Water filtration by burrowing sandprawns provides novel insights on endobenthic engineering and solutions for eutrophication

Abstract

Managing coastal ecosystems and preserving socio-ecological functioning require a comprehensive understanding of ecological services provided by resident organisms. Here, we provide novel information on water-filtration activities of endobenthic sandprawns (Callichirus kraussi), which are key ecosystem engineers in South African coasts. We demonstrate experimentally that benthic engineering by sandprawns reduces phytoplankton biomass by roughly 50%. Using long-term estuarine data, we demonstrate similar reductions in phytoplankton biomass (by roughly 70%) in sandprawndominated areas. Increased burrow wall chlorophyll-a relative to surface sediments that was evident in experiments suggests that pelagic filtration occurs through bi-directional water pumping and phytoplankton adsorption onto burrow walls. Our findings expand understanding of the ecological relevance of sandprawns and functionally similar organisms, the mechanisms by which they engineer ecosystems and their role in mediating coastal bentho-pelagic coupling. Our findings also highlight the potential for deposit-feeders to be used as nature-based solutions to counter coastal eutrophication. Coastal ecosystems are some of the most productive and ecologically significant habitats on earth 1-3. They are critical nursery and feeding grounds for resident and migrant species and subsidise offshore ecosystems through nutrient and trophic transfers 4,5. Coastal ecosystems also supply valuable goods and services that support human livelihoods and local economies 2,6. However, due to their proximity to human settlements and their aesthetic appeal, coastal systems rank amongst the most threatened and degraded ecosystems on earth, owing to multiple human stressors being applied simultaneously 6-10. Nutrient enrichment is arguably the most pervasive driver of coastal deterioration in the 21 st century, resulting in notable impairments of ecosystem multi-functionality and declines in the quality of goods and services provided 11,12. Government and management agencies therefore invest heavily in measures to counter socio-ecological losses arising from excessive nutrient inputs. The harnessing of ecological functions and services provided by biological systems to overcome environmental degradation, variously referred to as ecological engineering, nature-based solutions, bioremediation and/ or biomanipulation, is increasing in popularity as a sustainable, nature-based tool that can mitigate nutrient enrichment in coastal ecosystems 12-15. In this regard, suspension-feeding organisms (e.g. clams and mussels) and coastal vegetation have dominated mitigation narratives, leading to significant investments in conservation, restoration and engineering programs that exploit their water-purification capabilities 12,16,17. In contrast, burrowing deposit-feeding organisms have been overlooked, despite them being dominant components of sedimentary biotopes (numerically and ecologically) 18-20 , which are significant constituents of coastal ecosystems. In particular, there has bee...

Water filtration by endobenthic sandprawns enhances resilience against eutrophication under experimental global change conditions

“…A marina has been constructed on its eastern shores and periodic dredging of the main channel occurs in the lower reaches 36 . The water level in the estuary is mechanically regulated 35 and the mouth is opened once per month (spring high tide) during summer (low rainfall) but is kept open during winter (high rainfall) 15 , 36 . Riverine inputs that include discharge from urbanized and industrialized areas have resulted in the system being classified as eutrophic 35 , but this is likely exacerbated by sewage spills associated with ailing infrastructure.…”

“…Harmful algal blooms have been recorded, including that of toxic golden algae Prymnesium parvum , which has been linked to fish mortality in the system 36 . The lower reaches of the estuary are occupied by dense populations (114/m 2 –240/m 2 ) of the sandprawn Kraussillichirus kraussi 15 (Supplementary Fig. S1 ).…”

“…In contrast, vegetated ecosystems and filter-feeder assemblages have been more prominent as natural counter measures for eutrophication 13 , 14 . Recent research, however, has shown that some endobenthic deposit-feeding crustaceans (sandprawns), despite their functional designation, are capable of exerting top-down control on phytoplankton 15 . Specifically, sandprawn presence was shown to reduce phytoplankton biomass by almost 50% in experimental mesocosms, with similar effects recorded in situ.…”

“…Specifically, sandprawn presence was shown to reduce phytoplankton biomass by almost 50% in experimental mesocosms, with similar effects recorded in situ. Bi-directional water pumping during ventilation/irrigation was hypothesized to increase phytoplankton entrapment onto burrow walls, thereby reducing phytoplankton biomass in the water column 15 . This led to the suggestion that below-ground burrow superstructures of sandprawns, and similar endobenthic organisms, may function as biological filtration systems that can increase resilience against coastal eutrophication 15 .…”

“…Bi-directional water pumping during ventilation/irrigation was hypothesized to increase phytoplankton entrapment onto burrow walls, thereby reducing phytoplankton biomass in the water column 15 . This led to the suggestion that below-ground burrow superstructures of sandprawns, and similar endobenthic organisms, may function as biological filtration systems that can increase resilience against coastal eutrophication 15 . However, the robustness of sandprawn water filtration to future global change conditions is unknown, even though addressing this issue is of both scientific and management relevance.…”