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- Materials and Methods
Interactions between ants and plants that produce a more reliable (i.e. nonrandom) ant presence on plant foliage are generally mediated by one of three mechanisms – domatia, direct food resources and indirect food resources – featured alone or in various combinations (Buckley, 1982; Beattie, 1985). While ants can obtain nutrition from plants indirectly, by collecting wound sap or tending hemipteran trophobionts for honeydew, direct food rewards provided by plants are limited to extrafloral (EF) nectar and food bodies (FBs). Extrafloral nectaries are known from a considerable number of unrelated plant families, and plant–animal interactions mediated by EF nectar have been reviewed in detail (Bentley, 1976, 1977; Koptur, 1992). It has also been shown that energy-rich FBs are an important source of nutrition to ants (e.g. Janzen, 1967; Heil et al., 1997). Such structures are similarly known from a diverse range of unrelated plant taxa and can be a significant contribution to the dietary needs of ant colonies (Fiala et al., 1991; Schupp & Feener, 1991; Heil et al., 2004).
Darwin (1877) first applied the term ‘food bodies’ to the small structures found on the leaf tips of Acacia sphaerocephala and on special basal pads (trichilia) from Cecropia peltata petioles. Subsequently, Schimper (1888) suggested the use of the terms ‘Beltian bodies’ (BBs) and ‘Müllerian bodies’ (MBs) for the FBs of Acacia and Cecropia, respectively. More recently, FBs (also known as food corpuscles sensu Hölldobler & Wilson (1990), or trophosomes sensu Jolivet (1996)) have been described as small epidermal structures (Beattie, 1985; Hölldobler & Wilson, 1990), but a range of studies have concluded that they may also be composed of nonepidermal tissue (Penzig, 1893; Rickson, 1969, 1975; Buckley, 1982; O'Dowd, 1982; Heil & McKey, 2003). Many authors now use the term food body interchangeably with Beltian bodies (Heil et al., 2002, 2004), Müllerian bodies (Folgarait & Davidson, 1994, 1995; Del Val & Dirzo, 2003), and a diverse group of emergences known as ‘pearl bodies’ (PBs; Keeler, 1989; Schupp & Feener, 1991; Fiala & Maschwitz, 1992), and the current consensus seems to be that FBs can be grouped into these three subcategories.
Firstly, Beltian bodies are known only from 12 of the 13 neotropical ‘ant-acacias’ (Janzen, 1974; Seigler & Ebinger, 1995) and are produced as the final stage of leaf ontogeny at the tip of each rachis and pinnule (i.e. a modified leaflet tip; Janzen, 1967; Rickson, 1969; Buckley, 1982). The mature BB comprises differentiated living tissue with a central vascular bundle (Rickson, 1969, 1975), and once BBs have been harvested from a leaflet, they are not replaced (Raine et al., 2004). Beltian bodies contain high concentrations of protein, some lipids and a little starch (Rickson, 1969, 1975), and a recent quantification by Heil et al. (2004) confirmed carbohydrates, proteins, amino acids and lipids comprising between 15 and 25% DW BB tissue.
Secondly, Müllerian bodies are also known from a restricted range of species (Cecropiaceae), and have been thoroughly characterized in Cecropia spp. (Rickson, 1971, 1976a; Marshall & Rickson, 1973; Jolivet, 1996). Production of MBs takes place on a trichilium, which is covered in a dense mat of tannin-rich trichomes that protect the emerging growths (Rickson, 1976a, 1977). Trichilia are located on the abaxial interface of the leaf petiole and stem, and MB-producing trichilia are generally limited to the terminal two to three leaves of each branch (Longino, 1991) with an average productive life span of 3 months (Folgarait et al., 1994). Müllerian bodies are differentiated multicellular outgrowths with no vascular tissue, and are initiated in the subepidermal trichilial tissue (Rickson, 1976a,b). Müllerian bodies are unusual in that they contain a storage polysaccharide similar to glycogen, production of which is initiated when the MBs have reached 75% of full size (Rickson, 1971, 1976b; Marshall & Rickson, 1973). In addition to being rich in glycogen, mature MBs also contain significant quantities of lipids and protein (Rickson, 1976b, 1977; Belin-Depoux et al., 1997).
Lastly, pearl bodies (sensu O'Dowd, 1982) are known from a wide range of unrelated taxa (Rouppert, 1926; O'Dowd, 1982), are both morphologically and chemically heterogeneous (O'Dowd, 1980; Heil et al., 1998; Fischer et al., 2002), and are found on a variety of tissue types (Rickson, 1980; Rickson & Risch, 1984). This situation has resulted in conflicting conclusions over what constitutes a PB (Rickson & Risch, 1984; Schupp & Feener, 1991), although common features include a white lustrous colour, a spherical or elongated ‘club-like’ shape, basal constriction (i.e. a stem), and cells with a large content of lipid relative to the underlying tissue (O'Dowd, 1982). Rather than proceeding with an ever-increasing list of somewhat meaningless names (Rickson, 1980; Jolivet, 1996), O'Dowd (1982) built on the early work of Penzig (1893), Holmgren (1911) and Rouppert (1926), and proposed to group PBs into three ‘models’ according to their tissue of origin and cellular structure.
