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Revista Chapingo serie ciencias forestales y del ambiente

On-line version ISSN 2007-4018Print version ISSN 2007-3828

Rev. Chapingo ser. cienc. for. ambient vol.21 n.3 Chapingo Sep./Dec. 2015 

Individual variance in the attributes of Clusia salvinii Donn. Smith associated with the attraction of frugivores in the dispersal of fruits and seeds


Variación individual en atributos de Clusia salvinii Donn. Smith asociados a la atracción de frugívoros en la dispersión de frutos y semillas


Hermilo Sánchez-Sánchez1; Javier Manjarrez1; César A. Domínguez-Tejada2; Alina Morquecho-Contreras3*


1 Centro de Investigación en Recursos Bióticos, Facultad de Ciencias, Universidad Autónoma del Estado de México. Instituto Literario núm. 100, col. Centro. C. P. 50000. Toluca, Estado de México, MÉXICO.

2 Instituto de Ecología, Universidad Nacional Autónoma de México. Circuito exterior s/n, Ciudad Universitaria. C. P. 04510. Coyoacán, México, D. F.

3 Facultad de Ciencias Agrícolas, Universidad Autónoma del Estado de México. Instituto Literario núm. 100, col. Centro. C. P. 50000. Toluca, Estado de México. Correo-e: Tel.: +52 (722) 2965553 (*Autora para correspondencia).


Received: February 4, 2015.
Accepted: August 17, 2015.



Seed dispersal is one of the processes of plant-frugivore interactions that involves characteristics specific to the plant effecting the attraction of frugivores. In this paper, the individual variance in the attributes of Clusia salvinii in relation to the attraction of frugivores and its effect on the dispersal of fruits and seeds in the Reserva de Nanchititla, State of Mexico was studied. The morphometric characteristics of 25 trees of the C. salvinii species were evaluated (height, coverage, number of fruit, number of seeds per fruit, and fruit below the canopy). The removal of fruits and seeds (dispersal) was also estimated, as well as some of its attributes as estimators of the quantity of biomass assigned to the reproduction or as compensation for the dispersers (average weight per tree, average weight of the arils per tree). According to the results, tree height and harvest size or fruit production have an effect on the removal of seeds. On the other hand, the mass of the fruit, aril and seed had no relation to the removal of the fruit. Tree height and the quantity of fruit play an important role in the attraction of dispersers.

Keywords: Reproduction, descent, removal of fruits and seeds.



La dispersión de semillas es uno de los procesos de las interacciones planta-frugívoro que involucra características propias de la planta con efecto en la atracción de los frugívoros. En este trabajo se estudió la variación individual en los atributos de Clusia salvinii, relacionados con la atracción de frugívoros, y su efecto en la dispersión de frutos y semillas en la Reserva de Nanchititla, Estado de México. Las características morfométricas de 25 árboles de C. salvinii fueron evaluadas (altura, cobertura, número de frutos, número de semillas por fruto y frutos bajo las copas). También se estimó la remoción de frutos y semillas (dispersión) y algunos de sus atributos como estimadores de la cantidad de biomasa asignada para la reproducción o como recompensa para los dispersores (peso promedio por árbol, peso promedio de arilos por árbol). Acorde con los resultados, la altura de los árboles y el tamaño de la cosecha o producción de frutos tienen efecto sobre la remoción de semillas. Por otra parte, la masa del fruto, del arilo y de la semilla no presentó relación con la remoción de frutos. La altura de los árboles y la cantidad de frutos juegan un papel importante en la atracción de dispersores.

Palabras clave: Reproducción, descendencia, remoción de frutos y semillas.



The dispersal of fruits and seeds plays an important central role in ecology and plant evolution; it is a crucial point in the subsequent states of the life cycle (Alcántara & Rey, 2003; Wang & Smith, 2002; Willson & Traveset, 2000). Some studies have shown that certain characteristics of plants, such as size and weight of the fruit, serve as critical signals to attract dispersers (Alcántara & Rey, 2003; Valenta et al., 2013). According to Willson and Traveset (2000), the variance in the morphometric characteristics, such as weight of the fruit and weight of the arils, as well as the number and weight of the seeds, can have an effect on the dispersal. In this manner, it could be expected that the frugivores visit with higher frequency plants with more attractive fruit because of their visibility and abundance, and thus manage to disperse a greater number of seeds (Carlo, Collazo, & Groom, 2003; Jordano, García, Godoy, & García-Castaño, 2007).

