Letters Evidence for overlooked mechanisms of long-distance seed dispersal to and between oceanic islands The classic concept of long-distance seed dispersal

Ever since Darwin (1859), the dispersal of species from continents to oceanic islands, and between such islands, has been the subject of considerable speculation. These islands are those arising from the seafloor as a result of underwater geologic activity, typically volcanic or coralline, that have never been connected to continental land masses. In his seminal book Dispersal of Plants Throughout the World, Ridley (1930) collated considerable empirical evidence of long-distance dispersal (LDD) and proposed mechanisms responsible for the colonization of remote archipelagos. Later, van der Pijl (1982) summarized traits to define diaspore syndromes related to sea (hydrochory), wind (anemochory) and animal (zoochory) LDD. The latter includes endozoochory (dissemination of seeds in the disperser’s gut) and epizoochory (seeds externally attached to the disperser’s body). These three keystone publications aimed to build a framework to predict dispersal based on plant and vector features and empirical studies. Darwin (1859) performed sowing experiments with some seeds dispersed externally by waterbirds, finding that they often germinated, while Ridley (1930) found different aquatic species of unrelated genera (e.g. Juncus, Carex, Cyperus, Polygonum) along banks of isolated ponds, and associated this distribution to waterbirds. Although Ridley (1930) provided no direct evidence for waterfowl dispersal, he assumed that transport of seeds in mud on birds’ legs could be important for plants without special morphological adaptations for dispersal. Other botanists have since advanced this mechanism to explain the arrival to different oceanic islands of many small seeds lacking LDD adaptations. For instance, Carlquist (1967) estimated that c. 21% of plant species that have colonized Easter Island and 21% of those dispersed to the Juan Fernández archipelago did so in mud on the feet of birds because they lacked any special adaptation for LDD. Porter (1983) also argued that mud attached to animals was responsible for 42 out of 378 (11%) original dispersal events to the Galápagos. However, to our knowledge, there is limited evidence of LDD by terrestrial birds transporting seeds in their plumage or in mud on their legs and feet. Figuerola & Green (2002) reported that seeds of aquatic plants tend to be attached to the plumage of waterbirds and that transport by this means can be frequent over short distances. Our own experience in the archipelagos of Galápagos, Canaries and Azores, where we have captured and ringed over 10 000 terrestrial birds, leads us to argue that epizoochory is extremely rare. Additional evidence suggests that this mechanism of dispersal might be largely restricted to waterbirds, which also transport seeds of wetland plants in their guts (DeVlaming & Proctor, 1968; Proctor, 1968; Brochet et al., 2010). Given the inherent difficulties in studying seed dispersal to oceanic islands, it is often impossible to reconstruct how plants reached these islands (Thornton, 2007; Guillespie et al., 2012; Vargas et al., 2012). Distances from the mainland to such islands can range from tens of km (e.g. Canaries, 100 km) to thousands of km (e.g. Galápagos, 1000 km, Hawaii, 4000 km), but it is expected that in all cases colonization will require mechanisms of dispersal distinct from those that enable short distance dispersal (e.g. within 1 km of a parent plant) and which have no immediate biogeographical consequences (Normand et al., 2011). Our main goal here is to examine some possibly overlooked LDD mechanisms involved in seed transportation to and between oceanic islands. In doing this, we must be clear about the use of the term mechanism in contrast to syndrome, and vector of dispersal. Here, dispersal syndromes are considered to be morphological adaptations of diaspores, which increase the likelihood of their dispersal. Dispersal mechanisms are defined as typical (i.e. predictable) pathways by which seeds attain LDD, regardless of the adaptations they might possess. Finally, dispersal vectors are the actual means by which seeds are dispersed, independently of dispersal syndrome or mechanism.