Download Seed Dispersal and Ingestion of InsectInfested Seeds by Black

THE JOURNAL OF TROPICAL BIOLOGY AND CONSERVATION
BIOTROPICA 40(4): 471–476 2008
10.1111/j.1744-7429.2008.00400.x
Seed Dispersal and Ingestion of Insect-Infested Seeds by Black Howler Monkeys
in Flooded Forests of the Parana River, Argentina
Susana Patricia Bravo1
Laboratorio de Primatologı́a. Museo Argentino de Ciencias Naturales. Buenos Aires. Argentina, Laboratorio de Ecologı́a Funcional,
Departamento de Ecologı́a, Genética y Evolución, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Ciudad
Universitaria Pab. II, 4◦ piso, CP 1428, Buenos Aires, Argentina
ABSTRACT
All howler monkey species (Alouatta spp.) have a folivorous–frugivorous diet. Howler monkeys are reported to be seed dispersers in several areas, including black
howlers (Alouatta caraya), which are important seed dispersers in northern Argentinean forests. The goal of this work was to study the three-way interaction between
insects, seeds, and black howlers, and assess the functional significance of this tri-trophic interaction for seed dispersal. I determined through direct observation that
fruits of species with a high proportion of insect infestation were important components of howler monkey diet. Ocotea diospyrifolia seeds from fresh faeces of black
howlers contained dead larvae, but seeds were still able to germinate. Seeds in which larvae had reached an advanced stage of development did not germinate. Larvae
of infested Eugenia punicifolia fruits were killed by digestion when they occurred in the pulp early in the fruiting season, but were dispersed alive with seeds later in
the season. Banara arguta fruits contained both healthy and infested seeds; infested seeds were destroyed during digestion, while healthy seeds were dispersed. Black
howlers’ ingestion of infested fruits could result in the: (1) killing of larvae and dispersion of healthy seeds; (2) spread of larvae; or (3) destruction of infested seeds.
This will depend on the relationship between the time at which fruit is consumed by black howlers, the time at which insect infestation occurs, and also probably on
the hardness of the seed coat and the seed–insect size ratio.
Abstract in Spanish is available at http://www.blackwell-synergy.com/loi/btp.
Key words: Alouatta caraya; insect consumption; insect seed predation; three-way interaction.
THE FOLIVOROUS–FRUGIVOROUS DIET OF HOWLER MONKEYS IS WELL
KNOWN (Milton 1980, Julliot 1994, Stoner 1996, Silver et al. 1998).
Less well known is that howlers also ingest animal protein in low
proportions as a consequence of consuming insect-infested fruits
(e.g., fig fruits; Crockett & Eisenberg 1987, Prates et al. 1990).
Interactions between plants and seed-dispersing primates have also
been well documented (Julliot 1996, Garber & Lambert 1998,
Bravo 2003). However, little is known about the three-way interaction that results from a seed-dispersing animal that eats an
insect-infested seed. In such cases, what are the implications for the
insect, plant, and seed-dispersing animal? Does ingestion of infested
seeds impact seed fate? What are the consequences for the insects?
Seed-dispersing animals can be either attracted or repelled
by insect-infested fruits or seeds. For example, fruit-eating bats
in Philippines (Utzurrum & Heideman 1991), birds in Alaska
(Traveset et al. 1995), and the howler Alouatta seniculus in French
Guiana (Julliot 1996) have been reported to avoid eating infested
fruits or seeds. But other dispersers, such as the black-tufted-ear
marmoset Callithrix penicillata in Brazil (Redford et al. 1984), and
several vertebrates recorded by Valburg (1992) eating Acnistus arborescens in Costa Rica are attracted to infested fruits. These organisms are not only dispersal vectors for seeds, but may also spread
the insect infestation by dispersing viable insects in the seeds. For
example, Eugenia sp. and Syagrus romanzoffiana palm seeds infested
by a weevil larva Revena rubiginosa are dispersed by toucans Ramphastos dicolorus and R. vitellinus, and thrushes Turdus rufiventris in
southeastern Brazil; weevil larvae later emerge from the dispersed
Received 6 November 2006; revision accepted 15 November 2007.
