Ventilatory sensitivity to ammonia in the Pacific hagfish (Eptatretus stoutii), a representative of the oldest extant connection to the ancestral vertebrates

Abstract

Ventilatory sensitivity to ammonia occurs in teleosts, elasmobranchs and mammals. Here, we investigated whether the response is also present in hagfish. Ventilatory parameters (nostril flow, pressure amplitude, velar frequency and ventilatory index, the last representing the product of pressure amplitude and frequency), together with blood and water chemistry, were measured in hagfish exposed to either high environmental ammonia (HEA) in the external sea water or internal ammonia loading by intra-vascular injection. HEA exposure (10 mmol l −1 NH 4 HCO 3 or 10 mmol l −1 NH 4 Cl) caused a persistent hyperventilation by 3 h, but further detailed analysis of the NH 4 HCO 3 response showed that initially (within 5 min) there was a marked decrease in ventilation (80% reduction in ventilatory index and nostril flow), followed by a later 3-fold increase, by which time plasma total ammonia concentration had increased 11-fold. Thus, hyperventilation in HEA appeared to be an indirect response to internal ammonia elevation, rather than a direct response to external ammonia. HEA-mediated increases in oxygen consumption also occurred. Responses to NH 4 HCO 3 were greater than those to NH 4 Cl, reflecting greater increases over time in water pH and P NH3 in the former. Hagfish also exhibited hyperventilation in response to direct injection of isotonic NH 4 HCO 3 or NH 4 Cl solutions into the caudal sinus. In all cases where hyperventilation occurred, plasma total ammonia and P NH3 levels increased significantly, while blood acid-base status remained unchanged, indicating specific responses to internal ammonia elevation. The sensitivity of breathing to ammonia arose very early in vertebrate evolution.

Ammonia induced toxico‐physiological responses in fish and management interventions

“…Hyperventilation is a common response to elevated ammonia levels in fish. However, hyperventilation was directly related to internal ammonia rather than external ammonia 96 . Common carp exposed to ammonia exhibited reduced activity, exhaustion, and reduced feeding activity.…”

“…However, hyperventilation was directly related to internal ammonia rather than external ammonia. 96 Common carp exposed to ammonia exhibited reduced activity, exhaustion, and reduced feeding activity. The fish showed surfacing responses due to gill damage and respiratory hindrances.…”

Insights into the control and consequences of breathing adjustments in fishes-from larvae to adults

“…Owing to the limited data available on mechanisms of ammonia sensing, the following discussion focuses on the ventilatory effects of changes in environmental O 2 and CO 2 levels. However, readers interested in the ventilatory effects of the third respiratory gas, NH 3 , are directed to the following publications ( Zhang and Wood, 2009 ; Zhang et al, 2011 ; Zhang et al, 2013 ; De Boeck and Wood, 2015 ; Zhang et al, 2015 ; Eom et al, 2019 ; Eom et al, 2020 ; Eom and Wood, 2021 ; Porteus et al, 2021 ).…”

Dining on the dead in the deep: Active NH4+ excretion via Na+/H+(NH4+) exchange in the highly ammonia tolerant Pacific hagfish, Eptatretus stoutii

“…9 Notably, hypo-regulation is not associated with conversion of ammonia to alternative end-products such as glutamine or urea, 9 a strategy observed in airbreathing ammonia tolerant fishes. 27,28 Furthermore, hagfish metabolic rate is unabated during HEA exposure, 29 thus adding metabolically produced ammonia to exogenous ammonia loading. Taken together, these observations indicate that the ability of hagfish to hyporegulate [T amm ] p during HEA exposure is achieved by active NH 4 + excretion through a yet unidentified mechanism, possibly coupled to reduced permeability to environmental NH 3 to minimize loading.…”