Investigating the relationship between pollination strategies and the size- advantage model in zoophilous plants using the reproductive biology of Arum cylindraceum and other European Arum species as case studies Natacha Revel, Nadir Alvarez, Marc Gibernau & Anahí Espíndola Arthropod-Plant Interactions An international journal devoted to studies on interactions of insects, mites, and other arthropods with plants ISSN 1872-8855 Volume 6 Number 1 Arthropod-Plant Interactions (2012) 6:35-44 DOI 10.1007/s11829-011-9164-1 1 23 Your article is protected by copyright and all rights are held exclusively by Springer Science+Business Media B.V.. This e-offprint is for personal use only and shall not be self- archived in electronic repositories. If you wish to self-archive your work, please use the accepted author’s version for posting to your own website or your institution’s repository. You may further deposit the accepted author’s version on a funder’s repository at a funder’s request, provided it is not made publicly available until 12 months after publication. 1 23 Author's personal copy Arthropod-Plant Interactions (2012) 6:35–44 DOI 10.1007/s11829-011-9164-1 ORIGINAL PAPER Investigating the relationship between pollination strategies and the size-advantage model in zoophilous plants using the reproductive biology of Arum cylindraceum and other European Arum species as case studies Natacha Revel • Nadir Alvarez • Marc Gibernau • Anahı´ Espı´ndola Received: 4 August 2011 / Accepted: 11 October 2011 / Published online: 29 October 2011 Ó Springer Science+Business Media B.V. 2011 Abstract The size-advantage model (SAM) explains the variation of arthropods trapped in inflorescences, we show temporal variation of energetic investment on reproductive that some species (i.e. A. cylindraceum and A. italicum) structures (i.e. male and female gametes and reproductive display a generalist reproductive strategy, relying on the organs) in long-lived hermaphroditic plants and animals. It exploitation of a low number of dipterans, in contrast to the proposes that an increase in the resources available to an pattern seen in the specialist A. maculatum (pollinated organism induces a higher relative investment on the most specifically by two fly species only). Based on the model energetically costly sexual structures. In plants, pollination presented here, the application of the SAM is predicted for interactions are known to play an important role in the the first two and not expected in the latter species, those evolution of floral features. Because the SAM directly predictions being further confirmed by allometric mea- concerns flower characters, pollinators are expected to have sures. We here demonstrate that while an increase in the a strong influence on the application of the model. This female zone occurs in larger inflorescences of generalist hypothesis, however, has never been tested. Here, we species, this does not happen in species demonstrating investigate whether the identity and diversity of pollinators specific pollinators. This is the first time that this theory is can be used as a proxy to predict the application of the both proposed and empirically tested in zoophilous plants. SAM in exclusive zoophilous plants. We present a new Its overall biological importance is discussed through its approach to unravel the dynamics of the model and test it application in other non-Arum systems. on several widespread Arum (Araceae) species. By identi- fying the species composition, abundance and spatial Keywords Sex allocation Á Plant–insect interactions Á Araceae Á Flower evolution Á Reproductive strategy Handling editor: Jonathan Lundgren Electronic supplementary material The online version of this Introduction article (doi:10.1007/s11829-011-9164-1) contains supplementary material, which is available to authorized users. Energetic income is limited in all organisms, and natural selection optimises resource allocation strategies between N. Revel Laboratory of Evolutionary Entomology, Institute of Biology, growth/survival and reproduction according to physiolog- University of Neuchaˆtel, Emile-Argand 11, 2009 Neuchaˆtel, ical and environmental (biotic and abiotic) factors Switzerland (Policansky 1982; Lloyd and Bawa 1984; Guillon et al. 2006). As a consequence, it has been proposed that in N. Alvarez Á A. Espı´ndola (&) Department of Ecology and Evolution, University of Lausanne, hermaphroditic and long-lived organisms, the reproductive Biophore Building, 1015 Lausanne, Switzerland energetic allocation varies with the size of the organism. In e-mail: [email protected] general, when the amount of available resources increases, the size of an organism tends to increase, which favours the M. Gibernau CNRS-UMR 8172 Ecologie des Foreˆts de Guyane, BP 709, relative increase in the number of the most costly sexual 97387 Kourou, France structures. This model, namely the size-advantage model 123 Author's personal copy 36 N. Revel et al. (SAM), was first proposed (Ghiselin 1969) and tested pollination is expected to be low. In such circumstances, (Warner 1988) in animals, but