1 Corresponding author; e-mail: [email protected]
seeds (Guix & Ruiz 1995). Similarly, mockingbirds Mimus polyglottos disperse wasp-infested seeds of Rosa multiflora with viable wasps
in North Carolina (Nalepa & Piper 1994).
In addition to the attraction or repulsion of seed-dispersing
animals to insect-infested fruits or seeds, and the possibility that
insects are dispersed along with seeds, more complex interactions
were described, for example, in Africa among infested seeds of
Acacia spp., large mammalian herbivores and bruchid beetles (Or
& Ward 2003) and, in South America, among tapirs, palm seeds,
and bruchid beetles (Silvius & Fragoso 2002, Fragoso et al. 2003).
African mammals can kill larvae and disperse cleaned seeds, destroy
infested seeds and disperse only healthy ones, or, similar to tapirs in
South America, protect seeds from insect predators by eating fruits
before infestation by bruchids (Silvius & Fragoso 2002, Fragoso
et al. 2003, Or & Ward 2003). Several factors likely determine
which is the main result of the three-way interaction (Or & Ward
2003).
Insect infestation was detected in leaves, flowers, and fruits of
several species that represented 25.5 percent of the diet of black
howler monkeys Alouatta caraya living in the flooded forests of
islands in the northern Paraná River, Argentina (Bravo & Sallenave
2003). Black howler monkeys are seed dispersers of woody plants
of these forests, including three species whose fruits were heavily
infested by insects: Ocotea diospyrifolia, Eugenia punicifolia, and
Banara arguta (Bravo 2003). It is not known, however, if infestation
affects seed viability, how black howler ingestion of fruits affects
insect survivorship and what is the proportion of infested fruits in
the diet of black howlers.
The goals of this study were to obtain a description of this
three-way interaction and to assess its functional significance for
C 2008 The Author(s)
C 2008 by The Association for Tropical Biology and Conservation
Journal compilation 471
472
Bravo
seed dispersal. I tested the following hypotheses: (1) when available,
fruits of insect-infested species are an important item in the black
howler diet; (2) passage through the digestive tract of black howlers
increases the proportion of germinating insect-infested seeds because digestion kills the larvae; (3) insect infestation has a negative
effect on seed germination.
METHODS
STUDY SITE.—The study was carried out on Brasilera Island,
Argentina, located at the confluence of the Paraná and Paraguay
rivers (27◦ 30 S, 58◦ 41 W). The island area is 280 ha, half of which
(141 ha) is covered by flooded forests. The climate is subtropical,
with an annual average temperature of 21.0◦ C, and annual thermal
amplitude of 12.3◦ C. Annual precipitation is about 1500 mm. Even
though rainfall decreases during the winter, there is no marked dry
season.
The flooded forests of the Paraná River islands have the greatest
density of howler monkeys reported from Mexico to Argentina
(Crockett 1998). The black howler is the most abundant arboreal
frugivore in these ecosystems. This study was conducted in mature
forest stands, where black howler density is 4.25 ind/ha (Zunino
et al. 2000) and home range of groups are ca 2 ha (Bravo & Sallenave
2003).
Mature forests occupy 66 ha in the center of Brasilera Island and
are surrounded by lagoons. The canopy is dominated by O. diospyrifolia Meinz (Lauraceae) and Albizia inundata Mart. (Mimosaceae).
The understory vegetation is dominated by E. punicifolia Kurth
DC. (Myrtaceae) and Psychotria carthagenensis Jacq. (Rubiaceae).
Saplings of O. diospyrifolia are another important component of the
understory (9% of individuals). Additional details about the study
site can be found in Bravo and Sallenave (2003).
