Biol. Rev. (2019), pp. 000–000. 1 doi: 10.1111/brv.12520 Comparison of the ecology and evolution of with a generalist system between continents and islands worldwide

Stefan Abrahamczyk∗ Nees-Institute for Biodiversity of Plants, University of Bonn, 53115, Bonn, Germany

ABSTRACT

Thousands of worldwide are dependent on 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 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, , .

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 -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 or Johnson, Hargreaves & Brown, 2006). However, plants with sunbirds, acting as 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 have influenced the evolution of generalist-bird-pollinated () and Aloe (), 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 ‘ bird pollination’ in combination with geographical species pollinated by generalist birds and listed 32 plant terms, such as ‘Africa’, ‘’ 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 sample. Australian plant species, since Australian bird-pollinated To date, no study has analysed the biogeograph- plants are mostly pollinated by specialist pollinator groups, ical distribution, habitat preferences or evolution of such as honeyeaters and lories and only to a minor extent by generalist-bird-pollinated plant species. Comparisons of generalist birds. I discuss the unusual case of bird-pollinated

Biological Reviews (2019) 000–000 © 2019 Cambridge Philosophical Society Ecology & evolution of generalist bird pollination 3 plant assemblages in Australia in Section VII. For plant I compared the proportional distribution of states for species pollinated mostly by generalist birds but also by other mean elevation, habitat type, growth form, flowering season pollinator groups, I collected the number of other pollinator and reproductive system between plants occurring on species involved [i.e. specialist nectarivorous birds, bats, continents versus on islands using Fisher’s exact tests in R non-flying mammals, lizards, hymenoptera (excluding ants) (R Development Core Team, 2017). The few species that and lepidoptera]. I did not include introduced pollinator occurred both on islands and on continents were scored species or nectar or pollen thieves. Note that the absolute for both categories. For mean elevation and latitude of the number of pollinator species from different groups that visit study side I additionally conducted Kruskal–Wallis tests particular flowers is relatively uninformative, since different with non-categorized data to test whether both traits differed species differ strongly in their pollination effectiveness. between continents and islands; the results of both tests were For each generalist-bird-pollinated plant species I collected not significant (elevation: K = 0.252, P = 0.615; latitude: data on the geographical (continent; island) and mean K = 1.0, P = 0.317). I also compared the proportional altitudinal distribution (lowland: ≤ 800 m; montane: > distribution of states for mean elevation, habitat type, 800 m to ≤2000 m; upper montane: > 2000 m). I chose growth form, flowering season and reproductive system for the transition of 800 m between lowland and lower montane plants occurring on continents in the New versus the Old areas as a compromise between higher transition points World using Fisher’s exact tests. Since I only found 49 at the equator and lower transition points in temperate generalist-bird-pollinated plant species on islands I did not areas and on islands. Additionally, I gathered information subdivide these data further to test for differences in trait on habitat type (evergreen forest; seasonal forest; seasonal distribution between biogeographic regions. openland), growth form (tree; shrub; woody liana; herb), I listed all bird-pollinated plant lineages/species from flowering phenology (dry season; transition dry–rainy Hawaii mentioned in the literature (e.g. Baldwin & Wagner, season; transition rainy–dry season; rainy season) and 2010) to obtain an overview of the local bird-pollinated reproductive system (self-incompatible: seed set ≤30% or flora. For those plant lineages/species included in dated, species dioecious; self-compatible with reduced seed set: seed molecular phylogenies, I also tabled stem and crown set >30% to ≤70%; self-compatible: seed set >70%) for each ages (Table 1). I only included ages of plant lineages that plant species. This information was derived from the original were either shown to be bird-pollinated by ancestral state publications (see online Supporting information, Table S1). If reconstructions with at least 70% support or that included the period of flowering but not the season was provided in the a single bird-pollinated species/clade within a species-rich original publications, I searched for climate data for locations of insect-pollinated species, e.g. arboretum close to the study site and coded the wettest 6 months as the () is the only bird-pollinated Geranium species. rainy season and the driest 6 months as the dry season. If the Based on these ages I reconstructed the temporal changes flowering period of a species covered part of the rainy and dry of Hawaiian bird-pollinated plant assemblages by listing the seasons, I coded it as flowering in the ‘transition rainy–dry stem ages of the plant lineages involved. I also searched season’ or ‘transition dry–rainy season’ categories. for nectarivorous bird lineages of Hawaii included in Due to the large phylogenetic diversity of generalist-bird- dated, molecular phylogenies and reconstructed the temporal pollinated plants in both monocots and , I con- sequence of their stem ages. structed a phylogeny of all analysed species using a mega-tree approach in the R package V.PhyloMaker (Jin & Qian, 2019). This mega-tree contains 74,533 III. DISTRIBUTION AND PHENOLOGY OF species and includes all plant families. The tips of genera/ GENERALIST-BIRD-POLLINATED PLANTS species not included in the mega-tree were bind to the half point of the family/genus branch, representing the branch I found 124 species (from 70 genera and 36 families) of plants between the family/genus root node and the basal node as with a generalist bird pollination system, from all continents recommended by Qian & Jin (2016). I then tested for a except the Antarctic (Table S1). The majority of continental phylogenetic signal in the distribution of generalist-bird- species (80 plant species from 47 genera and 29 families) were pollinated plants on islands/continents using the phy- distributed in lowlands (57.5%), with a smaller proportion in logenetic dispersion index D for binary traits (Fritz & montane (26.3%) or upper montane (16.3%) areas (Fig. 1A). Purvis, 2010). For this analysis I applied 1000 per- On continents most generalist-bird-pollinated species occur mutations with random and Brownian-motion patterns in seasonal forest (45%) or seasonal openland (35%) with of evolution. I only found a weak phylogenetic signal a smaller proportion (20%) in evergreen forest (Fig. 1B). for the occurrence of generalist-bird-pollinated species Generalist-bird-pollinated plant species occur more often in on islands/continents [D = 0.113, E(D)random= 0, E(D) evergreen lowland forests and less often in seasonal forests Brownian motion = 0.257]. Due to the presence of only a in the New than in the Old World (Fig. 1E), potentially weak phylogentic signal, and because I found large variation reflecting the greater prevalence of tropical rainforests in the in all traits within genera and families, I did not account Neotropics. for phylogeny in further analyses. Thus, I assume that the On islands, I found 49 generalist-bird-pollinated species phylogenetic signal does not influence the overall results. (five species occur on islands as well as on continents and were

