically in southeastern Brazil.
The annual relative contribution of fruits to the diet of A. guariba is
5–16 percent (Mendes 1989, Chiarello 1994), whereas fruits represent 21–59 percent of B. arachnoides‘s diet (Milton 1984a, Carvalho
et al. 2004). Until now, data on seed dispersal concerning A. guariba
and B. arachnoides were obtained from a handful of studies (Brozek
1991, Moraes 1992, Figueiredo 1993, Figueiredo & Longatti 1997,
C 2005 The Author(s)
C 2005 by The Association for Tropical Biology and Conservation
Journal compilation 57
58
Martins
Vieira & Izar 1999). These investigators have pointed out that these
primates are able to maintain seed viability of a wide range of fruit
species as well as to enhance the success of germination of a subset of
them. Howler monkeys are often the only large seed dispersal agents
that may survive for a long time in small forest fragments and thus
may play a crucial role in plant regeneration processes. Therefore,
interactions between the primate species and the plant community
are highly relevant to the conservation of the threatened Atlantic
Forest.
Recent studies have revealed that primates differ in their effectiveness as seed dispersers (Zhang & Wang 1995, Andresen 1999,
Stevenson et al. 2002). For example, Ateles paniscus was more effective than sympatric A. seniculus for producing a highly scattered
seed rain (Andresen 1999). Dropping seeds in large aggregations is
likely to have a diminishing effect on the performance of a disperser
because the clumps attract more predators and impose higher intraspecific competition for the seeds ( Janzen 1970, Connell 1971).
Also, for a given plant species, two different primate species may affect germination success differently (Stevenson et al. 2002, Knogge
et al. 2003). Differences between species are not always apparent, however. For instance, the dispersal distance of seeds carried
by A. seniculus and Lagothrix lagotricha did not differ (Yumoto
et al. 1999), despite intergeneric divergence in their ranging
patterns.
Differences in feeding and behavioral patterns between
Alouatta and Brachyteles may lead to differences in seed dispersal
effectiveness. Because Brachyteles depends more on fruits, a higher
percentage of dung with seeds and more seed species dispersed
together may be expected for this species. In addition, B. arachnoides defecates 10–14 times in a single day (Milton 1984a), so
that fewer seeds are expected to be expelled together when compared to the large clumps voided by Alouatta (Howe 1989), which
defecates twice a day (see Julliot 1996, Andresen 2002). Individuals of Alouatta spp. have an average passage time of 20 h whereas
in Brachyteles this is about 8 h (Milton 1984b). Brachyteles move
faster and over a large ranging area (71–73 ha; Milton 1984a)
when compared to A. guariba (8 ha; Mendes 1989). Members of
Alouatta defecate collectively with individuals positioned on lower
perches (Andresen 1999), in contrast to B. arachnoides, which defecate individually and from high branches. The highly folivorous
howlers have more fiber in their gut which binds the seeds together
and leads to a more clumped fecal sample. Seeds voided by the
fruit-favoring muriquis will probably scatter and be deposited in
a scattered pattern. I predict that, compared to B. arachnoides, A.
guariba will enhance the germination success of fewer species (seeds
excessively abraded), carry seeds to shorter distances, and produce a
more clumped defecation pattern.
Specific questions addressed in this study were: (1) what is the
percentage of dung with intact seeds?; (2) what is the mean number
of seeds per fecal sample?; (3) how many seed species are dispersed
together?; (4) does gut passage increase the germination percentage
and/or decrease the latency to germination of seeds?; (5) how far
does each primate species disperse seeds?; (6) do primates defecate
seeds under or away from a conspecific canopy?; and (7) are their
patterns of deposition clumped or scattered?
MATERIALS AND METHODS
STUDY SITE.—This study was carried out in a 1450-ha forest fragment of the Fazenda Barreiro Rico, a privately owned cattle ranch
located near the confluence of the Piracicaba and Tietê Rivers
(22◦ 41 S, 48◦ 06 W), on the eastern range of the central Plateau
of the state of São Paulo, southeastern Brazil (450–586 m above sea
level). The vegetation is submontane, semideciduous forest, according to Oliveira-Filho and Fontes’s (2000) classification of the southern Atlantic Forest formations. Within the fragment, regenerating
old logged areas with moderately open understory are interspersed
with impoverished areas comprising canopy gaps and a dense understory of lianas. Canopy gaps and abundance of herbaceous vegetation and lianas result from logging activities. The predominant
climate is mesothermic, with a dry season from April to September when monthly rainfall is <70 mm. Mean annual rainfall for a
60-year period (1940–1999) is 1284.5 ± SD 285.5 mm (data from
the climatological station at the ranch).
