A Review on the State of the Art in Frugivory and Seed Dispersal on Islands and the Implications of Global Change

Vol:.(1234567890) The Botanical Review (2024) 90:160–185 https://doi.org/10.1007/s12229-023-09296-8 1 3 A Review ontheState oftheArt inFrugivory andSeed Dispersal onIslands andtheImplications ofGlobal Change ManuelNogales1 · KimR.McConkey2 · TomásA.Carlo3 · DebraM.Wotton4,5 · PeterJ.Bellingham6,7 · AnnaTraveset8 · AarónGonzález‑Castro1,9 · RubenHeleno10 · KentaWatanabe11 · HarukoAndo12 · HaldreRogers13 · JuliaH.Heinen14 · DonaldR.Drake15 1 Island Ecology andEvolution Research Group, Instituto de Productos Naturales y Agrobiología (IPNA-CSIC), Avda. Francisco Sánchez No. 3, 38206LaLaguna,Tenerife, CanaryIslands, Spain 2 School ofEnvironmental andGeographical Sciences, The University ofNottingham Malaysia, Selangor, Malaysia 3 Department ofBiology, Penn State University, StateCollege, PA, USA 4 Moa’s Ark Research, Wellington, NewZealand 5 Biological Sciences, University ofCanterbury, Christchurch, NewZealand 6 Manaaki Whenua - Landcare Research, Lincoln, NewZealand 7 School ofBiological Sciences, University ofAuckland, Auckland, NewZealand 8 Institut Mediterrani d’Estaudis Avançats (IMEDEA-CSIC), BalearicIslands, Spain 9 Department Animal Biology, Edaphology andGeology, University ofLa Laguna, LaLaguna, Spain 10 Centre forFunctional Ecology, TERRA Associate Laboratory, Department ofLife Sciences, University ofCoimbra, Coimbra, Portugal 11 Okinawa College, National Institute ofTechnology, Nago, Japan 12 Biodiversity Division, National Institute forEnvironmental Studies, Tsukuba, Japan 13 Department ofFish andWildlife Conservation, Virginia Tech, Blacksburg, VA24061, USA 14 Center forMacroecology, Evolution andClimate (CMEC), University ofCopenhagen, Copenhagen, Denmark 15 School ofLife Sciences, University ofHawaiʻi, Honolulu, HI, USA 16 Author for Correspondence; e-mail: [email protected] © The Author(s) 2024 Published online: 17 January 2024 Abstract We provide an overview of the current state of knowledge of island frugivory and seed dispersal and identify knowledge gaps that are important for fundamental research on—and applied conservation of—island ecosystems. We conducted a systematic literature search of frugivory and seed dispersal on islands, omitting large, continental islands. This revealed a total of 448 studies, most (75%) published during the last two decades, especially after 2010. Nearly 65% of them were focused on eight archipelagos. There is a paucity of studies in Pacific archipelagos near Asia and Australia, and in the Indian Ocean. Data on island frugivory and seed dispersal are diverse but highly uneven in geographic and conceptual coverage. Despite their limited biodiversity, islands are essential reservoirs of endemic plants and animals and their interactions. Due to the simplicity of insular ecosystems, we can assess the importance of seed dispersal theory and mechanisms at species and community levels. These include the 161 1 3 A Review ontheState oftheArt inFrugivory andSeed Dispersal… ecological and biogeographical meaning and prevalence of non-standard mechanisms of seed dispersal on islands; the seed dispersal effectiveness and the relative roles of different frugivore guilds (birds and reptiles being the most important); and patterns of community organization and their drivers as revealed by interaction networks. Island systems are characterized by the extinction of many natives and endemics, and high rates of species introductions. Therefore, understanding how these losses and additions alter seed dispersal processes has been a prevailing goal of island studies and an essential foundation for the effective restoration and conservation of islands. Keywords Conservation and restoration· Fleshy-fruited plants· Insular environments· Mutualistic interactions and ecological networks· Non-standard dispersal mechanisms· Seed dispersal effectiveness Introduction By definition, islands are geographically isolated, which results in lower species richness of plants and animals, but greater levels of endemism and occurrence of relict species when compared to continents (Darwin, 1859; Wallace, 1892). These characteristics have made islands ideal laboratories for studying ecological and evolutionary processes (Carlquist, 1974; MacArthur & Wilson, 1967; Whittaker & Fernández-Palacios, 2007). Islands also offer ideal frameworks for studying