In communities altered by extinction or invasion, the loss or gain of species may affect mutualisms, with cascading effects on ecosystem processes (Palmer et al. 2008, Traveset and Richardson 2014, Galetti et al. 2013). In the Hawaiian Islands, we show that non-native galliforms were largely seed predators for fruiting plants, with less than 5% of seeds surviving gut passage across all plant species examined. Further, gut passage by galliforms reduced germinability of ingested seeds, particularly for native plants. We also found that larger seeds were less likely to survive gut passage and to germinate following gut passage. In the wild, we found that galliforms were equally as likely to disperse seeds from native versus non-native plants, with variation between sites. Collectively, these findings suggest that non-native galliforms are poor dispersers, with the majority of ingested seeds not surviving gut passage or germination. They may act as a double-edged sword in Hawaiian forests – reducing the spread of non-native plants, but also reducing the dispersal of native plants. Galliforms are now the largest birds in Hawaiian forests, and their larger gape widths (16.7 mm for Kalij Pheasants and 15.1 mm for Erckel’s Francolins, Case and Tarwater 2020) suggest the potential to fill substitutive roles in dispersal of large-seeded plants. However, our results suggest an opposite scenario, by which gut passage by non-native galliforms reduces both seed survival and germination in large-seeded plant species. Hence, these birds may be replacing extinct native seed predators, rather than extinct native seed dispersers (Carpenter et al. 2020).
Galliforms are known to be major seed predators worldwide, likely due to their powerful gizzards. For instance, the Salvin’s Currasow (Mitu salvini) is highly frugivorous in its native range within the Amazon rainforest, but it destroys most of the seeds it consumes (Santamaría and Franco 2000). Destruction of non-native seeds is a potential conservation benefit of galliform introductions, and fruit removal by galliforms could reduce availability of invasive seeds and dispersal by other frugivores in the system. However, predation on native seeds may offset these benefits. In plants which produce a high number of seeds per fruit, even a low gut passage survival rate may contribute to substantial rates of dispersal. For instance, seeds of Rubus rosifolius, a common invader with 246 seeds per fruit, on average, had a mean gut passage survival rate of 5.4% for Kalij Pheasants. Given that an average of 38% of Rubus rosifolius seeds germinated following Kalij Pheasant ingestion, we predict five dispersed seeds to germinate after a single fruit is consumed by a Kalij Pheasant. Native plants with many seeds/fruit may similarly be dispersed. For instance, if we apply the same formula to Cyanea tritomantha, a native and federally endangered species, we predict nine dispersed seeds to germinate for each fruit consumed by a Kalij Pheasant. Further, we found that the duration of galliforms gut passage was notably long (median day that last seed was detected per trial = 5, range = 0–53 days, Appendix Fig. 1). Thus, in conjunction with animal movement, galliforms may be capable of long-distance dispersal events, potentially aiding in the range expansion of native or non-native plant species.
The effect of gut passage on seed germination varies across plant-frugivore species interactions, with both positive and negative effects observed (Traveset et al. 2001, Dracxler and Kissling 2021). We found that ingestion by non-native galliforms significantly reduced germination rates, and the effect was greater for the native plants that we tested. This suggests that even if ingestion rates were equal for seeds of native and non-native plants, intact seeds from non-native species would still be more likely to germinate compared to native seeds. Similar results have been found in other systems with introduced galliforms. For instance, in Patagonia, following gut passage of the introduced Silver Pheasant (Lophura nycthemera), seeds of non-native species are more likely to germinate compared with seeds native to the study area (Martin-Albarracin et al. 2018). From the 20 plant species that we tested, only 4 had higher germination rates following gut passage, 3 of which were non-native and belonged to the genus Rubus (Appendix Table 2); a genus that comprises numerous invasive species worldwide (Caplan and Yeakley 2013). The native and non-native species we examined did not significantly differ in seed width for species used in both survival and germination experiments, and broadly, fruit and seed traits are similar between native and non-native plants in Hawaiian forests (Sperry et al. 2021). It is currently unclear why native species may be more vulnerable to novel species interactions, and traits not examined here, such as seed-coat thickness (Traveset 1998), may be important for interaction outcomes. Further work is needed to identify the mechanisms that bias dispersal outcomes in relation to plant origin.
In novel ecosystems, one important consideration is how selection on functional traits may be altered following changes to communities (Strauss et al. 2006, McConkey et al. 2012). In modern forests of the Hawaiian Islands, non-native Passeriformes, with their small gape widths, dominate seed dispersal networks (Vizentin-Bugoni et al. 2019; 2021) and, as found here, smaller-seeded plants are more likely to survive and germinate following ingestion by galliforms. Thus, we may expect negative selection on seed width driven by the current frugivore assemblage, which may alter species interactions and affect the evolutionary trajectories of plants over time. For example, in Atlantic forests of the Amazon, the recent loss of large-gaped frugivores led to a rapid reduction in seed size in a common palm species (Galetti et al. 2013). If smaller seed widths are consistently selected for through interactions with frugivores, we may observe turnover in plant communities in relation to seed size or an evolutionary response in certain plants. A reduction in seed size may increase the probability of consumption, survival, and germination, but may reduce growth rate, reproduction, and survival in the later life history stages (Ambika et al. 2014). This will result in differing impacts on plant populations depending on which life stage is most important to population growth (Ambika et al. 2014).
Non-native birds now dominate seed dispersal networks in Hawaiian forests (Vizentin-Bugoni at al. 2019) and fill the most important roles in the seed dispersal network (Vizentin-Bugoni et al. 2021). The extent to which these birds disperse native versus non-native plant species may, not surprisingly, depend on the extent to which non-native plants are established where birds reside. For instance, on the island of Maui, non-native birds in native-dominated forests dispersed mostly native seeds in montane rain forests (Foster and Robinson 2007) and mostly non-native seeds in dry forest (Chimera and Drake 2010). On O‘ahu, where forests are highly invaded, non-native birds dispersed mostly seeds from non-native plants (Vizentin-Bugoni 2019). However, frugivore preferences for certain plants may also affect observed rates of seed dispersal (Aslan and Rejmánek 2012). Between our sites on O‘ahu and Hawai‘i, we did not detect differences in the probability of whether a given seed species within feces was native or non-native in origin (Appendix Table 3). To further distinguish how dispersal patterns for native versus non-native plants may depend on plant community composition, future work should consider the relative abundance of different fruits and galliform preferences for native and non-native plants. Further, we examined just two of at least 10 non-native galliforms with populations established in the Hawaiian Islands (Carpenter et al. 2020), and more work is needed to determine the impacts of the other species.
Global rates of species extinction are currently an estimated 1000 times greater than what would be expected without human influence (Pimm et al. 2014). Concurrent with species loss, humans have facilitated species invasions across all of the world’s biomes (Ricciardi 2007), with effects being particularly severe on oceanic islands (Fernández-Palacios et al. 2021). In the Hawaiian Islands, we found that novel species interactions between non-native galliforms and fruiting plants are often negative for plants. Further, we identified a functional mechanism driving interaction outcomes, with seed size influencing both survival during gut passage and germination thereafter. Collectively, these results indicate that the non-native frugivores studied here are not filling the role of extinct native large-gaped frugivores, potentially contributing to the decline of large-seeded native plants. Further, results suggest that seed size may be useful for predicting interaction outcomes and could be used in aiding management strategies. In the Hawaiian Islands, land managers will need to weigh costs and benefits of seed dispersal versus predation for native and non-native plant communities where galliforms are established. High rates of seed predation may warrant the exclusion or removal of galliforms from areas with native fruiting plants of conservation concern.