The fauna at the study site has become impoverished. Avian
frugivores such as toucanets (Baillonius bailloni and Selenidera maculirostris) and red-breasted toucans (Ramphastos dicolorus) have
not been observed for years (Magalhães 1999). Three other primate species inhabit the forest patch: the buffy tufted-ear marmoset (Callithrix aurita), the masked titi monkey (Callicebus
personatus nigrifrons), and the brown capuchin monkey (Cebus
apella), the first two species at extremely low abundance (Martins
2005).
COLLECTION OF DUNG.—Fecal samples of A. guariba and B. arachnoides were collected during 12 mo (June 2001 to May 2002)
concurrently with observations of their feeding behavior. One individual or group of each species was observed from dawn to dusk for
4–5 consecutive days per month, totaling 555 and 534 h of contact with A. guariba and B. arachnoides, respectively. Both primate
species fed on fruits from trees and lianas. The pattern of deposition
was determined for seeds from these two groups, but the dispersal
distance and the passage time was assessed only for tree seeds, and
the deposition site only for liana seeds. I used event sampling procedures to record fruit feeding and defecation events. Whenever
the animal consumed a fruit and swallowed the seeds, the tree was
marked and the animal continuously followed (from sleeping site
to sleeping site). If the primate fed on a second individual of the
same species, the record was discarded. This occurred very often for
lianas and prevented measurement of dispersal distance and passage
time. Soon after the defecation events, the following variables were
recorded: the species and height (m) of the disperser in the vegetation, the pattern of deposition of seeds in dung, and the deposition
site of liana seeds (whenever they occurred in dung). The pattern of
deposition of the seeds was assigned to one of the two categories:
clumped (most of seeds up to 10 cm apart) or scattered (most of
seeds more than 10 cm apart). Based on previous observations of
seeds in dung of both primate species, seeds separated 10 cm or
more from each other were rapidly accessed by arthropods such
as dung beetles. The deposition site of liana seeds was checked to
verify if it was under or away from a conspecific fruiting canopy.
Comparative Seed Dispersal by Primates 59
If fruits of a conspecific liana were found on the forest floor at
the deposition site, I recorded the deposition as having been made
under a conspecific fruiting canopy. When there were no fruits on
the forest floor, I assumed that liana seeds were voided away from
a conspecific canopy. This assumption was supported by the fact
that individuals of each of the two top-ranking liana species in the
primates’ diet (Diclidanthera sp. and Pereskia aculeata) fruited in
synchrony within a time window of about 7 weeks. Because fruiting
of trees was not synchronized, I was not confident in determining
whether seeds of trees were voided under conspecifics. After collecting the dung, the defecation site was marked with a flagging tape
attached to a wooden stick. I measured the distance (m) between
the parental tree and the defecation site using a 50-m measuring
tape. Because of the dense understory and absence of reference
points, measurement of the dispersal distance of farther defecations
presented problems. Thus, I collected all dung, but recorded only
distances up to 100 m. Measurements were as direct as possible
and the values were assigned to one of the three distance classes:
0–50.9, 51–99.9, and ≥100 m. This last distance class included
undetermined figures larger than 100 m. In order to estimate the
passage time of seeds, I used only fruit feeding records of those
species consumed rarely and seeds voided in observed defecation
events. Passage time in the primates’ gut was considered the time
(h) elapsed between consumption until the first appearance of the
seeds in dung. Seeds swallowed in the evening were usually voided
the following morning. Although overnight defecations were quite
rare, I looked for seeds on the forest floor under the sleeping site
when I arrived there at dawn, but these were not considered in the
passage time estimate. In the laboratory, the fecal sample was rinsed
and the seeds were identified and counted.
