Depth-dependent trophic strategies of Caribbean sponges on mesophotic coral reefs

Abstract

Mesophotic coral reef ecosystems (MCEs) are characterized by gradients in irradiance, temperature and trophic resources. As depth increases on Caribbean mesophotic reefs, particulate organic matter increases while dissolved organic matter decreases, and the increase in particulate organic matter is directly related to the increase in sponge abundances and growth rates on MCEs. To further understand the trophic ecology of sponges, changes in microbiome composition and function, stable isotopic composition and proximate biochemical composition of 4 Caribbean reef sponges (Amphimedon compressa, Agelas tubulata, Plakortis angulospiculatus and Xestospongia muta) were quantified along a shallow to mesophotic depth gradient on Grand Cayman Island. Increases in δ15N for all sponges were observed as depth increased, indicating an increasing reliance on heterotrophic food resources. Species-specific changes in symbiotic microbial community composition were also observed as depth increased, and the predicted functional genes associated with nitrogen and carbon cycling showed species-specific changes between depths. Regardless of species-specific changes in microbiome community structure or function, or whether sponges were classified as high microbial or low microbial abundance, sponges increased their consumption of particulate organic matter with increasing depth into the lower mesophotic zone.

Production of phytodetritus by a coral reef sponge increases from shallow to mesophotic depths

“…As depth increases sponge consumption of POM, specifically picoplankton with its lower C : N ratio, increases and is associated with increasing sponge biomass and growth rates (Macartney et al 2021 a , 2022). The increases in sponge biomass and growth appear to be supported by increasing tissue protein concentrations in Agelas tubulata , and other sponges, with increasing depth (Macartney et al 2022). This indicates that mesophotic sponges have a net positive balance between protein synthesis and degradation which is common in faster growing animals (Fraser and Rogers 2007).…”

“…Sponges, both high and low microbial abundance symbiotic states, known as HMA and LMA phenotypes, respectively, in the sponge biology literature (Hentschel et al 2006), also consume DOM with the rates of uptake and assimilation greater in high microbial abundance sponges compared to low microbial abundance sponges (Hoer et al 2018; McMurray et al 2018). Rates of pumping, choanocyte chamber densities and POM uptake and assimilation, however, are commonly higher in low microbial abundance sponges when assessed directly or when using stable isotopic analyses (Weisz et al 2008; Maldonado et al 2012; Poppell et al 2014; McMurray et al 2018; Rix et al 2020; Macartney et al 2021 a , b , 2022; Lesser et al 2022) with some low microbial abundance sponge species apparently not utilizing DOM at all (de Goeij et al 2017; Hoer et al 2018; McMurray et al 2018). In high microbial abundance sponges the majority of DOM uptake is driven by their microbiomes as host DOM uptake is equivalent between high microbial abundance and low microbial abundance sponges (Rix et al 2020).…”

“…Importantly, on coral reefs the particulate organic nitrogen (PON) fraction of the POM pool increases both in absolute terms, and as a proportion of the total organic nitrogen pool with increasing depth (Lesser et al 2020). As depth increases sponge consumption of POM, specifically picoplankton with its lower C : N ratio, increases and is associated with increasing sponge biomass and growth rates (Macartney et al 2021a(Macartney et al , 2022. The increases in sponge biomass and growth appear to be supported by increasing tissue protein concentrations in Agelas tubulata, and other sponges, with increasing depth (Macartney et al 2022).…”