Biol. Rev. (2019), pp. 000–000. 1 doi: 10.1111/brv.12520 Comparison of the ecology and evolution of plants with a generalist bird pollination system between continents and islands worldwide Stefan Abrahamczyk∗ Nees-Institute for Biodiversity of Plants, University of Bonn, 53115, Bonn, Germany ABSTRACT Thousands of plant species worldwide are dependent on birds for pollination. While the ecology and evolution of interactions between specialist nectarivorous birds and the plants they pollinate is relatively well understood, very little is known on pollination by generalist birds. The flower characters of this pollination syndrome are clearly defined but the geographical distribution patterns, habitat preferences and ecological factors driving the evolution of generalist-bird-pollinated plant species have never been analysed. Herein I provide an overview, compare the distribution of character states for plants growing on continents with those occurring on oceanic islands and discuss the environmental factors driving the evolution of both groups. The ecological niches of generalist-bird-pollinated plant species differ: on continents these plants mainly occur in habitats with pronounced climatic seasonality whereas on islands generalist-bird-pollinated plant species mainly occur in evergreen forests. Further, on continents generalist-bird-pollinated plant species are mostly shrubs and other large woody species producing numerous flowers with a self-incompatible reproductive system, while on islands they are mostly small shrubs producing fewer flowers and are self-compatible. This difference in character states indicates that diverging ecological factors are likely to have driven the evolution of these groups: on continents, plants that evolved generalist bird pollination escape from pollinator groups that tend to maintain self-pollination by installing feeding territories in single flowering trees or shrubs, such as social bees or specialist nectarivorous birds. This pattern is more pronounced in the New compared to the Old World. By contrast, on islands, plants evolved generalist bird pollination as an adaptation to birds as a reliable pollinator group, a pattern previously known from plants pollinated by specialist nectarivorous birds in tropical mountain ranges. Additionally, I discuss the evolutionary origins of bird pollination systems in comparison to systems involving specialist nectarivorous birds and reconstruct the bird pollination system of Hawaii, which may represent an intermediate between a specialist and generalist bird pollination system. I also discuss the interesting case of Australia, where it is difficult to distinguish between specialist and generalist bird pollination systems. Key words: Australia, breeding system, elevation, climatic seasonality, flowering phenology, Hawaiian honeycreepers, honeyeaters, hummingbird, sunbirds. CONTENTS I. Introduction .............................................................................................. 2 II. Materials and methods ................................................................................... 2 III. Distribution and phenology of generalist-bird-pollinated plants .......................................... 3 IV. Conditions favouring the evolution of generalist bird pollination ......................................... 5 (1) Continents ............................................................................................ 5 (2) Islands ................................................................................................ 7 V. Evolution of generalist bird pollination systems .......................................................... 7 * Address for correspondence (Tel: +49 228 734649; Fax: +49 228 733120; E-mail: [email protected]) Biological Reviews (2019) 000–000 © 2019 Cambridge Philosophical Society 2 Stefan Abrahamczyk VI. The hawaiian bird pollination system .................................................................... 7 VII. Bird-pollinated plant assemblages in australia ............................................................ 8 VIII. Conclusions .............................................................................................. 10 IX. Acknowledgements ....................................................................................... 10 X. References ................................................................................................ 10 XI. Supporting Information .................................................................................. 