STUDY GROUPS.—The A. guariba group consisted of two males
(adult and subadult), two adult females, a juvenile male, and an
infant male. Due to the usual absence of natural marks on B. arachnoides and to their noncohesive social units, it was very difficult to
recognize individuals whenever they wandered in large parties. For
this reason, the seed dispersal distance and the passage time were
only estimated whenever I was absolutely certain of following the
same individual that had remained solitary for days or had occasionally joined a small troop (two to three members). About 8–11
adults were investigated.
GERMINATION TRIALS.—I evaluated the germination success of seeds
found in dung or spat out by the primates through the germination
percentage (number of germinated seeds/total seeds) and latency
to germination (average number of days to germination). All seeds
larger than 2 mm in their longest dimension were identified to
genera or species level according to a reference collection housed at
the Laboratory of Vertebrate-Plant Interaction (LIVEP) of University of Campinas (Unicamp). Samples of uningested seeds (control)
were obtained by collecting ripe fruits either from fruiting plants or
from the ground under the crowns of the same plants fed upon by
the primates. The pulp was manually removed from the fruits or
the aril from the seeds for each plant species, with the exception of
Eugenia ligustrina. Ripe fruits of this species were tested versus seeds
spat out by B. arachnoides that swallowed only the pulp. Seeds with
no signs of damage by insects or fungal infestation as well as those
that did not float in water were selected for the germination trials.
The seeds were placed in plastic gearbox with sterilized vermiculite
and moistened with distilled water. Due to logistic constraints, tests
were not carried out in the field. Instead, they were performed in
the laboratory under constant white light. This procedure takes
into account the light sensitivity exhibited by small-seeded, early
successional species (Souza & Válio 2001) as well as the unknown
requirements for germination of the tested seeds. The samples were
checked daily and the emergence of the radicle was considered successful germination. If ungerminated seeds remained in the plastic
boxes, tests were terminated when 30 d had elapsed since the last
germination.
DATA ANALYSES.—To determine whether A. guariba and B. arachnoides differed in number of fecal samples with intact seeds and
number of seed species dispersed I used χ 2 and G-tests, respectively. The difference between the number of germinated seeds in
the two treatments (control × swallowed or spat seeds) was tested by
χ 2 . The difference between the primate species in number of seeds
per dung sample as well as the difference in days to germination
between defecated or spat seeds and control seeds were evaluated by
t-tests. Prior to these statistical analyses, data were tested for normality (Kolmogorov–Smirnov test statistics) and transformed to their
square root when necessary. Nontransformed data were tested by
Mann–Whitney U-test in case a nonnormal distribution persisted.
Differences in frequency of defecation events assigned to classes of
distance, location, and pattern of deposition were each tested by χ 2 .
The software STATISTICA v. 4.3 was used to carry out the tests.
I set α at 0.05 for all analyses. Data are presented as means ± SD
throughout.
RESULTS
SEEDS IN DUNG.—Two hundred and sixty-four fecal samples were
collected that contained 2334 intact seeds of 20 fruit species. B.
arachnoides dispersed more seed species and deposited a significantly higher percentage of dung with intact seeds. There was no
significant difference between the number of seeds per fecal sample
in A. guariba and B. arachnoides. Distribution of codispersed seed
species differed significantly between primate species: contrary to A.
guariba, B. arachnoides tended to disperse up to three seed species
more often in a single defecation event (Table 1).
GERMINATION SUCCESS.—Due to germination failure of some
species (swallowed and control) and reduced sample size of others, analyses were performed for eight species. Either A. guariba or
B. arachnoides significantly increased the germination of approximately half of the plant species tested (Table 2). Both A. guariba
and B. arachnoides decreased the germination of one species each.
Howlers significantly decreased the average germination time
of one out of five plant species tested, whereas B. arachnoides decreased germination time of four out of six tested species (Table 3).
60
Martins
TABLE 1.
Quantitative attributes of seed dispersal effectiveness of Alouatta
guariba and Brachyteles arachnoides. Significant results in bold.
TABLE 3.
Latency to germination of control seeds and seeds in dung of Alouatta
guariba and Brachyteles arachnoides. Sample size of tested seeds in
parentheses. Significant results in bold (+ = increase, − = decrease).