Biological Reviews (2019) 000–000 © 2019 Cambridge Philosophical Society 4 Stefan Abrahamczyk

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i D 0 Continent Island Old World New World N = 80 N = 49 N = 44 N = 36 Fig. 1. (A, D) Distribution of generalist-bird-pollinated plants in three elevation zones (light grey: ≤ 800 m; dark grey: > 800 m ≤ 2000 m; black: > 2000 m) between continents and islands (A) and continents in the Old and New World (D). (B, E) Distribution of habitat types of generalist-bird-pollinated plants (light grey: evergreen forest; dark grey: seasonal forest; black: seasonal openland) between continents and islands (B) and continents in the Old and New World (E). (C, F) Distribution of flowering season of generalist-bird-pollinated plants (light grey: dry season; mid grey: transition dry to rainy season; dark grey: transition rainy to dry season; black: rainy season) between continents and islands (C) and continents in the Old and New World (F). P values indicate results of Fisher’s exact tests comparing values for continental versus islands (A–C) or Old World versus New World (D–F). thus included in both categories) from 28 genera and 17 fam- greater proportion (61.2%) of generalist-bird-pollinated ilies. The altitudinal distribution pattern for islands, where plant species on islands occur in evergreen forests, with 57.1% of generalist-bird-pollinated species occur in low- only 20.4% in seasonal forest and 18.4% in seasonal lands, 40.8% in montane and 2.0% in upper montane areas openland (Fig. 1B). This pattern is not shaped by latitude is not significantly different to the pattern on the continents since generalist bird-pollinated plant species cover a similar (Fig. 1A). Compared to continental species, a significantly latitudinal range on continents and islands.

