Reproductive success of Cabralea canjerana (Meliaceae) in Atlantic forest fragments, Brazil
Éxito reproductivo de Cabralea canjerana (Meliaceae) en fragmentos de bosque del Atlántico, Brasil
Edivani Villaron Franceschinelli1*, Roselaini Mendes do Carmo2*, Carlos de Melo e Silva Neto1, ]]>
1 & Leonardo Lima Bergamini3*
Abstract
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In Brazil, the Atlantic forest remnants have high biological diversity and a high level of endemism, but very little is known about the reproductive success of native species. Cabralea canjerana is a common tree in the Montane Atlantic forest, and its reproduction is highly dependent on pollinators. In order to contribute with the particular knowledge on this species, we collected data in three fragmented and three continuous forest sites, where the effects of fragmentation on both mutualistic (pollination) ]]>
C. canjerana produced more fruits (z-value=-8.24; p<0.0001) and seeds per fruit (z-value=-6.58; p=0.002) in the continuous than in the ]]>
C. canjerana in forest fragments. Rev. Biol. Trop. 63 (2): 515-524. Epub 2015 June 01.
En Brasil, los remanentes de bosque del Atlántico tienen una alta diversidad biológica y un alto nivel de endemismo, pero se conoce muy poco sobre el éxito reproductivo de las especies nativas. Canjerana cabralea es un árbol común en el bosque Atlántico Montano y su reproducción es altamente dependiente de los polinizadores. Con el fin de contribuir con el conocimiento particular de esta especie, se recogieron los datos en tres sitios fragmentados y tres de bosques continuos, donde se analizaron los efectos de la fragmentación ]]>
C. ]]>
produjeron más frutos (Z=-8.24; p<0.0001) y semillas por fruto (Z=-6.58; p=0.002) en el continuo que en los sitios fragmentados. Esto fue probablemente debido a las diferencias en la polinización, porque el número de visitas de polinizadores fue mayor en el bosque continuo que en los fragmentos. Por otro lado, el aborto de semillas (Z=4.08, p<0.001) y la depredación (Z=3.72, p=0.0002) fueron mayores en los sitios fragmentados que en los continuos. Entonces, las interacciones ]]>
C. canjerana en fragmentos de ]]>
Palabras clave:Cabralea canjerana, fragmentación del hábitat, interacción planta-polinizador, polinización por polilla, depredación de semillas, producción de semillas, producción de frutos.
Habitat fragmentation may disrupt plant-pollinator interactions by changing the abundance and/or the identity of floral visitors (Lovejoy, 1980; Roubik, 1993; Aizen, & Feinsinger, 1994a; Aizen, & Feinsinger, 1994b; Matheson, Buchamann, O’Toole, Westrich, & Williams, 1996; Murcia, 1996; Prach, Pysek, & Smilauer, 1997). Because floral visitors can differ in their ]]>
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Abiotic changes caused by habitat fragmentation may also affect the predation rate on plant reproductive structures owing to changes in the local animal community (Cunningham, 2000). Seed predation is an important ecological interaction that may directly impact plant fertility. In some cases, seed predators may cause abortion of the entire fruit (Greig, 1993). Seed predation by insects may change the recruitment rate and the abundance of the host plant (e.g., Jules, 1998; Louda, 1982). Several studies have investigated seed predation in fragmented landscapes and have shown ]]>
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Effects of habitat fragmentation on plant-pollinator interaction in the Neotropical region have been studied in the Argentinean Chaco (Aizen, & Feinsinger, 1994a; 1994b; Aguilar, & Galetto, 2004), in Mexico (Quesada, Stoner, Rosas-Guerrero, Palacios-Guevara, & Lobo, 2003; Quesada et al., 2004) and in Costa Rica (Cascante, Quesada, Lobo, & Fuchs, 2002). Few studies have been conducted in Brazil (Dick, 2001; Lopes, & Buzato, 2007; Dunley, Freitas, & Galetto, 2009; Elias et al., 2012; ]]>
2 extending from Northeastern to Southern Brazil. Now, only 7% of this area is covered with natural forest. The remnants of the original forest consist of many small fragments, several medium-sized tracts and a few continuous areas of forest ]]>
The present study aims to evaluate pollination, seed predation and reproductive success of plants of Cabralea canjerana subsp. canjerana (Vell.) Mart. in continuous and in isolated forest fragments of the Atlantic forest. This subspecies is a dioecious tree whose reproduction is highly dependent on pollinators. Forest fragmentation affects negatively the population density of C. canjerana (Santos and Ono, unpublished data). However, the effects of ]]>
Materials and methods
Study site: The study area is ]]>
Fig. 1). The predominant vegetation type is wet montane forest. The matrix surrounding the studied fragments is composed of small farms with pasture, potato and carrot fields. Few C. canjerana
trees occur in the surrounding matrix.
