Color and odor of artificial fruit used to signal potential dispersers in the Atlantic forest in Brazil

Abstract

Fruit color and odor are the main features regulating the rate of fruit predation and dispersal. The aim of this study was to analyze the effect of odor and color on fruit predators and dispersers. The present study was conducted in a 30ha area of secondary forest in Southeastern Atlantic Brazil. This area was divided into two transects, in which four points were marked with a 30m distance from each other. Each sampling point contained a total of 30 artificial fruit which belong to six different treatment groups, with five artificial fruit per group. Each group was randomly placed on the ground and that artificial fruit was checked every seven days. For each group of five fruit, 5mL of essence (vanilla or pineapple) were placed, and no essence was used in the control group. Artificial fruit was made with green and red nontoxic modeling clay, as well as artificial essences (vanilla and pineapple). A total of 960 fruits were used. Predated fruit equaled 26.9% (258 units), from which the red/pineapple had the highest predation rate (81.9%), followed by red/vanilla (46.3%), while green/control fruits were not predated. Throughout the experiment, bitten fruit and pecked fruit equaled 58.3% and 41.7%, respectively. No significant differences were recorded (x2=7.57, df=5, p=0.182) between bitten and pecked fruit. Fruit color and odor are important in attracting predators and dispersers, which explains the high rate of predation of red/ vanilla and red/pineapple, and the absence of predated fruits in the green/control group. Regarding the potential disperser, there was no statistically significant difference between pecked fruit and bitten fruit. As a result, it should be taken into consideration that zoochory (mammalochory and ornithochory) is the most important dispersal; therefore, it should be concluded that birds are more attracted by color and mammals by odor.

Full text

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Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 60 (2): 925-931, June 2012
Color and odor of artificial fruit used to signal potential dispersers
in the Atlantic forest in Brazil
Aliny Oliveira Barcelos1, Clayton Perônico2 & Frederico Jacob Eutrópio3
1. Universidade Vila Velha, Programa de Mestrado em Ecologia de Ecossistemas-Rua Comissário José Dantas de Melo,
21, Boa Vista, Vila Velha, Espírito Santo, Brazil, CEP 29102-770; oliveira.aliny@gmail.com
2. Instituto Federal do Espírito Santo – IFES campus Piúma - Rua Augusto Costa de Oliveira, 660, Praia Doce Piúma,
Espírito Santo, Brazil, CEP 29285-000; cperonico@ifes.edu.br
3. Universidade Vila Velha, Programa de Doutorado em Ecologia de Ecossistemas-Rua Comissário José Dantas de Melo,
21, Boa Vista, Vila Velha, Espírito Santo, Brazil, CEP 29102-770; eutropiofj@gmail.com
Received 09-V-2011. Corrected 20-IX-2011. Accepted 19-X-2011.
Abstract: Fruit color and odor are the main features regulating the rate of fruit predation and dispersal. The aim
of this study was to analyze the effect of odor and color on fruit predators and dispersers. The present study was
conducted in a 30ha area of secondary forest in Southeastern Atlantic Brazil. This area was divided into two
transects, in which four points were marked with a 30m distance from each other. Each sampling point contained
a total of 30 artificial fruit which belong to six different treatment groups, with five artificial fruit per group. Each
group was randomly placed on the ground and that artificial fruit was checked every seven days. For each group
of five fruit, 5mL of essence (vanilla or pineapple) were placed, and no essence was used in the control group.
Artificial fruit was made with green and red nontoxic modeling clay, as well as artificial essences (vanilla and
pineapple). A total of 960 fruits were used. Predated fruit equaled 26.9% (258 units), from which the red/pine-
apple had the highest predation rate (81.9%), followed by red/vanilla (46.3%), while green/control fruits were
not predated. Throughout the experiment, bitten fruit and pecked fruit equaled 58.3% and 41.7%, respectively.
No significant differences were recorded (x2=7.57, df=5, p=0.182) between bitten and pecked fruit. Fruit color
and odor are important in attracting predators and dispersers, which explains the high rate of predation of red/
vanilla and red/pineapple, and the absence of predated fruits in the green/control group. Regarding the potential
disperser, there was no statistically significant difference between pecked fruit and bitten fruit. As a result, it
should be taken into consideration that zoochory (mammalochory and ornithochory) is the most important dis-
persal; therefore, it should be concluded that birds are more attracted by color and mammals by odor. Rev. Biol.
Trop. 60 (2): 925-931. Epub 2012 June 01.
Key words: frugivory, mammalochory, ornithochory, plant-animal interaction, predation, seed dispersal,
zoochory.
In plant communities, the dispersal syn-
drome deserves special mention, because of
the strong dependence of plants on dispersers
(Lomáscolo & Schaefer 2010). The survival of
a species depends on seed dispersal and a suit-
able place for germination. In tropical forests,
the most frequent dispersal syndrome found is
zoochory, i.e. fruits are eaten and dispersed by
animals. Mammalochory, dispersal by mam-
mals, and ornithochory, dispersal by birds, are
also found. It is estimated that between 50%
and 90% of tree species depend on this type of
dispersal (Howe & Smallwood 1982, Janson
1983, Fleming 1987, Tabarelli & Peres 2002,
Galetti et al. 2003).
The main characteristics that regulate the
predation rate of different groups of animals
include fruit size, color, odor, consistency,
quantity and nutritional quality (Gautier-Hion
et al. 1985, Galetti et al. 2003, Cáceres et al.

