Comparison of the ecology and evolution of plants with a generalist bird pollination system between continents and islands worldwide

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.

Plants are visited by more pollinator species than pollination syndromes predicted in an oceanic island community

“…Similar results were also found in community-level studies in Mediterranean climates of the northern hemisphere 63,64 and in Tasmania 12 . On tropical islands, pollination by generalist birds is common 46 , and flowering plants are frequently visited by non-flower-specialized birds which do not fit a typical ornithophilous syndrome 24 . Floral traits in most plant species on oceanic island may have the potential for adapting to new conditions under changing pollination environments 65,66 .…”

“…Plants on islands are faced with an environment where the species numbers of classical pollinator groups, such as bees, butterflies or birds are extremely low 60 , 61 . One strategy to adapt to a limited number of potential pollinators is the evolution of features promoting generalist pollination, since generalist pollinators are more common and reliable on oceanic islands 46 . Hence, generalized pollination systems may be advantageous to assist plants to expand their ranges into new habitats 62 and considered a reproductive assurance mechanism evolved primarily on oceanic island environments 31 .…”

“…A few studies have focused on the bird pollination syndrome on islands, for example, Biddick and Burns 10 found that the phenotypic trait matching between birds and flowering plants supported the pollination syndromes. Whereas plants evolved generalist bird pollination as an adaptation to birds as a reliable pollinator group 46 , and bird-visited flowers display mixed traits not fitting the classical ornithophilous syndrome on islands 24 . Therefore, studies dealing with the relationship between floral traits and different pollinator functional groups in oceanic island communities are urgently needed.…”

Ecological fitting is a sufficient driver of tight interactions between sunbirds and ornithophilous plants

“…Evolutionary trajectories and related adaptations of ornithophilous plants and nectarivorous birds differ on individual continents and in different phylogenetic plant and bird lineages (Abrahamczyk, ; Fleming & Muchhala, ). Considering specialized nectarivores, the three largest groups are hummingbirds (Trochilidae) in the New World, sunbirds, and spiderhunters (Nectariniidae) in Africa, Asia, and Australia and honeyeaters (Meliphagidae) in Australia, New Zealand, New Guinea, and many South Pacific islands (Cheke, Mann, & Allen, ; Cronk & Ojeda, ; Schuchmann, ).…”

Generalist birds outperform specialist sunbirds as pollinators of an AfricanAloe

“…Early work done on bird pollination systems in the Americas emphasized an apparent distinction between hummingbird and passerine bird pollination systems [1][2][3][4][5][6], but, at the global scale, a more useful functional dichotomy is that between specialist avian nectarivores, including hummingbirds and passerine sunbirds, and more generalist and opportunistic avian nectarivores, such as orioles, weavers and bulbuls [7]. Plants seem to show evolutionary specialization for pollination by specialist or opportunistic birds [8], manifested in divergent nectar properties among the plants pollinated by either of these groups of birds [7]. It is implicit in the specialization of plants for pollination by opportunistic birds that these birds can outperform specialist birds as pollinators under some circumstances, but it is still unclear whether this is because opportunistic birds are more effective on a per-visit basis or simply because they are more abundant as visitors.…”