Three fragments (F1, F2 and F3) and three sites in the continuous forest (C1, C2 and C3) were sampled between October of 2001 to October of 2002 (Fig. 1, Table 1). The distances between sampling sites varied from 1.0 to 8.5km. These sites ]]>
C. canjerana trees. In general, continuous sites are better preserved than the fragments. C1 has experienced selective logging in the past; however, the present owner protects the area from any further disturbance. C2 appears well preserved but shows evidence of earlier selective logging. C3 appears better preserved than C2 and shows no evidence of recent logging. Two isolated fragments (F1 ]]>
Fig. 1), but F3 has been disturbed by selective logging and grazing. Such as expected, continuous forest sites were better preserved than fragmented ones.
Study species:Cabralea canjerana subsp. canjerana is a very common tree of the montane forests of Southern Minas Gerais State (França, & Stehmann, 2004), where plants can reach 25m tall. It is found in the forests of Central and South America. It has compound pinnate leaves and axillary to cauliflorous inflorescences. This species is dioecious, with white ]]>
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This species was selected because it is abundant in the study area; it occurs primarily in the forest understory and has cauliflory and large red fruits, making it easy to observe its flowers and fruits. The seed aril of C. canjerana is a very important food source for many species of birds and mammals (Pizo, ]]>
Measurements: In each site, all fruits of 25 plants of 7-11m tall were counted when developed but not yet opened. These plants were randomly selected, but trees located in forest edges were avoided. Seven fruits randomly selected from each of ]]>
Pollinator visit frequencies (number of visits in 30min) to C. canjerana subsp. canjerana flowers were recorded in two forest fragments (F1 and F2) and in two areas of the continuous forest (C1 and C2). Four randomly selected plants in each area were observed from 20:00 to 22:30h and from 04:00 to 06:30h. ]]>
C. canjerana (Carmo, 2005). Each time ]]>
C. canjerana (October and November). ]]>
To test if fragmentation affects C. canjerana reproductive success, we ]]>
C. canjerana as response variables and fragmentation status (continuous vs. fragmented landscape) as the predictor variable. In the models for fruit set, each individual plant ]]>
Results
Cabralea
canjerana produced on average 71.7 (±71.0) fruits in continuous forest and 18.5 (±18.3) fruits in fragments, which means 74% less fruits in the fragmented than continuous forest (z-value=-8.24; p<0.0001). The seed number per fruit followed the same pattern, with plants producing on average 6.2 (±1.5) seeds per fruit in fragments and 8.2 (±1.3) seeds per fruit in continuous forest; which means 23% less seeds set in fragments than in continuous forest (z-value= -6.58; p=0.002). However, there was no difference in mean fruit weight between ]]>
The average proportion of aborted seed per fruit was 0.62 (±0.25) in fragments and 0.23 (±0.15) in continuous forest. Therefore, fragments presented 2.1 times more aborted seeds (z-value=4.08, p<0.001) than continuous forest. The average proportion of predated seed per fruit was 0.33 ]]>
Pollen grains were observed on the bodies of the collected moths. However, it was not possible to count them, because of the presence of body scales that easily mixed with the pollen grains, when we tried to remove them. The average number of ]]>
Discussion
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Lower fruit and seed set in plants of small habitat fragments have been observed for many species of tropical and temperate vegetation (e.g., Jennersten, 1988; Jennersten, & Nilsson, 1993; Aizen, & Feinsinger, 1994a; Byers, 1995; Oostermeijer, Altenburg, & den Nijs, 1995; Ågren, 1996; Cunningham, 2000; Quesada et al., 2003). Other species either do not show any different response in reproductive output between fragmented and continuous forest or present even higher reproductive output in smaller fragments and open areas than in continuous forest (e.g., ]]>
Cabralea
canjerana is an example of a species that shows a reduction in its reproductive success in fragmented habitats. Plants of C. canjerana produce lower fruit, seed per fruit and higher seed predation in fragments than in continuous forest.
