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Abstract
An increasing number of double mutualisms (i.e. two interacting species benefiting each other in two different functions, e.g. pollination and seed dispersal) have been reported, mainly from island ecosystems, although we still lack much information on how effective such species are in both processes. Here, we assessed the pollination effectiveness of a double mutualism between an ancient Mediterranean gymnosperm, Ephedra fragilis, and a lizard, Podarcis lilfordi. On the one hand, we assessed the lizard contribution to different fitness measures (seed set and germination success), relative to that of insects and the wind effect; on the other, we determined the lizards’ seed removal rate (i.e. the quantity component of seed dispersal effectiveness). In both processes, we further tested for differences in their contributions among male, female and juvenile lizards. Ephedra fragilis showed to be mostly anemophilous, lizards and insects playing only a minor role on seed set. However, lizards qualitatively contributed to pollination success, as seeds coming from lizard-pollinated cones germinated at higher rates than those pollinated by wind or insects, although this was detected only for small seeds (<8 mg). The plant produced a low seed set (c. 23 %), which was compensated by a high seed germinability (c. 70 %). Adult male lizards were those most implicated in pollination, quantitatively more important than insects, and in seed dispersal. This work, thus, reports the importance of a lizard species in one of the few double mutualisms found in the World involving a gymnosperm, and it represents the first documentation of a double mutualism in the Mediterranean region. Our findings further contribute to highlight the role of both inter- and intraspecific differences in the effectiveness of mutualistic interactions.
Highlights
Most plants that depend on animal pollination and seed dispersal are often served by different taxa for each of these ecological functions (Herrera and Pellmyr 2002)
Our study provides evidence that this plant–lizard relationship constitutes one of the five pollination/seed dispersal double mutualisms found around the World between an animal and a gymnosperm (Fuster et al 2018), besides representing the first double mutualism reported in the Mediterranean region
E. fragilis shows to be mainly pollinated by wind, we found that lizards, while obtaining energy resources from this gymnosperm, they are relevant for its reproduction as they (i) transport large amounts of pollen from male to female cones when feeding on pollination drops, (ii) increase the germination of light seeds and (iii) act as their main seed dispersers, at least on Dragonera Island (Rodríguez-Pérez et al 2012; Neghme et al 2017; this study)
Summary
Most plants that depend on animal pollination and seed dispersal are often served by different taxa for each of these ecological functions (Herrera and Pellmyr 2002). Despite the increasing number of studies reporting vertebrates as opportunistic nectar consumers (Traveset and Sáez 1997; Banack 1998; Olesen and Valido 2003; OrtegaOlivencia et al 2005; Sazima et al 2005; Le Péchon et al 2013; da Silva et al 2014; Traveset et al 2015; Zoeller et al 2016), still few evaluate the quantitative and qualitative component of pollination effectiveness (but see Rodríguez-Rodríguez and Valido 2008; Hansen and Müller 2009a; Ortega-Olivencia et al 2012; RodríguezRodríguez et al 2013; Hervías-Parejo and Traveset 2018; Ratto et al 2018) Such information is relevant, especially if we want to foresee the consequences of potential mutualistic disruptions due to the different drivers of global change (Toby Kiers et al 2010). Behaviour which might influence both the pollination and seed dispersal processes (Rodríguez-Rodríguez et al 2013; Pérez-Méndez et al 2018)
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