colonization processes and the characteristics of species that successfully arrive and establish. When a new species becomes established on an island, it engages in new interactions (and may alter existing local ones), including animal-plant mutualisms such as pollination and seed dispersal (see Traveset etal., 2013; Heleno etal., 2013a and references therein), or antagonisms, such as seed predation (Carpenter etal., 2020). Therefore, the varied assemblages of animals and plants that colonize different islands may give rise to unique interactions that shape the ecological and evolutionary trajectories of the species involved. In particular, interactions between animals and plants, and their ecological roles, often differ from those of their ancestors on continents or less isolated islands, and niche shifts are common (Banack, 1998; Valido & Olesen, 2019). Birds and mammals are the most common seed dispersers on continents (Kitamura etal., 2002; Donatti etal., 2011; Fleming & Kress 2013; Timóteo etal. 2018), but they differ in their capacity for island colonization. As a consequence, whereas birds remain important on islands, the relative importance of certain groups of mammals (bats) and reptiles (mainly tortoises, iguanas, and other lizards) relative to birds increases, sometimes even surpassing that of birds in some isolated archipelagos (Olesen & Valido, 2003; Heleno etal., 2013a; Nogales etal., 2005, 2017; Valido & Olesen, 2019, Falcon etal., 2020; Albert etal., 2021). Endozoochory (i.e., the dispersal of seeds by animals after ingestion) is an important dispersal mechanism during island colonization and establishment (Ridley, 1930). One of the peculiarities of island communities is their ‘disharmony’ as compared to continental ones (Darwin 1859). Disharmony occurs when taxa on islands are overor 162 M.Nogales et al. 1 3 under-represented relative to comparable continental environments, at least in part because of differences in rates of long-distance dispersal over water (Whittaker & Fernández-Palacios, 2007). As a consequence, some animals (Nogales etal., 1999), but also plants (Price & Wagner, 2004) undergo niche shifts and perform different ecological roles after colonizing islands, filling niches that would be occupied by unrelated taxa on continents. Thus, when animal species arrive on islands, they often expand their niche breadth to occupy multiple trophic niches (i.e., the so-called ecological release) (Wright, 1980), which may involve the range of interactions that animals have with seeds, along the continuum from mutualism (dispersal) to antagonism (predation). Therefore, island environments are advantageous for the in-depth assessment of a number of ecological processes that can be elusive to measure in more diverse continental sites. These include: the overlooked importance and role of non-standard dispersal mechanisms; determining the comparative effectiveness of seed dispersal interactions by disparate agents; the structure of interactions at community and ecosystem scales (e.g., ecological networks and fluxes); and the lasting effects of trait anachronisms and species extinctions, both of which are common on island systems. Islands have suffered high rates of species decline and extinction, as well as species introductions, and are therefore in need of studies on the conservation biology and ecology of many species and communities (Fernández-Palacios etal., 2021). The breakdown of interactions as native species become rare or extinct, and the establishment of novel interactions as non-native species invade, offer opportunities to understand how ecological networks are assembled and how seed dispersal functions are altered (Vizentin-Bugoni etal., 2019, 2021). The application of seed dispersal theory and knowledge can be used to inform the ecological restoration of altered island environments (Culliney etal. 2012; Albert etal., 2020, 2021). Studies of frugivory and seed dispersal on islands often claim that this important ecological interaction is understudied and therefore remains incompletely understood. However, it is hard to judge the extent to which these claims are true, as most literature is highly scattered and there has never been a global review on this topic. This review has four goals. First, we present the current state of knowledge on mutualistic seed dispersal interactions between plants and frugivorous animals on islands