Anthropogenic impacts on pollination networks and plant mating systems

Abstract

School of Natural Sciences and Trinity Centre for Biodiversity Research, Trinity College Dublin, Dublin 2, IrelandHabitat modification and fragmentation through humanactivity are key drivers of change to plant–pollinationinteractions (Kuldna et al. 2009; Winfree et al. 2009).Many studies have focussed on the effects of these driverson pollinator species richness and diversity, plant repro-ductive success, and community composition of bothpollinators and plants (e.g. Eckert et al. 2010; Montero-Castano & Vil~ a 2012; Stanley & Stout 2013). Recently,there has been a huge increase in the number of studiesusing food web approaches to quantifying impacts of habi-tat modification on plant–pollinator interaction networks(e.g. Forup et al. 2008; Vila et al. 2009; Power & Stout2011; Geslin et al. 2013). By analysing changes to thestructure of interaction networks, specifically changes toparameters such as interaction symmetry and diversity,nestedness and connectance, authors have attempted totest how anthropogenic activity affects the stability of com-munities (Tylianakis et al. 2010). However, visitation net-works do not necessarily reflect pollination events (King,Ballantyne & Willmer 2013), and few studies have linkedcommunity-level interaction networks with variation inplant mating (including outcrossing rates, paternity, iden-tity of pollen donors), meaning that the relationshipsbetween network structure and plant reproductive functionhave not been clear (Gomez, Perfectti & Jordano 2011).In this issue of Functional Ecology, Vanbergen et al.(2014) quantified the effect of livestock grazing in wood-lands, and surrounding habitat context, on not only visita-tion networks, but also on plant mating systems. Manystudies have shown that highly mobile pollinator speciesabundance and diversity can be influenced by the composi-tion and configuration of the landscape around the site inwhich they are being sampled, although there are taxon-specific differences in responses (e.g. Rundlof, Bengtsson S Kennedy et al. 2013). This can influenceinsect-pollinated plant communities (Power, Kelly & Stout2012) and can be modified by local processes such as graz-ing intensity (Sjodin, Bengtsson & Ekbom 2008). However,few studies have analysed whether interaction networkstructure varies with landscape context (Kaartinen R Ferreira, Boscolo & Viana 2013), and nonehave taken the next step and examined the consequencesfor plant mating systems. Using the self-compatible marshthistle, Cirsium palustre, as a model species, Vanbergenet al. (2014) were able to relate both local management(presence or absence of livestock grazing) and landscapecontext (habitat of the surrounding area) with networkparameters, as well as outcrossing rates, paternity, inbreed-ing and relatedness among pollen donors of C. palustre.In general, there is a trade-off associated with creatingnetworks to test hypotheses about human impacts onplant–pollinator interactions: in order to make generalconclusions and encompass site to site variation, a largenumber of sites are required; but sampling at each site istime-consuming, requires high taxonomic resolution, andthe sampling method used can influence the structure ofthe network (Hegland et al. 2010; Gibson et al. 2011;Chacoff et al. 2012). Partners interacting in a network canalso vary greatly from year to year (Petanidou et al. 2008).Thus, the temporal and spatial resolution of studies usinga network approach is usually limited (Kaiser-Bunburyet al. 2010). In this case, the trade-off used by Vanbergenet al. (2014) was to sample eight sites for a relatively shortperiod (10 mins), but each site was visited 20 timesthroughout a single season to quantify interaction net-works. The authors demonstrated that this sampling wassufficient to represent structural properties (connectance),if not species richness. By combining network data withdata on the mating system of C. palustre, this studyrevealed some interesting patterns.For example, Vanbergen et al. (2014) showed that graz-ing increased species richness of floral resources (but notabundance of flowers) and resulted in more species interac-tions. If the study had stopped here, we might have con-cluded that there were positive impacts of grazing onpollination interactions and pollination services. However,visitation networks were less nested in grazed sites, andsince nestedness confers robustness, grazed networks maybe more vulnerable to species and habitat loss and furtherenvironmental changes (Memmott, Waser & Price 2004;Fortuna & Bascompte 2006). In addition, using microsatel-lites to genotype seeds of C. palustre to determine matingsystem parameters, Vanbergen et al. (2014) found that out-crossing rates in C. palustre decreased as networks becamemore connected in grazed habitats. This was despite the