Quantitative
attributes
Number of species
dispersed
Fecal samples with
A. guariba
B. arachnoides
14
18
55 (N = 147)
79 (N = 117)
Statistics
Species
Range
1–97
9.9 ± 10.5
1–10
U = 3482.5; P > 0.05
1–57
Seed species per fecal sample
1
2
3
73
7
0
G = 6.3; P < 0.05
74
15
3
Contrary to my expectation, A. guariba did not affect fewer species
than B. arachnoides in germination percentage. There was, however,
a more pronounced effect of B. arachnoides in latency to germination. As predicted, and in accordance with the literature, average
passage time of A. guariba (19 ± 4 h, N = 31) was longer than
average retention time of B. arachnoides (14 ± 6 h, N = 38).
DISPERSAL DISTANCE AND PATTERNS OF DEPOSITION.—Determination of seed dispersal distance, characterization of the deposition
Germination percentage of control seeds and seeds in dung of Alouatta
guariba and Brachyteles arachnoides. Sample size of tested seeds in
parentheses. Significant results in bold (+ = increase, − = decrease).
Rate of germination
Species
Control
A. guariba
Celtis spinosa
44 (50)
88 (50)
χ 2 = 21.57; P < 0.001 (+)
15 (20)
52 (100)
92.6 (54)
100 (5)
85 (100)
14 (50)
χ 2 = 13.28; P < 0.001 (+)
χ 2 = 25.23; P < 0.001 (+)
χ 2 = 64.74; P < 0.001 (−)
56.7 (30)
42.5 (40)
χ2
Celtis spinosa
Diclidanthera sp.
Eugenia ligustrina
44 (50)
52 (100)
80 (25)a
42 (100)
93 (100)
100 (60)b
χ 2 = 0.05; P = 0.82
χ 2 = 42.15; P < 0.001 (+)
χ 2 = 12.75; P < 0.001 (+)
Eugenia sp.1
Jacaratia spinosa
Rudgea sp.
56.7 (30)
34 (94)
93.8 (16)
25 (20)
56 (50)
20 (27)
χ 2 = 4.8; P < 0.05 (−)
χ 2 = 6.47; P < 0.05 (+)
χ 2 = 2.56; P = 0.11
Cordia sellowiana
Diclidanthera sp.
Eugenia pyriformis
Eugenia sp.1
Dung
Statistics
= 1.37; P = 0.24
B. arachnoides
b Seeds
Dung
Statistics
Celtis spinosa
Cordia sellowiana
Diclidanthera sp.
51 (22)
19 (3)
14 (52)
48 (44)
13 (5)
13 (85)
U = 416.5; P = 0.36
U = 5.00; P = 0.46
t = 0.26; P = 0.79
Eugenia pyriformis
Eugenia sp.1
32 (50)
62 (17)
15 (7)
56 (17)
U = 66; P < 0.05 (−)
t = 1.71; P = 0.97
A. guariba
Seeds per fecal sample
Mean
17.6 ± 24.3
Mode
1–10
a Unremoved
Control
χ 2 = 16.8; P < 0.05
seeds (%)
TABLE 2.
Average days
to germination
pulp.
spat out under parent tree.
B. arachnoides
Celtis spinosa
51 (22)
50 (42)
U = 409.0; P = 0.45
Diclidanthera sp.
Eugenia ligustrina
Eugenia sp.1
14 (52)
21 (20)a
62 (17)
12 (93)
09 (60)b
53 (5)
U = 1.881; P < 0.05 (−)
t = 9.03; P < 0.001 (−)
U = 20.5; P = 0.08
Jacaratia spinosa
Rudgea sp.
38 (32)
38 (15)
30 (28)
31 (20)
U = 241; P < 0.05 (−)
U = 88.50; P < 0.05 (−)
a Unremoved
b Seeds
pulp.
spat out under parent tree.
site, and definition of deposition patterns were each possible for
only a subset of 147 and 117 droppings of A. guariba and B.
arachnoides, respectively. Frequencies of dispersal events in distinct
distance classes of dispersal (Fig. 1a) were similar for both species
(χ 2 = 4.79; P > 0.05). The frequency of dispersal of liana seeds
away from conspecific fruiting canopies was significantly higher
(χ 2 = 8.71; P < 0.05) for B. arachnoides (Fig. 1b). Brachyteles
used higher perches than Alouatta (19.5 ± 4.4 m × 14.8 ± 4.6 m;
t = 7.38; P < 0.05) during defecation events, which contributed
to distinct patterns of deposition. Thus, the predominant spatial
distribution pattern of voided seeds was dependent on the disperser
(χ 2 = 4.06; P < 0.05); A. guariba showed a greater frequency of
clumped defecations than B. arachnoides (Fig. 1c).
