The exception seems to be the rule: Nectaries in Serpocaulon and an update of their presence in Polypodiaceae

Highlights

• Nectary anatomy is presented for the first time in the fern genus Serpocaulon.

• In the studied taxa, nectaries are non-structural and active only in young fronds.

• The nectar is released through modified prominent stomata.

• Nectaries have been recorded only in ca. 1% of Polypodiaceae species.

• Future efforts are needed to understand secretion-mediated interactions in ferns.

Abstract

Although nectaries are widely known among angiosperms, few records exist for ferns, and there are even fewer studies focusing on their anatomy. We noticed nectaries in Serpocaulon (Polypodiaceae) and confirmed their presence in six taxa of the genus. We conducted a structural analysis using light and scanning electron microscopy and revised occurrence records of nectaries in polypodiaceous ferns. Nectar secretion was observed in young fronds and was restricted to the basal pinnae/segments. We did not detect any differentiated glandular tissue in the portions where the nectar was released, which implies that the nectar secreting glands in the studied taxa should be regarded as non-structural nectaries. Nonetheless, we found the mesophyll in these portions to usually be compact (i. e. with inconspicuous and relatively fewer intercellular spaces), sometimes with cells with distinct dense protoplast. In addition, prominent stomata with elevated guard cells were observed in nectary portions, probably constituting pathways through which nectar exudates. An update record for nectaries in Polypodiaceae was presented; these structures were recorded in 8% of Serpocaulon and ca. 1% of the species of the family, most being epiphytic with pinnatisect laminae dissection. While extrafloral nectaries are mostly related to protection against herbivores, nectary ecology in ferns is poorly understood, and a protective role of these structures cannot be discarded. However, further investigation is needed and encouraged to develop a comprehensive understanding of fern nectaries in light of their evolutionary history and ecological roles.

Introduction

Plants secrete nectar to achieve two very important mutualistic interactions with animals: pollination/dispersion and indirect defense (Brandenburg et al., 2009; Heil, 2011). In general, the structures that attend to the former interaction have been described as ‘floral nectaries’, which produce nectar as a reward for pollinators (Roy et al., 2017) and are abundant in the angiosperms (Marazzi et al., 2013). However, the structures that mediate an indirect defense response have been mainly recognized as extrafloral nectaries (Power and Skog, 1987; Jabbour, 2017) or defense nectaries (Keeler and Kaul, 1984). Although these nectaries are more frequently recorded among angiosperms, they have also been noticed in Marattiales and leptosporangiate ferns (Koptur et al., 2013), groups dating from the Paleozoic (Schuettpelz and Pryer, 2008).

Since ferns lack flowers, Koptur et al. (2013) suggested that describing these nectaries as ‘extrafloral’ would be incorrect; or as pointed by Nepi et al. (2009) this is “an unfortunate terminological anachronism, as fern sugar secretions were the first occurrence among all vascular plants”. Thus, since these glands are always on the fronds (leaves) in ferns, they might be best described as ‘foliar nectaries’ (term presented by Schmid, 1988), ‘defense nectaries’ (as per Keeler and Kaul, 1984) or simply ‘nectaries’ (Nepi et al., 2009; Koptur et al., 2013; Nepi, 2017).

Nectaries have been recorded for several groups of ferns, including Angiopteris (Marattiaceae) (Bonnier, 1879), Pteridium (Dennstaedtiaceae) (Darwin, 1876; Bonnier, 1879; Cooper-Driver, 1990; Rashbrook et al., 1992), Cyathea (Cyatheaceae) (Arens and Smith, 1998; White and Turner, 2012) and Polybotrya (Dryopteridaceae) (Koptur et al., 1982; Moran, 1987). There have only been a few records of the occurrence of nectaries within Polypodiaceae (Koptur et al., 1982, 1998, 2013; Mehltreter, 2010; Weber and Keller, 2013), despite it being the most diverse and divergent fern family with approx. 65 genera and 1652 species (PPG, 2016).

Most contributions regarding nectaries in polypodiaceous ferns are related to the analysis of nectar based primarily on sugar tests (Dümmer, 1911; Lüttge, 1961; Koptur et al., 1982), indications of this structure in fronds (Koptur et al., 1982, 1998, 2013; León, 1993; Sanín, 2018; Sanín and Salino, 2020), or through ecological observation (Koptur et al., 1982, 1998, 2013). However, data on the structure of nectaries are limited to a few groups within Polypodiaceae (Potes, 2010), with the biology of these nectaries being largely unknown (Koptur et al., 1982, 1998, 2013; Marazzi et al., 2013). For instance, although foliar nectaries probably arose independently multiple times in ferns and angiosperms (Elias, 1983; Potes, 2010; Koptur et al., 2013; Weber and Keeler, 2013), few studies have gathered data to unveil the evolutionary relationships among these lineages (Nayar, 1961; Page, 1982; Power and Skog, 1987; Rumpf et al., 1994; Potes, 2010). Also, Koptur et al. (1998, 2013) explored the ecological significance of nectaries in ferns and attributed to these structures a role against herbivory. However, important questions, including many aspects of the functional role, mediated interactions and evolution of these nectaries remain unanswered. This reinforces the need for further efforts towards a comprehensive understanding of these structures, both in narrow and broad taxonomic scales (Marazzi et al., 2013).

Among the genera of Polypodiaceae in which nectar secretions have been observed is Serpocaulon (Sanín, 2018; Sanín and Salino, 2020), a Neotropical genus (Smith et al., 2006) with 37 species and six hybrids (Sanín, 2020). These species are characterized by clathrate rhizome scales and areolate venation (Smith et al., 2006; Sanín 2018, 2020), and exhibit three laminae division patterns, with most species (24) having pinnatisect laminae, 12 species exhibiting pinnate laminae, and only one species (S. levigatum) with simple laminae (Sanín, 2020). Among the species of the genus, nectaries have been reported only in S. demissum (Sanín and Salino, 2020) and S. triseriale (Sanín, 2018). However, a recent taxonomic revision of Serpocaulon (Sanín, 2020) revealed the presence of nectaries in several additional species. Thus, in this study we present an expanded record of nectaries in Serpocaulon, along with the first anatomical descriptions of these structures in the genus. Our main goals were to confirm the presence of these structures in five species and one hybrid of the genus, describe their structure and secretory activity and present an updated record on the occurrence of nectaries in Polypodiaceae.