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

Diversity’s link to ecosystem services, like pollination, can be better understood with a shift from focusing on species richness to functional trait-based approaches, which can provide more insight, particularly when paired with comparative phylogenetics. Here, we assessed the functional ecology and phylogenetic diversity of hymenopterans visiting apple flowers in orchards surrounded by either ‘natural’ or ‘disturbed’ landscapes. We investigated 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. 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 a 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.

Description of the data and file structure

1. aln-short-final.phy - Aligned bp sequence data for 48 Hymenopteran morphospecies obtained from ultra-conserved element phylogenomics (1,382,620 DNA nucleotide base pairs from 1,969 loci).

2. bee_traits.pl.csv - Trait matrix of three functional traits (body size as measured by ITD, glossa length, and hairiness) for the bee morphospecies documented visiting Pink Lady apple flower (NSW, Australia) rounded to the nearest integer. Columns include Morphospecies (the morphospecies identity for each of the 17 bee morphospecies included in analyses), ITD (in mm; Inter-tegular distance, the distance between an insect's tegulae and a proxy for body size), Glossa (in mm; glossa or tongue length), and Hairiness_index (a 13 point evaluation of an insect's hairiness scaled from 0 to 1). For the three functional traits (ITD, Glossa, and Hairiness index), a value close to zero indicates a small value for this trait, whereas a higher value (maximum value is 5) indicates a larger value for this trait. Trait values here are scaled for the whole community into integers for functional diversity analyses, raw trait values for the whole evaluated Hymenopteran community.

3. bee.comm.pl.csv - Bee community matrix (based on morphospecies identification) across farms and years. Each row represents the assemblage from a single farm on a year (in the format FF_PL_YY where FF stands for the farm's initials and YY represents the year (2018 as 18 and 2019 as 19)). Farms in Bilpin include BS, CL, SS, and TT, and farms in Orange are GE, JC, and RC. The first column represents the previously described farm and year identity, and all subsequent columns represent the abundance of individual morphospecies for the 17 bee morphospecies in these analyses; a value of zero indicates that that morphospecies was not detected on that farm in that year.

4. contree.nex - Nexus tree file used to create a consensus phylogenetic tree for 48 Hymenopteran morphospecies, which is identical to the Maximum-likelihood tree.

5. final.nex - Nexus tree file used to calculate phylogenetic diversity and to make Figure S2.

6. frequency.csv - Hymenopteran morphospecies frequency on Pink Lady apple flowers organized by region (Bilpin or Orange) and the data set used to make Figure S1.

7. traits.csv - Functional trait matrix for all members of the Hymenopteran assemblage with 5+ individuals. The first column contains the morphospecies name and the subsequent five columns contain the values for the five functional traits evaluated in this study. ITD (in mm; intertegular distance, a measure of body size), Glossa (in mm; glossa or tongue length), and Hairiness_index (0-1) were measured in this study, Pollen load purity (proportion of apple pollen present within the body pollen carried by the insect), and Dry pollen (probability that the insect carried loose dry pollen on their body) were obtained from Bernauer et al. 2022(opens in new window).