Role of crab holobionts in benthic N cycling in mangroves with different trophic status

Abstract

Microbial dinitrogen (N2) fixation and intense bioturbation by macrofauna can contribute to reduce nitrogen (N) limitation in mangrove systems. In particular, crabs are important ecosystem engineers that rework sediments, redistribute organic matter, accelerate nutrient cycling and shape microbial communities in mangrove sediments. Hosting functionally diverse microbial communities, crabs form a discrete ecological unit (a holobiont). In this study, we report rates of respiration, inorganic N fluxes, net N2 fixation, denitrification and dissimilatory nitrate reduction to ammonium (DNRA) measured in the fiddler crab Leptuca thayeri and sesarmid crab Armases rubripes holobionts, which are dominant in oligotrophic and eutrophic mangrove systems of southeast Brazil, respectively. We measured lower biomass-specific rates of respiration and ammonium (NH4+) production for the larger L. thayeri compared to A. rubripes, with very different molar ratios of O2 respiration to NH4+ production (152:1 vs. 20:1, respectively). This suggests a size-metabolism relationship, different food quality or different coupling of N excretion and assimilation by the crab holobionts in the 2 systems. Both crab holobionts contributed to net denitrification and DNRA, with faster N cycling in A. rubripes in the eutrophic system. Net N2 fixation was also detected, with nearly 4-fold higher rates in A. rubripes compared to L. thayeri. Overall, our results illustrate active and complex N cycling associated with the 2 dominant crab holobionts and highlight their potential and overlooked role as important conduits of fixed N, which may double N2 fixation rates in the mangrove’s rhizosphere.

Research in a RAMSAR site: The Cananéia-Iguape-Peruíbe estuarine-lagoon complex, Brazil

“…Some previous studies carried out in the CIELC have monitored the environmental properties of this region, such as Besnard (1950), Kato (1966aKato ( , 1966bKato ( , 1966c, Teixeira (1968), Tundisi and Teixeira (1968), Miyao et al (1986), Miyao and Harari (1989), Braga (1995), Tessler and Souza (1998), Braga and Chiozzini (2008), and Maluf (2009). In recent decades, several scientific studies have been carried out to understand the oceanographic dynamics of the CIELC, considering the circulation patterns of the adjacent shelf and tidal inflows (Camargo and Harari, 1994;Mesquita and Harari, 2003); the physical and chemical properties of the water Chiozzini et al, 2010;Azevedo and Braga, 2011;Aguiar et al, 2013;Souza et al, 2011aSouza et al, , 2011bEschrique et al, 2014;Haytsmann, 2018;Mindaugas et al, 2023); sedimentary and geomorphological characterization and metal inputs (Mahiques et al, 2009;2013;2014;Cornaggia et al, 2018;Tramonte et al, 2018); geochemical aspects (Amorim, et al 2008;Barcellos et al, 2005;Aguiar et al, 2008;Perretti and Braga, 2022;Sutti et al, 2022;Millo et al, 2021); the composition of the ichthyofauna (Sadowsky, 1974;Tanji, 1981, 1983;Rios, 2001;Contente, 2013;<...…”