Biological Reviews (2019) 000–000 © 2019 Cambridge Philosophical Society Ecology & evolution of generalist bird pollination 5

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D 0 Continent Island Old World New World N = 49 N = 24 N = 22 N = 27 Fig. 2. (A, C) Distribution of growth forms of generalist-bird-pollinated plants (light grey: herb; mid grey: shrub; dark grey: tree; black: woody liana) between continents and islands (A) and continents in the Old and New World (C). (B, D) Distribution of breeding systems of generalist-bird-pollinated plants (light grey: self-incompatible; dark grey: self-compatible with reduced seed set; black: self-compatible) between continents and islands (B) and continents in the Old and New World (D). P values indicate results of Fisher’s exact tests comparing values for continental versus islands (A, B) or Old World versus New World (C, D). On continents, most generalist-bird-pollinated species be most common in evergreen tropical montane and upper flower during the dry season (61.3%), or during the transitions montane forests and flowering occurs year long (Cruden, from dry to rainy season (8.8%) or rainy to dry season (10%). 1972; Kessler & Kromer,¨ 2000; Maglianesi et al., 2015; Only 20% of generalist-bird-pollinated species flower during Boehm et al., 2018). On islands generalist-bird-pollinated the rainy season. This pattern is more pronounced in the plants are most diverse in lowland evergreen forests but New compared to the Old World (Fig. 1F). Thus, generalist flowering is seasonal. In combination with differences in birds mainly feed on nectar during the dry season (Franklin, flower morphology and nectar chemistry (Johnson & Nicol- 1999), when it may represent a valuable source of both energy son, 2007; Rocca & Sazima, 2010), these biogeographical and water (Sazima, Sazima & Sazima, 2009). On islands, and phenological data justify the recognition of a generalist a similar phenological pattern is found: flowering occurs bird pollination syndrome and indicate that the evolution of largely in the dry season (46.8%), 10.6% of species flower plants pollinated by generalist birds may differ from that of during the transition between the dry and rainy season, plants pollinated by specialized nectarivorous birds. 19.2% during the transition between rainy and dry season, and 23.4% during the rainy season (Fig. 1C). IV. CONDITIONS FAVOURING THE The spatial and phenological niche of plants pollinated EVOLUTION OF GENERALIST BIRD mainly by generalist birds differs from that of plants POLLINATION pollinated by specialist nectarivorous birds, especially by hummingbirds and sunbirds. While plants pollinated mainly (1) Continents by generalist birds are most diverse in lowland seasonal forests on continents and flower during the dry season (Fig. 1A–C), Previous analyses have established that plants pollinated plants pollinated by specialist nectarivorous birds tend to by specialist nectarivorous birds are most common in

Biological Reviews (2019) 000–000 © 2019 Cambridge Philosophical Society 6 Stefan Abrahamczyk