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2009). This causes fruits to develop a large
number of strategies and special characteristics
to attract consumer-dispersing species (Arruda
et al. 2008). Among these characteristics, color
and odor have shown to be important fruit
detection attributes for predators (Schmidt et
al. 2004, Lomáscolo et al. 2008). However, the
contrast between fruit color and its background
had never been included in any study on disper-
sal syndromes (Lomáscolo & Schaefer 2010).
Few studies have recently examined the
direct effect of fruit odor and color, or the
interaction between these factors, upon the
rate of removal and/or predation by different
consumer groups. This study aimed to test the
effect of fruit odor and color on the preda-
tion rate, as well as to relate it to the different
groups of predators/dispersers.
MATERIALS AND METHODS
Study site: The Atlantic Forest is one of
the most threatened ecosystems on the planet,
retaining only 8% of its original area (Myers et
al. 2000, Galindo-Leal & Câmara 2005). The
study was conducted in the municipality of
Marechal Floriano, Espírito Santo State. The
study area (20°26’32” S - 40°464’4” W) is
located 720m above sea level and covers 30ha
of secondary Atlantic Forest, with 90 years of
regeneration. In the Serra do Mar region, the
Atlantic Forest has sub-humid climate, poor
soil and high rainfall (Tabarelli et al. 2005).
Data collection: Four samples were taken
between November 2009 and January 2010
with 15 day-intervals. Each sampling was
conducted in two 100m equidistant linear tran-
sects, parallel to the forest edge. Four sampling
points were established for each transect, at
30m distance (Álvarez & Galetti 2007). A total
of 30 fruits with six randomly disposed treat-
ments were arranged at each sampling point,
i.e. five fruits per sample group. Artificial fruits
were placed on the ground to analyze which
ones remained visible after seven days and the
types of animals that forage for them. New
fruit was employed in each new sampling. Five
milliliters of essence (vanilla or pineapple)
were placed in each group of five fruits, and
no essence was used for the control groups.
Artificial fruit was made using 5g (2cm in
diameter) of green and red starchy, nontoxic,
odorless, water-resistant modeling clay, for
a total of 960 artificial fruits by the end of
the samplings (Arruda et al. 2008). Fruit was
considered predated when it was moved from
where it was placed.
Potential predators of artificial fruit were
identified based on Alves-Costa & Lopes
(2001) and França & Marini (2009), where
“V” or “U” shapes characterized bird pecking
and teeth marks characterized as mammalian
bites. Disposable gloves were used at all times
to avoid the interference of human odor on
predators/dispersers´ behavior.
Treatments were compared using Kruskal
Wallis (p<0.05) and Tukey’s nonparametric
tests (p<0.05). Contingency tables (chi-square
p<0.05) were used to evaluate whether the num-
ber of artificial fruits pecked or bitten was the
same for each one of the treatments (Zar 2008).
Values of predated fruits per treatment were
expressed as a mean and as standard deviation.
RESULTS
Of the 960 artificial fruits used in the
experiment, 258 (26.9%) were predated. Con-
sidering the predation rate on the artificial
fruit per treatment, the red/pineapple treat-
ment had the highest predation rate (81.9%),
followed by red/vanilla (46.3%), while green/
control fruits were not predated (Table 1). The
mean of fruit predation was higher with red/
pineapple (4.1±0.78) followed by red/vanilla
(2.3±0.47) (Fig. 1).
Throughout the experiment, pecking
(41.7%) and bites (58.3%) were recorded
but no significant differences were detected
(x2=7.57, gl=5, p=0.182). The red/control treat-
ment registered only pecks, and for the green/
control treatment no predated fruits were found
(Fig. 2 and 3).

