The role of mutualisms in the evolution of flower and fruit traits in the Haemanthinae (Amaryllidaceae)

Abstract

Diversification of flower and fruit traits are distinctive features of angiosperm radiation. Evolutionary shifts between different animal pollinator groups are usually accompanied by modifications in flower traits. Similarly, shifts between different animal seed dispersers are usually accompanied by modifications of fruit traits. The aim of this study was to assess the functional importance of flower and fruit traits in the African sub-tribe Haemanthinae (Amaryllidaceae) which consists of the closely related genera Scadoxus and Haemanthus. These genera occur in multiple habitats and exhibit a diversity of floral and fruit traits that are potentially related to their pollination and seed dispersal systems which has not been previously studied. The species of Scadoxus can be categorized according to two types of inflorescence architecture – ‘paintbrush’, where the reproductive parts of the flowers are tightly packed together, or ‘open brush’, where the reproductive parts are widely spaced. All Haemanthus species have ‘paintbrush’ inflorescences. I investigated the functional significance for pollination of these two inflorescence types. The genus Scadoxus appears to have undergone several shifts from butterfly to bird pollination. I found that both subspecies of S. multiflorus with open brush inflorescences are pollinated by butterflies and that S. puniceus and S. membranaceus with paintbrush inflorescences are pollinated by sunbirds. The system of butterfly pollination involves pollen being transferred from plant to plant via the surface of the butterfly’s wings. This system, previously thought to be unusual, is apparently common in the South African Amaryllidaceae and I speculated that nine species are pollinated this way. I found that S. multiflorus subspecies katherinae displays a system of late-acting self-incompatibility, whereby the tubes of self pollen are stopped at the ovary, as shown previously for other Amaryllidaceae. Self-incompatibility was also found for the sunbird pollinated S. puniceus. Intriguingly, S. membranaceus, which is very similar in appearance to S. puniceus, but rarely visited by sunbirds in its coastal forest habitat, was found to be self-compatible and capable of autonomous seed production. The genus Haemanthus, a sister clade to Scadoxus, occurs only in South Africa and Namibia, and consists entirely of species with ‘paintbrush’ style inflorescences. Haemanthus deformis is geoflorous with a very short peduncle and is pollinated by sunbirds that stand on the ground next to the inflorescence and bend over to feed on the nectar in the flowers. In the closely related H. albiflos, the inflorescence stem is longer and used as a perch. Both species have white flowers which is unusual for sunbird-pollinated plants. Haemanthus coccineus is found in the Cape Floral Region and has red flowers and bracts. This species has a much longer peduncle and is pollinated by sunbirds which grip onto the peduncle or bracts when feeding. H. humilis subsp. hirsutis is also visited by sunbirds which use the long peduncle as a perch when feeding on the pink flowers. Selective exclusion experiments indicated that H. humilis subsp. hirsutis is pollinated by both birds and insects, while H. coccineus and H. deformis are reliant on sunbirds. The tribe Haemantheae is defined by having fleshy, brightly coloured baccate fruits with large, recalcitrant seeds. No other species in the family have such a fruit type and the closest related tribe, Amaryllideae, have fruits characteristic of abiotic dispersal. S. multiflorus subsp. katherinae and S. puniceus occur in similar habitat of coastal to inland forested vegetation. I found that seeds of both taxa are dispersed by monkeys, which eat the fruits, depulping the seeds, and then spitting them out. In the genus Haemanthus, fruits are softer, and many species occurs in habitats without monkeys. I found that seeds of H. deformis are dispersed by birds and rodents which either depulp the seeds right next to the plant or disperse the seeds further away by carrying the fruits elsewhere. The seedlings require a shady microhabitat in bushclumps for survival and the dispersal system appears to favour either short distance dispersal into the immediate bushclump habitat or longer distance dispersal to different bushclumps. In conclusion, inflorescence and flower structure in the subtribe Haemanthinae play key roles in different pollination systems, with flowers in the paintbrush style inflorescences of Scadoxus puniceus and several Haemanthus species being pollinated by sunbirds, and flowers in open brush style inflorescence of S. multiflorus being pollinated by butterflies. Furthermore, the fruits of Haeminthinae are shown to be specialised for frugivory by various animals which discard the recalcitrant seeds. Mutualisms between various animals in Haemanthinae have therefore had an important impact on the evolution of flowers and fruit traits in this amaryllid subtribe.