What is the primary function of the early teleost gill? Evidence for Na+/NH+4 exchange in developing rainbow trout (Oncorhynchus mykiss)

Abstract

Post-hatch fishes lack a functional gill and use cutaneous surfaces for exchange with the surrounding environment. The ionoregulatory hypothesis posits that ionoregulation is the first physiological process to be limited by cutaneous exchange, necessitating its shift to the gills.We hypothesized that the ontogeny of branchial ammonia excretion (Jamm) is coupled to Na+ uptake (JNain) in accordance with the current model for Na+=NH4+ exchange in freshwater. Using divided chambers, branchial and cutaneous Jamm, JNain and oxygen consumption (MO2) by larval rainbow trout were assessed. Following hatch, the skin accounted for 97% and 86% of total Jamm and JNain, respectively. Jamm and JNain shifted to the gills simultaneously at 15 days post-hatch (dph) and were highly correlated (R2 = 0.951) at the gills, but not the skin, over development. Contrastingly, MO2 shifted significantly later at 27 dph, in agreement with the ionoregulatory hypothesis. Moreover, the mRNA expression and/ or enzymatic activity of Rhesus proteins, Na+/H+-exchanger, H+-ATPase, Na+/K+-ATPase and carbonic anhydrase, all key components of the Na+=NH4+-exchange system, increased in the gills over larval development. We propose that the ontogeny of branchial JNain occurs as Na+=NH4+ exchange and provide evidence for a novel element to the ionoregulatory hypothesis, the excretion of potentially lethal metabolic ammonia.