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Morphological Patterns of Extrafloral Nectaries in Woody Plant Species Of Plant Biology ISSN 1435-8603 1 RESEARCH PAPER 2 3 Morphological patterns of extrafloral nectaries in woody 4 plant species of the Brazilian cerrado 5 1 2 2 3 6 S. R. Machado , L. P. C. Morellato , M. G. Sajo & P. S. Oliveira 7 1 Departamento de Botaˆ nica, Instituto de Biocieˆ ncias, Universidade Estadual Paulista (UNESP), Botucatu, Brazil 8 2 Departamento de Botaˆ nica and Plant Phenology and Seed Dispersal Group, Instituto de Biocieˆ ncias, Universidade Estadual Paulista (UNESP), 9 Rio Claro, Brazil 10 3 Departamento de Zoologia, Universidade Estadual de Campinas (UNICAMP), Campinas, Brazil 11 12 13 14 15 16 Keywords 17 ABSTRACT Ant–plant mutualism; cerrado; extrafloral 18 nectary; nectary anatomy; savanna. Extrafloral nectaries are nectar-secreting structures that are especially com- 19 mon among the woody flora of the Brazilian cerrado, a savanna-like vegeta- 20 Correspondence tion. In this study, we provide morphological and anatomical descriptions 21 L. P. C. Morellato, Departamento de Botaˆ nica, of extrafloral nectaries (EFNs) occurring on vegetative and reproductive 22 Universidade Estadual Paulista, Av. 24A, organs of several plant species from the cerrado, and discuss their function 23 1515, C.P.199, 13506-900 Rio Claro, Sa˜ o and ecological relevance. We describe the morphology and anatomy of EFNs Paulo, Brazil. of 40 species belonging to 15 woody families using scanning electron 24 E-mail: [email protected] microscopy and light microscopy. We categorise EFNs following a struc- 25 tural–topographical classification, and characterise the vascularised and 26 Editor complex nectaries, amorphous nectaries and secretory trichomes. Fabaceae, 27 J. Arroyo Bignoniaceae, Malpighiaceae and Vochysiaceae were the plant families with 28 the majority of species having EFNs. Ten species possess more than one 29 Received: 28 May 2007; Accepted: 16 morphotype of gland structure. Observations and experimental field studies 30 November 2007 in the cerrado support the anti-herbivore role of EFN-gathering ants in this 31 habitat. Additional morphological studies of EFNs-bearing plants, including doi:10.1111/j.1438-8677.2008.00068.x 32 other growth forms (e.g. herbs and lianas), are being undertaken and will 33 hopefully cast further light on the ecological relevance of these glands in the 34 cerrado, especially with respect to their attractiveness to multiple visitors. 35 36 37 buds, calyx, inflorescence axis, flower peduncles and fruits 38 INTRODUCTION (Elias 1983; Oliveira & Leita˜o-Filho 1987; Koptur 1992; 39 Extrafloral nectaries (EFNs) occur in 93 flowering plant Dı´az-Castelazo et al. 2004, 2005). 40 and five fern families and can be abundant among the Contrary to floral nectaries that attract and reward ver- 41 flora of many habitats worldwide, especially in the tropics tebrate and invertebrate pollinators, EFNs are especially 42 (Bentley 1977; Koptur 1992; Oliveira & Freitas 2004). For attractive to ants and a variety of other nectar-foraging 43 instance, plants bearing such glands account for 33% of insects such as wasps, bees, flies and beetles, and more 44 the species (woody and climbing plants) in the rain forest rarely spiders and mites (e.g. Oliveira & Branda˜o 1991; 45 of Barro Colorado Island in Panama (Schupp & Feen- Koptur 1992; Pemberton & Lee 1996; Kawano et al. 1999; 46 er1991), and for 12% of the woody species in a West Ruhren & Handel 1999; Cuautle & Rico-Gray 2003). 47 1Malaysian rain forest (Fiala & Linsenmair 1995). In dif- Numerous experimental field studies have shown that aggression towards herbivores by EFN-gathering insects, 48 ferent vegetation types in the Brazilian Amazon, 18–53% of the woody species possess EFNs, comprising up to most especially ants, can positively affect plant fitness by 49 50% of the local individuals (Morellato & Oliveira 1991). decreasing herbivore damage (e.g. Bentley 1977; Koptur 50 These nectar-secreting glands are structurally diverse and 1984; Rico-Gray & Thien 1989; Oliveira et al. 1999; Cu- 51 occur on virtually all aboveground plant organs; they are autle & Rico-Gray 2003; Rudgers & Gardener 2004; Wa¨c- 52 especially common on the leaf blade, petiole, young kers & Bonifay 2004). Plant protection, however, is not 53 stems, stipules and on reproductive structures such as universal and ant visitation to EFNs may afford no appar- Plant Biology ª 2008 German Botanical Society and The Royal Botanical Society of the Netherlands 1 PLB 068 Dispatch: 9.3.08 Journal: PLB CE: Maniraj Journal Name Manuscript No. B Author Received: No. of pages: 14 PE: Bhuvana Extrafloral nectaries in the Brazilian cerrado Machado, Morellato, Sajo & Oliveira 1 ent benefit to plants (O’Dowd & Catchpole 1983; Rash- entire range of woody plant density; the whole biome is 2 brook et al. 1992). Field experiments performed in the collectively referred to as the cerrados (Oliveira-Filho & 3 Brazilian cerrado, a savanna-like vegetation, show that Ratter 2002). Material was collected in different areas of ⁄ 4 ants visiting EFNs may prey on and or attack insect her- cerrado sensu stricto (i.e. dense scrub of shrubs and trees) 5 bivores on plants and significantly reduce herbivore dam- in the state of Sa˜o Paulo, Southeast Brazil. Voucher speci- age to leaves, buds or flowers. Ant-derived benefits to mens are deposited in the herbarium of the Universidade 6 plants, however, may vary with the species of visiting ant, Estadual de Campinas (UEC), and the herbarium of the 7 with the defensive tactics of associated herbivores, as well Universidade Estadual Paulista, Instituto de Biocieˆncias, 8 as with the plant species (Costa et al. 1992; Del-Claro Botucatu (BOTU). 