Why are some plant–nectar robber interactions commensalisms?

Abstract

Many plants that bear hidden or recessed floral nectar experience nectar robbing, the removal of nectar by a floral visitor through holes pierced in the corolla. Although robbing can reduce plant reproductive success, many studies fail to find such effects. We outline three mechanistic hypotheses that can explain when interactions between plants and nectar‐robbers should be commensal rather than antagonistic: the non‐discrimination (pollinators do not avoid robbed flowers), visitor prevalence (robber visitation is rare relative to pollinator visitation), and pollen saturation (stigmas receive sufficient pollen to fertilize all ovules with one or very few pollinator visits) hypotheses. We then explore these mechanisms in the North American subalpine, bumble bee‐pollinated and nectar‐robbed plant Corydalis caseana (Fumariaceae). We first confirmed that the effects of nectar robbing on female reproductive success were neutral in C. caseana. We then tested the three mechanisms underlying these neutral effects using a combination of observational studies and experiments. We found evidence for all three mechanisms. First, consistent with the non‐discrimination hypothesis, pollinators failed to discriminate against experimentally robbed flowers or inflorescences even though naturally robbed flowers offered significantly lower nectar rewards than unrobbed flowers. Second, C. caseana was more commonly visited by pollinators than by nectar robbers, in accordance with the visitor prevalence hypothesis. Third, stigmas of unvisited flowers as well as those visited once by pollinators were saturated with pollen, with all stigmas bearing pollen loads several orders of magnitude higher than the number of ovules per fruit, consistent with the pollen saturation hypothesis. Our investigation of the mechanisms driving the commensal outcome of nectar robbing in this system deepens our understanding of the ecology of nectar robbing and contributes to a more general understanding of the variation in the outcomes of interactions between species.

Nectar robbing and plant reproduction: an interplay of positive and negative effects

“…These processes, together with the reproductive traits, allow the plant to achieve similar outputs in robbed and non-robbed flowers because crosspollination can be fulfilled either by legitimate visitors or by nectar robbers. Therefore, although in some plant-pollinator-nectar robbing systems the neutral consequences for the plants are the result of nectar robbers being commensals with negligible effects on plant fitness (Heiling et al 2018), in other systems nectar robbers deliver negative but also positive consequences, both directly or indirectly, implying changes in pollination services by legitimate visitors (Hazlehurst and Karubian 2016 and this study).…”

“…To achieve this objective, we studied the details of the reproductive compatibility system of the plant by comparing pollen tube growth after manual crossings with different pollen donors, and with pollen tube growth after single visits of the most common nectar robbers. The second hypothesis is that the neutral effects observed in L. etrusca are related to a commensalistic interaction, as observed by Heiling et al (2018), with legitimate pollinators maintaining similar foraging behaviour despite nectar robbing. To test this hypothesis we addressed a second objective that was to test whether visitation rates of nectar robbers affect visitation rates of legitimate visitors.…”

“…Also, neutral consequences have been inferred when no significant consequences for plant reproduction occurs (Navarro et al 1993, Morris 1996). In the latter, nectar robbers are considered commensals that do not carry costs or benefits for the plant (Heiling et al 2018). This can occur when the foraging behaviour of legitimate visitors is not modified by robbing, allowing the plant to maintain reproductive success (Maloof 2000, 2001).…”

Novel nectar robbing negatively affects reproduction in Digitalis purpurea

“…In contrast to findings we present here, many studies suggest robbing can have limited or no negative effects on the female component of fitness (Andalo et al., 2019 ; Carrió & Güemes, 2019 ; Maloof, 2001 ; Richardson, 2004 ; dos Santos et al., 2020 ; Varma et al., 2020 ; Varma & Sinu, 2019 ; Zimmerman & Cook, 1985 ). This lack of an effect on reproductive output could be due to the legitimate pollinators still visiting the plant and saturating the stigmas with enough pollen so the plant can achieve full seed set (Heiling et al., 2018 ; Stout et al., 2000 ). One potential caveat in this study is that our ability to detect differences in mean seed production could be biased by the standardized three‐hour visitation periods per day in our experiment.…”

Do honeybees act as pollen thieves or pollinators of <i>Datura wrightii</i>?

“…Florivores reduce plant fitness either directly through consumption of gametes, or indirectly by affecting pollinator activity (McCall & Irwin 2006;González-Browne 2016) but there are also cases where florivores have a negligible effect on fitness components (Pohl 2006;McCall 2007), Another relationship is nectar robbery, wherein an organism acquires nectar without pollination. Nectar robbing often results in decreased female plant fitness (González-Browne et al 2016) but neutral (Rojas-Nossa et al 2016;Heiling et al 2018) or positive effects on plant fitness are also possible (see Irwin et al 2010 andSingh et al 2014).…”