|
| |
|
|
|
|
||||
| Home Help Feedback Subscriptions Archive Search Table of Contents | ||||
First published online June 29, 2006
Journal of Experimental Biology 209, 2696-2703 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02288
Characterization of diurnal urea excretion in the mangrove killifish, Rivulus marmoratus
Department of Integrative Biology, University of Guelph, Guelph, ON, N1G 2W1, Canada
* Author for correspondence (e-mail: patwrigh{at}uoguelph.ca)
Accepted 25 April 2006
 |
Summary |
|---|
 TOP Summary IntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Key words: nitrogen excretion, ammonia excretion, photoperiod, Danio rerio, Rivulus marmoratus, free-running, entrainment
|
Introduction |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
). Closely coupled biochemical and molecular mechanisms are
upregulated in the central pacemaker, triggering neuroendocrine cascades that
result in the coordination of various oscillators in the central and
peripheral tissues (Jin et al.,
1999; Whitmore et al.,
2000; Cahill,
2002).
Many catabolic processes are extremely complex. They require an internal
temporal organization and integration of various physiological and biochemical
pathways. The central pacemaker facilitates the synchronization of these
functions. Excretion of nitrogenous wastes requires the coordination of
digestive pathways, catabolic processes in the liver and transport proteins in
various tissues. The majority of teleosts are ammoniotelic, excreting 70-90%
of their nitrogenous waste products as ammonia
(Wood, 1993). The remaining
10-30% is largely due to the excretion of urea
(Kajimura et al., 2004). The
mangrove killifish Rivulus marmoratus is no exception to this general
rule, although an unusual characteristic of urea excretion
(Jurea) is the fact that urea is excreted in a diurnal
pattern, whereas ammonia is excreted (Jamm) at a steady
rate (Frick and Wright,
2002a). The majority of urea is excreted during the day, with the
peak of Jurea occurring between the hours of 12:00 h and
18:00 h. Two other teleosts studied to date, the gobiid fish Mugilogobius
abei and the marine toadfish Opsanus beta, both ureogenic, have
a non-uniform pattern of Jurea. The ammoniotelic R.
marmoratus is a small (
100 mg) self-fertilizing fish that inhabits
temporal pools and crab burrows in mangrove habitats. They are also known to
survive for weeks in moist leaf litter and detritus, as well as tolerating a
range of water conditions including variations in water temperature, salinity
and oxygen tensions (Abel et al.,
1987; King et al.,
1989; Davis et al.,
1990; Frick and Wright,
2002a; Frick and Wright,
2002b). The purpose of our study was to determine whether the
diurnal pattern of Jurea in R. marmoratus meets
the criteria for a circadian rhythm.
The foremost defining feature of circadian rhythms is a periodicity of
approximately 24 h, with only slight deviations from this value. Although
biotic and abiotic factors may influence the timing of the phases and length
of the period, the rhythm should remain in the absence of these factors. If a
diurnal or nocturnal pattern is sustained under constant conditions, the
rhythm is defined as free-running. For instance, goldfish Carassius
auratus, held under conditions of constant darkness, showed free-running
rhythms in locomotor and feeding activity with an average of 25.3±1.8 h
and 24.4±1.7 h, respectively
(Sánchez-Vázquez et al.,
1996). Observations on locomotor activity in zebrafish Danio
rerio under similar constant conditions demonstrated a comparable pattern
with a period of 25.5 h (Cahill et al.,
1998; Hurd et al.,
1998). The third characteristic of a circadian rhythm is that they
can be entrained to new environmental stimuli, which can change or reset the
phase of a circadian clock. The light:dark cycle clearly appears to be the
dominant zeitgeber for all organisms; however, other non-photic stimuli such
as feeding can have an equally powerful effect on resetting the clock
(Yanelli and Harrington,
2004). Light-sensitive circadian oscillators have been isolated in
many peripheral tissues of the zebrafish, including the heart, kidney and
liver (Whitmore et al., 1998;
Whitmore et al., 2000). The
rhythms in zebrafish are entrained fairly quickly, that is, within 2-3 days of
exposure to the new photoperiod. Furthermore, cell lines derived from
zebrafish embryos have demonstrated that these light-entrainable circadian
oscillators are present quite early in development
(Pando et al., 2001).