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TABLE 1
Total number of fruits, predated fruits and predated fruit percentage for each color/odor treatment
Treatment Fruit (N) Predated fruit Predated fruit (%)
Red/Pineapple 160 131 81.9
Red/Vanilla 160 74 46.3
Red/Control 160 14 8.8
Green/Pineapple 160 34 21.3
Green/Vanilla 160 5 3.1
Green/Control 160 0 0
Fig. 1. Mean of predated fruits per color/odor treatment. Letters indicate significant differences between treatments using
Kruskal Wallis and Tukey’s tests (p<0.05).
6
5
4
3
2
1
0
Mean predated fruits
a
a
b
b
bb
Red/Pineapple
Red/Vanilla
Red/Control
Green/Pineapple
Green/Vanilla
Green/Control
Fig. 2. Marks left by possible fruit predators: (A) Birds. (B) Mammals (rodents) and (C) Mammals.

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DISCUSSION
The results of this study show that fruits
with red color were more frequently eaten
by birds. This finding is in concordance with
Arruda et al. (2008) who found that among the
263 pecked fruits 62.2% were red. In addition,
studies in Peru and Costa Rica by Wheelwright
& Janson (1985) pointed out that 36% of the
fruits pecked were red. This preference for red
was also observed in the field by Gervais et al.
(1999) and Alves-Costa & Lopes (2001) and in
captivity by McPherson (1988) and Willson et
al. (1990). The cryptic color of fruit functions
mainly to attract the attention of potential dis-
persers that use vision as the key sense to search
for food, influencing the selective pressure by
birds at foraging (Wheelwright & Janson 1985,
Willson et al. 1990, Arruda et al. 2008).
Burns & Dalen (2002), Schmidt et al.
(2004), Schaefer et al. (2006) and Schaefer et
al. (2007) attribute birds´ preference for red
fruits to the contrast with the background foli-
age. Furthermore, the red color has a longer
wavelength, more visible to birds than other
colors (Arruda et al. 2008). However, accord-
ing to Pizo (2003), some birds prey less attrac-
tive colors, such as green, for another type of
dispersal; this was observed by Spironello et
al. (2004) who registered 3 910 unmoved fruits,
that is, 0.5% was predated in an immature
phase by parrots and rats.
The low predation rate of green fruit helps
understand the co-evolution between plants and
seed dispersers, where dispersed plants, mainly
by ornithocoric means, have immature green
fruits as a strategy to avoid dispersal of those
that are not yet ready to germinate (Schaefer
et al. 2007, Lomáscolo & Schaefer 2010). For
Burns et al. (2009) and Cazetta et al. (2007)
fruit color is related to the detection of potential
dispersers, and tropical regions generally have
higher diversity of fruit color, as they have the
highest number of seed dispersers due to the
increased plant diversity. In addition, Burns et
al. (2009) mention that the fruit color evolu-
tion hypothesis is not exclusively ascribed to
the selection of potential seed dispersers, since
there is no greater diversity of fruit color than
Fig. 3. Percentage of bites and pecks on predated fruit per color/odor treatment.
120
100
80
60
40
20
0
Predated fruits (%)
Pecks
Bites
Red/Pineapple
Red/Vanilla
Red/Control
Green/Pineapple
Green/Vanilla
Green/Control

