Bioturbation by Benthic Stingrays Alters the Biogeomorphology of Tidal Flats

Abstract
Fishing-down-marine-food-webs has resulted in alarming declines of various species worldwide. Benthic rays are one examples of such overexploited species. On tidal flats, these rays are highly abundant and play an ecologically important role. They use tidal flats as refuge, feeding and resting grounds, during which they bury into the sediment, which results in sediment bioturbation. Changes in bioturbation intensity, following ray removal, may affect the biogeomorphology of tidal flats with possible cascading effects on the macrozoobenthic community. However, it is poorly understood how these indirect effects could influence ecosystem function. We therefore studied the geomorphic impact of benthic rays (specifically the pearl whipray/stingray Fontitrygon margaritella) on the tropical tidal flats of the Bijagós Archipelago, Guinea-Bissau, on a landscape scale. We investigated 1) bioturbation rates by rays using drone and ground surveys, 2) the spatial distribution of ray pits on multiple tidal flats, 3) the impact of rays on sediment properties and macrozoobenthos by experimental exclusion (15 months). Benthic rays bioturbated 3.7 ± 0.35% of the tidal flat’s sediment surface per day over one single 24-h period, which equals a complete top-sediment-surface turnover every 27 days. The spatial distribution of ray pits was affected by tidal flat geomorphology since pits decayed faster at areas exposed to strong hydrodynamic forces. Predator exclusion altered sediment properties, leading to changes in sedimentation (− 17%) and erosion (− 43%) rates. In addition, macrozoobenthic species composition changed, marked by an increase in Capitellidae worms and a greater biomass of Malacostraca over time. These changes indicated substantial effects of ray bioturbation on the biotic and geomorphic landscape of tidal flats. Overall, we conclude that changing abundances of benthic rays can have clear landscape-wide geomorphological effects on intertidal ecosystems. These indirect consequences of fisheries should be incorporated in integrative management plans to preserve tidal flats and connected ecosystems.

Acknowledgements
Many thanks go to L. Dos Santos, S. João Correia, Luta, Quintino, O. Clements T. Zuidewind for field assistance. We would like to thank IBAP for being a partner and providing logistical support. In addition, thanks to NGO Tiniguena-Esta Terra É Nossa, Management authorities of the Urok and Orango National Parks, MAVA foundation and local communities for providing access to their lands. Our thanks go to A. Coelho, M. Henriques, L. Kleine Schaars, M. Laveleye and L. Niemeijer for providing identification keys to the macrozoobenthos. We would like to thank M. Zwarts and J. Heusinkveld from the Fieldwork Company for drone and logistic assistance. This study was funded by the MAVA Foundation (Waders of the Bijagós) and LG by the Dutch Research Council (NWO016.VENI.181.087). Appropriate ethics, permits and other approvals were obtained for the research included in this manuscript.

Publisher
Springer Science and Business Media LLC

Journal
Ecosystems

DOI
10.1007/s10021-024-00901-4

Additional Links
https://link.springer.com/10.1007/s10021-024-00901-4