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Resource Or Pollination Limitation? Anais da Academia Brasileira de Ciências (2014) 86(1): 229-238 (Annals of the Brazilian Academy of Sciences) Printed version ISSN 0001-3765 / Online version ISSN 1678-2690 http://dx.doi.org/10.1590/0001-37652014101712 www.scielo.br/aabc Wind pollination and propagule formation in Rhizophora mangle L. (Rhizophoraceae): resource or pollination limitation? TARCILA L. NADIA1 and ISABEL C. MACHADO2 1Centro Acadêmico de Vitória, Universidade Federal de Pernambuco, Rua Alto do Reservatório, s/n, Bela Vista, 55608-680 Vitória de Santo Antão, PE, Brasil 2Departamento de Botânica, Centro de Ciências Biológicas, Universidade Federal de Pernambuco, Rua Prof. Moraes Rego, s/n, Cidade Universitária, 50372-970 Recife, PE, Brasil Manuscript received on April 23, 2012; accepted for publication on April 3, 2013 ABSTRACT Rhizophora mangle is considered as a self-compatible mangrove, and is pollinated by wind and insects. However, there is no information about fruit production by autogamy and agamospermy and on the foraging behavior of its flower visitors. Hence, the present study analyzed the pollination and reproductive systems of R. mangle in a mangrove community in northern Pernambuco, Brazil. Floral morphology, sequence of anthesis, and behavior of flower visitors were described; the proportion of flowers that resulted in mature propagules was also recorded. Autogamy, agamospermy, and wind pollination tests were performed, and a new anemophily index is proposed. The flowers of R. mangle are hermaphrodite, protandric, and have high P/O rate. Flies were observed on flowers only during the male phase, probably feeding on mites that consume pollen. Rhizophora mangle is not agamospermic and its fruit production rate by spontaneous self-pollination is low (2.56%) compared to wind pollination (19.44%). The anemophily index was high 0.98, and thus it was considered as a good indicator. Only 13.79% of the flowers formed mature propagules. The early stages of fruit development are the most critical and susceptible to predation. Rhizophora mangle is, therefore, exclusively anemophilous in the study area and the propagule dispersal seems to be limited by herbivory. Key words: anemophily index, autogamy, entomophily, mangrove, red mangrove. INTRODUCTION stabilization and primary production, increasing the Mangrove species occur in tropical coastal productivity of nearby communities (Grasso and regions, occupying intertidal zones and estuarine Tognella 1995, Mantovani 2002, Hogarth 2007). margins (Tomlinson 1994). True mangroves live Mangroves are heavily used by humans for exclusively in the ecosystem known as mangal, and timber, tannin, and bioactive compounds, as well they comprise approximately 55 plant species of 20 as for silviculture and ecotourism (Grasso and genera and 16 families (Tomlinson 1994, Hogarth Tognella 1995, Ellison 2000, Hogarth 2007). 2007). These species form dense forests, sometimes Hence, this ecosystem has been devastated at a monospecific, which play an important role in soil rate higher than 1.5% per year (Ellison 2000). For projects of restoration and sustainable use Correspondence to: Isabel Cristina Machado E-mail: [email protected] of mangroves, knowledge about plant-animal An Acad Bras Cienc (2014) 86 (1) 230 TARCILA L. NADIA and ISABEL C. MACHADO interactions, population physiology and biology, Regarding the reproductive system of as well as pollination and reproductive system are Rhizophora mangle, self-compatibility has been needed (Endress 1994, Kearns and Inouye 1997, already recorded, and self-pollination is considered Kearns et al. 1998, Ellison 2000). as the main pollination mechanism (Menezes et al. The family Rhizophoraceae, which dominates 1997). However, there is no information about the mangroves all over the world, encompasses occurrence of agamospermy and the possibility of 16 genera and approximately 150 species with fruit production by spontaneous self-pollination pantropical distribution, not exclusive to mangroves in R. mangle; this information would lead us to a (Hogarth 2007, Souza and Lorenzi 2008). The tribe better understanding of the reproductive system Rhizophorae is composed of four genera endemic of the species. In addition, few studies recorded to mangroves, Bruguiera, Ceriops, Kandelia, and the proportion of flower buds that become Rhizophora, which have as a peculiar characteristic mature propagules and in which phase of their vivipary, i.e., the seedling remains attached to the development they are more vulnerable, which are mother-plant during its development (Tomlinson important steps for the process of recruitment and 1994). Rhizophora is the single genus of this tribe that maintenance of mangrove communities (Duke et occurs in the western center of mangrove