In the context of dispersal, the intra-specific variance on the characteristics of the fruit is of great importance, if this variance affects the behavior of the dispersers (Rey, Gutiérrez, Alcántara, & Valera, 1997). Consequently, animals that consume fruit and disperse the seeds could constitute a strong selective pressure of great evolutionary importance for the dispersal plants (Rosenthal & Berenbaum, 2012). Hence, it is possible that the individuals of a community of plants manifest "competition" in being dispersed (Rosenthal & Berenbaum, 2012). Various studies have related plant characteristics with the attraction of frugivores (Jordano, 2000; Mack, 1993; Schupp, 1995), trying to understand significant levels of phylogenetic inertia between the characteristics of the fruit and vertebrates (Jordano, 1995; Jordano et al., 2007), or the importance of the dispersers as dispersal agents (Cipollini & Levey, 1997; Fuentes, 1992). Nevertheless, there is little information that supports the importance of individual variance in the plant characteristics involved in the dispersal process, following an adaptive approximation of attraction to the frugivores (Nathan & Muller-Landau, 2000). This paper explored the adaptive meaning of the individual variance on the morphometric characteristics of trees and fruits of Clusia salvinii Donn. Smith (cinnamon flower or guayabillo), related to the attraction of frugivores and their effect on the dispersal process of fruits and seeds. It is considered that C. salvinii species fulfills an important ecological function as a nursing plant for other species that inhabit the ecosystem (Lüttge, 2007).



Site of study

The study was developed in the Reserva de Nanchititla, State of Mexico (100° 15' - 100° 37' WL and 18° 46' - 19° 02' NL). The region is characterized for having a semi-warm, sub-humid climate with rain in the summer. The average temperature is 20 °C and the average yearly precipitation is 1,130 mm, greatest in the month of June. The vegetation is characteristic of a mixed pine-oak forest with small areas of riparian vegetation and tropical deciduous forest (Casas-Andreu & Aguilar-Miguel, 2005).

Characteristics of C. salvinii

Clusia salvinii is a dioecious tree 5 to 14 m tall with a distribution from Mexico to Panama in cloud and evergreen forests at a height of 900 to 2,000 m (Mats, Gustafsson, Winter, & Bittrich, 2007); the tree is plentiful in the riparian forest of the Reserva de Nanchititla, Estado de Mexico. The reproduction of C. salvinii starts in the second half of the rainy season with the appearance of flower buds on feminine trees and three weeks later on the masculine trees (Aguilar-Rodríguez & Castro-Plata, 2006). The flowers are white and aromatic, produce nectar, and are mainly pollinated by bees and wasps (Lemes-Martins, Wendt, Margis, & Scarano, 2007). The fruit develops during the dry season of the following year. They are globule and five to seven orange arils which contain the seeds form inside the fruit. The fruit adjusts to an ornithochory syndrome in which birds mainly consume the arils; nevertheless, it has been observed that mammals frequently consume fruit and arils that detach from the fruit and are later consumed by ants (Lemes-Martins et al., 2007). Likewise, damage done by herbivores has been observed on the leaves of seedlings and adult trees, as well as predation pre-dispersal due to insect larvae inside the fruit.

Evaluation of the morphometric characteristics of trees and fruits of C. salvinii

During the spring and summer of two consecutive years, 25 trees from the Reserva de Nanchititla were selected. The trees' height and coverage (m2, area of an ellipse) were measured by trigonometric estimation utilizing a Brunton compass (Rossbach model BBC-90, Mexico). Only the most accessible trees with fruit within the riparian forest of the reserve were considered. The trees were separated by an average distance of 282.6 ± 131.1 m (range of 91 to 516 m). In each tree, the number of fruit produced was counted (harvest size) from the start (November) until the end of maturity (June). The average weight of the fruit, arils and seeds (per fruit per tree) was determined for each tree. The evaluated characteristics of the fruit were considered estimators for the quantity of biomass that a plant assigns for its reproduction or as compensation for the dispersers.