RELEVANCE OF INFESTED FRUIT IN THE DIET OF BLACK HOWLERS.—
Two groups of black howlers were followed from dawn to dusk, from
May 1998 to February 2000, in periods of 7–10 continuous days
(sample period), every other month. However, only results of sample
periods in which infested fruits were detected are reported here.
These were the fruiting periods of O. diospyrifolia, E. punicifolia,
and B. arguta. The behavior of all detected individuals was recorded
every 15 min by scan sampling (Martin & Bateson 1993). Every
record of animals feeding during scans will be referred as a feeding
record; a total of 2205 feeding records were obtained. The species
name and tree structure (new leaves, mature leaves, buds, flowers, or
fruits) on which howlers were feeding were recorded. The percentage
of each of these food items in the diet for each sample period was
calculated as
I % = (n i /N) × 100,
where I% is the percent ingestion for item i, n i is the number of
feeding records on item i during a sample period, and N is the total
number of feeding records (N = ni) taken during a sample period.
The characteristics of the fruits eaten by black howlers are presented
in Table 1.
INSECT INFESTATION.—During the behavioral observations described above the presence of larvae in the fruits of all tree and
vine species in the forest was checked. Fruits from trees of species
with insect-infested fruits were collected from the crowns to assess
the degree of infestation. A fruit was considered infested when any
arthropod larva was detected inside the pulp or seed. A seed was considered infested when the larvae were located inside the seed. Other
types of infestations such as fungi, yeast, or viruses were not considered in this study; however, some of these infesting agents have
been observed to play a role in fruit consumption by vertebrates in
other species (e.g., Cipollini & Stiles 1993, Levey 2004).
To measure infestation rates, I used only fruits of similar color
to those eaten and only fruits from trees known to be used by black
howler monkeys, in order to select fruits with the same degree of
ripeness, as the stage of fruit development may affect both the proportion of germination and of infestation. One hundred fruits from
15 O. diospyrifolia trees were collected in July 1998, 200 fruits from
10 B. arguta (Flacourtiaceae) trees in May 1999, and 200 fruits
from 10 E. punicifolia trees in February 2000.
Percent infested fruits per tree, and number of insects per
fruit or seed were calculated for each plant species. The location of
larvae within the fruits (pulp/seed) was also recorded for each plant
species. Fruits and seeds were examined under a stereomicroscope
to determine if insects were alive or dead and if the embryos had
been attacked and also to estimate the percentage of endosperm
consumed.
For O. diospyrifolia, more details of infestation could be
recorded. Endosperm consumed and arthropod developmental
stage was evaluated in 66 seeds. I used five categories of endosperm
consumption: < 5 percent (classified as 1); 5–25 percent (2); 25–
50 percent (3); 50–75 percent (4); and > 75 percent (5), and four
categories of arthropod development: eggs (1); small larvae (2); big
larvae (3); or pupae (4). Larvae, which were 50 percent smaller than
TABLE 1. Characteristics (mean ± SE) of ripe fruits of plant species consumed by two black howler groups in Brasilera Island (Argentina). N = number of fruits measured.
Species (fruit type)
N
Wet weight (g)
Major axis (mm)
Minor axis (mm)
Water content (%)
Color
Seeds/fruit
Ocotea diospyrifolia (Drupe)
30
0.94 ± 0.04
14.6 ± 0.3
9.0 ± 0.1
55.0 ± 0.2
Black
1
Eugenia punicifolia (Drupe)
Banara arguta (Berry)
60
100
1.47 ± 0.03
0.96 ± 0.03
9.0 ± 0.3
11.5 ± 0.3
8.0 ± 0.2
9.4 ± 0.1
86.3 ± 0.4
82.4 ± 0.5
Black
Green
1
20–90
Insect-Infested Seed Ingestion and Dispersal
prepupae (ca 5mm), were classified as small and larger ones as big.