worldwide. Second, we highlight the specific ecological and evolutionary characteristics of frugivory and seed dispersal phenomena on islands. Third, we assess the known conservation implications of altered seed dispersal on islands. Finally, we aim to identify major gaps in knowledge of frugivory and seed dispersal on islands, and suggest avenues for future research. Methods We focused our review on relatively isolated (mainly oceanic) islands, and excluded the larger continental islands (e.g., Great Britain, Madagascar, Japan, New Guinea, and New Zealand), though their respective offshore islands and islets have been included. These larger islands have more continental floras and faunas and have different ecological dynamics than the smaller islands (Whittaker & Fernández-Palacios 2007). 163 1 3 A Review ontheState oftheArt inFrugivory andSeed Dispersal… A systematic literature search was performed using Internet scientific search engines (http:// www. schol ar. google. com and http:// www. isikn owled ge. com/ WOS), to identify all papers published until August 2022. Simultaneously, a search in each geographic region was carried out by people with expertise in each insular region to incorporate personal datasets, MSc and PhD theses, and potentially important grey literature. The key words used in the searches were: frugivory (consumption of fruits by animals), seed dispersal and seed predation (by ingestion), and island or insular. Because the study was basically focused on seed dispersal by frugivorous animals (or fruitand seed-consuming animals) we concentrated our search on those contributions that include frugivory and fleshy-fruited plants. However, we included only studies in which data on frugivory and/or seed dispersal or predation by animals were provided, excluding those in which these interactions were treated collaterally. Although in the general search, the number of publications focused on islands was slightly more than 8000, we selected only those contributions whose basic topics were frugivory, seed dispersal and seed predation; this number was about 450. Those studies that included more than one of the three categories (i.e. both frugivory and dispersal, or both dispersal and predation, or all three) were counted more than once in the frequency analyses. While seed dispersal by frugivores is generally beneficial to plants, and seed predation by seed predators is harmful, we recognize that there is in fact a continuum of outcomes for seeds handled by animals (cf. Perea etal. 2013), and have therefore included seed predation along with frugivory and seed dispersal. We organised this information according to geographical region, following the hierarchical sequence: (1) the three main oceans—Atlantic, Pacific and Indian, (2) the main groups of archipelagos, and (3) the individual archipelagos or islands themselves (Appendix 1). We compiled summary statistics for all references in the bibliography. Each contribution was scored for: (1) study site and date, (2) the type of interactions (frugivory, seed dispersal and/or seed predation), (3) experiments performed on seed germination or viability, (4) the origin of the studied plants (native or non-native), and (5) main disperser guilds involved. Types of interactions (frugivory, seed dispersal and seed predation) and frugivores in the three oceans (Atlantic, Pacific and Indian) were analysed by Chi-square tests and they were performed by R (R Core Team, 2022), using ‘Bonferroni corrections’ to avoid type I Error in those cases in which multiple comparisons were carried out. Results andDiscussion Geographical Areas andStudies Information on frugivory and seed dispersal on islands is scattered and unevenly distributed across the world’s archipelagos (see Fig.1 and Appendix 1 and 2 for general statistics of the contributions). Aside from 29 general contributions of wide geographical scope, 419 contributions covered specific islands, archipelagos, or 164 M.Nogales et al. 1 3 island groups, with nearly 65% of them focusing on eight archipelagos (Canaries: 19%, Puerto Rico: 10%, Japanese offshore islands: 11%, Galápagos: 8%, Hawaiʻi: 6%, New Zealand offshore islands: 5%, Balearics: 5% and the Marianas: 5%). Other islands have moderate coverage, but gaps clearly exist in the smaller Melanesian (e.g., Vanuatu or Solomon Islands) and Micronesian islands (e.g. Palau, Marshalls or Kiribati), where numerous archipelagos