Removal of the fruits and seeds of C. salvinii

From the start to the end of maturity of the fruit, dispersal was estimated through the calculation of the difference of total fruit produced per tree and the fruit that fell below the canopies (considered non-dispersed fruit). The fruit not found below the canopies or on the tree was considered as having been removed or transported by some disperser; however, this estimation does not consider the possible embryo mortality by the same removers or dispersers. From a 10 % sample of the fruit taken from each tree, the average number of seeds per fruit was estimated and multiplied by the number of fruit produced, for the end result of estimating the approximate size of the total harvest of seeds produced per individual. The removal of seeds was quantified in a manner analogous to the fruit dispersal. The removal of fruits or seeds from each tree was estimated in terms of number and percentage; the percentages were comparable with the total quantity of fruits or seeds produced in proportional terms.

Relation of the individual variance and the dispersal of fruits and seeds

With the objective of defining which attributes of the trees are associated with seed dispersal, a linear regression analysis was carried out to determine which morphometric characteristics of the trees are related to the harvest size, as well as the quantity and percentage of removed fruits and seeds. Furthermore, a second linear regression analysis was implemented to determine which attributes of the fruit (mass and arils per tree) correlate with the number and percentage of the removal of fruits and seeds. All the statistical analyses were carried out with the software STATISTICA 8.0 (Weiβ, 2007) with a P = 0.05 value.



Individual variance of C. salvinii and harvest size

The C. salvinii trees showed great variance in the morphometric characteristics. Table 1 shows the results of height, coverage, and reproductive attributes (harvest size, fruit mass, and seeds).

The linear regression analysis showed that 28 % of the variance in size of the fruit harvest is explained by elevation (P = 0.012, R2 = 0.286; Figure 1) and 33 % by coverage (P = 0.002, R2 = 0.336; Figure 2), which indicates that larger trees tend to produce a greater quantity of fruit. The taller tree height exposes the fruit to a greater extent by protruding from a homogeneous arboreal layer in its elevation, being more visible and, therefore, more attractive to the frugivores (Carlo et al., 2003). It is possible that tree height facilitates the foraging of some frugivores such as birds, which act as selective agents in seed dispersal (Rey et al., 1997). On the other hand, it was found that 48 % of the variation in the mass of the seeds (P = 0.0001, R2 = 0.4815) is explained by the mass of the fruit, which suggests that when the mass of the fruit is greater, the seed content is higher.

Harvest size of the fruits and seeds of C. salvinii

In total, 2,054 fruits were produced in the population studied during the sampling months. The fruits that fall outside the canopies of the progenitors are considered as having been dispersed and correspond to only 27 % of the total harvest (Figure 3). On the other hand, the total number of seeds calculated for the population was 69,023; of this figure, 60 % corresponds to the category of dispersed seeds. The discrepancy between the reported removal values for fruits and seeds is due to the fact that a large part of the seeds is removed or consumed by frugivores (Jordano et al., 2007), leaving the rest of the fruit on the parent plant.

The harvest size or the quantity of fruit produced by a single plant can influence seed dispersal. It would be expected that the plants that produce more fruit increase the probability of being dispersed (Jordano et al., 2007; Willson & Traveset, 2000). Nevertheless, the results of the relation between removed fruit and harvest size of C. salvinii showed a "diminished returns" behavior (Charnov, 1976; Rodríguez-Martínez, 2010); i.e., the number of removed fruit increases in function to the harvest size up to the point of saturation where it is probable that the fruits no longer disperse in their totality. This hypothesis is supported by our results of C. salvinii, as the removal of the number and percentage of fruits and seeds shows that when the harvest is small, the majority of the fruit produced are removed, and as it increases, the removal of the fruit decreases. Therefore, the individuals of C. salvinii with a very large harvest size are at a disadvantage with regard to individuals with a small harvest size.