As no seeds contained pupae, endosperm consumed up to this level
of development was estimated from seeds reserved to identify adults
(see below). Correlation between endosperm consumed and insect
developmental stage was evaluated using a Kendall tau rank correlation test. A random subpool of seeds of each species was reserved to
identify adult arthropods. Insects were identified by Dr. Bachmann,
curator of the Entomological Division of the Museo Argentino de
Ciencias Naturales. The number of larvae per E. punicifolia fruit
was estimated in the field by counting oviposition holes per fruit
(N = 200). These fruits could not be examined under the stereomicroscope because they arrived in the laboratory in poor condition,
they had rotted, and the larvae could not be recovered.
THE EFFECT OF DIGESTION ON LARVAE AND SEED FATE.—Seeds of
the three species (O. diospyrifolia, E. punicifolia, and B. arguta) were
collected from fresh faeces of black howlers to evaluate seed infestation under the stereomicroscope. The number of seeds collected
per species varied in relation to their abundance in faeces: 167 seeds
of O. diospyrifolia, 75 of E. punicifolia, and 936 of B. arguta were
collected from faeces of all 18 adult and subadult monkeys in the
two groups.
As ingestion kills most larvae in O. diospyrifolia seeds, the effect
of digestion on germination of this plant species was evaluated. Seeds
collected from faeces and healthy seeds collected from trees were
used in germination trials. Trials were performed in the laboratory
by placing seeds in pots with humid filter paper. The experiment
was finished when no new germination occurred after 30 d. Each
of the 45 pots with seeds from faeces and with healthy seeds from
trees was considered a replicate (N = 90). The proportions of seeds
germinating from each source were compared using the Mann–
Whitney U-test.
THE EFFECT OF INSECT INFESTATION ON GERMINATION.—Infested
O. diospyrifolia and E. punicifolia seeds were able to germinate because the seeds were not completely destroyed by larvae. Laboratory
studies were only performed on infested O. diospyrifolia seeds because the soft fruits of E. punicifolia had decomposed, and their
larvae had died, before reaching the laboratory.
During May 2004, 722 infested seeds and 598 healthy seeds
were collected from 29 trees in the territories of five groups of black
howlers. Hundreds of seeds were taken from each tree until ca 20
healthy seeds were obtained from each one. Seeds were stored in pots
with humid filter paper to determine the proportion germinated
from each group. Results were evaluated by paired t-tests considering
individual trees as replicates.
RESULTS
RELEVANCE OF INFESTED FRUIT IN THE DIET OF BLACK HOWLER
GROUPS.—Black howlers ate infested fruits of all three species. Although I was not able to assess whether black howler monkeys
selected or avoided infested fruits, I suggest that they ate them in
473
proportion to their availability in the tree, as percent infested fruits
per tree was high and I did not observe any behavior that indicated
detailed visual or olfactory inspection of fruits. From the total of
feeding records (N = 2205) 31 percent were on fruits of species
that exhibited high levels of insect infestation of the fruit crops.
Species with insect-infested fruits were only three of the more than
25 food items in black howler monkey diets (Table S1). In each of
the sampled periods, however, fruits of these species were three of
the most important items eaten by black howlers, with percent consumption reached only by Inga verna flowers and A. inundata new
leaves, other insect-infested items, both consumed in November
1998. These results support hypothesis one regarding the relevance
of insect-infested fruits in the diet of black howler groups that
inhabit the Paraná islands in Argentina.
In general, fruits were eaten in similar proportion by the two
groups of howlers studied. There were only two occasions when percentages were different. In July 1998, consumption of O. diospyrifolia was about 16 percent lower for Group I, and in February 2000
consumption of E. punicifolia was about 20 percent lower for the
same group (Table S1). This low proportion of fruits was eaten
because Group I lost access to fruiting trees as it was displaced by
Group II. Infested fruits of B. arguta were eaten less often than the
other two species (Table S1).
