| Abstract: | Deforestation results in habitat fragmentation, decreasing diversity, and functional degradation. For mangroves, no data are available on the impact of deforestation on the diversity and functionality of the specialized invertebrate fauna, critical for their functioning. We compiled a global dataset of mangrove invertebrate fauna comprising 364 species from 16 locations, classified into 64 functional entities (FEs). For each location, we calculated taxonomic distinctness (Δ+), functional richness (FRi), functional redundancy (FRe), and functional vulnerability (FVu) to assess functional integrity. Δ+ and FRi were significantly related to air temperature but not to geomorphic characteristics, mirroring the global biodiversity anomaly of mangrove trees. Neither of those two indices was linked to forest area, but both sharply decreased in human-impacted mangroves. About 60% of the locations showed an average FRe < 2, indicating that most of the FEs comprised one species only. Notable exceptions were the Eastern Indian Ocean and west Pacific Ocean locations, but also in this region, 57% of the FEs had no redundancy, placing mangroves among the most vulnerable ecosystems on the planet. Our study shows that despite low redundancy, even small mangrove patches host truly multifunctional faunal assemblages, ultimately underpinning their services. However, our analyses also suggest that even a modest local loss of invertebrate diversity could have significant negative consequences for many mangroves and cascading effects for adjacent ecosystems. This pattern of faunal-mediated ecosystem functionality is crucial for assessing the vulnerability of mangrove forests to anthropogenic impact and provides an approach to planning their effective conservation and restoration.Mangrove forests, once dominant intertidal ecosystems in the tropics (1), are disappearing at devastating rates worldwide (2, 3). Estimates of their loss are often uncertain due to the nature of available datasets (4) and the imprecision in determining mangrove area (5), but the current consensus on mangrove loss in the last quarter century ranges between 35 to 86% in the worst affected countries (2). Although recent estimates show a decrease in mangrove deforestation (6), global destruction is still happening, putting mangrove ecosystem functionality and, ultimately, provisioning of ecosystem services at risk (7). As recently reassessed (8), mangroves are unrivaled carbon sinks (9) and often contribute significant carbon and nitrogen to offshore habitats (10). They also act as nurseries for species from connected ecosystems (11) and protect tropical coasts from erosion (12) as well as extreme events (13).As theoretical and empirical studies have shown (14, 15), species extinctions in natural ecosystems often lead to loss in functional diversity, reflected by a decrease in the number of functional traits (16). Models predict that species-poor systems have low functional redundancy and are more likely to experience functional loss with species extinction (14, 17). In comparison with many tropical terrestrial forests, mangroves are characterized by low tree species diversity (1). The continued reduction of mangrove area and cover, coupled with simplistic restoration efforts often establishing monocultures (18), is expected to result in a sharp decrease in mangrove tree biodiversity at a global scale (2). A relationship between such decline in tree diversity and the loss of mangrove ecosystem functionality has been assumed rather than demonstrated (19), as this relationship has proven difficult to measure. Significant positive correlations, however, have been demonstrated between the species richness of mangrove trees, the associated macrofauna, and potential influence on aboveground primary productivity (20). The nexus between biodiversity and ecosystem functionality of species-poor systems is yet to be clarified, but a recent study of scavenging (measured by rate of fish carcasses consumed by scavengers) in Australian mangrove-fringed estuaries has highlighted the vulnerability of such systems to species loss (21).While reliable datasets are available on global mangrove tree diversity (1, 5), no such information exists for the species composition, functional diversity, and functional redundancy of the associated fauna. The harsh environmental conditions characteristic of mangrove forests (i.e., wide daily or seasonal variability in salinity and pH, hypo-, or even anoxia of the soil) and the small number of foundation plant species compared to terrestrial forests (2) suggest a lower niche availability among mangrove resident macrofauna (22).Mangrove ecosystems support unique faunal assemblages (22, 23), including a diverse array of sessile and mobile invertebrates, particularly crustaceans and mollusks (24, 25). Brachyuran crab assemblages are highly diverse in Indo-West Pacific (IWP) mangroves (25, 26) and are known to play a major role in ecosystem functioning (8, 20, 23). Their bioturbation activity has a significant engineering effect on the sediment through constant irrigation and oxygenation (27, 28). These crabs can also play a critical role in shaping tree dominance (29), influencing carbon cycling (30, 31), and structuring the sediment microbiome (32). The diversity of mangrove-associated gastropods also peaks in the IWP region but shows a bimodal distribution, with modes in the eastern Pacific coast of Central and South America and in Southeast Asia (33). Both gastropods and bivalves are known to be important bioengineers and bio-irrigators, playing a major role in shaping the biochemical properties of mangrove sediment and water (23).Despite growing evidence that the functions of mangrove forests are strongly dependent on viable and diverse invertebrate assemblages (20, 23), only few studies at local scales have focused on the diversity and taxonomic structure of such assemblages. The functional richness and redundancy of the latter, critical to the ecosystems’ capacity for essential services, are unknown, as are their functional vulnerability. The functional diversity of a community with species distributed in a multidimensional functional space within a given ecosystem can be quantified through indices such as functional richness [FRi—the volume of multidimensional space occupied by all species in a community within functional space (34, 35)] and functional redundancy [FRe—how redundant species and functional groups are at a given location (36)], which are increasingly used for assessing ecosystem functioning. Recently, these measures, used in parallel with functional vulnerability [FVu—the potential decrease of functional diversity as a consequence of species loss (36)], have also proven to be useful tools for assessing impacts of disturbances on ecosystems (37, 38) and for forecasting possible responses to anthropogenic perturbations (16).In this study, we assessed the vulnerability of global mangrove ecosystems to the loss of functions mediated by macrobenthic species by computing taxonomic distinctness Δ+ (39), FRi, FRe, and FVu indices based on crustacean and mollusk assemblages recorded from 16 different mangrove forests across the world. We assigned functional traits to the 209 crustacean and 155 mollusk species in our database according to their respective 1) feeding habits, 2) behavioral traits potentially affecting ecosystem characteristics, and 3) microhabitats. By using functional traits as proxies for functions, this approach allowed us to establish global patterns of macrobenthic taxonomic richness and ecosystem functionality in mangroves and to assess the vulnerability of the mangrove fauna as well as resilience of ecosystem functions mediated by them to current and future anthropogenic threats. |
