Is chiropterophily an evolutionary dead end? A phylogenetic test in the pantropical genus Parkia (Leguminosae, Caesalpinioideae, mimosoid clade)

Background and aims – Pollination systems often reflect adaptations to specific groups of pollinators, and these morphological specialisations have been important in the diversification of the angiosperms. Here, we study the evolution of the capitulum and pollination system in the pantropical genus Parkia, which comprises 35 species of trees distributed largely in the forests of South and Central America, Africa, Madagascar, and the Indo-Pacific. The flowers are grouped into capitula that are composed of one, two, or three distinct morphological types, and are principally pollinated either by insects or by bats. Material and methods – Using BEAST, we estimated the ages of nodes in a phylogeny based on four chloroplast regions (matK, trnL, psbA-trnH, and rps16-trnQ) and the nuclear region ITS/18S/26S. This analysis also enabled us to reconstruct the ancestral state of the capitulum and hence infer the ancestral pollination system. Euclidean distance-based cluster analysis was performed to determine which characters are consistently related to a specific pollination system.Key results – Our results indicate that the ancestral capitulum in the genus had three types of flowers and a morphology associated with bat-pollination in both the Paleotropics and Neotropics. In one derived Neotropical clade, the number of floral types in each capitulum was reduced to two (capitulum also bat-pollinated) or one (insect-pollinated). Thus, entomophily, as seen in some Neotropical species of Parkia, has been derived from a bat-pollinated ancestor. Cluster analysis showed that the floral characters were mostly consistent with pollination systems.Conclusion – Chiropterophily is not an evolutionary dead end in Parkia because during the evolutionary history of the genus there has been at least one transition to entomophily. Parkia provides a unique example of evolutionary transitions from chiropterophily to entomophily in a pantropical genus of trees.

Phylogeny and Systematics of Crescentieae (Bignoniaceae), a Neotropical Clade of Cauliflorous and Bat-Pollinated Trees

Abstract—The tribe Crescentieae includes Amphitecna (21 species), Crescentia (six species), and Parmentiera (10 species), three genera of understory trees with a center of diversity in Central America and a small number of species in the Antilles and northern South America. Species in Crescentieae are united by their fleshy, indehiscent fruit and cauliflorous, bat-pollinated flowers. To lay a foundation for examining morphological, ecological, and biogeographic patterns within the tribe, we inferred the phylogeny for Crescentieae using both chloroplast (ndhF, trnL-F) and nuclear markers (PepC, ITS). The most recent circumscription of Crescentieae, containing Amphitecna, Crescentia, and Parmentiera is supported by our phylogenetic results. Likewise, the sister relationship between Crescentieae and the Antillean-endemic Spirotecoma is also corroborated by our findings. This relationship implies the evolution of fleshy and indehiscent fruits from dry and dehiscent ones, as well as the evolution of bat pollination from insect pollination. Fruits and seeds from species in Crescentieae are consumed by humans, ungulates, birds, and fish.

Citizen Science Confirms the Rarity of Fruit Bat Pollination of Baobab (Adansonia digitata) Flowers in Southern Africa

The iconic African baobab tree (Adansonia digitata) has “chiropterophilous” flowers that are adapted for pollination by fruit bats. Although bat pollination of baobabs has been documented in east and west Africa, it has not been confirmed in southern Africa where it has been suggested that hawk moths (Nephele comma) may also be involved in baobab pollination. We used a citizen science approach to monitor baobab tree and flower visitors from dusk till midnight at 23 individual baobab trees over 27 nights during the flowering seasons (November–December) of 2016 and 2017 in northern South Africa and southern Zimbabwe (about 1650 visitors). Insect visitors frequently visited baobab flowers, including hawk moths, but, with one exception in southeastern Zimbabwe, no fruit bats visited flowers. Citizen science enabled us to substantiate preliminary conclusions about the relative importance of moth versus bat pollination of baobabs in southern Africa, with important implications for resource management.

Flowers up! The effect of floral height along the shoot axis on the fitness of bat-pollinated species