INSECT INFESTATION.—All trees of the three species used by black
howlers to forage had infested fruits. The percentage of fruit infested
by tree varied between species. Thirty five percent of O. dispyrifolia
fruits from trees used by Group I (N = 50) and 82 percent from
trees used by Group II (N = 50) were infested. I found only one
larva per seed of at least two curculionid species in seeds of O.
diospyrifolia (the most abundant being Heilipus sp.). Larvae were
absent in fruit pulp because adults of these curculionid species place
the egg directly within the seeds. The complete development of
the larva takes place inside the seed; the larva consuming the entire
cotyledons and embryo. The pupa then developed within the seed
when there was no more endosperm, and adults emerged 3 mo after
seeds were collected. So, the percentage of endosperm consumed
depended on larval development stage (Fig. 1; τ = 0.88, df = 64,
P < 0.0001). Seeds did not appear externally damaged except for
the small oviposition puncture.
Mature fruits of E. punicifolia remained on each tree for only
2–3 d, but due to the small differences among trees in time of fruit
maturation, mature fruits were available in the forest for about one
week. Fruits of E. punicifolia were infested by insects at maturation;
eggs were deposited in the fleshy pulp and the larvae moved into
the seed afterwards. Eighty-six percent of fruit were infested by
1.9 ± 0.6 larvae/fruit (N = 200). I observed in the field that the
endosperm of these seeds could be completely consumed.
Approximately half (49 ± 3%) of the seeds of B. arguta from
all fruits collected (N = 200) were infested by one wasp. Eggs were
placed within the seeds when fruits were still immature. The shape
of the infested seeds was different from that of healthy ones. Wasps
were able to complete development before fruit maturation, eating
the entire cotyledons and embryo at the larval stage.
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Bravo
wasps emerged. In addition, the seeds from which these parasitoids
emerged germinated.
As mentioned above, infested seeds of B. arguta did not
germinate because they were destroyed by wasps before reaching
maturity.
DISCUSSION
FIGURE 1.
Correlation between Heilipus sp. developmental stage and en-
dosperm of Ocotea diospyrifolia seeds consumed. Values of developmental stage
represent 1 = egg, 2 = small larva, 3 = big larva, 4 = pupa. Larvae, which were
50 percent smaller than prepupae (ca 5 mm), were classified as small. Numbers
in parentheses indicate the number of seeds represented by each point.
INGESTION EFFECT ON LARVA AND SEED FATE.—Only 8 percent
(N = 167) of larvae infesting O. diospyrifolia seeds survived passage
through the digestive tract of howlers, the rest of the seeds contained
dead larvae. Consistent with hypothesis two, ingestion by black
howlers destroyed most of the curculionid larvae without affecting
the seed embryo. Healthy O. diospyrifolia seeds taken directly from
trees (53 ± 27% and 61 ± 23% for each group) germinated at a
similar rate as seeds from faeces (55 ± 25% and 64 ± 20% for each
group; U = 972.5, P = 0.77, N 1 = N 2 = 45 and U = 989.5, P =
0.85, N 1 = N 2 = 45), which included healthy and infested seeds
with dead larvae, and a low proportion of infested seeds with living
larvae.
Larvae were not observed in E. punicifolia seeds from faeces.
However, contrary to hypothesis two, in April 2000 the seeds of this
species were completely empty (probably devoid of endosperm)
in old faeces. So, larvae infesting E. punicifolia were affected by
digestion only at an early stage of development when larvae were
located in the pulp, before burrowing into the seeds. Even though
wasps infesting B. arguta seeds died after ingestion by black howlers,
there was no endosperm or embryo left in these seeds, thus resulting
in complete germination failure.
