Disease Outbreak in a Keystone Grazer Population Brings Hope to the Recovery of Macroalgal Forests in a Barren Dominated Island

Francesca Gizzi,Rodrigo Silva,João Gama Monteiro,Sahar Chebaane,Filipe Henriques,Alejandro Bernal-Ibáñez,Nuno Castro,Silvia Almeida,Susanne Schäfer,Ignacio Gestoso,João Canning-Clode

doi:10.3389/fmars.2021.645578

Abstract

Macroalgal forests play a key role in shallow temperate rocky reefs worldwide, supporting communities with high productivity and providing several ecosystem services. Sea urchin grazing has been increasingly influencing spatial and temporal variation in algae distributions and it has become the main cause for the loss of these habitats in many coastal areas, causing a phase shift from macroalgae habitats to barren grounds. The low productive barrens often establish as alternative stable states and only a major reduction in sea urchin density can trigger the recovery of macroalgal forests. The present study aims to assess if the 2018 disease outbreak, responsible for a strong reduction in the sea urchinDiadema africanumdensities in Madeira Island, was able to trigger a reverse shift from barren grounds into macroalgae-dominated state. By assessing the diversity and abundance of benthic sessile organisms, macroinvertebrates and fishes before, during and after that particular mass mortality event, we evaluate changes in benthic assemblages and relate them to variations in grazer and herbivore densities. Our results revealed a clear shift from barren state to a macroalgae habitat, with barrens characterized by bare substrate, sessile invertebrate and Crustose Coralline Algae (CCA) disappearing after the mortality event. Overall variations in benthic assemblages was best explained by four taxa (among grazers and herbivores species). However, it was the 2018 demise ofD. africanumand its density reduction that most contributed to the reverse shift from a long stable barren state to a richer benthic assemblage with higher abundance of macroalgae. Despite this recent increase in macroalgae dominated habitats, their stability and persistence in Madeira Island is fragile, since it was triggered by an unpredictable disease outbreak and depends on howD. africanumpopulations will recover. With no control mechanisms, local urchin populations can easily reach the tipping point needed to promote a new shift into barren states. New conservation measures and active restoration are likely required to maintain and promote the local stability of macroalgal forests.

Highlights

Coastal habitats represent one of the most productive and valued ecosystems of our planet (Costanza et al, 1997) but they are seriously threatened by multiple factors and compounding pressures such as habitat loss and degradation, pollution, overexploitation, species introductions and climate change
The present study aims to assess whether the 2018 abrupt reduction in D. africanum densities (Gizzi et al, 2020) triggered areas that were previously barren to transform into algae dominated areas by correlating urchin densities with the occurrence of distinct benthic assemblages
The general decreasing trend in the abundance of benthos categories and sessile functional groups that are typically dominant in barren states, were accompanied by a yearly decrease in the density of individuals from grazer taxa (Figure 3)

Summary

Introduction

Coastal habitats represent one of the most productive and valued ecosystems of our planet (Costanza et al, 1997) but they are seriously threatened by multiple factors and compounding pressures such as habitat loss and degradation, pollution, overexploitation, species introductions and climate change (see Solan and Whiteley, 2016 and references therein). In macroalgal forests, local herbivore populations are often able to drive fluctuations in spatial and temporal distribution of algal communities (Stachowicz et al, 2007; Schmitz, 2008; Owen-Smith, 2014), determine algal abundance and species composition (Van Alstyne, 1989), influence algal growth rates and reproductive output (Shurin et al, 2002; Steneck et al, 2002) For this reason, major increases in local populations of key grazers and herbivores can lead to the replacement of productive macroalgae forests with impoverished barrens dominated by encrusting organisms (Pinna et al, 2020 and references therein). Numerous studies have unequivocally demonstrated an inverse relationship between urchin density and algal biomass as well as their role in promoting a shift of habitats with complex macroalgae forests into urchin barrens (e.g., Filbee-Dexter and Scheibling, 2014; Ling et al, 2015; Hernández, 2017; Melis et al, 2019; Pinna et al, 2020)

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Results

Conclusion