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Fig. 3. Overview of the selective forces leading to the evolution of generalist bird pollination in plants on continents and islands. evergreen tropical and subtropical mountain forests, where establish territories within one plant individual if flower the abundance of insect pollinators is comparatively abundance is sufficiently high (Gill & Wolf, 1975; Ford, 1981; low (Abrahamczyk & Kessler, 2015; Krauss et al., 2017). Evans, 1996; Abrahamczyk & Kessler, 2015). One strategy Specialist nectarivorous bird pollination has therefore been to avoid this could be to restrict flowering to seasons when interpreted as an adaptation to a more reliable pollinator fewer specialist nectarivorous birds or social bees are present, group. These plant species are mainly herbs, shrubs or and/or to evolve mechanisms to deter ineffective pollinators. epiphytes (Abrahamczyk & Kessler, 2015) and are mostly Generalist birds perhaps represent more reliable pollinators self-compatible, although sometimes with reduced seed since they are abundant even in seasonal habitats because set when self-pollinated (Keighery, 1982; Wolowski et al., of their diverse feeding strategy and are more likely to move 2013). By contrast, plants with generalist bird pollination between different trees and shrubs to search for food, increas- are mostly trees (45.0%) or shrubs (47.5%; Fig. 2A); only ing the chances of outcrossing (Botes, Johnson & Cowling, 5.0% are herbs and 2.5% are woody lianas. Further, 2008). A majority of continental generalist-bird-pollinated generalist-bird-pollinated species on continents are mostly plant species occur in seasonal habitats (Fig. 1B) and flower self-incompatible (60.4%) or suffer from a reduced seed during the dry season (Fig. 1C) when the abundance of set when self-pollinated (20.8%; Fig. 2B). Only 18.8% are specialist nectarivorous birds is reduced (Arizmendi & self-compatible. These patterns are most pronounced in Ornelas, 1990; Craig & Hulley, 1994; Araujo & Sazima, the New World (Fig. 2C, D). Most plant species pollinated 2003; Cotton, 2007). These plant species in many cases have by specialist nectarivorous birds exclude generalist birds by evolved mechanisms to deter or prevent ineffective pollina- having long and stiff corolla tubes and producing a limited tors such as bees from visiting their flowers since bees remain number of flowers per day, but they may have an extended abundant year round in the tropics and subtropics (Abra- flowering period (Feinsinger, 1978; Stiles, 1981). Such plant hamczyk et al., 2011). Such adaptations include unfavourable species are often pollinated by trap-lining birds, whose flower positions (Toledo, 1977; Vicentini & Fischer, 1999)**, movement from plant to plant provides at least some degree closed flowers that require specific adaptations in order to of outcrossing (Wolowski et al., 2013). Plants pollinated by open them (Etcheverry & Aleman,´ 2005) or bitter nectar generalist birds instead tend to conduct mass flowering with (Johnson, Hargreaves & Brown, 2006; Nicolson et al., 2015). up to several thousand open flowers per day (Rocca & Saz- In conclusion, the more reliable presence of generalist ima, 2010) and are strongly dependent on cross-pollination birds may have led to features that can be associated with the (Fig. 2B). Such flowering phenology would result in a high evolution of generalist bird pollination in many continental likelihood of self-pollination if the pollinating species were plant lineages (Fig. 3): a tendency to mass-flowering, a largely social bees or specialist nectarivorous birds, which tend to self-incompatible reproductive system, and flowering during