THE EFFECT OF INSECT INFESTATION ON GERMINATION.—Twenty
two percent (± 3%) of the infested seeds (N = 722) and 44 ±
4 percent of healthy seeds (N = 598) of O. diospyrifolia germinated
in laboratory studies, thus supporting hypothesis three (t = 3.55,
df = 28, P = 0.001). Braconidae wasps emerged from 1.4 percent
of the infested seeds of O. diospyrifolia 1 mo after seed collection,
while Heilipus sp. adults emerged about 2 mo later. No Heilipus
sp. were observed to emerge from seeds from which Braconidae
Results from the three plant species studied supported hypothesis
one and three: fruits were important dietary items of black howler
monkeys, and pulp and seeds of at least three of the most important fruiting trees eaten were infested with insects. Insect infestation
also had a negative effect on germination of all three trees species
examined. Results from only one of the three fruiting species, O.
dispyrifolia, were fully consistent with hypothesis two, which predicted that digestion by black howlers kills larvae and increases the
potential for germination. As observed in a previous study (Bravo
& Zunino 1998), in which black howler digestion killed 90 percent
of larvae present in the seeds of O. diospyrifolia, passage through the
howler’s digestive tract killed the insects; in addition, according to
the laboratory trials of the present study, seed germination was not
affected. However, the benefit that passage through the digestive
tract of black howlers had for seeds of O. diospyrifolia was inversely
proportional to the period of time that infested fruits remained
on the tree. The longer a fruit is in the tree, the smaller will be
the residual endosperm in the seed. As black howlers consume the
fruits since their maturation until they disappear from the trees,
the balance of this relationship between O. diospyrifolia and black
howlers changes over time. The effect of black howlers is most
beneficial for the plant when fruit are removed soon after infestation. At the end of larval development, the relationship is beneficial
only for black howlers, because larvae are larger, whereas very little
endosperm remains and the seed is not viable. Fruit consumption
during this last stage then, may contribute little to the reproductive
fitness of the trees as dispersed seeds have little chance of survival
after germination.
Infested O. diospyrifolia seeds that were not consumed by black
howlers had a relatively low chance of germination (22%); noninfested seeds had a significant higher percentage of germination in
laboratory test. Most species of Braconidae family are parasitoids
(Borror et al. 1989, Godfray 1994) so, the wasps that emerged from
infested O. diospyrifolia seeds may also have facilitated germination
by killing Heilipus sp. larvae at an early stage, before the embryo
was affected.
Many infested E. punicifolia fruits, which are removed from
trees in high proportion by black howlers (Bravo 2003), had larvae
killed by howler ingestion, consistent with hypothesis two. However,
observations in the field suggest that once larvae moved into the
seeds at the end of the fruiting period, they were not damaged by
black howler digestion. So, contrary to second hypothesis, at the
end of the fruiting period black howlers could be spreading insect
infestation, as toucans and thrushes spread larvae that infest Eugenia
sp. in southeastern Brazil (Guix & Ruiz 1995).
Insect-Infested Seed Ingestion and Dispersal
In contrast to the expectation from hypothesis two that passage
through the black howler digestive tract will increase the proportion
of infested seeds germinating, digestion had a neutral effect on seeds
of B. arguta because, even if wasps die, they have already eaten all
the endosperm by the time of fruit removal. The dispersal of these
seeds does not affect the dispersal probability of healthy seeds found
in the same fruit (ca 50% of seeds of all fruits were infested). The
proportion of B. arguta fruit removed by black howlers from trees
was considerably lower than for O. diospyrifolia or E. punicifolia
fruits. When B. arguta trees were fruiting they were not visited by
howlers on a daily basis (as they did with the other two species). For
example, during the weeks sampled in July 1998 and November
1998 only one of the howler groups used the fruiting trees. Birds
may play a more important role as seed dispersers for B. arguta than
howlers since more birds were observed feeding on fruits of this
species than on the other two species.