In the present study we hypothesized that the diurnal
Jurea pattern in R. marmoratus follows a
circadian rhythm. We predict that Jurea in R.
marmoratus has a periodicity of 24 h, which is sustained under constant
conditions, and can be entrained to different photoperiods.
Jurea and Jamm were measured in fasted
fish under normal conditions (12 h:12 h light:dark), continuous darkness (0
h:24 h light:dark), and under an inverted photoperiod. Comparisons were made
between fasted and fed individuals under normal light:dark conditions to
determine if feeding influenced the diurnal pattern. Furthermore, nitrogen
excretion rates were measured in zebrafish Danio rerio, a tropical
fish of similar size and metabolic demand to R. marmoratus. In a
companion study, we investigated the mechanisms regulating
Jurea patterns in R. marmoratus
(Rodela and Wright, 2006).
|
Materials and methods |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
seawater) (Frick and
Wright, 2002a). Mature fish (0.07-0.25 g) were held in individual
translucent containers in 60 ml of 15 artificial seawater (pH 8.1)
using distilled water and marine salt (Instant OceanTM, Crystal Sea,
Baltimore, MA, USA). Water in all containers was changed biweekly. The fish
were held in environmental chambers at 25°C on a photoperiod of 12 h:12 h
light (L):dark (D). Fish were fed Artermia salina nauplii once a day
every other day. To eliminate effects of recent feeding on nitrogen metabolism
and excretion, fish were deprived of food 48 h prior to the initiation of an
experiment unless otherwise indicated. Adult zebrafish Danio rerio Hamilton (DAP International, Etobicoke, ON, Canada) were kept in static aerated freshwater (pH 8.1, 25°C, 12 h:12 h L:D) in 2 l plastic holding tanks. Zebrafish (0.27-0.37 g) were fed TetraMin fish flakes (Pet Paradise, Guelph, ON, Canada) every other day except 48 h prior and for the duration of the experiments. Treatment of animals followed approved experimental protocols and guidelines of the University of Guelph Animal Care Committee.
Experimental protocol
Diurnal nitrogen excretion rhythms
To investigate the diurnal nitrogen excretion rhythms, five series of
experiments were conducted.
Series I: nitrogen excretion measurements under 12 h:12 h L:D in fasted R. marmoratus.
Series II: nitrogen excretion measurements under 12 h:12 h L:D in fed R. marmoratus.
Series III: nitrogen excretion measurements under 0 h:24 h L:D in fasted R. marmoratus.
Series IV: nitrogen excretion measurements under 12 h:12 h D:L in fasted R. marmoratus.
Series V: nitrogen excretion measurements under 12 h:12 h L:D in fasted D. rerio.
Series I
Initial experiments were conducted on fish under their natural photoperiod
(pH 8.1, 25°C, 12 h:12 h L:D) in containers with 30 ml of water. Water
samples were collected every 6 h for a 3-day period for measurement of
Jamm and Jurea. Water was changed
after each sampling interval to avoid the accumulation of urea or ammonia in
the water. To eliminate the stress of handling, the fish were kept in a double
container. The inner container was made out of mesh in the exact same
configuration as the plastic translucent holding container. When a water
change was required, the inner mesh container with the fish was removed and
placed in a new outer chamber containing fresh brackish water. Fish were
acclimated to the double-walled containers 2 days prior to the start of the
experiment. Water samples were frozen at -20°C for up to 1 month and later
analyzed for urea and ammonia content.
Series II-IV
For Series II-V, the fish were acclimated to the experimental conditions 2
days preceding the start of the experiment. For Series II, fish were fed 5 ml
of Artemia nauplii at 12:30 h daily and the photoperiod remained
unchanged (12 h:12 h L:D). In Series III, food-deprived fish were exposed to
complete darkness for 24 h (0 h:24 h L:D). For the final series of experiments
(IV) in R. marmoratus, the fish were deprived of food and excretion
rates were measured under an inverse photoperiod (12 h:12 h D:L).
