Around the world, the human-induced collapses of populations and species have triggered a sixth mass extinction crisis, with rare species often being the first to disappear. Although the role of species diversity in the maintenance of ecosystem processes has been widely investigated, the role of rare species remains controversial. A critical issue is whether common species insure against the loss of functions supported by rare species. This issue is even more critical in species-rich ecosystems where high functional redundancy among species is likely and where it is thus often assumed that ecosystem functioning is buffered against species loss. Here, using extensive datasets of species occurrences and functional traits from three highly diverse ecosystems (846 coral reef fishes, 2,979 alpine plants, and 662 tropical trees), we demonstrate that the most distinct combinations of traits are supported predominantly by rare species both in terms of local abundance and regional occupancy. Moreover, species that have low functional redundancy and are likely to support the most vulnerable functions, with no other species carrying similar combinations of traits, are rarer than expected by chance in all three ecosystems. For instance, 63% and 98% of fish species that are likely to support highly vulnerable functions in coral reef ecosystems are locally and regionally rare, respectively. For alpine plants, 32% and 89% of such species are locally and regionally rare, respectively. Remarkably, 47% of fish species and 55% of tropical tree species that are likely to support highly vulnerable functions have only one individual per sample on average. Our results emphasize the importance of rare species conservation, even in highly diverse ecosystems, which are thought to exhibit high functional redundancy. Rare species offer more than aesthetic, cultural, or taxonomic diversity value; they disproportionately increase the potential breadth of functions provided by ecosystems across spatial scales. As such, they are likely to insure against future uncertainty arising from climate change and the ever-increasing anthropogenic pressures on ecosystems. Our results call for a more detailed understanding of the role of rarity and functional vulnerability in ecosystem functioning. In ecological systems most species are rare—that is, represented by only a few individuals or restricted to particular habitats—and are vulnerable to being lost. Yet the ecological consequences of such biodiversity loss are often overlooked and remain controversial. In the best-case scenario, the functions that these rare species provide to their ecosystems might be insured by more common species, which share combinations of functional traits with the rare species, thereby helping to maintain ecosystem functioning despite rare species loss. In the worst-case scenario, rare species would have functional traits that are distinct from those of common species; thus, the functions they support would also be vulnerable to extinction. We examined three highly diverse ecosystems (coral reefs, alpine meadows, and tropical forests) and addressed whether common species would insure against the loss of functions carried by rare species. We demonstrate that highly distinct combinations of traits are supported predominantly by rare species. It is thus not only the quantity but also the quality of biodiversity that matters. Thus, our findings highlight that we need to change how we think about biodiversity in general, and about conservation strategies in particular, by moving beyond the protection of biodiversity per se and beyond focusing on iconic, charismatic, or phylogenetically distinct species, to protecting species that support irreplaceable functional roles and associated services.

Significance: Our results indicate that, even in highly diverse systems like coral reefs, we can no longer assume that the erosion of species diversity can be discounted by the high probability of functional redundancy: i.e., that several species can support the same function. Indeed, we show that fish species tend to disproportionately pack into a few particular functions while leaving many functions highly vulnerable, i.e., they are supported by just one species. Even the Coral Triangle, which has a high concentration of tropical-reef fishes, may experience a loss of functional diversity following fisheries pressure and local species extirpation. Our results suggest that the promised benefits of functional insurance from high species diversity may not be as strong as we once hoped.

Difficulties in scaling up theoretical and experimental results have raised controversy over the consequences of biodiversity loss for the functioning of natural ecosystems. Using a global survey of reef fish assemblages, we show that in contrast to previous theoretical and experimental studies, ecosystem functioning (as measured by standing biomass) scales in a non-saturating manner with biodiversity (as measured by species and functional richness) in this ecosystem. Our field study also shows a significant and negative interaction between human population density and biodiversity on ecosystem functioning (i.e., for the same human density there were larger reductions in standing biomass at more diverse reefs). Human effects were found to be related to fishing, coastal development, and land use stressors, and currently affect over 75% of the world's coral reefs. Our results indicate that the consequences of biodiversity loss in coral reefs have been considerably underestimated based on existing knowledge and that reef fish assemblages, particularly the most diverse, are greatly vulnerable to the expansion and intensity of anthropogenic stressors in coastal areas. The increasing intensity of human disturbance worldwide is triggering unprecedented biodiversity losses, which is raising concerns over whether ecosystems will work and continue delivering goods and services to humanity. In contrast to previous experimental studies, which describe saturating relationships between ecosystem functioning and biodiversity, we show that in reef fish systems, functioning (as standing biomass) accelerates with the addition of new species. This non-saturating relationship implies unique contributions of species to the functioning of this ecosystem and indicates that the consequences of losing biodiversity are significantly greater than previously anticipated. We also demonstrate a negative effect of human density on reef fish functioning such that for the same number of people the loss of standing biomass is significantly larger in more diverse ecosystems. Unfortunately, human effects can arise through multiple stressors (such as fishing, coastal development, and land use) and are widespread and likely to worsen, as some 75% of the world's coral reefs are currently nearby human settlements and because almost all countries with coral reefs are expected to double their populations within the next 50 to 100 years. Our results call for both further investigation of the impact of biodiversity on ecosystem functioning and strategies to manage and prevent the increasing intensity and expansion of anthropogenic stressors in coastal areas.

Delineating regions is an important first step in understanding the evolution and biogeography of faunas. However, quantitative approaches are often limited at a global scale, particularly in the marine realm. Reef fishes are the most diversified group of marine fishes, and compared to most other phyla, their taxonomy and geographical distributions are relatively well known. Based on 169 checklists spread across all tropical oceans, the present work aims to quantitatively delineate biogeographical entities for reef fishes at a global scale. Four different classifications were used to account for uncertainty related to species identification and the quality of checklists. The four classifications delivered converging results, with biogeographical entities that can be hierarchically delineated into realms, regions and provinces. All classifications indicated that the Indo-Pacific has a weak internal structure, with a high similarity from east to west. In contrast, the Atlantic and the Eastern Tropical Pacific were more strongly structured, which may be related to the higher levels of endemism in these two realms. The “Coral Triangle”, an area of the Indo-Pacific which contains the highest species diversity for reef fishes, was not clearly delineated by its species composition. Our results show a global concordance with recent works based upon endemism, environmental factors, expert knowledge, or their combination. Our quantitative delineation of biogeographical entities, however, tests the robustness of the results and yields easily replicated patterns. The similarity between our results and those from other phyla, such as corals, suggests that our approach may be of broad utility in describing and understanding global marine biodiversity patterns.

Significance: Marine organisms disperse mostly by ocean currents as larval propagules. Therefore, it is commonly thought that the duration of the larval stage is the fundamental determinant of geographic range size. Using a global compilation of reef fish traits, we test an alternative hypothesis: adult traits associated with population establishment and persistence in novel areas are better predictors of geographic range size than larval traits. We conclude that colonization success is as primary determinant of successful range extension and of geographic range size among tropical reef fishes.