are located. Furthermore, coverage of the Indian Ocean was also patchy. In this regard, it is interesting to note that, of the 85,138 islands identified globally, based on the application of the Flanders Marine Institute (2021), 43% were located in the Pacific Ocean, 34% in the Atlantic and 12% in the Indian Ocean (A. Naranjo Cigala, pers. comm.). However, when considering those islands larger than 1 km2, the percentage of islands in the Pacific is even higher (Weigelt etal., 2013), highlighting the large information gap existing in many of its islands and archipelagos. Chronology oftheStudies The first reports on seed dispersal processes came from travellers and naturalists who described how seed morphology facilitated dispersal across oceans, and included descriptive information on frugivory and seed dispersal (Darwin, 1859; Wallace, 1892; Guppy, 1906, 1917; Ridley, 1930). Later, the seminal work of Snow & Snow (1971, 1988), sparked the field of frugivory and seed dispersal on islands with studies from birds and fruiting plants of Trinidad in the Caribbean. Subsequently, Carlquist (1974), Porter (1983) and Bramwell (1985) attempted to understand how plants, including species potentially dispersed by endozoochory, arrived on some oceanic archipelagos such as Hawaiʻi, Galápagos, and the Canary Islands, respectively. However, most publications on frugivory and seed dispersal (89%) on islands have been published since 1980 (Fig.2; Appendix 3). Types ofInteractions Considering the more specific papers, a total of 448 frugivory, seed dispersal, and seed predation studies were conducted on islands (see Fig.3A; Appendix 1 and 2). Most (73%) of the publications focused on seed dispersal, followed by frugivory (30%), and seed predation (11%). Seed dispersal and frugivory have been studied more than seed predation (χ 24 = 29.10; P < 0.001) in islands from all three oceans (Atlantic, Pacific and Indian). While most frugivory studies were conducted on the offshore islands of Japan, Canaries and Puerto Rico, seed predation studies were significantly more prevalent in the Pacific, especially in the Galápagos and Hawaiian archipelagos. Less than 20% of the studies included seed germination experiments. These were more frequently carried out in the Atlantic and Indian oceans, especially in the Canaries and Mauritius. Most of the total studies (81%) included native plants, and non-native plants featured in 30% of them. 165 1 3 A Review ontheState oftheArt inFrugivory andSeed Dispersal… >35publications 15-34“ 6-14 “ <6 “ Fig. 1 A global view of the publications carried out on frugivory and seed dispersal on islands until 2022 inclusive 166 M.Nogales et al. 1 3 Types ofFrugivores There are three main guilds of vertebrate frugivores represented in these studies: reptiles, birds, and mammals (Fig.3B). Among these, tortoises, lizards, passerine and non-passerine birds, and bats were the main groups. Invertebrates were uncommon, and included only land crabs (n = 8) and orthopterans (New Zealand weta) (n = 1). Regarding reptiles, contributions on tortoises were frequent in the Pacific and Indian Oceans (this group having become extinct in the Atlantic islands; see LópezJurado & Mateo, 1993), whereas those on lizards were more frequent in the Atlantic (χ24 = 51.08; P < 0.001). Studies on lizard seed dispersal were especially numerous in the Canary and Balearic archipelagos, and surprisingly scarce in the Caribbean islands, given the abundance of lizard taxa there and their potential importance as seed dispersers (Malone etal., 2000; Pinto etal., 2008; Seokmin etal., 2022). Most of these studies involved native species. Native bird species have been studied more frequently than non-native species in the three oceans (χ22 = 20.03; P < 0.001). However, in the Hawaiian Islands and the offshore islands of Japan and New Zealand, non-native birds have received considerable attention. The most frequently studied taxa across three oceans were passerines. Non-passerines (larger body size, mainly pigeons) were more frequently studied in Pacific archipelagos (e.g., offshore islands of Japan and New Zealand, Philippines, western and central Polynesia: Tonga, Samoa, Cook Islands, and Micronesia: the Marianas) than in the Atlantic and Indian Oceans (χ22 = 6.52; P = 0.038). 