Series V
As a comparison to other tropical teleost species, both
Jurea and Jamm were measured in
food-deprived zebrafish Danio rerio, exposed to a 12 h:12 h L:D
photoperiod, also kept at 25°C. Water was sampled and renewed as described
above for the killifish experiments. Following the termination of each series
of experiments, the fish were blotted dry and weighed for calculation of
excretion rates.
Analytical techniques
Urea and ammonia analysis
Urea levels in both freshwater and seawater samples were quantified by a
colorimetric assay (Rahmatullah and Boyde,
1980) using an Ultrospec 3300 Pro spectrophotometer
(Biochrom, Cambridge, UK). Ammonia content of seawater samples was measured as
described elsewhere (Ivancic and Degobbis,
1984). Freshwater samples were analyzed for ammonia using a
colorimetric assay method previously described
(Verdouw et al., 1978). The
rates of excretion (J) were calculated using the methodology outlined
elsewhere (Wright and Wood,
1985).
Control experiments were performed to determine if bacterial contamination from fish sources, water sources or attached to the experimental chamber could have influenced nitrogen excretion rates. Fish were placed in 30 ml of water for a 1 h interval and subsequently removed. Ammonia and urea content were monitored in the water over the following 6 h. Analysis revealed that microbial contamination did not significantly affect nitrogen excretion rates (P>0.05).
Statistical analysis
The data are presented as mean ± standard error of the mean
(s.e.m.). Evaluation of circadian rhythmicity was accomplished using the
single cosinor method (Halberg et al.,
1972; Nelson et al.,
1979). In this model a sinusoidal curve with a predefined period
of 24 h is fitted to the data by least squares regression. The cosine function
 |
defines three circadian parameters: Co represents the mesor, a
rhythm-adjusted median value; C is the amplitude (one half the difference
between the maximum and minimum values); 
is the time at which the curve
reaches its highest value or acrophase. Time, which is represented by
ti, is measured as a fraction of 24 h. An F-test
was used to determine the statistical significance of the circadian rhythm
(P<0.05). This test allows subjective analysis of the hypothesis
that the rhythm amplitude differs from zero. Furthermore, comparisons of the
maximal absolute urea and ammonia excretion values between experimental series
were performed using t-tests with either assumptions for equal or
unequal variances (P<0.05).Verification of equal variances was
accomplished using an F-test (P<0.05).
|
Results |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
|
Series II
Fed fish demonstrated a significant circadian rhythm in both
Jurea (F2,9=18.3, P=0.0007)
and Jamm (F2,9=11.6,
P=0.0032). Jurea in fed fish had peaks and
troughs at times identical to the pattern observed in fasted fish
(Fig. 2A). The amplitude of the
oscillation was marked; it was 72% of the meson and the peak of the rhythm
occurred at 15:45±00:18 h. In comparison with fasted fish
(Fig. 1A), fed fish
(Fig. 2A) excreted
approximately 2.3-6.3 times more urea, the variations for the minimum and
maximum rates respectively. Diurnal Jamm comprised 57-85%
of total nitrogen wastes excreted in fed fish
(Fig. 2B). The amplitude of the
diurnal Jamm pattern was 88% of the meson with the highest
rates of excretion occurring between 12:00 h and 18:00 h and the lowest rates
occurring between 06:00 h to 12:00 h, just prior to feeding. The acrophase for
the circadian rhythm for Jamm occurred at
15:50±0:12 h. Jamm rates were 1.4-8.3 times larger
compared with values obtained from fasted fish.
|
Series III
When food-deprived R. marmoratus were kept in darkness for 24 h (0
h:24 h L:D) the circadian pattern of Jurea persisted
(F2,9=60.7, P=0.00001;
Fig. 3). The highest rates of
Jurea occurred during 12:00 h and 18:00 h with the
amplitude of the oscillation equaling 48% of the meson. The absolute rates of
Jurea were significantly (1.6-1.8 times) lower relative to
values obtained from fasted fish (12 h:12 h L:D). The acrophase occurred at
14:31±00:33 h. Jamm was constant over time
(F2,9=0.003, P=0.99) and excretion rates were not
significantly different than values obtained from fasted fish (12 h:12 h L:D)
(data not shown).