diversity, al. 1984, Coupland et al. 2006). Hence, the present which comprises the western coast of Africa, the study aimed at answering the following questions: eastern and western coasts of South and Central 1) How does the sequence of anthesis occur in R. America, and southern Florida (Tomlinson 1994). mangle?; 2) Which are the flower visitors of R. In the eastern diversity center, which comprises mangle and what is their role in pollination?; 3) eastern Africa, southern and southeastern Asia, What is the importance of wind for fruit production and northern Oceania, all four genera of the tribe in R. mangle?; and 4) What is the rate of fruit and Rhizophorae are found. In Brazil, only three propagule production in R. mangle? Rhizophora species occur, Rhizophora harrisonii, R. mangle, and R. racemosa. Rhizophora mangle MATERIALS AND METHODS is broadly distributed, occurring all along the coast, STUDY SITE AND SPECIES STUDIED and the other two species have their distribution restricted to northern region (Tomlinson 1994). Field observations were carried out in a mangrove There is a wide variety of pollination area in Goiana, northern coast of Pernambuco, mechanisms in the family Rhizophoraceae, but northeastern Brazil (7°40’39.8”S and 34°50’21.8”W). Rhizophora is considered as mainly anemophilous The region exhibits a rainy season from February to (Tomlinson et al. 1979). However, there are August and a dry season from September to January, sporadic records of flower visitors, such as bees, characterized by monthly rainfall below 100 mm (data butterflies, and birds, in some species of the genus provided by Instituto de Tecnologia de Pernambuco – (Tomlinson et al. 1979). However, the role of these ITEP). The average annual rainfall is 2,053 mm, the animals in the pollination of Rhizophora species average maximum temperature is 29.9°C, and the has not been determined yet. Although in a R. average minimum temperature is 21.9°C (ITEP). mangle population in northern Brazil the insects Rhizophora mangle usually occurs in areas observed on flowers were considered as secondary close to the sea or in river margins (Tomlinson pollinators (Menezes et al. 1997), there is no 1994, Hogarth 2007). It is a dominant species in description of these insects’ behavior on flowers the study area, occurring also in the mangrove- that classifies them as pollinators or robbers. ‘terra firme’ ecotone, with an average density of An Acad Bras Cienc (2014) 86 (1) WIND POLLINATION IN Rhizophora mangle 231 0.6 individuals.m-2 (T.L. Nadia, unpublished data). the contact with the reproductive whorls. Animals Flowering and fruiting occur throughout the year, were collected for identification by specialists and with both phenophases having their peaks in the were posteriorly deposited in the entomological rainy season (Nadia et al. 2012). collection of the Laboratory of Floral and Reproductive Biology of the Universidade Federal FLORaL BIOLOgy de Pernambuco. To test for the role of wind in Pre-anthesis buds (n = 20) and flowers (n = 20) of the pollination of R. mangle, young flower buds ten individuals were collected and fixed in 70% (n = 36) of different individuals were used, which ethanol for the analysis of floral morphology in were covered with knitted fabric with mesh size of the laboratory under a stereomicroscope. The 1.6 mm, allowing the passage of pollen carried by length of flower parts (sepals, petals, stamens, and the wind and hindering the access of flower visitors gynoecium) was measured with a millimeter ruler to inflorescences and flowers. on 18 fixed flowers. The number of pollen grains REPRODUCTIVE SYSTEM per flower was estimated for ten young flower buds of ten different individuals in a Neubauer chamber Flowers (n = 116) of 23 individuals were marked (Maêda 1985). The number of ovules was counted to observe fruit production under natural conditions in the same ten flower buds, and the pollen-ovule (control). The fruits formed in this treatment were rate was calculated (Cruden 1977). Pollen viability followed monthly until the development and dispersal was observed using the cytoplasmatic staining of propagules. The survival rate at each stage of technique with aceto carmine (Radford et al. 1974); development (anthesis, ovary in development, fruit, approximately 2,000 pollen grains per anther were and propagule) was calculated as follows: randomly counted in ten pre-anthesis buds of ten n S = i × 100, where: different individuals. N Duration and sequence of anthesis were moni- S = survival rate (%) tored in 30 previously marked flowers of different N = number of survivors at stage i individuals. Flower opening was considered as the n = number of survivors at stage i+1 largest distance between sepals, and was measured i with a millimeter ruler
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