Functional trait mismatch between native and introduced bee pollinators servicing a global fruit crop

Understanding connections between biodiversity and ecosystem services can be enhanced by shifting focus from species richness to functional trait-based approaches, that when paired with comparative phylogenetic methods can provide even deeper insights. We investigated the functional ecology and phylogenetic diversity of pollination services provided by hymenopteran insects visiting apple flowers in orchards surrounded by either 'natural' or 'disturbed' landscapes in New South Wales, Australia. We assessed whether morphological and behavioural traits (hairiness, body size, glossa length, pollen load purity, and probability of loose pollen) exhibited non-random phylogenetic patterns. Then, explored whether bees, the primary pollinators in this system, filled unique or overlapping functional entities (FEs). For each landscape, we calculated phylogenetic diversity and used FEs to assess functional richness, evenness, and diversion.

A phylogenomic matrix based on ultraconserved elements (UCEs; 1,382,620 bp from 1,969 loci) was used to infer a fully-resolved and well-supported maximum likelihood phylogeny for 48 hymenopteran morphospecies. There was no significant difference in species richness between landscape categories. Pollinator communities at natural sites had higher phylogenetic complexity (X = 2.37) and functional divergence (x̄ = 0.74 ± 0.02 s.e.) than disturbed sites (X = 1.65 and x̄ = 0.6 ± 0.01 s.e.). Hairiness showed significant phylogenetic clustering (K = 0.94), whereas body size, glossa length, and loose pollen showed weaker non-random phylogenetic patterns (K between 0.3-0.5). Pollen load purity showed no association with phylogeny. The assemblage of 17 bee morphospecies comprised nine FEs: eight FEs consisted of native bees with three containing 65% of all native bee taxa. The introduced honey bee (Apis mellifera) occupied a unique FE, likely due to its different evolutionary history. Both landscape types supported six FEs each with three overlapping: two native bee FEs and the honey bee FE.

Bee hairiness was the only functional trait to exhibit demonstrable phylogenetic signal. Despite differences in species richness, and functional and phylogenetic diversity between orchard landscape types, both maintained equal bee FE numbers. While no native bee taxon was analogous to the honey bee FE, four native bee FEs shared the same hairiness level as honey bees. Health threats to honey bee populations in Australia will likely disrupt pollination services to apple, and other pollination-dependent food crops, given the low level of functional redundancy within the investigated pollinator assemblages.