|
Series IV
A significant circadian rhythm in Jurea
(F2,9=39.6, P=0.00003) was present in fish
acclimated to an inverted photoperiod (12 h:12 h D:L). The period of the
single cycle remained at 24 h, however, the occurrence of the
Jurea peaks and troughs were different from individuals on
a normal photoperiod (12:12 h L:D). The highest rates of
Jurea occurred between the 00:00 h and 06:00 h, with an
amplitude 52% of the meson (Fig.
4). The acrophase occurred at 02:16±00:28 h. The absolute
values of Jurea were significantly lower by 1.6 (peak) to
2.3 (trough) times compared to fish on a normal photoperiod.
Jamm remained constant over time
(F2,9=0.48, P=0.63) and there was no significant
difference between Jamm rates in fish on an inverted
photoperiod compared to a normal photoperiod (data not shown).
|
Series V
In fasted D. rerio, there was no significant circadian rhythm in
urea and ammonia excretion (F2,9=2.33, P=0.15,
F2,9=1.28, P=0.33;
Fig. 5A,B). Approximately 83%
of total nitrogen in D. rerio was excreted in the form of ammonia.
Jurea was up to 2.6 times higher in R. marmoratus
compared to D. rerio with the largest difference occurring during the
daytime (12:00 h to 18:00 h).
|
|
Discussion |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Natural 24 h light:dark cycles play an important part in circadian rhythms
as daily biological patterns often parallel environmental changes. In many
cases, this synchrony between the animal and its external milieu gives the
individual the ability to anticipate temporal changes in the surroundings.
However, a true endogenously generated rhythm persists even in the absence of
abiotic cues and continues unperturbed until the animal is presented with a
new external cue that acts to reset the central clock
(Whitmore et al., 2000;
Pando and Sassone-Corsi,
2002). Locomotor activity in several fish species continues in a
diurnal fashion with a periodicity of 24.4-25.5 h under constant dim or
darkened conditions
(Sánchez-Vázquez et al.,
1996; Cahill et al.,
1998; Hurd et al.,
1998; Gerkema et al.,
2000). Free-running rhythms in darkness have been recorded in
electric discharge of the gymnotid electric fish, Eigenmannia
virescens (Deng and Tseng,
2000). Furthermore, a daily pattern in Jurea
in M. abei was maintained in darkness
(Kajimura et al., 2002). In
R. marmoratus, the peak of Jurea in constant
darkness occurred during the time of subjective day of the previous
photoperiod (12 h:12 h L:D). Aschoff demonstrated that the free-running rhythm
in diurnal animals tends to be slightly longer than 24 h, whereas the period
length in nocturnal animals under free-running conditions is somewhat shorter
than 24 h (Aschoff, 1981). As
measurements for Jurea and Jamm in
R. marmoratus were made over 6 h intervals, a precise estimation of
period length was not possible.
An intriguing feature of the free-running rhythm (0 h:24 h L:D) in fasted
R. marmoratus is that the absolute rates of Jurea
were significantly lower (1.6-1.8 times) than values obtained from fasted fish
held under a normal photoperiod (12 h:12 h L:D). Usually, under constant
conditions, when some peripheral oscillators are removed from the
light-sensitive influence of the master pacemaker the amplitude of the
circadian rhythm becomes diminished over time and eventually ceases. For
example, circulating thyroxine levels in red drum Sciaenops ocellatus
(Leiner and MacKenzie, 2001)
and melatonin rhythms in the pineal organ of the ayu Plecoglossus
altivelis are reduced over time in constant darkness
(Iigo et al., 2004). As well,
circadian rhythms of Clock mRNA in the kidney and heart of zebrafish
oscillated with a lower amplitude until they disappeared after a period of 2-3
days in darkness (Whitmore et al.,
2000). Urea excretion rates in R. marmoratus were
measured for three complete cycles after a 2-day acclimation period. It is
possible that Jurea is under control of a peripheral
oscillator and perhaps over time, a period of several weeks, the rhythm may
become dampened and eventually cease under conditions of continuous
darkness.