0 20 40 60 80 100 120 140 160 180 200 No. Publicaons Decades Atlanc Ocean Pacific Ocean Indian Ocean Fig. 2 Cumulative number of contributions on the topic of frugivory and seed dispersal on islands from different oceans since 1900 167 1 3 A Review ontheState oftheArt inFrugivory andSeed Dispersal… Regarding mammals, native species were more often studied in the Pacific and Indian oceans whereas in the Atlantic, non-native mammals have received more attention (χ24 = 20.40; P < 0.001). Native bats were commonly studied in all three oceans, especially in archipelagos located at tropical latitudes (Atlantic Ocean: Caribbean islands; Pacific Ocean: Polynesia, Indonesia, and Melanesia; Indian Ocean: Andaman, Seychelles, and Mauritius). Primates (macaques) have been recently Fig. 3 A. Number of publications of the different types of interactions. B. Main guilds of frugivores included in the literature reviewed 168 M.Nogales et al. 1 3 studied in Mauritius where they were introduced (Reinegger etal., 2021), and in continental offshore islands of Japan, where they are native; they are naturally absent from all oceanic islands. Most contributions on non-native mammals have been carried out in the Atlantic and the Pacific, with rodents (especially rats, Rattus spp.) frequently being studied in many oceanic archipelagos worldwide. Other introduced mammals that have received attention include other rodents (ground squirrels in the Canaries and tree squirrels in Japan), as well as rabbits, carnivores (cats, pine martens, genets), insectivores (hedgehogs), and feral ungulates such as deer, goats, and pigs. In summary, reptiles, birds, and mammals are the three main groups of animals in studies of island frugivory and seed dispersal. While birds feature in studies across all archipelagos, mammals are better represented in studies on tropical continental islands and some oceanic islands, and reptiles are more frequently involved on oceanic islands. In a global review on lizard seed dispersal, Valido & Olesen (2019) reported that seed dispersal by lizards is disproportionately common on islands. These authors also comment that insular ecosystems are commonly poor in arthropods, so lizards may have undergone a niche shift to forage for fleshy fruits as a supplementary food source. By contrast, seed dispersal by tortoises is not exclusively an island phenomenon (Falcon etal., 2020). With regard to birds, frugivorous species of pigeons are mostly represented on islands too (Marrero 2009). Islands asIdeal Environments toExamine Seed Dispersal Theory andMechanisms atSpecies andCommunity Levels The Potential Importance ofNon‑Standard Dispersal Mechanisms Seed dispersal by mechanisms other than those to which a species appears to be adapted has been defined as “non-standard dispersal mechanisms” (Higgins etal., 2003). These appear to be especially important—or at least easier to detect—-on islands, whereas on continents they remain relatively unexplored. Several studies have recorded a high percentage of plants that lack obvious long-distance dispersal syndromes (hereafter LDD) (e.g., thalassochory, endozoochory, epizoochory or anemochory; sensu van der Pijl 1982) yet are capable of colonizing islands (Vargas etal., 2012; Heleno & Vargas, 2015; Arjona etal., 2018). As determined by their morphological traits, the dispersal syndromes of plants (see van der Pijl, 1982) can usually be associated with mechanisms that generate predictable seed dispersal pathways. However, in some cases, the actual dispersal vector might be quite different from the expected one (Nogales etal., 2012; Heleno & Vargas, 2015). Seed dispersal by large, omnivorous birds (ravens and gulls; see Nogales etal., 1999, 2001; Thorsen, 2003), legitimate dispersal of seeds by ‘seed predators’ (sometimes migratory birds) (see Fridriksson, 1975; Heleno etal., 2011; Ando etal. 2022), and secondary dispersal by endozoochory of birds that prey upon smaller frugivorous vertebrates (lizards and birds) (Nogales et al., 1998; Padilla et al., 2012), could be typical of underappreciated mechanisms of LDD to and between islands. Furthermore, in some cases, shorebirds (Hancock & Prince, 2021) 175 1 3 A Review ontheState oftheArt inFrugivory andSeed Dispersal… Conservation andtheRole ofFrugivory andSeed Dispersal inEcological Restoration Deforestation and landscape transformations have significantly altered nearly all islands that have been colonised by people (Kirch, 1997; Walker & Bellingham 2011; Fernández-Palacios etal., 2021). Human impacts pose a paradox for the