14 I. INTRODUCTION such patterns to those of plants pollinated by specialist nectarivorous birds might help us to understand general Pollination by nectar-feeding birds is an essential ecosystem principles in the evolution of pollination systems. Studies function for thousands of plant species worldwide (e.g. on the ecology of single generalist-bird-pollinated plant Sekercioglu, 2006; Abrahamczyk & Kessler, 2015; Anderson species indicate a broad distribution across habitat types et al., 2016). These mutualistic interactions of plants and birds over the tropics and subtropics (e.g. Knox et al., 1985; have long fascinated scientists and involve not only highly Vicentini & Fischer, 1999; Raju, Rao & Ezradanam, 2004b; specialized nectarivorous birds, such as hummingbirds or Johnson, Hargreaves & Brown, 2006). However, plants with sunbirds, acting as pollinators but also birds with more a generalist bird pollination system are not restricted to generalist feeding behaviour (feeding mainly on insects, continents but also occur on oceanic islands (e.g. Lammers seeds or fruits), such as parrots, starlings, warblers, doves & Freeman, 1986; Valido, Dupont & Olesen, 2004; Olesen and woodpeckers (e.g. Porsch, 1924, 1929; van Leeuwen, et al., 2012). Since ecological conditions often differ strongly 1931; Gryj, del Rio & Baker, 1990). However, until recently, between continents and islands, it remains to be tested research has largely focused on the mutualistic interactions whether the same ecological factors shaped the evolution of of specialized nectarivorous birds, especially hummingbirds, generalist-bird-pollinated species on continents and islands. and their preferred plants (e.g. Feinsinger, 1978; Stiles, 1981; Herein, I summarize information on the biogeographical Abrahamczyk & Kessler, 2015). The ecology, distribution distribution patterns, habitat preferences, growth form, phe- and evolution of plant species pollinated by generalist birds nology and reproductive system of generalist-bird-pollinated have largely been ignored, even though this pollination plant species and compare them between species occurring system is relatively common and conspicuous. For example, on continents and on islands. Based on these results I discuss several widely distributed plant species pollinated by how environmental factors and plant reproductive traits generalist birds, such as species from the genera Erythrina have influenced the evolution of generalist-bird-pollinated (Fabaceae) and Aloe (Asphodelaceae), are frequently used as plants and draw conclusions on why so many plant species ornamental plants in the tropics and subtropics. Existing attract generalist birds for pollination, some even sympatric studies have mostly analysed the reproductive ecology of with specialist-bird-pollinated species. single generalist-bird-pollinated species (e.g. Toledo, 1975, 1977; Knox et al., 1985; Vicentini & Fischer, 1999; Johnson, Hargreaves & Brown, 2006). Recently scientists have started II. MATERIALS AND METHODS to analyse aspects of the generalist bird pollination system more systematically: Johnson & Nicolson (2007) showed I searched Google Scholar (www.scholar.google.de) for litera- that the nectar sugar composition of flowers pollinated ture on plant species that are mainly pollinated by generalist by generalist birds differs significantly from that of plants birds (i.e. birds feeding mainly on insects, seeds and/or fruits pollinated by hummingbirds or sunbirds. Rocca & Sazima and ≤ 30% on nectar), using the search terms ‘generalist’ or (2010) reviewed the pollination syndrome of Neotropical ‘passerine bird pollination’ in combination with geographical species pollinated by generalist birds and listed 32 plant terms, such as ‘Africa’, ‘Canary Islands’ or ‘New Zealand’. and 166 bird species involved. These studies demonstrate Additionally, I searched for taxonomic terms, such as convincingly that generalist-bird-pollinated plants form a ‘honeycreeper’, ‘white-eye’ or ‘flowerpecker’ in combination distinct pollination syndrome, characterized for example with ‘pollination’. To determine whether a species should by open, brush-like, vividly coloured flowers, with large be included in the list of generalist-bird-pollinated plants quantities of dilute, hexose-rich nectar. Rocca & Sazima I checked whether the birds were reported to contact the (2010) also pointed out that generalist-bird-pollinated plants reproductive organs of the flowers and whether the bird are commonly large, woody species, with a self-incompatible species involved commonly visits the flowers. I excluded reproductive system and no clear flowering season. However, plant species that are mostly (> 50%) pollinated by other pol- due to their relatively small sample size and restricted linator groups and only occasionally visited or visited but not geographic distribution, their general conclusions need to be pollinated by generalist birds. This led to exclusion of most validated with a larger, less geographically restricted