Pearl bodies have been found on almost all types of above-ground plant structures, including vegetative and reproductive tissue (Dale, 1900; Holmgren, 1911; Rickson, 1976b; O'Dowd, 1980; Fiala & Maschwitz, 1992) and on the inner walls of petiolar ant domatia (Risch et al., 1977). Pearl body tissue lacks chloroplasts (with the exception of those in epidermal guard cells, when these are present (Dale, 1901; Holmgren, 1911)) and vascular tissue (Rickson, 1980; O'Dowd, 1982) and displays all the cytological characteristics of active, living cells (Walter, 1921; O'Dowd, 1980). The chemical constituents of PBs are highly variable, not only in the type of compounds but also in their relative proportions (Penzig, 1893; Nestler, 1893; Risch et al., 1977; O'Dowd, 1980; Rickson, 1980; Rickson & Risch, 1984; Heil et al., 1998; Fischer et al., 2002).
Plant taxa providing direct food rewards span the gamut of ecosystem habitats from the deep shade of a forest understorey to high-light disturbed areas (Bentley, 1977; Buckley, 1982; O'Dowd, 1982). In tropical rainforest ecosystems, direct food rewards are more common in light gap species or species of successional communities than in shade-tolerant species (Bentley, 1976, 1977; O'Dowd, 1982; Keeler, 1989; Schupp & Feener, 1991). Thus, most understorey myrmecophytic symbioses are mediated by indirect food sources, such as hemipteran trophobionts (Stout, 1979; Fonseca, 1994; Alonso, 1998). One of the few exceptions is the Leonardoxa africana species complex (understorey trees; McKey, 2000) where domatia-dwelling Petalomyrmex ants are provided with EF nectar from large foliar nectaries (Elias, 1980; McKey, 1984, 1991, 2000; Gaume et al., 1997).
The rainforests of northern Australia are known for their low diversity of arboreal ants, relative to other tropical regions (Majer, 1990; Andersen & Majer, 2000; Majer et al., 2001). Davidson & McKey (1993) suggested that the origin of Australian rainforests may have been too recent to have allowed significant radiation of weakly competitive plant-ant genera before the arrival of other dominant ant species. Although the recent work of Blüthgen and colleagues (Blüthgen & Reifenrath, 2003; Blüthgen et al., 2004) has documented ant interactions with EF nectaries in tropical lowland rainforests of northern Queensland, to the best of our knowledge, there is no published documentation of FBs in any Australian plant.
When seedlings of the Australian rainforest endemic, Ryparosa kurrangii (Achariaceae), growing in a glasshouse developed small outgrowths on their leaves and stems, it was initially assumed they were of pathogenic origin. Foliar pesticide and fungicide sprays and plant isolation failed to prevent further outgrowths from forming, and invertebrate-induced galls could be ruled out because of the controlled conditions in which glasshouse seedlings were raised. Field observations of FBs are rare because of their continual harvesting by invertebrates (Raciborski, 1898; O'Dowd, 1979; Keeler, 1989) and FBs have been frequently discovered for the first time on tropical plants that have been raised in glasshouses (Rouppert, 1926; O'Dowd, 1980; Benson, 1985).
Food bodies are not known from Ryparosa, yet many early taxonomic papers describe the presence of ‘tubercles’, ‘verrucosities’ or ‘lenticels’ on young stems in a range of Ryparosa taxa (Sleumer, 1954). Furthermore, the documentation of stem-nesting ants in Ryparosa amplifolia (syn. R. javanica sensu Sleumer, 1954; formerly Gertrudia amplifolia (Schumann & Lauterbach, 1901; Mildbraed, 1928)), R. porcata (Jarvie & Stevens, 1998) and R. fasciculata (Moog et al., 1997; Agosti et al., 1999; Moog et al., 2003), the latter with associated pseudococcids (Heckroth et al., 1998; Agosti et al., 1999), suggests that ant–plant associations in Ryparosa may be stronger than currently thought. Although there have been no reports of associated ants in R. kurrangii, it seemed plausible that the plant growths observed in R. kurrangii may be a form of FB, and they will, hereafter, be referred to as such. The objectives of our study were to provide a detailed characterization of the developmental morphology of R. kurrangii FBs, and conduct a histological analysis of the predominant contents of FB cells. Documentation of the interactions between R. kurrangii FBs and ants, and the broader taxonomic implications of ant-plant features in Ryparosa, will be presented elsewhere (Webber et al., 2007).