Fruits and Frugivores of the Brazilian Cerrado: Ecological And
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Acta Botanica Brasilica - 30(3): 495-507. July-September 2016. doi: 10.1590/0102-33062016abb0192 Fruits and frugivores of the Brazilian Cerrado: ecological and phylogenetic considerations Marcelo Kuhlmann1* and José Felipe Ribeiro2 Received: June 8, 2016 Accepted: August 28, 2016 . ABSTRACT Knowing the morphological and phylogenetic patterns of fruits of a plant community may elucidate plant-frugivore interactions, and analysis of dispersal syndromes is a practical approach to understanding these mutualisms. We investigated diff erent zoochorous fruits and frugivorous animals among Cerrado formations (forest, savanna and grassland), mapped dispersal syndromes on a Cerrado angiosperm phylogeny and tested for phylogenetic signal. For a core region in Cerrado, we found that, among almost a thousand fruit species and 258 fruit-eating vertebrates, 60% of the fruits had an ornithochorous syndrome and that 70% of the frugivores were birds. Most fruit and frugivorous species (~80%) inhabit forest formations, but many of them also occurred in more than one Cerrado formation. Th e zoochorous syndromes were found to have little phylogenetic signal, with many plant families exhibiting more than one fruit syndrome, and with ornithochory being widely distributed throughout the phylogeny. Our results suggest that plant-frugivore interactions tend to be evolutionarily labile in this Neotropical region, although birds have had a prominent role in fruit evolution. Furthermore, we found that all three Cerrado formations seem to be interrelated in maintaining functional stability of the plant-frugivore mutualisms in the Cerrado biome. Keywords: Cerrado biome, diaspores, dispersal syndromes, forest, fruit-eating animals, grassland, plant-frugivore interactions, phylogenetic signal, savanna Introduction traits of plant fruits, resulting in the coevolution of these organisms over tens of millions of years (Fleming & Kress 2013). Fruits with fl eshy tissues are an important food Plant-frugivore interactions are vital for the natural regeneration of plants that depend on animals for seed resources for a wide variety of animals, and the availability dispersal (Jordano 2000; Jordano et al. 2011). Th ere is of fruit in a given location can infl uence the abundance and considerable evidence that this mutualism has played an diversity of these frugivores (Jordano & Herrera 1995; Howe important role in the evolutionary diversifi cation of the & Westley 2009). Knowing the morphology of fruits and plants and animals involved (Herrera 1985; Eriksson et al. dispersal units in a plant community may help to better 2000; Tiff ney 2004; Eriksson 2008; Bolmgren & Eriksson understand plant-animal interactions and the diff erent 2010), with plants selecting particular traits of their plant colonization strategies (Galetti et al. 2006; Wiesbauer consumers in the same way that frugivores select particular et al. 2008; Howe 2016). 1 Institute of Biological Sciences, University of Brasilia, Campus Universitário Darcy Ribeiro, Asa Norte, Brasília - DF, 70910-900 2 Embrapa Cerrados, BR 020 Km 18. Planaltina - DF, 73310-970 * Corresponding author: [email protected] Diagramação e XML SciELO Publishing Schema: www.editoraletra1.com.br Marcelo Kuhlmann and José Felipe Ribeiro Different morphological traits of fruits and seeds, vascular plants (Ratter et al. 1997; Mendonça et al. 2008), it such as size, color, hardness, scent lures, amount and type is estimated that about one third of all species, and 60%-70% of pulp reward, nutritive value and accessibility, have an of woody plant species, depend on animals for seed dispersal, influence on what kind of animal will be attracted, such and especially so for those of forest formations (Batalha & as birds, non-flying mammals, bats or ants, and reflect Martins 2004; Gottsberger & Silberbauer-Gottsberger 2006; different dispersal syndromes (Howe & Smallwood 1982; Kuhlmann & Ribeiro 2016). Human occupation and land use Pijl 1982; Fleming et al. 1987). These “dispersal syndromes” in the Cerrado have led to the loss of more than 50% of the (suites of traits of fruits or seeds) indicate the most likely original vegetation of the biome (Ratter et al. 1997; Sano et dispersal agents and have potential usefulness in predicting al. 2008), bringing consequences such as soil degradation, the dispersal processes within a community at a given increase in invasive species and disruption of water cycles place and time (Howe 2016). However, it is important to (Klink & Machado 2005; Costa & Pires 2010). A variety of emphasize that not all animals that eat fruits are good human activities, such as forest fragmentation, hunting and seed dispersers, and that different factors can influence