The transition between dark and light appears to be the dominant zeitgeber
for all organisms. Lighting cues appear to play an important role in resetting
the clock that controls Jurea in R. marmoratus.
Like most animals, R. marmoratus can become entrained to new
photoregimens within a day or two (Pohl,
1978). Measurements of zebrafish Clock gene expression in
the heart and kidney revealed inherent and independent light-sensitive
circadian oscillators that entrained to altered photoperiods within 2-3 days
(Whitmore et al., 1998;
Whitmore et al., 2000).
Under the influence of an inverted photoperiod, the amplitude of
Jurea in food-deprived R. marmoratus was
significantly lower (by twofold) relative to fish exposed to a normal
photoperiod (Table 1). There
are several possible explanations for this difference in amplitude. Non-photic
stimuli such as feeding may act as an important cue regulating and resetting
the clock (Yanelli and Harrington,
2004). It is possible that while light may have a role in
entraining the Jurea pattern in R. marmoratus
there may also be some confounding influences from a prior non-photic
zeitgeber that may be resisting the change to the new photoperiod. Stokkan et
al. reported that rhythmicity of certain genes in the liver of rats retain a
phase relation to previous restricted feeding schedule even during fasting
(Stokkan et al., 2001).
Furthermore, there is a partial coupling between food-entrained and
light-entrained activity in sea bass, Dicentrarchus labrax
(Sánchez-Vázquez et al., 1995). When goldfish were held under
conflicting zeitgebers (light and feeding cycles), activity rhythms were
initially synchronized to the light cycle but gradually feeding time assumed
greater importance (Aranada et al., 2001). In R. marmoratus,
Jurea may depend on temporal regulation of the rate of food
digestion, urea synthesis pathways, and changes in transport mechanisms that
may ultimately be under control of light and food entrainable circadian
clocks.
|
Rates of nitrogen excretion in fed fish are typically correlated with
dietary protein content and the proportion of nitrogen wastes excreted as urea
versus ammonia remains constant (e.g.
Wright, 1993;
Walsh and Milligan, 1995;
Verbeeten et al., 1999).
Indeed, the ratio of nitrogen waste products did not vary under different
feeding regimes in R. marmoratus. Both Jurea and
Jamm demonstrated up to a six- and eightfold increase,
respectively, in absolute rates and this is consistent with trends described
by other studies (Brett and Zala,
1975; Kaushik,
1980; Kaushik et al.,
1983; Wright,
1993; Alsop and Wood,
1997).
Jurea and Jamm in zebrafish were
steady over time, whereas Jurea in captive (this study)
and wild R. marmoratus (Frick and
Wright, 2002a) demonstrate a circadian rhythm. This disparity
between nitrogen excretion strategies may relate to the ecology and life
history of each species. Zebrafish are primarily a freshwater species that
prefers to inhabit lotic bodies of water, such as rivers and streams, and they
will often remain near the surface of the water column in large groups
(Talwar and Jhingran, 1991).
R. marmoratus tend to exhibit a more solitary and fossorial
lifestyle, often seeking shelter in detritus and leaf litter; however, they
also frequently inhabit the burrows of land crabs in estuarine environments
(Taylor, 1988;
Davis et al., 1990). Limited
water flow and elevated ammonia concentrations appear to be major shortcomings
for the cryptic burrowing strategy used by R. marmoratus
(Frick and Wright, 2002a). A
few exceptional species shift towards ureotelism under these conditions
(Forster and Goldstein, 1966;
Gordon et al., 1978;
Ramaswamy and Gopalakrishna Reddy,
1983; Saha and Ratha,
1990; Wood et al.,
1998), but this is not the case for R. marmoratus.
