Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology
ReviewPulsatile urea excretion in the gulf toadfish: mechanisms and controls☆
Introduction
Mommsen and Walsh (1989) reported that two members (Opsanus beta and Opsanus tau) of the teleost family Batrachoididae (the toadfishes and midshipmen) express a full complement of the ornithine–urea cycle (OUC) in their livers, while Randall et al. (1989) documented the same phenomenon in the Lake Magadi tilapia (Alcolapia grahami, formerly Oreochromis alcalicus grahami). The data on O. tau confirmed the earlier report of Read (1971) on liver biochemistry in this species, which prior to this time had been considered an anomaly, because general belief held that the genes for the OUC were silent or deleted in the teleosts. The presence of the OUC, accompanied by substantial ureotelism (i.e., predominance of urea-N as the major form of N-waste excreted) has subsequently been shown in several other teleost species (reviewed by Walsh, 1997, Anderson, 2001). The phenomenon is now interpreted as retention of an embryonic characteristic, which is probably expressed in the early life stages of most species (e.g., Wright et al., 1995), the majority of which are ammoniotelic later in life (reviewed by Wright and Land, 1998, Wright and Fyhn, 2001). Since ureotelism is metabolically expensive relative to ammoniotelism, costing 2 to 2.5 additional ATP per unit N excreted, expression of this trait in adult fish presumably has adaptive significance. This is most obvious in A. grahami where the high water pH (approx. 10) of Lake Magadi prevents ammonia excretion across the gills, and the excretion of urea-N provides a solution to this problem (Wood et al., 1989).
In the gulf toadfish (O. beta), the phenomenon has proven particularly interesting, because the species is facultatively ureotelic. When held under ‘non-stressful’ conditions in the laboratory (Walsh and Milligan, 1995) or when freshly collected from the field (Hopkins et al., 1999) the fish is predominantly ammoniotelic, while ‘proxy’ biochemical measurements on field-collected animals (Hopkins et al., 1997) indicate that either ammoniotelism, ureotelism or a mixture of the two strategies may occur in wild fish. However, a variety of laboratory treatments will induce a clear switchover to ureotelism. For some treatments, which inhibit ammonia excretion (e.g., air emersion, exposure to high environmental ammonia; Walsh et al., 1990, Wang and Walsh, 2000), the adaptive significance of ureotelism is obvious. However, for others it is not. In particular, when toadfishes are crowded together and/or when individual toadfish are isolated in single small containers, they become ureotelic in 1–3 days even when water flow is maintained so as to keep environmental ammonia at background levels (Walsh et al., 1994a, Walsh and Milligan, 1995). Especially interesting under these circumstances is the fact that the urea excretion is pulsatile, with more than 90% of the fish's waste-N production excreted in one or two short-lasting (0.5–3 h) pulses per day (Wood et al., 1995). In the last few years, we have made significant progress in understanding the mechanisms by which the urea pulsing occurs, though the adaptive significance of this behavior remains elusive.
In the present report, we synthesize our recent published and unpublished findings on these mechanisms in O. beta, present new data about the possible involvement of neural and endocrine factors in controlling pulsatile urea-N excretion, suggest promising areas for future research and speculate on the adaptive significance of this behavior. Comparable data on O. tau are very limited, but suggest that the same principles apply. For a review of earlier findings, the reader is referred to Walsh (1997).
Section snippets
Materials and methods
In general, experiments were carried out on sexually mature specimens (30–400 g) of O. beta collected by roller trawl from Biscayne Bay, south Florida, and held initially at low density (<12 g fish per liter seawater; ‘ammoniotelic conditions’) in sand-covered 80-l aquaria served with flowing seawater (30–33 ppt) at ambient temperature (20–28 °C). During the first few days in the laboratory, the fish were subjected to one or more prophylactic treatments with malachite green and formalin to kill
Rates and routes of pulsatile urea-N excretion
Confined toadfish typically excrete more than 80% of their waste-N in the form of urea at rates averaging approximately 100 μmol-N kg−1 h−1; the great majority of this occurs in one or two discrete pulses per day, each of 0.5–3 h duration (e.g., Fig. 1). Absolute values vary somewhat between studies, probably dependent on size, temperature and the nutritional history of the fish. For starved toadfish, mean urea-N excretion rates in different studies ranged from 30 to 220 μmol-N kg−1 h−1, mean
Acknowledgements
The new research reported here, and most of the earlier research summarized in this review, has been supported by NSF grants (IBN-9118819, -9507239, -0090355) to PJW and NSERC Research and Discovery grants to CMW. We thank our many collaborators for their invaluable contributions, and two anonymous referees for constructive comments. CMW is supported by the Canada Research Chair Program.
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2020, Physiology and BehaviorCitation Excerpt :Furthermore, naïve toadfish exposed to only the chemical cues of a conspecific have a reduced pulse latency (or time it takes to pulse) of 6 h compared to 20 h when exposed to clean seawater [21, 30]. Lastly, elevated plasma concentrations of the stress hormone cortisol and the neurochemical serotonin (5-HT; 5-hydroxytryptamine) are involved in the control of pulsatile urea excretion [22, 47, 75, 76]. Both cortisol and 5-HT are tightly linked to social behaviors and after agonistic encounters, subordinate fish of many species have elevated cortisol (toadfish included; [65]) and brain 5-HT activity (reviewed by [70]).
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2017, Comparative Biochemistry and Physiology -Part A : Molecular and Integrative PhysiologyCitation Excerpt :However, it is unknown if 5-HT is released from sources peripheral to the gill or from local sources within the gill possibly under nervous control. Data from an earlier study suggest that the extrinsic innervation of the gill may play a role in 5-HT availability and the control of pulsatile urea excretion (Wood et al., 2003). Teleost gills are innervated extrinsically by the facial (cranial nerve VII; innervates the pseudobranch which is absent in toadfish), glossopharyngeal (cranial nerve IX; innervates the first gill arch only), and vagus nerves (cranial nerve X; Jonz and Nurse, 2003; Nilsson, 1984; Sundin and Nilsson, 2002).
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This paper is based on a presentation at the International Symposium ‘Function of Marine Organisms – Mechanisms of Adaptation to Diverse Environments’, held in Tokyo on February 22–23, 2003.