Pollen transfer networks reveal alien species as main heterospecific pollen donors with fitness consequences for natives

Abstract

The ecological dynamics of co‐flowering communities are largely mediated by pollinators. However, current understanding of pollinator‐mediated interactions primarily relies on how co‐flowering plants influence attraction of shared pollinators, and much less is known about plant–plant interactions that occur via heterospecific pollen (HP) transfer. Invaded communities in particular can be highly affected by the transfer of alien pollen, but the strength, drivers and fitness consequences of these interactions at a community scale are not well understood. Here we analyse HP transfer networks in nine coastal communities in the Yucatan Mexico that vary in the relative abundance of invasive flowers to evaluate how HP donation and receipt varies between native and alien plants. We further evaluate whether HP donation and receipt are mediated by floral traits (e.g. display, flower size) or pollinator visitation rate. Finally, we evaluated whether post‐pollination success (proportion of pollen tubes produced) was affected by alien HP receipt and whether the effect varied between native and alien recipients. HP transfer networks exhibit relatively high connectance (c. 15%), suggesting high HP transfer within the studied communities. Significant network nestedness further suggests the existence of species that predominantly act as HP donors or recipients in the community. Species‐level analyses showed that natives receive 80% more HP compared to alien species, and that alien plants donate 40% more HP than natives. HP receipt and donation were mediated by different floral traits and such effects were independent of plant origin (native or alien). The proportion of alien HP received significantly affected conspecific pollen tube success in natives, but not that of alien species. Synthesis. Our results suggest that HP transfer in invaded communities is widespread, and that native and alien species play different roles within HP transfer networks, which are mediated by a different suite of floral traits. Alien species, in particular, play a central role as HP donors and are more tolerant to HP receipt than natives—a finding that points to two overlooked mechanisms facilitating alien plant invasion and success within native co‐flowering communities.

Impacts of plant invasions in native plant–pollinator networks

“…adaptive foraging) (Richardson et al ., 2000; Valdovinos, 2019), and more recently (3) tolerance to changes in pollen transfer dynamics among plant species (heterospecific pollen (HP) transfer, e.g. Arceo‐Gómez & Ashman, 2016, Parra‐Tabla et al ., 2021) (Fig. 1a).…”

“…For instance, in order to fully integrate into native PPN invasive plants may need to successfully avoid (minimize HP deposition on stigmas), or tolerate (minimize the reproductive cost of HP receipt), the negative effects of HP receipt (Fig. 1a; specific HP tolerance and avoidance mechanisms are reviewed in Ashman & Arceo‐Gómez (2013); also see Arceo‐Gómez & Ashman, 2016, Suárez‐Mariño et al ., 2019, Parra‐Tabla et al ., 2021). Evidence of HP tolerance or avoidance as a mechanism facilitating plant species invasion and ‘integration’ into PPN is still scarce.…”

“…Evidence of HP tolerance or avoidance as a mechanism facilitating plant species invasion and ‘integration’ into PPN is still scarce. However, recent studies have shown some of the first empirical evidence suggesting a greater ability of invasive species in avoiding and tolerating negative HP fitness effects (Suárez‐Mariño et al ., 2019; Parra‐Tabla et al ., 2021). Interestingly, a meta‐analysis of 56 study cases has also revealed that invasive HP donors tend to cause a stronger decrease in seed production compared to native HP donors (Arceo‐Gómez & Ashman, 2016).…”

“…2; Suárez‐Mariño et al ., 2019). Thus, although still limited, the combined evidence so far suggests that HP tolerance and avoidance strategies may play a so far overlooked role in mediating the ‘integration’ of invasive species into native PPN (Arceo‐Gómez & Ashman, 2016; Suárez‐Mariño et al ., 2019; Parra‐Tabla et al ., 2021).…”

“…Specifically, both studies show that invasive species are better pollen donors and play more central roles (i.e. hubs) within HP transfer networks than natives (Johnson & Ashman, 2018; Parra‐Tabla et al ., 2021). One study also showed that native plants are more affected (stronger decrease in reproductive success) by HP than invasives (Parra‐Tabla et al ., 2021).…”