maintenance of plant populations. On one hand, disturbances create new opportunities for plant colonisation and spread from remnant sources, but on the other hand they can pose strong barriers for dispersal if dispersal agents are negatively affected by changes or the new environments hamper recruitment (Holl, 1999; Zimmerman etal., 2000). Disturbances may also provide opportunities for the spread of nonnative species, many of which have become integrated into dispersal networks (as described above). Frugivory and seed dispersal are responsible for the regeneration of forests insitu (i.e., cyclic regeneration), and for new successional forests recolonizing deforested landscapes (Carlo & Morales, 2016; Wandrag etal., 2015, 2017; González-Castro etal., 2019; Albert etal., 2020). In Puerto Rico, for example, birds disperse about 70% of the woody tree and shrub species (Carlo & Morales, 2016). Thus, the conservation of frugivore populations is critical for the health of entire ecosystems there, given that a myriad of other life forms and processes also depend, directly or indirectly, on habitats formed by frugivore-dispersed plants. However, deforestation results in lower population sizes for native frugivores and fruiting plants; this, when accompanied by the introduction of non-native species into island communities, can deeply alter interaction networks (Heleno etal., 2013a, 2013b, 2022; Vizentin-Bugoni etal., 2019, 2021; Costa etal., 2022). Aside from increasing population sizes, ensuring restoration of the interaction functionality between species (with sufficient habitat range overlap, encounter, and success rates) is necessary to achieve self-sustaining island ecosystems (Heinen etal., 2020). In the context of forest regeneration and restoration efforts, the combined reduction in numbers of frugivores and plants creates a dual problem of source limitation (dispersal limited by the availability of seeds) and of dispersal limitation (dispersal limited by the lack of seed dispersers) (Nathan & Muller-Landau, 2000), which may be particularly acute on islands. Source limitation may potentially be dealt with if plant species can be cultivated, strategically planted, and then set fruit in areas where they become integrated into active networks of frugivory and seed dispersal (Peters etal., 2016). This means increasing the seed sources where there are strong numbers of frugivores naturally active. This can work in most cases because most island frugivores are generalists with broad diets that feed on a variety of fruiting species (Banack, 1998; Whelan etal., 1998), resulting in positive (facilitative) interactions between different species that co-occur in the same locality (Carlo, 2005). For example, Costa etal. (2022) have recently shown that well-preserved native forest fragments in Seychelles’ inselbergs do act as sources of native seed propagules to the surrounding invaded forests due to the action of frugivores, thus providing a critical insurance service for future forests. In contrast, for those species whose dispersal agents are extinct or extirpated, as described for many large-seeded plants and large-bodied frugivores, then assisted dispersal by humans, by reintroduced frugivores, or even by rewilding with non-native taxon 176 M.Nogales et al. 1 3 substitutes may be necessary. In a dramatic example of the latter, dispersal and subsequent recruitment of a critically-endangered, large-seeded tree (Diospyros egrettarum) were restored when Aldabran tortoises (Aldabrachelys gigantea) were introduced to replace the function of extinct tortoises on Ile aux Aigrettes off Mauritius (rewilding) (Griffiths etal., 2011). However, in many cases, seed dispersing animals may recover, recolonise, or be reintroduced following habitat restoration, for example by eradicating invasive mammalian predators or herbivores (Anderson etal., 2006; Bellingham etal., 2010). In some cases, seeds may be dispersed in sufficient numbers, but to areas where they have little chance of recruitment (Holl, 1999). Understanding the structure of frugivore-plant networks on islands, and how they change across habitat boundaries, can reveal which frugivore species are keystones in the dispersal process owing to their greater ability to cross habitat boundaries and disperse seeds into degraded habitats (Carlo & Morales, 2016; Rehm etal., 2017; Thierry etal., 2022; Costa etal., 2022). On the other