Removal of fruits and seeds

The variation of the individual reproductive characteristics of the trees could act as a factor for the frugivores to select the fruit to consume and, therefore, constitutes a source of selection (Alcántara & Rey, 2003). In order to evidence this relation, the variance of the individual reproductive characteristics of the trees was analyzed (Table 1) and, subsequently, the effect of such variance on the removal of fruits and seeds. The analysis of the dispersal of fruits and seeds indicates that only the height of the tree partially explains (24 %) the fruit dispersal (P = 0.012, R2 = 0.246). This relation suggests that the tallest individuals of C. salvinii disperse a greater number of fruit (Figure 4), possibly because the trees that reach greater heights manage to expose their fruit in such a form that results in them being more visible and attractive to the frugivores (Fruit removed = 7.84 [height] - 31.86). The coverage did not show a relation with the dispersal of fruits and seeds.

The harvest size (fruits and seeds) only explained 17 % of the removal of the fruit, but in the case of the seeds, it explained 88 % of the removal (fruit: P = 0.039, R2 = 0.172; seeds: P = 0.0001, R2 = 0.8794). This high percentage of seed removal suggests that although the removal of the fruit is relatively low, the number of seeds removed is much higher. In Figure 5, a logarithmic curve can be graphically observed [Fruit removed = 3.013In (harvest size) - 1.636], which shows that in the trees with greater harvests a greater number of fruit is removed; however, the relation reaches a maximum threshold and stabilizes. The plants with large harvests possibly have the potential to disperse more fruits and seeds; however, it is likely that the selection pressures act against the plants that increase the size of the unrestrictedly produced harvest (Nathan & Muller-Landau, 2000).

No relation was found between the percentage of fruit and seed removal with the harvest size, but there was a relation in the absolute number, which indicates that the plants with large harvest size disperse more fruits or seeds; however, in relative terms they disperse a slightly lower proportion.

The dispersal did not depend on the attributes related to the reproduction of the fruit. The fact that the individual variance of the reproductive attributes such as the mass of the fruit, aril, and seed show no relation with the removal of fruit, suggests that the attraction of frugivores does not depend on these characteristics. This can also be interpreted as a selection in function of the quantity and not the quality of the fruit or that possibly they are characteristics that the frugivores do not select in function of the dispersal (Alcántara & Rey, 2003; Jordano et al., 2007), at least under the current ecological scene in which our study was carried out.

The dispersal of C. salvinii seeds by frugivores can be interpreted as a determinant process ofthe establishment of new individuals. The process depends on some characteristics of the trees such as height and harvest size and is independent on the characteristics of the fruit (attributes) or variances in the compensation for the dispersers. This explanation can be of great importance by explaining the adaption tendencies (Alcántara & Rey, 2003). Our analysis suggests that a high variance in seed dispersal, as shown by the elevated value of the standard deviation with regard to the average number of seeds (Table 1). The relation between the fruit dispersal and some characteristics of the plants poses the hypothesis that the evolution of such plants is the combined result of the pressure that the dispersers have exercised, in order to maximize the height or harvest size with other factors that favor dispersers.

It is possible that other characteristics of the fruit (reproductive attributes not evaluated in C. salvinii) are involved in the attraction of the frugivores and that they show a relation with the dispersal as could be the nutritional quality or some others, such as the color and form, which could be selected in function of the dispersal. At any rate, in C. salvinii, the harvest size (number of fruit) could be considered the sole characteristic related to the attraction of frugivores. It is possible that the frugivores are attracted by trees that can offer a greater resource (trees with larger harvests); however, the frugivores show a maximum limit of fruit removal in trees with very large harvests.



The individual variance in the height of C. salvinii trees is positively related to the quantity of removed fruit. The harvest size shows a relation with the removal of fruits and seeds; therefore, it is possible that a larger portion of the seeds is dispersed than that of the fruit taking into account the harvest size. The plants that produce small harvests manage to disperse all of their fruit unlike those that produce large harvests, which show the "diminishing returns" effect.



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