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in the tropics where coloration may be associ-
ated to the reflective properties of leaves.
Birds have good vision and hearing, but a
poorly developed sense of smell, while mam-
mals have a sharper sense of smell, but not
good color definition, especially nocturnal spe-
cies (Lomáscolo et al. 2008); therefore, accord-
ing to Janson (1983), fruits eaten by nocturnal
species are probably large and odorous. The
results of this study indicating that 58.3% of
fruit was bitten differed from those of Arruda
et al. (2008), who reported 1.3% of the fruit
being bitten. However, Arruda et al. (2008) did
not use essences, which evidences smell as the
main sense of orientation in mammals and con-
firms the work by Vieira et al. (2011) and Iob &
Vieira (2008), who used vanilla extract in traps
to attract grid mammals having a high capture
rate, these being rodents, followed by marsupi-
als. Nevertheless, few studies have discussed
mammalian odor attraction in the process of
predation and dispersal of fruits.
Wheelwright & Janson (1985) and
Lomáscolo et al. (2008) reported that both
color and odor in fruits are important in attract-
ing predators and dispersers, which explains
the high rate of predation of red/pineapple and
red/vanilla and no predation of the green fruits
of the control treatment group. The abundance
of fruit, fruit predation rate and the presence of
predator/disperser can be influenced by the size
of the fragment, the edge effect (Galetti et al.
2003) and the regeneration state of the habitat
(Tabarelli & Peres 2002).
Treatments using essences showed a higher
percentage of bitten fruit, while treatments with
red color presented more pecking, although no
significant differences were observed between
pecked and bitten fruit, indicating that there
is no preference between birds and mammals.
For Gauthier-Hion et al. (1985), this dichotomy
between fruit dispersed by birds or mammals
is not strong, unlike aspects related to fruit
size, protection or color. Consequently, it is not
possible to specify the most effective potential
disperser of a plant species, only based on mor-
phological characteristics of the fruit.
Regarding the potential disperser, no sta-
tistically significant differences were found
between pecked fruit and bitten fruit, which
clearly suggests that both birds and mammals
are potential fruit dispersers, thus, indispens-
able elements in the dynamics of communities,
spatial distribution of plants, and structure and
restoration of degraded areas. The foregoing
confirms that zoochory (both mammalochory
and ornithochory) is the main dispersal meth-
od, although, in general, birds are more attract-
ed by color and mammals by odor. The use of
artificial fruit is a good study tool to analyze
potential dispersers that allows for the identi-
fication of species. This corroborates Arruda et
al. (2008), who confirmed that artificial fruits
are effective to record fruit consumption, assist
in the identification of potential dispersers, and
are easy to handle in the field.
In order to specifically determine the dis-
perser of a plant, further studies should be
conducted related to fruit color, size, nutritional
value and position, as well as animal character-
istics and fragment size, edge effects, species
composition and plant regeneration time.
ACKNOWLEDGMENTS
We would like to thank Cesar Abel Kroh-
ling for his help during fieldwork and his sup-
port on the logistics and Dominik Lenz and
Elieth Salazar for editing the English.
RESUMEN
El olor y el color de los frutos son las características
principales que regulan el nivel de consumo y la dispersión
de las semillas. Este estudio tuvo como objetivo analizar
el efecto que tiene el olor y el color de los frutos sobre los
depredadores y dispersores de semillas. El área de estudio
abarca 30ha de bosque secundario localizado en el Atlánti-
co sureste de Brasil. Este espacio se dividió en dos sectores,
en los cuales se marcaron cuatro puntos con una distancia
de 30m entre sí. En cada punto de muestreo se utilizaron
30 frutos que se distribuyeron en seis tratamientos, con
cinco frutos artificiales para cada tratamiento. Además,
cabe resaltar que cada tratamiento se colocó en el suelo de
forma aleatoria y que los frutos artificiales se verificaron
cada siete días. Para cada grupo de cinco frutos se utiliza-
ron 5mL de esencia (vainilla y ananá) y para el grupo de

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control no se utilizó ningún aditivo de olor. Los frutos se
confeccionaron con plastilina atóxica de color verde y roja,
además de esencias artificiales (ananá y vainilla), asimismo
se obtuvieron 960 frutos. El nivel de frutos consumidos fue
del 26.9% (258 unidades), de los cuales los rojos/ananá
fueron los más consumidos (81.9%), seguidos del rojo/
vainilla (46.3%), mientras que los verde/control no fueron
comidos. Durante el experimento la tasa de frutos mordidos
fue del 58.3% y de picoteados un 41.7%. No se registró
una diferencia significativa (x2=7.57, gl=5, p=0.182) entre
frutos mordidos y picoteados. El color y el olor de los
frutos son aspectos importantes para atraer depredadores y
dispersores, lo que explica los niveles de consumo de los
frutos rojos/vainilla y rojo/ananá y la ausencia de frutos
comidos en el tratamiento del verde/control. En cuanto
al potencial dispersor, no hubo una diferencia estadística
significativa entre frutos mordidos y picoteados, por lo
que se debe tomar en cuenta que la dispersión principal es
la zoocoria (ornitocoria y mamalocoria). Por lo tanto, se
puede concluir que las aves son atraídas por el color y los
mamíferos por el olor.
Palabras clave: frugivoría, mamalocoria, ornitocoria,
interacción planta-animal, depredación, dispersión de
semillas, zoocoria.
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