Exclusion of bird pollinators impacts mating system and reduces offspring fitness in a pollination-generalist tree

Compared to pollinating insects and non-flying mammals (NFM), nectarivorous birds may display behaviours leading to greater pollen carryover. Therefore, plants pollinated by birds may display higher levels of paternal diversity and outcrossing than those pollinated by insects and NFM, with associated fitness benefits for seeds and seedlings. Here, we test these predictions using a plant where birds, insects and NFM are all frequent visitors to flowers. An experiment manipulating access to flowers of Banksia menziesii (Proteaceae) was conducted. Treatments applied to whole plants were: (i) open to all pollinators; (ii) insect access, birds and NFM excluded; (iii) NFM access, insects and birds excluded; and (iv) complete pollinator exclusion. Reproductive output was quantified in terms of fruit and seed production. The genetic consequences for offspring were tested using microsatellite markers to genotype individuals and quantify the mating system, and through field trials to quantify seedling vigour. When birds were excluded from flowers, maternal fitness was reduced. Compared to open pollinated flowers, fruit set was reduced by 76% when only NFM could access flowers. When only insects (primarily introduced honeybees) could access flowers, the number of viable seeds per fruit was reduced by 20% because the proportion of aborted seeds doubled, compared to pollination that included birds. For seedlings, heterozygosity was reduced by 22%, outcrossing rates by 30%, and paternal diversity by 15%, when birds were excluded. Seedling mortality was strongly associated with inbreeding, and selfing largely only occurred when birds were excluded. All parameters were lowest when only NFM had access to flowers. Although honeybees were effective pollinators of B. menziesii due to their abundance, birds were inferred to be the most effective, with their exclusion resulting in a reduction of fecundity and offspring vigour. These negative effects were largely a consequence of selection against the products of self-pollination, which was associated with pollination by insects or NFMs. Our findings highlight how a genetic component of pollination that increases offspring fitness could favour the evolution of bird pollination.