Nectar robbing rather than pollinator availability constrains reproduction of a bee‐flowered plant at high elevations

Abstract

Abiotic factors are generally assumed to determine whether species can exist at the extreme ends of environmental gradients, for example, at high elevations, whereas the role of biotic interactions is less clear. On temperate mountains, insect‐pollinated plant species with bilaterally symmetrical flowers exhibit a parallel elevational decline in species richness and abundance with bees. This suggests that the lack of mutualistic interaction partners sets the elevational range limits of plants via a reduction in reproductive success. We used the bee‐pollinated mountain plant Clinopodium alpinum (Lamiaceae), which blooms along a continuous 1000‐m elevational gradient and has bilaterally symmetrical flowers, as a model to test the predicted parallel elevational decline in flower visitation and seed production. Although the community of flower visitors changed with elevation, the flower visitation rate by the most frequent visitors, bumble bees (33.8% of legitimate visits), and the overall rate of flower visitation by potential pollinators did not vary significantly with elevation. However, we discovered that nectar robbing by bumble bees and nectar theft by ants, two interactions with potentially negative effects on flowers, sharply increased with elevation. Seed set depended on pollinators across elevations and followed a weak hump‐shaped pattern, peaking at mid‐elevations and decreasing by about 20% toward both elevational range edges. Considering the mid‐ and high elevations, elevational variation in seed production could not be explained by legitimate bee visitation rates but was inversely correlated with the frequency of nectar robbing. Our observations challenge the hypothesis that a decrease in the availability of pollinators limits seed production of bee‐flowered plants at high elevations but suggest that an increase in negative interactions (nectar robbing and larceny) constrains reproductive success.

Nectar robbing effects on pollinators of a key nectar source plant (Tecoma fulva, Bignoniaceae) in a dry tropical Andean valley

“…Individual plants were considered as random factor. Pooled number of visits per flower category (unrobbed, primary robbed, and secondary robbed) was used as response variable, with 20 replicates per category (i.e., Kohl & Steffan‐Dewenter, 2022). In addition, we also evaluated pooled visits to compare unrobbed vs robbed flowers (all primary and secondary robbed flowers).…”

“…Negative effects have been found for avian pollinators as some birds may be able to detect changes in nectar supply and are therefore less likely to visit nectar-robbed flowers (Irwin, 2000;Richman et al, 2017). In contrast, the effects usually can be neutral and positive when pollinators and nectar robbers are both insects (Irwin et al, 2001(Irwin et al, , 2010, as they may not be able to detect differences in nectar reward (but see Kohl &Steffan-Dewenter, 2022, andTie et al, 2023).…”

Nectar robbing by bees affects the reproductive fitness of the distylous plant Tirpitzia sinensis (Linaceae)

“…Sprengel (1793) first reported that Bombus species pierced the nectar spur, and Darwin (1859, 1876) also observed Bombus species robbing the nectar of Trifolium pratense . Since then, an increasing number of studies have focused on the ecology of nectar‐robbing behavior (Bronstein et al., 2017; Kohl & Steffan‐Dewenter, 2022; Richman et al., 2021). Nectar robbing is widely observed in nature and has been found in 59 families and 214 genera (Irwin et al., 2004), such as Polemoniaceae (Irwin & Brody, 1999), Gentianaceae (Zhang et al., 2011), and Rubiaceae (Pimienta & Koptur, 2022), and usually occurs in homostylous plants with long floral tubes or nectar spurs.…”

“…Sprengel (1793) first reported that Bombus species pierced the nectar spur, and Darwin (1859Darwin ( , 1876) also observed Bombus species robbing the nectar of Trifolium pratense. Since then, an increasing number of studies have focused on the ecology of nectar-robbing behavior (Bronstein et al, 2017;Kohl & Steffan-Dewenter, 2022;Richman et al, 2021).…”