A similar three-way interaction was studied between Acacia
spp., large mammalian herbivores, and bruchid beetles. Seeds ingested by African herbivores were scarcely infested because seeds
were consumed prior to infestation by bruchids, which in this case
take place on the ground, and because seed ingestion may kill
bruchid larvae in an early stage of development (Or & Ward 2003).
The first factor, ingestion before infestation, is similar to the mechanism reported here for E. punicifolia fruits and also similar to the
tapir–palm–bruchid beetle interaction found in Brazil, where tapirs
disperse palm seeds over long distances before they are infested by
bruchids (Silvius & Fragoso 2002, Fragoso et al. 2003). The second
factor, larvae killed by mammal ingestion, is similar to the mechanism reported here for O. diospyrifolia infested seeds. However,
the difference is that black howler ingestion kills larvae infesting O.
diospyrifolia seeds at any stage of development. Acacia seeds with
larvae at a late stage of development can be destroyed during digestion because tunneling larvae may weaken the seeds (Coe & Coe
1987). This is a mechanism similar to the one reported here for B.
arguta infested seeds and passage through digestive tract of black
howlers. The destruction of infested seeds by herbivore ingestion
may depend on the ratio between seed size and the size or number
of beetles developing in one seed, because hollow seeds are easily
destroyed (Or & Ward 2003). This ratio may also help explain why
B. arguta infested seeds were destroyed by black howler digestion,
while O. diospyrifolia survived without damage, and larvae at a late
stage of development inside E. punicifolia seeds were not killed by
black howler ingestion.
Studies on Acacia seeds (A. raddiana, A. pachyceras) demonstrated that bruchid infestation affects germination, as reported
here comparing infested and healthy O. diospyrifolia seeds (Or &
Ward 2003). From scanning electron microscope photographs Coe
and Coe (1987) deduced that ingestion by large herbivores was
necessary to scarify the testa of Acacia seeds, allowing water to enter
and stimulate germination. The increase in germination of ingested
O. diospyrifolia seeds was due only to elimination of larvae during
black howler digestion and did not imply any scarification, because
healthy seeds from trees germinated in the same proportion than
ingested seeds collected from black howlers faeces.
475
In summary, black howler monkeys ingest a high proportion
of insect-infested fruits. Insect infestation has a negative effect on
germination of the three species studied, but passage through the
guts of black howlers affects larval survivorship, although its effects
varies among the three tree species. Passage of O. diospyrifolia seeds
through black howler guts kills most of the larvae and enhances seed
germination. However, at the end of larval development seeds had
no chance to germinate. Larvae of infested E. punicifolia fruits were
killed during digestion early in the fruiting season, when they were
located in the pulp, but not later, when the larvae had moved to
the seeds. Banara arguta fruits contained both healthy and infested
seeds, the latter being destroyed during digestion while the former
were dispersed. Black howlers may play an important ecological role
by ingesting infested fruits and dispersing their seeds, triggering a
series of species-specific indirect effects with seeds and insects. This
could result in the: (1) dispersion of healthy seeds; (2) spread of
larvae; or (3) destruction of infested seeds; depending at which
time fruit is consumed by black howlers in relation to when insect
infestation occurred, and probably also by the hardness of the seed
coat as well as the seed-insect size ratio.
ACKNOWLEDGMENTS
I thank A. Bachman for help with arthropod determination, G. Pirk,
P. Garber, B. Loiselle, V. Cueto, F. Milesi, G. Goldstein, the editors,
and two anonymous reviewers for their valuable comments on the
manuscript, and the several students who participated as field assistants. I am especially grateful to Mr. Gallo and Titina Gallo for their
logistic support in the field. This study was funded by CONICET
and IFS (International Foundation for Science D/2686–1).
SUPPLEMENTARY MATERIAL
The following supplementary material for this article is available
online at: www.blackwell-synergy.com/loi/btp
TABLE S1. Percentage of feeding records on each food item recorded in
the diet of black howlers when species with insect-infested fruits were
fruiting.
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