hand, effective disperser communities can lead to undesirable outcomes for attempts to restore deforested islands and for securing remaining remnants of forests, if dispersers favour (through high abundance of fruit) non-native plant species over native plant species with slower growth rates (e.g., Pittosporum undulatum in Jamaica, Bellingham etal., 2018) and the Azores (Heleno etal., 2013a, b), Miconia calvescens in Tahiti (Spotswood etal., 2012), Morella faya (Huenneke & Vitousek, 1990; Woodward etal., 1990) or Clidemia hirta (Sperry etal., 2021) in Hawaiʻi, C. hirta and Cinnamomum verum in the Seychelles (Costa etal., 2022), Bischofia javanica in the Ogasawara Islands (Abe et al., 2018) or Aristotelia chilensis in Juan Fernández (Smith-Ramírez et al., 2013). This is especially pertinent on islands where natural disturbance regimes (e.g., cyclones, volcanoes) may enhance opportunities for expansion of populations of nonnative, fast-growing species (Fernández-Palacios etal., 2021). At the same time, strategic planting of a species with properties that make it a strong interactor in frugivory networks (e.g., long fruiting periods, González-Castro etal., 2015b; Peters etal., 2016) can make it serve as an attractor and facilitation nexus for the formation of forest nuclei (Holl etal., 2017). It is clear that restoration efforts should be guided by theoretical advances in our understanding of mutualistic networks (Peters etal., 2016). Therefore, more studies in island settings are needed to test and develop appropriate strategies to restore and conserve communities of native plants that rely on frugivorous agents of dispersal. Conclusions, Information Gaps andFuture Avenues ofResearch This is the first review on frugivory and seed dispersal studies carried out on islands worldwide. Despite the descriptive observations of voyagers and naturalists in earlier centuries, most information on frugivory and endozoochory has been published during the last two decades. One of the first patterns emerging from the review is that knowledge measured as the number of papers published on frugivory and seed dispersal on islands is unevenly distributed among biogeographic regions, with most information deriving from the subtropics, especially the Canary Islands and Puerto Rico. The disproportionate contributions to the literature from a subset of authors/ researchers account for some of this biogeographic disparity. Much of the research is concentrated in the archipelagos where there are research universities or research 177 1 3 A Review ontheState oftheArt inFrugivory andSeed Dispersal… stations. Furthermore, a serious gap clearly exist in parts of the Indian Ocean and in the Pacific Ocean (e.g. the smaller Melanesian and Micronesian islands), where numerous archipelagos are located. This uneven distribution among biogeographic regions gives us an incomplete view of frugivory and seed dispersal on islands. To advance our knowledge of frugivory and seed dispersal on islands, it would be valuable to compile complete lists of fleshy-fruited plants and frugivorous animals for each archipelago, or at least a significant representation of them, given the great number of existing islands. These lists would be further improved if they were supplemented with functional trait data for the existing species of plants and animals (native and non-native), and inferred traits of extinct species. Compiling these lists requires considerable effort and time, but if they were available for many islands and archipelagos across all biogeographic regions, they would facilitate macroecological studies and allow us to determine whether patterns that have been described from individual islands and archipelagos are general. The compilation of this information would also advance our understanding of how islands differ from continental systems. Islands are ideal places to study ecological drivers of key interactions, especially if studies are coordinated among islands by using comparable methods to examine questions across gradients of diversity, isolation, or disturbance. A parallel situation may exist with respect to vertebrate seed predators and the plants they consume. On many oceanic islands, the original seed predators were largely endemic birds, including parrots, pigeons, and a variety of large, flightless species. Today, roughly 90% of the endemic, seed-eating vertebrates on some islands have been replaced