Biological Reviews (2019) 000–000 © 2019 Cambridge Philosophical Society Ecology & evolution of generalist bird pollination 7 the dry season. An additional selective pressure for flowering distributed through the monocots and eudicots (∼97% in the dry season may be that fruits then ripen during the rainy of the angiosperms). This indicates that generalist bird season, increasing the chances of seedling establishment. pollination has evolved many times independently. Up to However, the main mechanism driving the evolution of both 54 bird species plus additional insect, mammal or lizard generalist and specialist bird pollination in continental plant species may be involved in the pollination of a single lineages is likely the guarantee of reproductive success. plant species (Symes & Yoganand, 2013). Generalist bird pollination is likely to have evolved either from insect (2) Islands or from specialist nectarivorous bird-pollinated ancestors. Evolution of generalist bird pollination from bee-pollinated On islands all around the world plants are faced with an species has evolved at least three times independently in environment where the species numbers and abundance the (Olesen et al., 2012) and five times of classical pollinator groups, such as bees, butterflies or independently in different families on the Macaronesian specialist nectarivorous birds is extremely low (Inoue, 1993; Islands (Ojeda et al., 2016). Evolution of generalist from Valido & Olesen, 2010; Hervías-Parejo & Traveset, 2018). specialist bird pollination has been documented in Erythrina One strategy to adapt to a limited number of potential (Fabaceae) independently in the New and Old World pollinators is the evolution of features promoting generalist (Bruneau, 1997) and in canariensis (Campanulaceae) bird pollination, since generalist birds are more common and on the Canary Islands (Olesen et al., 2012). reliable pollinators on oceanic islands than bees, butterflies Ojeda (2013) demonstrated a temporal increase of plant or specialized nectarivorous birds (Rodríguez-Rodríguez lineages in the assemblage of plants pollinated by generalist & Valido, 2008). Due to the different selective pressures birds within the Macaronesian Islands. Interestingly, the involved, bird-pollinated plants on islands have not tended oldest generalist-bird-pollinated plant lineage far exceeded to evolve mechanisms to deter social bees or specialized the oldest bird lineage age on the Canary Islands, possibly nectarivorous birds: the evolution of bitter nectar or due to high levels of extinction within bird lineages (Ojeda, closed flowers have only been reported from continental 2013). Within the plant lineages allopatric diversification species (Toledo, 1977; Vicentini & Fischer, 1999; Johnson, occurred, mostly on different islands [e.g. in Lotus (Fabaceae) Hargreaves & Brown, 2006; Nicolson et al., 2015). The and Isoplexis (Plantaginaceae)]. To some extent this system growth forms of generalist-bird-pollinated plants on islands resembles hummingbird-pollinated systems in temperate are significantly different from those on continents, with North and and in the West Indies (Abraham- most being small shrubs (57.1%), herbs (16.3%) or woody czyk et al., 2015; Abrahamczyk & Renner, 2015), however lianas (4.1%) and a reduced proportion of trees (22.5%) in the case of the Canary Islands the bird pollinators did not (Fig. 2A). Their generally smaller habit, meaning that evolve by radiation of a single lineage but originated from each plant will produce fewer flowers and that therefore different, unrelated bird lineages (Valido, Dupont & Olesen, pollinating birds will have to move among plants and 2004), forming an exemplar generalist bird pollination provide cross-pollination (Botes, Johnson & Cowling, 2008), system. Similar evolutionary scenarios seem likely for other in combination with the relative scarcity of social bees and species-rich generalist-bird-pollinated systems, for example specialist nectarivorous birds, could have led to selection for in the South African Cape region, the Indian Eastern a self-compatible breeding system on islands. The available Ghats or subtropical South America. Unfortunately, there data indeed show that more generalist-bird-pollinated plants are insufficient phylogenetic data available for the plants on islands are either fully self-compatible (40.8%) or have involved. However, the stem ages of some of the bird genera reduced seed set when self-pollinated (25.9%); only 33.3% involved, such as Cyanerpes and Diglossa (Thraupidae), Icterus are self-incompatible (Fig. 2B). (Icteridae), Loriculus (Psittacidae) and Zosterops (Zosteropidae) Diverging environmental factors between islands and indicate that the origins of generalist bird pollination systems continents may thus have influenced the evolution of may date back at least into the late Miocene (Moyle et al., generalist bird pollination in different ways. The plant traits 2009; Kundu et al., 2012; Barker et al., 2015). and habitat of generalist-bird-pollinated plants on islands (Fig. 3) resemble more closely those of plants pollinated by specialist nectarivorous birds on continents. The factor VI. THE HAWAIIAN BIRD POLLINATION underlying the evolutionary switch from insect to bird SYSTEM pollination in these two environments is likely to be the low abundance and unpredictable activity of insect pollinators. In Hawaii, a bird pollination system evolved including both specialist nectar-feeders and generalists, involving 177 bird-pollinated plant species from 22 genera and 12 families, V. EVOLUTION OF GENERALIST BIRD representing >15.5% of the native flora (Sakai, Wagner POLLINATION SYSTEMS & Mehrhoff, 2002). Two unrelated bird lineages with non-nectarivorous ancestors, the Hawaiian honeycreepers Pollination by generalist birds occurs in at least 70 plant (Drepanidinae, Fringillidae; 42 spp.) and the Mohoidae (5 genera from 36 plant families (Table S1), which are spp.) evolved into partially specialized nectar feeders (with a

Biological Reviews (2019) 000–000 © 2019 Cambridge Philosophical Society 8 Stefan Abrahamczyk

Table 1. Phylogenetic ages of generalist bird-pollinated plant lineages on Hawaii. Numbers in parentheses indicate numbers of species of bird-pollinated lineages