Exposure to ammonia concentrations up to 10 mmol l-1 does not
change the proportion of ammonia versus urea excreted in R.
marmoratus (Frick and Wright,
2002a). An alternative explanation may relate to predation. O.
beta, a facultative ureotelic teleost, is a preferred prey item of the
grey snapper (Lutjanus griseus). Preliminary data from behavioral
assays indicates that the grey snapper has a stronger attraction to ammonia
than either urea alone or an ammonia/urea mixture
(Barimo and Walsh, 2005).
Hence, it is possible that the circadian Jurea pattern in
R. marmoratus is correlated with potential predator activity but
further ecological data is required to verify this hypothesis.
In conclusion, this study provides strong evidence that the diurnal Jurea pattern in R. marmoratus meets the criteria for a circadian rhythm, namely a 24 h periodicity, a free-running rhythm in constant darkness, and entrainment to a reversed photoperiod. The findings suggest that light cues may have an important role in coordinating the various physiological processes involved in nitrogen metabolism, primarily catabolism of proteins, urea synthesis and urea transport in R. marmoratus. The absence of a diurnal pattern of Jurea in D. rerio is consistent with the majority of teleost fishes.
|
Acknowledgments |
|---|
|
References |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Abel, D. C., Koenig, C. C. and Davis, W. P. (1987). Emersion in the mangrove forest fish. Rivulus marmoratus: a unique response to hydrogen sulfide. Environ. Biol. Fishes 18,67 -72.
Alsop, D. H. and Wood, C. M. (1997). The interactive effects of feeding and exercise on oxygen consumption, swimming performance and protein usage in juvenile rainbow trout. J. Exp. Biol. 200,2337 -2346.[Abstract]
Aranda, A., Madrid, J. A. and Sanchez-Vazquez, F. J.
(2001). Influence of light on feeding anticipatory activity in
goldfish. J. Biol. Rhythms
16, 50-57.
Aschoff, J. (1981). Freerunning and entrained circadian rhythms. In Handbook of Behavioral Neurobiology: Vol. 4, Biological Rhythms (ed. J. Aschoff), pp.81 -93. New York: Plenum Press.
Barimo, J. F. and Walsh, P. J. (2005). Ureotely in the gulf toadfish, Opsanus beta: a means of predator avoidance by chemical crypsis? Integr. Comp. Biol. 44, 520.
Brett, J. R. and Zola, C. A. (1975). Daily pattern of nitrogen excretion and oxygen consumption of sockeye salmon (Oncorhynchus nerka) under controlled conditions. J. Fish Res. Bd. Can. 32,2479 -2486.
Cahill, G. M. (2002). Clock mechanisms in zebrafish. Cell Tissue Res. 309, 27-34.[CrossRef][Medline]
Cahill, G. M., Hurd, M. W. and Batchelor, M. M. (1998). Circadian rhythmicity in the locomotor activity of larval zebrafish. Neuroreport 9,3445 -3449.[Medline]
Davis, W. P., Taylor, D. S. and Turner, T. J. (1990). Field observations of the ecology and habits of mangrove Rivulus (Rivulus marmoratus) in Belize and Florida (Teleostei: Cyprinodontiformes: Rivulidae). Environ. Res. Lab. 2, 1-14.
Deng, T. S. and Tseng, T. C. (2000). Evidence of circadian rhythm of electric discharge in Eigenmannia virescens system. Chronobiol. Int. 17, 43-48.[CrossRef][Medline]
Forster, R. P. and Goldstein, L. (1966). Urea
synthesis in the lungfish: relative importance of purine and ornithine cycle
pathways. Science 153,1650
-1652.
Frick, N. T. and Wright, P. A. (2002a).
Nitrogen metabolism and excretion in the mangrove killifish Rivulus
marmoratus. I. The influence of environmental salinity and external
ammonia. J. Exp. Biol.
205, 79-89.
Frick, N. T. and Wright, P. A. (2002b).
Nitrogen metabolism and excretion in the mangrove killifish Rivulus
marmoratus. II. Significant ammonia volatilization in a teleost during
air-exposure. J. Exp. Biol.
