Proximate biochemistry of benthic and benthopelagic chondrichthyans: analysis of metabolic poise and relative trophic position with depth

Abstract

Understanding the energetic requirements and trophic positions of understudied chondrichthyan species (sharks, skates, rays and chimaeras) is important in terms of monitoring their overall ecological importance with depth because of increasing fishing pressure and global climate change. Data on deep-dwelling species is almost entirely lacking in terms of metabolic rates and quantitative trophic level information. In order to address this gap in knowledge, biochemical indices of aerobic and anaerobic metabolic capacity and bulk analyses of stable nitrogen (δ15N) and carbon (δ13C) isotopic compositions were measured in 14 species of benthic and benthopelagic chondrichthyan fishes over a broad depth range (~90--2200m) off the west coast of the U.S.A. The aerobic enzymes citrate synthase (CS) and malate dehydrogenase (MDH) and the anaerobic enzymes lactate dehydrogenase (LDH) and pyruvate kinase (PK) were analyzed in both red (RM) and white muscle (WM) at a common reference temperature of 10°C in order to determine metabolic poise and locomotory capacity of each species. Significant decreases observed in WM anaerobic enzyme activities with increasing median depth of occurrence (MDO) are most likely explained by the "visual-interactions hypothesis (VIH)." The VIH explains these trends as the result of a relaxed selective pressure for burst locomotion with declining light levels and smaller reactive distances between predator and prey. Phylogeny and locomotory mode are shown to have very little influence on aerobic and anaerobic metabolic poise compared to MDO, and similar metabolic potential is observed in co-occurring demersal sharks and rays. Bulk stable isotope analysis reveals a decrease in δ13C with depth that may indicate increased dietary reliance on pelagic vertical migrators and/or epipelagic carrion that are depleted in 13C relative to nearshore and benthic prey sources. Furthermore, the observed enrichment in 15N is likely due, in part, to the 15N enrichment in glutamic acid leaving the liver for the formation of muscle protein as a result of a decrease in urea:TMAO with increasing depth. This suggests a potentially unique increase in trophic discrimination factors (TDF) with depth in chondrichthyans as well as a current overestimation of trophic level calculations for these species at depth when using a standard 3.4‰ TDF. The low metabolic activities and potentially overestimated trophic levels observed in these toppredator, k-selected species makes them more susceptible to changes in the environment than previously thought. This information is key to accurately portraying ecosystem based food web and energetic dynamics in the deep-sea.