Plant species/clade Reference (for ages of (species number) Plant family Stem age (Mya) Crown age (Mya) bird-pollinated lineages) Geranium arboreum* Geraniaceae 0.29 – Fiz et al. (2008) procera 0.63 – Jabaily et al. (2014) Hawaiian Hibiscus (4)* 0.99 – Koopman & Baum (2008) Santalum freycinetianum/ haleakalae* Santalaceae 1.0–1.5 – Harbaugh & Baldwin (2007) cosmoides* 1.0–3.0 Knope et al. (2012) Stenogyne (22) Lamiaceae 2.7 2.29 Roy et al. (2013) (1.61–4.24) Schiedea trinervis clade (4)* Caryophyllaceae 3.1 1.9 Willyard et al. (2011) Hesperomannia (4)* Asteraceae 3.36 – Kim et al. (1998)

Haiwaiin (4) 3.9 – Percy et al. (2008) Kokia (4)* Malvaceae (2.6–6.3) 4.34 – Koopman & Baum (2008) Scaevola glabra Goodeniaceae 8.83 – Jabaily et al. (2014) Hawaiian lobeliads (120) Campanulaceae 13.18 12.84 Givnish et al. (2009) Vaccinium calycium Ericaceae – – Erythrina sandwicensis* Fabaceae – – Mezoneuron kavaiense* Fabaceae – – Sesbania tomentosa* Fabaceae – – Sophora chrysophylla Fabaceae – – Abutilon (3)* Malvaceae – – Freycinetia arborea Pandanaceae – –

Asterisks mark species or clades that are inferred to be pollinated by generalist birds based on their pollination syndrome. –, information not available; Mya, million years ago. mean nectar content in their total diet of 10–30%; Wilman Unfortunately, the Hawaiian bird pollination system has et al., 2014). Two honeycreeper species, Chlorodrepanis flava been heavily disrupted by extinctions: all five Mohoidae and Magumma parva, evolved into specialist nectar feeders species and about 40% of the 42 (30–50% nectar in the total diet) and three further species, species are already extinct (James, 2004) and others are Drepanis coccinea, Himatione sanguinea and Palmeria dolei have highly threatened (Fleischer et al., 2008; Lerner et al., 2011). become highly specialist nectar feeders (70–90% nectar As a result, also several bird-pollinated plant species have in the total diet; Wilman et al., 2014). The Mohoidae become rare or even extinct (∼ 20% extinction in Hawaiian split from their sister family 18.0–14.0 million years ago lobeliads; Givnish et al., 2009). At least some pollination (Mya) (Fleischer, James & Olson, 2008) while the Hawaiian services have been taken over by the Japanese white-eye honeycreepers split from their sister clade 5.77 Mya and Zosterops japonicus, an introduced species from east Asia (Cox, began to diversify 4.73 Mya (Lerner et al., 2011). The age 1983; Elmore, 2008; Aslan et al., 2014a). This species is of the Mohoidae is similar to the stem age of the Hawaiian able to maintain the gene flow in many endangered plant lobeliad clade (13.18 mya), the oldest bird-pollinated lineage species and has thus become an essential component of on the islands (Givnish et al., 2009). However, the gradual this labile pollination system (Aslan et al., 2014a). A similar increase in the number of bird-pollinated lineages mostly assumption of pollination services has been reported for the took place after the origin of the Hawaiian nectarivorous silver-eye Zosterops lateralis in New Zealand (Pattemore & honeycreepers (Table 1). Bird pollination is known from Wilcove, 2012). Here too, as native bird pollinators became 19 plant lineages on Hawaii today (Table 1). The bird rare, the recent immigrant species has supported gene flow pollination system of Hawaii appears to be intermediate among endangered plants. These two examples illustrate between a specialist nectarivorous bird pollination system that the bird-pollination systems of many oceanic islands and a generalist bird pollination system. The birds in can be dynamic, and how new species can help to maintain Hawaii exhibiting specializations to nectar-feeding and important ecosystem services. come from just two diversified lineages, but most of these species retain an element of opportunistic feeding behaviour with nectar representing only 10–30% of their diet. These observations are reflected by some plant traits: the corolla VII. BIRD-POLLINATED PLANT ASSEMBLAGES tubes of most species are short and nectar sugars are IN AUSTRALIA dominated by hexoses (Lammers & Freeman, 1986). Other, generalist birds also pollinate the flowers of some species Australia harbours a particularly rich bird-pollinated flora (Cox, 1983). (e.g. up to 15% of species in southwestern Australian shrub

