Metabolism, nitrogen excretion, and heat shock proteins in the central mudminnow (Umbra limi), a facultative air-breathing fish living in a variable environment

Abstract

The central mudminnow ( Umbra limi (Kirtland, 1841)) is a continuous, facultative air-breathing freshwater fish found in swamps of central Canada and northeastern USA. The first goal of this field and laboratory-based study was to characterize the physicochemical conditions of mudminnow habitat during the summer. Our second goal was to determine the metabolic, stress response, and nitrogen excretion strategies of this fish following variations in water temperature, dissolved oxygen, external ammonia, and short-term periods of air exposure. We report profound diurnal fluctuations in water temperature (13–31 °C), dissolved oxygen (2%–159% air saturation), and ammonia levels (10–240 μmol·L−1) in habitat of central mudminnow measured on three dates at six different sites over 24 h. The central mudminnow does not induce urea synthesis as a mechanism of ammonia detoxification, either in response to emersion (6 or 20 h) or elevated external ammonia (10 mmol·L–1). Acute exposure to high temperature (~31 °C), aquatic hypoxia, or air resulted in significant increases in blood glucose and liver heat shock protein (Hsp) 70 and hypoxia also caused an increased reliance on anaerobic metabolism. This is the first description of the heat shock response in a facultative air-breathing fish following either hypoxia or air exposure. These metabolic and molecular responses are part of a strategy that allows the mudminnow to thrive in extremely variable freshwater environments.

Air breathing in the Arctic: influence of temperature, hypoxia, activity and restricted air access on respiratory physiology of Alaska blackfish (Dallia pectoralis)

“…In any case, because Ṁ O 2 was measured for 24 h and stabilized within this time, we feel assured that the values reported here are representative of standard Ṁ O2 . Ṁ O2 has also been measured in the central mudminnow Umbra limi (Currie et al, 2010), which is the closest air-breathing relative to the Alaska blackfish (Peckham and Dineen, 1957 , calculated from Currie et al (Currie et al, 2010) by scaling to a body mass of 50 g using an exponent of -20 (Clark and Johnston, 1999)]. As expected, the standard Ṁ O 2 of Alaska blackfish increased from 5 to 15°C, with a Q 10 of 2.2.…”

“…The Journal of Experimental Biology (2014) is lower than the 2.4 reported for an increase in temperature from 15 to 31°C (Currie et al, 2010) and the 2.7 found when temperature increased from 5 to 15°C (Klinger et al, 1982) in the central mudminnow, indicating that the Ṁ O 2 of Alaska blackfish has a slightly lower temperature sensitivity. Unexpectedly, respiratory partitioning remained below 20% from air, even at 15°C.…”

Growth hormone transgenesis and polyploidy increase metabolic rate, alter the cardiorespiratory response and influence HSP expression to acute hypoxia in Atlantic salmon (Salmo salar) yolk-sac alevins

“…In contrast, HSPs were induced with hypoxia in rainbow trout gill epithelial cells (Airaksinen and Nikinmaa, 1995). Likewise, the air breathing mudminnow, Umbra limi, responded to hypoxia and 6 h of air exposure with significant increases in HSP70 and HSP90 in liver tissue (Currie et al, 2010). In the anoxia-tolerant western painted turtle, long-term but not short-term anoxia led to an induction of HSPs (constitutive HSP73, inducible HSP72 and HSP90) in several tissues (Ramaglia and Buck, 2004).…”

“…The cellular stress response to low environmental O 2 levels is variable in fish, and high levels of tissue, cell and temporal specificity in terms of the levels of HSP expression have been reported (Airaksinen and Nikinmaa, 1995;Currie and Tufts, 1997;Currie and Boutilier, 2001;Currie et al, 2010). Furthermore, a decrease in HSP70 mRNA production in hepatic tissue of sparids (family Sparidae) has been reported after exogenous administration of growth hormone (Deane et al, 1999).…”

Amphibious fishes: evolution and phenotypic plasticity

“…Amphibious fishes typically inhabit shallow waters, tide pools or transient aquatic habitats that can vary from hyperoxic (due to algal or plant photosynthesis) to hypoxic ( poor mixing, organismic respiration, low flow) either daily or seasonally (e.g. Bridges, 1988;Graham, 1985;Martin and Bridges, 1999;Currie et al, 2010). In addition, respiratory challenges in stagnant waters may be exacerbated by high levels of CO 2 or H 2 S, which interfere with O 2 binding and transport (Dehadrai and Tripathi, 1976;Abel et al, 1987).…”