Background and Aims Bat-pollination is an important system in terms of occurrence and distribution, although it remains little studied. Thus, the role of particular flower traits in this interaction remains uncertain. Flower height along the shoot axis, associated with flower exposure, has often been deemed a key trait in this system, but its effect on fitness has not previously been assessed. We aimed to test its role and propose that taller flowers attain higher fitness due to a higher degree of accessibility and conspicuity to foraging bats. Methods We assessed the effect of floral height on bat visiting rates to individual flowers of Crescentia cujete (Bignoniaceae), a cauliflorous model bat-pollinated species with a marked gradient in flower height along the shoot axis. Additionally, we tested the effect of this variable on seed/ovule ratio measurements from seven other species from different families along a herb–tree gradient. Hypotheses were tested through mixed-effect linear models. Key Results Bat visiting rates varied positively as a function of flower height in C. cujete, but significance was found only for the subset of flowers located on the trunk, closer to the ground. Similarly, seed/ovule ratios were positively correlated with flower height only for the three species with the shortest statures along the height gradient and shortest average floral heights. These results suggest that proximity to the ground, associated with herbaceous or bushy surrounding vegetation, may be an obstacle to the foraging of nectar-feeding bats, which in turn should explain the morphological convergence of inflorescence length and exposure strategies of short-statured bat-pollinated plants. Conclusions Flower height has a species-specific effect on plant fitness. This study provides a novel numerical perspective to the role of an unexplored trait in bat-pollination, and has elucidated some aspects of the adaptive importance of flower height based on limitations imposed by ecologically complex pollinators.

Reproductive biology of the sausage tree (Kigelia africana) in Kruger National Park, South Africa

Kigelia africana has large flowers that are vertebrate pollinated and very large fruits that are likely to be vertebrate dispersed. Our field surveys of size–class distributions of K. africana in the southern Kruger National Park (KNP) suggest a lack of recruitment. This is possibly the result of a failure of mutualistic relationships with vertebrate dispersers and/or pollinators. Breeding system experiments indicated that K. africana is an obligate out-crosser. Despite being primarily adapted for bat pollination, in KNP that K. africana is presently mainly pollinated by a diversity of largely facultatively nectarivorous bird species. Fruit-set is high, although trees isolated by > 50 m were found to suffer depressed seed output. Our preliminary investigation of dispersal suggests that fruits are largely ignored and are thus weakly attractive to potential dispersers. Seedlings placed out in the field in KNP suffered high levels (> 50%) of mortality compared to 17.5% in control plots. This threefold difference is the result of herbivory over a 2-month period. In summary, the adult centric population structure is probably not because of pollen or seed limitation but may result from dispersal limitation or excessive herbivory.

A revision of Harpochilus sheds light on new combinations under Justicia (Acanthaceae)

Until recently, Harpochilus (Acanthaceae) contained two morphologically distinct species, Harpochilus neesianus and H. phaeocarpus, from northeastern Brazil. During an analysis of herbarium collections, we found an undescribed species of Harpochilus from the Brazilian semiarid region. However, another group of botanists simultaneously discovered the species and described it as H. paraibanus. Harpochilus neesianus and H. paraibanus are similar due to their morphologically complex flowers specialized for bat pollination, nocturnal anthesis, and anthers with non-appendiculate thecae. Unlike H. neesianus and H. paraibanus, the floral morphology of H. phaeocarpus and Cyrtanthera citrina, a name used for several misidentified collections of H. paraibanus, is more similar to that of Justicia. Thus, these species are here combined under Justicia. We also provide additional information on the morphology, geographic distribution and conservation status of H. paraibanus, and propose lectotypes for Harpochilus, H. neesianus, and C. citrina.

Escape from extreme specialization: passionflowers, bats and the sword-billed hummingbird

A striking example of plant/pollinator trait matching is found between Andean species of Passiflora with 6–14-cm-long nectar tubes and the sword-billed hummingbird, Ensifera ensifera , with up to 11-cm-long bills. Because of the position of their anthers and stigmas, and self-incompatibility, these passionflower species depend on E. ensifera for pollination. Field observations show that the bird and plant distribution match completely and that scarcity of Ensifera results in reduced passionflower seed set. We here use nuclear and plastid DNA sequences to investigate how often and when these mutualisms evolved and under which conditions, if ever, they were lost. The phylogeny includes 26 (70%) of the 37 extremely long-tubed species, 13 (68%) of the 19 species with tubes too short for Ensifera and four of the seven bat-pollinated species for a total of 43 (69%) of all species in Passiflora supersection Tacsonia (plus 11 outgroups). We time-calibrated the phylogeny to infer the speed of any pollinator switching. Results show that Tacsonia is monophyletic and that its stem group dates to 10.7 Ma, matching the divergence at 11.6 Ma of E. ensifera from its short-billed sister species. Whether pollination by short-billed hummingbirds or by Ensifera is the ancestral condition cannot be securely inferred, but extremely long-tubed flowers exclusively pollinated by Ensifera evolved early during the radiation of the Tacsonia clade. There is also evidence of several losses of Ensifera dependence, involving shifts to bat pollination and shorter billed birds. Besides being extremely asymmetric—a single bird species coevolving with a speciose plant clade—the Ensifera / Passiflora system is a prime example of a specialized pollinator not driving plant speciation, but instead being the precondition for the maintenance of isolated populations (through reliable seed set) that then underwent allopatric speciation.