Fasting in the ureotelic Lake Magadi tilapia, Alcolapia grahami, does not reduce its high metabolic demand, increasing its vulnerability to siltation events.

Gudrun De Boeck,John N Maina,Chris M Wood,Amit K Sinha,Rodi O Ojoo,Geraldine D Kavembe,Victoria Matey,Kevin V Brix,Mosiany L Kisipan,Adalto Bianchini,Lucas F Bianchini,Michael B Papah,Ora E Johannsson,Anne Todgham

doi:10.1093/conphys/coz060

Abstract

Lake Magadi, Kenya, is one of the most extreme aquatic environments on Earth (pH~10, anoxic to hyperoxic, high temperatures). Recently, increased water demand and siltation have threatened the viable hot springs near the margins of the lake where Alcolapia grahami, the only fish surviving in the lake, live. These Lake Magadi tilapia largely depend on nitrogen-rich cyanobacteria for food and are 100% ureotelic. Their exceptionally high aerobic metabolic rate, together with their emaciated appearance, suggests that they are energy-limited. Therefore, we hypothesized that during food deprivation, Magadi tilapia would economize their energy expenditure and reduce metabolic rate, aerobic performance and urea-N excretion. Surprisingly, during a 5-day fasting period, routine metabolic rates increased and swimming performance (critical swimming speed) was not affected. Urea-N excretion remained stable despite the lack of their N-rich food source. Their nitrogen use switched to endogenous sources as liver and muscle protein levels decreased after a 5-day fast, indicating proteolysis. Additionally, fish relied on carbohydrates with lowered muscle glycogen levels, but there were no signs indicating use of lipid stores. Gene expression of gill and gut urea transporters were transiently reduced as were gill rhesus glycoprotein Rhbg and Rhcg-2. The reduction in gill glutamine synthetase expression concomitant with the reduction in Rh glycoprotein gene expression indicates reduced nitrogen/ammonia metabolism, most likely decreased protein synthesis. Additionally, fish showed reduced plasma total CO2, osmolality and Na+ (but not Cl−) levels, possibly related to reduced drinking rates and metabolic acidosis. Our work shows that Lake Magadi tilapia have the capacity to survive short periods of starvation which could occur when siltation linked to flash floods covers their main food source, but their seemingly hardwired high metabolic rates would compromise long-term survival.

Highlights

East African Rift valley alkaline soda lakes are an unusual and harsh habitat for living organisms
Due to the extremely demanding conditions they live in, Lake Magadi tilapia have some of the highest metabolic rates seen in fish
The lake has been subjected to siltation and flash floods due to human activities, which could endanger the growth of the cyanobacteria Arthrospira sp., the main food source of the tilapia

Summary

Introduction

East African Rift valley alkaline soda lakes are an unusual and harsh habitat for living organisms. Even when covered with thick soda crusts, they still contain viable niches in the lake margins, lagoons and the nearby springs that supply the lakes with volcanic groundwater (Fig. 1) (Coe 1966, Kavembe et al, 2016) One of these lakes is Lake Magadi in Kenya that has an extremely high pH (up to 10.0), extreme alkalinity (>300 mmol L−1), high temperature (>40◦C at some sites), high levels of reactive O2 species (>8 μmol L−1 at some sites during daytime irradiation by high UV light levels), a salinity close to 60% seawater, and large daily fluctuations in O2 levels ranging from anoxia or hypoxia to hyperoxia (Coe, 1966; Johansen et al, 1975., Narahara et al, 1996; Johannsson et al, 2014, Wood et al, 2016). This unique fish is under threat from anthropogenic factors, and in 2006, A. grahami was placed on the IUCN Red List of Threatened Species, where it is classified as vulnerable (Bayona and Akinyi, 2006)

Objectives

Methods

Results

Conclusion