Deep-sea sponges in an Anthropocene ocean

Sponges (Porifera) are among the oldest multicellular animals on planet earth and are abundant throughout all oceans. From shallow, warm waters to the dark, cold deep sea. Sponges move large quantities of seawater through their body while efficiently removing dissolved and particulate nutrients. Their large filter capacity makes them important links in marine food webs as they are able to access nutrient sources that are unavailable to the majority of marine fauna and channel this energy to higher trophic levels. In the North Atlantic Ocean (NAO) sponges form dense aggregations, so called sponge rounds, that provide ecosystem services such as habitat provision, nutrient cycling and provision of novel, bioactive compounds. It remains unclear whether these deep-sea sponge grounds can continue to provide these services in a changing ocean that is increasingly industrialized. The physicochemical properties of the North Atlantic Ocean will be altered by human induced climate change. The aim of this thesis is to address this knowledge gaps by quantifying the basic eco-physiological processes such as oxygen consumption, clearance rate and uptake/release of inorganic nutrients of two habitat forming deep-sea sponges under the cumulative impacts of warmer, acidified seawater and the exposure to different types of re-suspended particles. The research underlying this thesis was part of the EU-funded research project Deep-sea Sponge Grounds Ecosystems of the North Atlantic: an integrated approach towards their preservation and sustainable exploitation (SponGES). Two model deep sea sponge species were used, Geodia barretti and Vazella pourtalesi. G. barretti collected from 300 m water depth in the Barents Sea, were exposed to four treatments resembling future ocean conditions (no treatment, 4 °C increase in seawater temperature, decrease of seawater pH by 0.3, and a combination of the high temperature, low pH). Over the course of 39 weeks, oxygen consumption, dissolved inorganic nutrient fluxes, and bacterioplankton clearance rates were measured as indicators of metabolic activity. All indicators within each sponge individual and per treatment were highly variable over time, and no effect of manipulated seawater treatments on these parameters could be demonstrated. Oxygen consumption rates in all groups closely followed a seasonal pattern, potentially caused by (a)biotic cues in the natural seawater flowing through the experimental aquaria. While similar metabolic rates across all treatments suggest that G. barretti physiologically coped with simulated future ocean conditions, tissue necrosis that developed in experimental animals might indicate that the response of the complex, high microbial G. barretti sponge (i.e., sponge host and microbial symbionts) to future ocean conditions may not be reflected in basic physiological processes. In addition to large scale changes of ocean conditions, also bottom trawling activities interact with the dense sponge aggregations. Bottom trawling has been identified as the most severe direct industrial threat to abundant sponge grounds by removing sponge biomass and indirect by re-suspending bottom sediments. Plumes of re-suspended sediment potentially smother and clog the aquiferous system of filter-feeding sponges with unknown implications for their health. The physiological responses of repeated exposure to natural sediment were studied in the glass sponge Vazella pourtalesii, which forms dense sponge grounds in Emerald Basin off Nova Scotia, Canada. Ex situ chamber-based measurements of bacterial clearance and oxygen consumption (respiration) rates indicated that the animals were able to cope with elevated concentrations of suspended sediment, as they expressed normal clearance and respiration rates over 7 days of sediment exposure. However, clearance rates significantly declined after 14 days of sediment exposure and the animals visibly accumulated sediment in their tissue. Therefore, long-term exposure to elevated concentrations of suspended sediment should be avoided in order to minimize adverse effects on the abundant Vazella sponge grounds. While sponges seem to cope with environmental changes and limited exposure to suspended particles as occurs in their natural environment, the response to cumulative stressors indicated impaired health. Exposure to a field relevant concentration of suspended sediment (50 mg L-1) and future ocean conditions (pH decrease of 0.2 units, temperature increase of 3 °C) on the physiological performance of Geodia barretti resulted in a cessation of pumping. Oxygen consumption rates remained unchanged under low pH and high temperature treatments and indicate mechanisms of pumping-independent mass transfer of oxygen. A small, but statistically significant shift in the microbiome associated with G. barretti was observed and possibly related to coping with cumulative stressors in this deep-sea sponge species. The synergistic nature of the treatment-specific effects has the potential to adversely affect the physiological fitness of this dominating sponge species in the North Atlantic Ocean. In addition to deep-sea fisheries the nascent industry of subsea mining is prospecting abundant mineral resources present in the deep sea. The extraction of subsea minerals, such as seafloor massive sulphide (SMS) deposits, will expose adjacent marine ecosystems to suspended particle plumes charged with elevated concentrations of heavy metals and other potentially toxic compounds. Up to date there is no information about the impact of mining activities on deep-sea benthic ecosystems such as abundant deep-sea sponge grounds in the North Atlantic Ocean. To simulate the effects of mining plumes on benthic life in the deep-sea, Geodia barretti and an associated brittle star genus were exposed to a field-relevant concentration of 30 mg L-1 suspended particles of crushed SMS deposits. Three weeks of exposure to suspended particles of crushed SMS resulted in a tenfold higher rate of tissue necrosis in sponges. All brittle stars in the experiment already perished within ten days of exposure. SMS particles were evidently accumulated in the sponge’s mesohyl and concentrations of iron and copper were 10 times elevated in SMS exposed individuals. Oxygen consumption and clearance rates were significantly retarded after the exposure to SMS particles, hampering the physiological performance of G. barretti. These adverse effects of crushed SMS deposits on G. barretti and its associated brittle star species potentially cascade in disruptions of benthic-pelagic coupling processes in the deep sea. More elaborate studies are advisable to identify threshold levels, management concepts and mitigation measures to minimize the impact of deep-sea mining plumes on benthic life. Sponges were shown to express high coping capacities towards fluctuations of environmental parameters within their habitat. However, additional stressors or persistence of sub-optimal conditions over extended time scales can challenge sponge’s ability to endure cumulative effects. Given the ecosystem services sponge grounds in the North Atlantic Ocean provide, industrial operations should ascertain refuges for deep-sea sponges faced with global ocean changes.

Wurz E., 2022. Multiple stress effects on deep-sea sponges. PhD thesis, Wageningen University, 155 p. Thesis.


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