extensive agriculture can impact seed dispersal mutualisms, these plant-frugivore mutualisms, such as fruit phenology, affecting frugivores visitation, dispersal distance and seed abundance of fruits and frugivorous animals, competition, removal (Markl et al. 2012; Sebastián-González et al. 2015). predation, and weather conditions (Howe 2016). Animal In this way, the preservation of biodiversity and persistence traits, such as body size, behavior, method of locomotion, of the flora in biomes such as the Cerrado depend on the physiology, sensory capabilities and foraging tactics also conservation and, when necessary, the restoration of seed- can influence the selection of fruits and the effectiveness of dispersal processes and plant-animal interactions (Howe seed dispersal (Janzen 1969; Wheelwright 1985; Galetti et 2016). al. 2013). Given these considerations, analysis of dispersal The first step in conserving or restoring seed-dispersal syndromes provides a practical approach to understand processes is to understand what species of fruits and patterns of interactions within a community, assuming frugivores that interact within a given community. Since that the patterns we see today (phenotype) emerged from communities comprise groups of species that share certain past selective pressures involving plants and frugivores similarities, both ecological and phylogenetic (Tilman 1988; (Fleming & Kress 2013). Cavender‐Bares et al. 2009), grouping plants according to Since species are phylogenetically related, their their dispersal syndromes can help to make predictions morphological traits are not fully independent and so about the seed-dispersal processes (Thomson et al. 2010; the amount of “phylogenetic signal” of traits needs to be Fleming & Kress 2013). Although a “syndrome” approach measured statistically (Revell et al. 2008). Phylogenetic must be taken with care because of variation in place and signal can be defined as the tendency for related species time (Howe 2016), it promises to increase understanding to resemble each other more than they resemble species of the reproductive strategies of angiosperms and, thereby, drawn at random from the phylogenetic tree (Blomberg et facilitate programs for the recovery of degraded areas, such al. 2003; Losos 2008). When the phylogenetic relationship as PLANAVEG (2014) in the Cerrado. The Cerrado biome is of a group of organisms in a community is known, it is a complex mosaic of vegetation that comprises numerous possible to investigate how strongly certain morphological different phytophysiognomies, which can be grouped into and ecological characteristics are phylogenetically correlated, three main vegetative formations: forests, savannas and and if they form groups or niches that are strongly grasslands (Ribeiro & Walter 2008), each of which contains phylogenetically linked (Mouquet et al. 2012; Münkemüller species of flora and fauna with different survival strategies et al. 2012). Knowing the phylogeny can also indicate the (Diniz et al. 2010). With this in mind, we investigated extent which closely related groups tend to establish similar the proportions of different zoochorous syndromes and mutualistic interactions (Rezende et al. 2007), such as those different groups of frugivores in these Cerrado formations. involving fruits and frugivores and their syndromes. Moreover, we identified and mapped the distribution of It is estimated that in tropical forests over 90% of woody these syndromes on a phylogeny of Cerrado angiosperms to plant species produce fruits that are eaten and dispersed by test for the presence of phylogenetic signal. We intended to animals, and a high proportion of animals, especially birds address the following questions: (i) What are the proportions and mammals, feed on fruits (Jordano 2000; Kissling et al. of different zoochorous syndromes among angiosperms of 2009). The natural world would be drastically affected by the Cerrado? (ii) What is the proportion of bird and mammal the absence of dispersing animals (Bello et al. 2015) and, species that feed on fruits in the Cerrado? (iii) Are there depending on the vegetation type, natural regeneration differences in the proportions of zoochoric syndromes and cycles of most plants would be compromised (Janzen 1974; frugivore groups between forest, savanna and grassland Howe et al. 1985), leading to local extinctions (Jordano et formations? and (iv) Are zoochorous syndromes strongly al. 2011). For the Brazilian Cerrado, a complex and mega- conserved throughout angiosperms phylogeny or they are diverse Neotropical biome with over 12,000 species of evolutionarily labile? 496 Acta Botanica Brasilica - 30(3): 495-507. July-September 2016 Diagramação e XML SciELO Publishing Schema: www.editoraletra1.com.br Fruits and frugivores of the Brazilian Cerrado: ecological