by globally invasive species of birds, rodents, and pigs (Carpenter etal., 2020). The non-native rodents, with their teeth and generalist diets, may interact with plants very differently from native granivorous birds, for example by adding a novel secondary-dispersal stage to bat-dispersed seeds (McConkey etal. 2003; Drake & McConkey 2021). One aspect of islands that both complicates our understanding of frugivory and seed dispersal, while also offering unprecedented opportunities, results from the fact that ecosystems on nearly all islands have been strongly modified by humans. In addition to habitat destruction, islands have experienced high rates of species extinctions and invasions of both plants and animals relative to comparable continental ecosystems (Fernández-Palacios etal., 2021). These changes have resulted in profound impacts on interactions among native species, while simultaneously creating novel interactions among species brought together for the first time (Fricke & Svenning 2020). However, we still have incomplete knowledge about the disruption of seed dispersal (and seed predation) interactions caused by extinctions and/or by novel interactions with invasive animals, especially those that show wide distributions, such as rodents (rats and mice), ungulates (especially goats), lagomorphs (mainly rabbits) and carnivores (feral cats, ferrets, or mongooses). As we gain knowledge about how patterns of frugivory and seed dispersal on islands have changed through time, we can apply that knowledge to conservation. Conservation efforts can be focused on species identified as playing key roles in networks. Introduced alien species can be assessed for their ability to replace the roles of extinct native species or to reconnect species that had dropped out of networks when their native partners were lost. Conversely, problematic invasive species can 178 M.Nogales et al. 1 3 be identified and removed from networks if they are determined to be facilitating invasion (invasional meltdown). Though much island biodiversity has been lost, it may be possible to halt or reverse the ongoing decline by gaining a deeper understanding of key biological interactions that maintain biodiversity, such as frugivory and seed dispersal, and employing that knowledge to conserve and restore functioning island ecosystems. Supplementary Information The online version contains supplementary material available at https:// doi. org/ 10. 1007/ s1222902309296-8. Acknowledgements We thank our respective institutions but especially to the University of Hawaiʻi at Mānoa, for providing us with basic funds to hold the ‘embryo meeting’ that triggered this publication. Many colleagues and friends, but especially Cecilia Smith, Janet Wilmshurst, Claire Aslan and Jason Gleditsch, helped us during the compilation and revision of this manuscript. Conchi Nieves helped us with the management of the bibliography and graphs, and Agustín Naranjo with the distribution and number of islands at a global scale. MN, AT and RH were partially funded by the Ministerio de Economía y Competitividad (Spain), projects: CGL2013-44386-P, CGL67865-P, CGL2017-88122-P and PID2022-137906NB-I00), funded by Ministerio de Ciencia, Innovación y Universidades (Spain). PJB was partially funded by the New Zealand Ministry for Business, Innovation and Employment’s Strategic Science Investment Fund. JHH was funded by Carlsberg grant no. CF19-0695. Author Contributions All authors contributed to conceiving the study ideas and revision of bibliography in their respective geographical areas. MN compiled all the information sent by all authors, made the statistical analyses and prepared the figures and tables. MN, KM, TC, PB, AT, AGC, RH and DD led the writing but all co-authors contributed significantly to improve the manuscript. All authors have approved the final version. Funding Open Access funding provided thanks to the CRUE-CSIC agreement with Springer Nature. Declarations Conflict of Interest The authors declare that the present work has non-financial interest and that there is no conflict of interest regarding the publication of this article. All data that support the findings of this study will be available contacting with the first author of the manuscript (MN). Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/. References Abe, T., Tanaka, N., & Shimizu, Y. (2018). 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