On a Reef Far, Far Away: Anthropogenic Impacts Following Extreme Storms Affect Sponge Health and Bacterial Communities

Amanda Shore,Sarah W Davies,Lory Z Santiago-Vázquez,Carsten G B Grupstra,Lauren Stadler,Adrienne M S Correa,Jordan A Sims,Shawn M Doyle,Lauren I Howe-Kerr,Kathryn E F Shamberger,Michael Grimes,Jason B Sylvan

doi:10.3389/fmars.2021.608036

Abstract

Terrestrial runoff can negatively impact marine ecosystems through stressors including excess nutrients, freshwater, sediments, and contaminants. Severe storms, which are increasing with global climate change, generate massive inputs of runoff over short timescales (hours to days); such runoff impacted offshore reefs in the northwest Gulf of Mexico (NW GoM) following severe storms in 2016 and 2017. Several weeks after coastal flooding from these events, NW GoM reef corals, sponges, and other benthic invertebrates ∼185 km offshore experienced mortality (2016 only) and/or sub-lethal stress (both years). To assess the impact of storm-derived runoff on reef filter feeders, we characterized the bacterial communities of two sponges, Agelas clathrodes and Xestospongia muta, from offshore reefs during periods of sub-lethal stress and no stress over a three-year period (2016—2018). Sponge-associated and seawater-associated bacterial communities were altered during both flood years. Additionally, we found evidence of wastewater contamination (based on 16S rRNA gene libraries and quantitative PCR) in offshore sponge samples, but not in seawater samples, following these flood years. Signs of wastewater contamination were absent during the no-flood year. We show that flood events from severe storms have the capacity to reach offshore reef ecosystems and impact resident benthic organisms. Such impacts are most readily detected if baseline data on organismal physiology and associated microbiome composition are available. This highlights the need for molecular and microbial time series of benthic organisms in near- and offshore reef ecosystems, and the continued mitigation of stormwater runoff and climate change impacts.

Highlights

Tropical coral reef ecosystems have evolved in the context of nutrient-poor waters
Suggest that floodwaters can reach and impact offshore benthic reef organisms. Bacterial communities of both X. muta and A. clathrodes showed disruptions to their community structure following two flood events in 2016 and 2017, relative to sponges collected during the same season in a no-flood year in 2018
We quantified an increased relative abundance of Enterobacteriaceae and two known human pathogens (E. coli and K. pneumoniae) in post-flood sponge samples, indicating that bacteria of terrestrial origin may interact with offshore reefs following extreme storm events

Summary

Introduction

Tropical coral reef ecosystems have evolved in the context of nutrient-poor (oligotrophic) waters. When nutrient-laden (eutrophic) terrestrial runoff mixes with reef-associated waters, this can directly or indirectly stress or kill reef organisms (Knight and Fell, 1987; Kerswell and Jones, 2003; Fabricius, 2005; Humphrey et al, 2008). Terrestrial runoff exposes reef organisms to decreased salinity, and increased levels of turbidity and contaminants (e.g., microbial pathogens, chemical pollutants) (Fabricius, 2005). Terrestrial runoff can reduce dissolved oxygen levels in reef-associated waters through several mechanisms (Nelson and Altieri, 2019). Floodwaters originating in urban areas may constitute a greater threat, if they contain high nutrient and contaminant loads due to overflows of wastewater management systems (Chen et al, 2019; Humphrey et al, 2019). Storm-associated runoff is increasingly recognized as a threat to reefs since the intensity and precipitation associated with tropical storms is increasing with climate change (Knutson et al, 2010; Emanuel, 2017)

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