Widespread vulnerability of flowering plant seed production to pollinator declines

Abstract

Despite evidence of pollinator declines from many regions across the globe, the threat this poses to plant populations is not clear because plants can often produce seeds without animal pollinators. Here, we quantify pollinator contribution to seed production by comparing fertility in the presence versus the absence of pollinators for a global dataset of 1174 plant species. We estimate that, without pollinators, a third of flowering plant species would produce no seeds and half would suffer an 80% or more reduction in fertility. Pollinator contribution to plant reproduction is higher in plants with tree growth form, multiple reproductive episodes, more specialized pollination systems, and tropical distributions, making these groups especially vulnerable to reduced service from pollinators. These results suggest that, without mitigating efforts, pollinator declines have the potential to reduce reproduction for most plant species, increasing the risk of population declines.

Fig. 1.. Global dataset of pollinator contribution (PC) in wild flowering plants.

PC measures the proportion of seed production that is attributable to pollinator visitation, with values of 0 indicating that pollinators do not affect seed production and values of 1 indicating that seed production only occurs when pollinators visit flowers. (A) Frequency distribution, (B) phylogenetic distribution, and (C) geographical distribution of PC in our dataset. The frequency distribution (A) is based on our dataset of 1174 animal-pollinated species adjusted for 12% of angiosperm species being wind-pollinated (1). First quartile = 0.08; third quartile = 1. For the left-hand bar, colors represent species as follows: gray, PC = 0 due to wind pollination; stippled blue, PC = 0 although visited by animal pollinators; solid blue, 0 < PC < 0.05. For the right-hand bar, colors represent species as follows: stippled red, PC = 1; solid red, 0.95 < PC < 1. For other colored bars, colors represent PC as indicated in the legend at bottom right. On the phylogeny (B), angiosperm orders and the Magnoliid clade are shown with segments around the outside and PC values are depicted by the color of the bars. There is significant phylogenetic signal in PC (λ = 0.452, P < 0.001). The points on the map (C) represent study locations, with color indicating population PC values and the line graph to the right indicating the latitudinal pattern in PC in animal-pollinated species from a loess fit (not controlling for phylogeny or any additional variables). Wind-pollinated species are not represented on the phylogeny (B) and map (C).

Fig. 2.. Pollinator contribution is related to plant functional group, flower morphological specialization, number of pollinator functional groups, and alien status.

All trees and shrubs analyzed are polycarpic (having multiple reproductive episodes). Specialized flowers are those with bilateral symmetry, specialized shapes, specialized rewards, and/or restricted access to rewards. Examples of pollinator functional groups are bats, nonflying mammals, and hymenopterans (bees and wasps). Different levels of the same factors are shown in the same color, and different letters above boxes of the same color indicate significant differences between factor levels in phylogenetic generalized least squares analyses. Numbers below boxes indicate sample sizes (populations). Diamonds indicate means and horizontal lines across boxes indicate medians. Tops and bottoms of boxes indicate quartiles and whiskers that extend to the last value within 1.5 times the interquartile range.

Fig. 3.. Vulnerability of flowering plants to future pollinator declines through pollinator contribution and opportunities for reproduction.

Pollinator declines will have little impact on seed production of species with low PC (bottom two quadrants). Plant species with high PC (top two quadrants) will experience reduced seed production if their pollinators decline. However, those that are longer lived and have multiple opportunities to reproduce (top left quadrant) are only expected to experience population declines after a lag period, while short-lived species that reproduce only once in their lives (top right quadrant) may experience more rapid population declines when their pollinators decline. The 12% of angiosperm species that are resilient to pollinator decline due to wind pollination are shown by the gray slice. The photographs show representative species for each category of animal-pollinated angiosperm species, clockwise from top right: Digitalis purpurea, Silene noctiflora, Acacia dealbata, and Rhododendron calendulaceum. Images from inaturalist.org by L. Jiang (CC-BY 4.0), C. Altmann (CC-BY 4.0), J. Sullivan (CC-BY 4.0), and E. M. Eraskin (CC-BY 4.0).