Several plant characteristics may contribute to the decrease in reproductive success in fragmented habitats, such as pollinator dependence and self-incompatibility (Rathcke, & Jules, 1993; Aguilar, Ashworth, Galetto, & Aizen, 2006). Sexual system may be another important trait that influences the reproductive output in fragmented habitats. It is probable that the occurrence of male and female flowers in separate plants makes C. canjerana totally dependent on pollinators and vulnerable to their population decreases. The low reproductive success of plants in isolated areas may result from the lower visitation rate of their pollinators to their flowers.
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The low visitation rate of pollinators to C. canjerana flowers in fragments may have caused not only the deposition of low numbers of pollen grains on stigmas, but probably lower-quality pollen loads. Moths do not carry large numbers ]]>
C. canjerana (Carmo, 2005), probably high visit ]]>
Fragmentation was negatively related to the density and size of C. canjerana in the areas studied (Santos, & Ono, unpublished data). More intensive selective logging of C. canjerana in the fragments than in continuous forest may have contributed to the decrease in density and plant size in fragments. ]]>
C. canjerana in fragmented sites. These populations have also showed higher rates of inbreeding than populations of the continuous forest (Carmo, 2005), which may influence plant fertility as well. Although variations in pollinator visits in different areas are generally related to population size and flower abundance (Murcia, 1990), in C. canjerana, this variation may also be related to differences in the amount and quality of the food resource for the moth larvae. According to Faegri & Pijl (1979), the presence of moths in an area depends more on the occurrence of the plants used by the larvae than on the occurrence of the plants used by the adults. The food resources for the moth larvae may be lower in the fragmented than in the continuous ]]>
The reproductive success of C. canjerana was also influenced by seed consumers. In C. canjerana, the number of pre-dispersed seeds damaged by dipteran larvae is higher in fragmented than in continuous forest. Other studies have found similar results (Didham, Ghazoul, Stork, & Davies, 1996; Kruess, & Tscharntke, 1994; Santos, & Telleria, 1994; Simberloff, 1993). High seed predation in fragmented areas has been related to the greater fruit exposure to seed predators and to abiotic variations in factors such as temperature, sunlight and humidity that may influence the ]]>
Cabralea canjerana, which is an ]]>
This study is the ]]>
C. canjerana is sensitive to changes in fruit and seed production. Moreover, the low reproductive ]]>
Acknowledgments ]]>
This work was supported by a grant from PROBIO/MMA (Projeto de Conservação e Utilização Sustentável da Diversidade Biológica Brasileira/Ministério do Meio Ambiente) to the first author. We are indebted to Roderic B. Martines and Antonio Pereira da Silva for their assistance in in the field. We are grateful to Altair Rezende de Souza, Sebastião Loreano, Brás, Antonio Bueno de Souza, Antonio Pereira da Silva and Joaquim Costa for ]]>
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1. Departamento de Botânica, Instituto de Ciências Biológicas, Universidade Federal de Goiás, Campus II-Samambaia; Goiânia-GO, Brasil; edivanif@gmail.com, goncalves.b.b@gmail.com, carloskoa@gmail.com
2. Departamento de Botânica, ICB, Universidade Federal de Minas Gerais, Av. Antônio Carlos 6627, Pampulha, Belo Horizonte MG, Brazil; roselainicarmo@gmail.com
3. Departamento de Ecologia, Instituto de Ciências Biológicas, Universidade Federal de Goiás, Campus II - Samambaia; Goiânia - GO, Brasil; llbergamini@gmail.com
Received 21-IV-2014. Corrected 07-X-2014. Accepted 19-XI-2014.