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Table 2. Geographical distribution, habitat, reproductive characters and evolution of plants pollinated either by specialized nectarivorous or generalist birds

Specialized nectarivorous bird-pollinated plants pollinated by: Generalist bird-pollinated plants occurring on: Hummingbirds & Honeyeaters sunbirds (+ generalist birds) Continents Islands (including Hawaii) Geographical Centre of diversity in the Centre of diversity in Centre of diversity in the Centre of diversity in the distribution humid tropics but Papua and E + SW subtropics but reaching subtropics but reaching in reaching into temperate Australia but occur the adjacent temperate the adjacent temperate zones throughout Australasia zone and tropics zone and the tropics Altitudinal Lowlands to alpine Lowlands to alpine Lowlands to subalpine Lowlands to subalpine distribution regions; centre of regions; centres of regions; centre of regions; centre of diversity diversity in evergreen diversity in lowland diversity in the lowlands in the lowlands montane and upper shrubs as well as in montane forests montane forests Habitat type All kinds of openland and All kinds of openland and Mostly dry forest and Mostly evergreen forest but forest; centre of forest openland also dry forests and diversity in montane openland and upper montane forest Growth form Mostly herbs, shrubs and Mostly herbs, shrubs and Mostly trees and shrubs Mostly shrubs and trees but epiphytes epiphytes more herbs and less trees than on continents Flowering season Year around Year around Most flower during dry Most flower during dry season season but less pronounced than on continents Flower characters Mostly long-tubed flowers Mostly short-tubed to Mostly open to Mostly short-tubed but also with sucrose-rich nectar open flowers with short-tubed flowers with open flowers with hexose- or sucrose-rich hexose-rich nectar hexose-rich nectar nectar Breeding system Mostly self-compatible but Mostly self-compatible but Mostly self-incompatible Mostly self-compatible or sometimes with reduced often with reduced seed but also self-compatible self-compatible with seed set set often with reduced seed reduced seed set set Evolution Temporal increase in No existing data Insufficiently documented Temporal increase in plant numbers of plant and lineages (in Hawaii and bird lineages with possibly some Australasian regionally similar regions) and of bird maximum ages known lineages with regional for plant–hummingbird similar maximum ages mutualisms Maximum age of Bird crown age: 24–25 Honeyeaters stem age Insufficiently documented Bird stem age: 14–18 Mya the mutualism Mya (hummingbirds); 27.5 (22.0–33.0) Mya; but bird lineages (Mohoidae); plant crown age: crown age 24.17 involved date back at age: 13.18 Mya (Hawaiian 39 Mya (Heliconia;Iles (18.62–29.72) Mya least to late Miocene lobeliads); for most island et al., 2017) (Marki et al., 2017) systems insufficiently known

land are bird-pollinated; Keighery, 1980). However for the spatial and ecological profile of bird-pollinated plants the Australian flora it was difficult to categorize plants as in Australia differs from the general distribution pattern of pollinated by specialist nectarivorous versus generalist birds. specialist-bird-pollinated species (see Table 2), since these Numerous studies documented that many mainly specialist- Australian plants are commonly found in tropical and bird-pollinated genera, such as Banksia (Proteaceae), Euca- subtropical lowlands as well as in montane forests (Paton & lyptus (Myrtaceae), Grevillea (Proteaceae) or Melaleuca (Myr- Ford, 1977; Keighery, 1980, 1982; Krauss et al., 2017). taceae) are commonly visited and pollinated by a diverse guild The two main groups of specialized nectarivorous of generalist birds as well (e.g. Newland & Wooller, 1985; birds in Australia are honeyeaters and lories. Both are Franklin, 1999; Noske & Franklin, 1999; Franklin & Noske, comparatively large-bodied birds with short to medium-sized 2000). This overlap in pollinator groups is much more pro- bills, include significant amounts of fruits and insects in nounced in Australia than on other continents. Additionally, their diet – in contrast to hummingbirds and sunbirds – and