DISCUSSION
B. arachnoides was a more effective seed disperser than A. guariba.
As for the quantitative component of effectiveness, B. arachnoides
dispersed more seed species than A. guariba. Also, seeds were more
often found in fecal samples produced by the former than by the latter. These differences are most likely due to distinct digestive strategies between the genera Alouatta and Brachyteles (Milton 1979).
Greater reliance on leaves, which requires many hours to process
the fiber content in the howler guts leads to few daily opportunities
for the swallowed seeds to be voided. By contrast, the relatively
higher amount of readily absorbed carbohydrates from fruits in B.
arachnoides’ gastrointestinal tract is associated with a distribution of
seed ballast in several defecations. Despite the consistency between
Comparative Seed Dispersal by Primates 61
FIGURE 1. Percentage of seed dispersal events by Alouatta guariba and
Brachyteles arachnoides. (a) Dispersal distance (m) of tree seeds, (b) deposition of
liana seeds under or away from a conspecific canopy, and (c) pattern of deposition
of tree and liana seeds (∗ = P < 0.05).
A. guariba and B. arachnoides in average density of seeds per dung,
B. arachnoides presented a wider range of codispersed seed species.
Because seed species may compete more strongly when in proximity,
as demonstrated with bird droppings (Loiselle 1990), seed species
composition in primate fecal samples may affect seedling survival.
The proportion of species that had their germination percentage affected by gut passage or pulp removal was similar in both
A. guariba and B. arachnoides. Therefore, both contributed equally
to the germination success and seedling recruitment of some plant
species. These findings reinforce the evidence of enhanced seed
germination by large-sized Neotropical primates (Moraes 1992,
Figueiredo 1993, Julliot 1996, Bravo & Zunino 2000, Stevenson
et al. 2002). However, evidence that shorter passage time of the digesta in the gut may lead to positive effects on germination (Murray
et al. 1994, Traveset & Verdú 2002) cannot be supported by the
present results. The lack of difference between howlers and muriquis
indicates that seed retention time is not the only factor affecting
plant species responses. Indeed, Stevenson et al. (2002) found no
significant correlation between passage time and percentage of seed
species consumed by primates with higher proportion of germination rates or shorter latency periods. It has been suggested that
besides variation in seed retention time between different groups of
frugivores, chemical composition of food ingested along with fruits
may determine the extent to which seeds are abraded (Traveset &
Verdú 2002 and references therein). Chemical composition of food
probably also explains why A. guariba affected a lower proportion of
species than B. arachnoides in germination latency. Such variability
between howlers and muriquis does not necessarily lead to differential effectiveness in seed dispersal, however. Whether reduced or
prolonged germination time represents an advantage to plant fitness
will depend on environmental circumstances (Barnea et al. 1991)
rather than those intrinsic to primate physiology. Another source
of variability was the separation of seeds from pulp, which was observed only in B. arachnoides. Although E. ligustrina seeds were not
swallowed by B. arachnoides, germination success was enhanced.
Compared to unprocessed seeds, those cleaned by birds (Izhaki &
Safriel 1990) or monkeys (Lambert 2001) have higher germination
rates. E. ligustrina seeds still covered with pulp were attacked by
fungus during the tests. Lambert (2001) demonstrated that fungal
pathogens induced detrimental effects on the survival of seeds of
fleshy fruits dropped under the parental crown.