was later applied to dioe- female gametes should be favoured in large plants, because cious and hermaphroditic plants (Lloyd and Bawa 1984), pollen dispersion is expected to be low and intra-plant e.g., in species within the genera Acer L. (Sapindaceae) pollen competition expected to be high (Klinkhamer et al. (Primack and McCall 1986), Arisaema Mart. (Araceae) 1997). In addition, by investing in female flowers, the (Vitt et al. 2003) and Arum L. (Araceae) (Me´ndez 2001). number of pollinated ovules would quickly increase as According to the model, floral resource allocation, i.e. soon as an eventual pollen-carrier visits the flower. In the quantity of energy invested by a plant in the production contrast, an investment in male gametes in such a situation of female versus male sexual structures (Lloyd and Bawa would translate into a large male gamete loss. Alterna- 1984), depends on the energy available at a certain time: tively, if pollinators are abundant, cross-pollination is when only the amount of available resources increases, efficient, or both, the probability of cross-pollination is plants can become bigger and thus present larger inflores- expected to be high. In such a situation, it is likely that the cences, which are predicted to harbour a higher proportion pollen produced will present a high probability of reaching of female flowers (i.e. the most energetically costly sexual another flower, diminishing potential intra-plant pollen structure) than smaller inflorescences of the same species. competition. Matching the SAM in such a context is Since its first application, the comprehensiveness of the expected to be counter-selected because the plant has the SAM has been progressively enhanced by the inclusion of possibility to favour both its fruit set and male gamete additional factors such as local sexual competition and dispersion (Chartier and Gibernau 2009). differential gamete dispersion (Lloyd and Bawa 1984), While the number of pollinators visiting a plant is wind-pollination syndromes (Burd and Allen 1988), plant simple to quantify, the efficiency of pollination could be geometry (Bickel and Freeman 1993), variation in envi- inferred from pollinator diversity (in terms of number of ronmental quality (Guillon et al. 2006) and mortality risks different taxa visiting a flower). This can be considered as a (Brooks and Iwasa 2010). However, even if pollination proxy of the level of specificity of a plant species’ total biology is known to strongly shape floral characters (Raven pollination interaction (along a continuum between gen- et al. 2005), few studies have tested its influence on the eralist and species-specific pollination, Ollerton et al. 2007) application of the SAM. A notable exception is the general and thus indirectly represents the proportion of specific study presented by Cruden (1977), largely criticised by pollen that pollinators bring to the flower. It is important to Charnov (1982) some years later. The basis of this criticism mention here that the level of specificity of the interaction relied on Cruden’s assumption that male reproductive in this case is then considered to be happening at the pol- success was a function of seed-set only, indirectly sug- linator species and not at the individual level (Chittka et al. gesting that male gametes had no effect on the final fitness 1999). From this perspective, a generalist pollinator species gain of the plant. As a result of this well-founded criticism, would carry mostly non-specific pollen, thus representing studies that considered the effect of pollination system on an inefficient crosser (Harder and Thomson 1989), while SAM became rare (Barrett et al. 1996). From a modelling the opposite should be true for a specific pollinator. We approach, the lack of investigation on this topic might have would thus expect generalist flowers to apply the SAM, also been a consequence of the complexity of some since male gamete losses are very likely to occur. mathematical models developed to understand the SAM The overall probability of cross-pollination in a zoophi- (Guillon et al. 2006). lous plant appears then to be related both to the efficiency of Despite the criticism and the apparent complexity of the pollinators (i.e. its visitation rate, constancy and capability to subject, we consider that some simple predictions may be cross-pollinate) and to the nature of the interaction proposed regarding the possible influence of pollinators on (i.e. specific or generalist). From this perspective, we expect the investment towards a given gamete type. Historically, that very efficient and specific pollinators would provide a Lloyd and Bawa (1984) proposed that a gamete positive- high probability of cross-pollination, which would not bias is expected for the gamete dispersing longer distances, favour the application of the SAM, because high rates of since this would avoid intra-plant gamete competition. pollen dispersion and low intra-plant gamete competition are Here, we revisit this hypothesis from the point of view of expected. Selection towards SAM expression should be an pollinators.