9 et al. 1996; Freitas & Oliveira 1996; Oliveira 1997; Olive- We fixed the samples in FAA 50 (Johansen 1940) and 10 ira & Freitas 2004). preserved in 70% alcohol. For scanning electron micros- 11 The ecological importance of the EFNs has motivated copy (SEM) studies, the samples were dehydrated with a 12 many authors to study the morphology, distribution and graded ethanol series; critical-point dried using CO2, 13 frequency of these structures in different plant taxa (e.g. gold-coated and examined using a Philips 515 SEM at 14 Zimmerman 1932; Bentley 1977; Metcalfe & Chalk 1979; 20 kV. For light microscopy, the material was dehydrated 15 Elias 1983; Oliveira & Leita˜o-Filho 1987; Oliveira & with a graded ethanol series, infiltrated and embedded in 16 Oliveira-Filho 1991; Morellato & Oliveira 1994; McDade glycol–methacrylate historesin, as per standard methods. & Turner 1997), as well as the composition of their nec- The sections (6–8 lm thick) were stained with toluidine 17 tar and its role in insect attraction (Koptur 1992). While blue (O’Brien et al. 1964). The following histochemical 18 there is increasing understanding of the evolutionary sig- tests were performed: PAS reaction for neutral polysac- 19 nificance of EFNs in tropical communities, ecological charides; ruthenium red for pectins and mucilage (Jensen 20 studies of ant–plant mutualisms have until recently con- 1962); Sudan IV for lipids; and 10% aqueous ferric chlo- 21 sidered only the distribution of these structures among ride to detect phenolic compounds (Johansen 1940). The 22 plant organs, neglecting their morphology. According to nectaries were characterised following the structural and 23 Dı´az-Castelazo et al. (2005), the effect of EFN attributes topographical classification originally proposed by Zimm- 24 such as gland structure, distribution and secretion on erman (1932) and Elias (1983), and the vascularised and 25 preference by ants and in the structure of the associated complex nectaries, amorphous nectaries and secretory 26 ant community needs further investigation. trichomes were also characterised. In addition to the 27 Floristic surveys carried out by Oliveira & Leita˜o-Filho EFN, we also examined all species for the presence of (1987) in five areas of cerrado in Southeast Brazil revealed other secretory structures such as glands, glandular tric- 28 that 34 woody species from 15 families have EFNs, homes and secretory spaces. These structures were charac- 29 accounting for up to 20% of the species within each local terised by their structural–topographical features. Families 30 woody flora. Plant species had EFNs associated with vege- were organised according to the APGII classification for 31 tative (leaves, stems) and ⁄ or reproductive organs (bud or the families of the flowering plants (Angiosperm Phylog- 32 flower). The Leguminosae, Bignoniaceae and Vochysia- eny Group 2003). 33 ceae were the families most frequently having such glands 34 (see also Oliveira & Oliveira-Filho 1991). Anatomical data 35 of EFNs for cerrado plant species are practically non-exis- RESULTS AND DISCUSSION tent (Paiva et al. 2001; Paiva & Machado 2006a,b,c), 36 Descriptions of extrafloral nectaries (EFNs) 37 although general morphological information on the 38 glands of certain genera is available (Elias 1983; Lersten & Rosids Brubaker 1987; Koptur 1992; Lersten & Curtis 1994; Pas- Combretaceae (Myrtales): Terminalia argentea and T. bra- 39 cal et al. 2000; Dı´az-Castelazo et al. 2005). siliensis have slightly elevated nectaries on both sides of 40 In the current paper we describe the morphology and the distal part of the petiole; the nectaries are surrounded 41 anatomy of the EFNs present in 40 woody species from by non-secretory trichomes (Fig. 1). Stomata with wide 42 the Brazilian cerrado, and discuss their function and eco- pores occur scattered on the nectary surface. In longitudi- 43 logical relevance. We categorise the glands following the nal section, the nectary has a one-layered epidermis cov- 44 structural and topographical system originally proposed ered by a thick cuticle and a multilayered subepidermal 45 by Zimmerman (1932) and Elias (1983). region of compactly arranged parenchymatous cells vascu- 46 larised by phloem elements. Phenolic compounds, detected by ferric chloride treatment inside the vacuole 47 MATERIALS AND METHODS 48 and druse inclusions, are abundant in the cells of the sub- Æ 2 49 The Brazilian cerrado covers nearly 2 million km , repre- epidermal region.
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