Biological Reviews (2019) 000–000 © 2019 Cambridge Philosophical Society 10 Stefan Abrahamczyk are less territorial (Pyke, 1980). However, they also show a reliable pollinator group) although species with both some morphological and physiological characters typical of pollination systems can co-occur. The underlying mechanism specialized nectarivorous birds, such as brush tongues and driving the evolution of both bird pollination systems is likely the ability to digest sucrose efficiently (Fleming et al., 2008; the guarantee of reproductive success. Fleming & Muchhala, 2008). Thus, in their morphology and (3) The environmental factors that can be linked feeding ecology they represent an intermediate stage between with the evolution of generalist bird pollination differ generalist birds and the highly specialized hummingbirds and between continents and islands (Fig. 3). On continents sunbirds (Fleming & Muchhala, 2008; Higgins, Christidis generalist-bird-pollinated plants tend to be self-incompatible & Ford, 2008). This is mirrored in the characteristics of and are shrubs or trees with a profuse flowering strategy, many of their food plants: for example trees and shrubs a pattern that is more pronounced in species from the from the Myrthaceae or Proteaceae with relatively large New World. Adaptation to a reliable pollinator group is the inflorescences and open, often brush-like, flowers (Keighery, most likely explanation for the evolution of generalist bird 1982). Only some of these plant species produce the pollination on islands. strongly sucrose-dominated nectar typical of plants pollinated (4) Bird pollination systems involving generalist or by specialist nectarivorous birds; the remainder produce specialist birds share some common evolutionary characters. strongly hexose-dominated nectar more typical of plants But they differ in that generalist bird pollination systems pollinated by generalist birds (Nicolson, 1994; Nicolson & involve a large number of phylogenetically independent bird van Wyk, 1998). Easily accessible flowers with copious nectar lineages, whereas specialist bird pollination systems tend to production ensures that these species are visited by generalist involve radiations or at least closely related lineages of birds. birds, especially during the dry season (Paton & Ford, 1977; (5) These results underline how fragmentary our Ford, Paton & Forde, 1979; Franklin & Noske, 2000), but very knowledge on the evolution of pollination systems still few Australian plant species are pollinated solely by generalist remains. Thus, analytical studies on the evolution of birds (e.g. Knox et al., 1985). A small group of species is visited pollination systems are much needed. mostly or only by specialist nectarivorous birds. These plants, e.g. species of Styphelioideae (Ericaceae) or , are mostly herbs, small shrubs and epiphytes with tubular flowers and nectar that is inaccessible to generalist birds IX. ACKNOWLEDGEMENTS (Bernhardt & Calder, 1981; Reid, 1990; Johnson, 2013). In Australia niche differences between plants pollinated I thank Steven Johnson, Bastian Steudel, the editors Tim by generalist versus specialist nectarivorous birds may be Benton and Alison Cooper, and the two anonymous less pronounced because: (i) both generalist and specialist reviewers for helpful comments, Nicole Schmandt for nectarivorous birds are pollinators of many plant species; technical support and Yi Jin for support with phylo.maker. and (ii) several plant and bird species show intermediate combinations of specialized and generalized character states. This pattern may be the result of phylogenetic constraints X. REFERENCES on plants and/or birds, but more likely may be due to the relatively arid climate of Australia. This may constrain References marked with asterisk have been cited within the supporting information. birds such as honeyeaters from becoming more specialized Abrahamczyk,S.&Kessler,M.(2015). 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(Received 21 January 2019; revised 15 April 2019; accepted 18 April 2019 )

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