The area covered by the focal B. arachnoides group included
the home range of at least five A. guariba groups, suggesting that
dispersal distance of seeds would be higher for Brachyteles. It seems
that differences in home range size, rather than in average daily path,
are more important for predicting seed dispersal distance. Traveling
routes of Lagothrix lagothricha were usually nonlinear and longer
travel distances did not correlate with increased seed dispersal distance (Stevenson 2000). Indeed, the complex routes of individuals
within the range of seed dispersal studied may have concealed a
potential difference in dispersal distances. For example, my focal
groups of A. guariba and B. arachnoides voided seeds in the morning near a fruiting tree they had fed upon on the previous evening
in similar proportions: 4.9 and 3.1 percent, respectively. Likewise,
Yumoto et al. (1999) did not find a difference in dispersal distance
of seeds carried by A. seniculus and L. lagotricha. Also, the fact that
distances above 100 m were lumped in one category may be one
reason for the lack of difference between the distance seeds were
dispersed.
Unlike A. guariba, B. arachnoides dispersed liana seeds only at
sites free from conspecifics. Many seedlings of the consumed lianas
P. aculeata and Diclidanthera sp. sprouted from the primates’ dung
in sites with no conspecific canopy above. This indicates that a considerable amount of ingested seeds had not experienced predation.
62
Martins
Also, B. arachnoides, which defecated from high branches and presented a similar contribution of clumped and scattered seeds in
dung, was more effective than A. guariba in scattering dispersed
seeds at the deposition site. Such differences in the deposition patterns parallel those found between A. seniculus and A. paniscus in a
Peruvian forest (Andresen 1999) and have implications for dispersal effectiveness. On the other hand, predation on seeds deposited
either in a clumped or scattered pattern is similar in Neotropical
sites (Notman et al. 1996, Pizo & Simão 2001). Also, the 10-cm
criterion between dispersed seeds used in the present study may
not be large enough to detect a difference when considering seed
predators such as rodents.
Burial activities of dung beetles are indeed crucial in decreasing
predation on seeds voided by primates (Estrada & Coates-Estrada
1991, Andresen 1999, Feer 1999), independently from the spatial
distribution pattern of the experimental seeds (Andresen 2002).
Several dung beetles were observed burying seeds at the study site,
especially during the rainy season. In addition, Howe (1989) suggested the development of chemical defenses by seed species that
depend on clump-disperser animals. In this study, A. guariba showed
less effectiveness than B. arachnoides by voiding seeds at sites where
they are expected to suffer high mortality rates. Nevertheless, it remains to be determined whether dung beetles as well as defensive
chemical strategies of plants in Barreiro Rico have notable effects on
the postdispersal seed fate and, therefore, on the quality of dispersal
services provided by the primates.
Given the interspecific variation in the pattern of recruitment
of tropical plants (Chapman & Chapman 1995, 1996), the quantitative and qualitative divergences between howlers and muriquis
in their function as seed dispersers may crucially influence the composition and maintenance of seedling diversity within the community. I have shown that behavioral strategies typical of Alouatta
and Brachyteles (Rosenberger & Strier 1989) lead to divergences in
seed dispersal. Such differences are probably relevant to mediumsized southeastern Atlantic Forest sites, where the fauna has been
partially depleted and more fruits are available to primates. Extirpation of large-sized frugivores from tropical forests as a result
of anthropogenic interference has implications for seedling recruitment (Chapman & Chapman 1995). Coexistence of plant species
with large competitive differences, a recognized attribute of the spatial heterogeneity of tropical forests, may be achieved by exceeding
the seed dispersal limitation threshold (Webb & Peart 2001). For
seeds with different competitive abilities, finding suitable places for
recruitment will probably also depend on dissimilar performances of
large-bodied sympatric dispersers with abilities to thrive in less protected forest patches. Further investigations on postdispersal events
may determine how similar and different A. guariba and B. arachnoides are in their net contribution to forest regeneration.
ACKNOWLEDGMENTS
I am grateful to J. C. Magalhães for granting permission to carry
out the study on his property. I also thank W. R. Silva for access
to laboratory equipment, M. A. Pizo, C. Tutin, B. Kaplin, and an
anonymous reviewer for helpful comments on the early draft. J. C.
Oliveira provided valuable field assistance. These results are part
of the requirements for a Ph.D. degree to MMM who received a
fellowship from Fapesp (99/06217-2). The study was supported by
grants from Margot Marsh Biodiversity Foundation and Primate
Conservation, Inc.
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