205,91
-100.
Gerkema, M. P., Videler, J. J., de Wiljes, J., van Lavieren, H., Gerritsen, H. and Karel, M. (2000). Photic entrainment of circadian activity patterns in the tropical labrid fish Halichoeres chrysus. Chronobiol. Int. 17,613 -622.
Gordon, M. S., Ng, W. W. and Yip, A. Y. (1978). Aspects of the physiology of terrestrial life in amphibious fishes. III. The Chinese mudskipper Periophthalmus cantonensis. J. Exp. Biol. 72,57 -75.
Halberg, F., Johnson, E. A., Nelson, W., Runge, W. and Sothern, R. B. (1972). Autorhythmometry: procedures for physiologic self-measurement and their analysis. Physiol. Teach. 1, 1-11.
Hurd, M. W., Debruyne, J., Straume, M. and Cahill, G. M. (1998). Circadian rhythms of locomotor activity in zebrafish. Physiol. Behav. 65,465 -472.[CrossRef][Medline]
Iigo, M., Fujimoto, Y., Gunji-Suzuki, M., Yokosuka, M., Hara, M., Ohtani-Kaneko, R., Tabata, M., Aida, K. and Hirata, K. (2004). Circadian rhythm of melatonin release from the photoreceptive pineal organ of a teleost, ayu (Plecoglossus altivelis) in flow-thorough culture. J. Neuroendocrinol. 16,45 -51.[CrossRef][Medline]
Ivancic, I. and Degobbis, D. (1984). An optimal manual procedure for ammonia analysis in natural waters by the indophenol blue method. Water Res. 18,1143 -1147.[CrossRef]
Jin, X., Shearman, L. P., Weaver, D. R., Zylka, M. J., de Vries, G. J. and Reppert, S. M. (1999). A molecular mechanism regulating rhythmic output from the suprachiasmatic nucleus. Cell 96,57 -68.[CrossRef][Medline]
Kajimura, M., Iwata, K. and Numata, H. (2002). Diurnal nitrogen excretion rhythm of the functionally ureogenic gobiid fish Mugilogobius abei. Comp. Biochem. Physiol. 131B,227 -239.
Kajimura, M., Croke, S. J., Glover, C. N. and Wood, C. M.
(2004). Dogmas and controversies in the handling of nitrogenous
wastes: the effect of feeding and fasting on the excretion of ammonia, urea
and other nitrogenous waste products in rainbow trout. J. Exp.
Biol. 207,1993
-2002.
Kaushik, S. J. (1980). Influence of nutritional status on the daily patterns of nitrogen excretion in the carp (Cyprinus carpio L.) and the rainbow trout (Salmo gairdneri). Reprod. Nutr. Dev. 20,1751 -1756.
Kaushik, S. J., Dabrowski, K. R., Dabrowska, H., Olah, E. and Luquet, P. (1983). Utilization of dietary urea in rainbow trout. Ann. Nutr. Metab. 27, 94-106.[Medline]
King, J. C., Abel, D. C. and DiBona, D. R. (1989). Effects of salinity on chloride cells in the euryhaline cyprinodont fish Rivulus marmoratus. Cell Tissue Res. 257,367 -377.[CrossRef]
Leiner, K. A. and MacKenzie, D. S. (2001). The effects of photoperiod on growth rate and circulating thyroid hormone levels in the red drum, Sciaenops ocellatus: evidence for a free-running circadian rhythm of T(4) secretion. Comp. Biochem. Physiol. 130A,141 -149.[CrossRef]
Nelson, W., Tong, Y. L., Lee, J. K. and Halberg, F. (1979). Methods for cosinor-rhythmometry. Chronobiologia 6,304 -323.
Pando, M. P. and Sassone-Corsi, P. (2002). Unraveling the mechanisms of the vertebrate circadian clock: zebfrafish may light the way. BioEssays 24,419 -426.[CrossRef][Medline]
Pando, M. P., Pinchak, A. B., Cermakian, N. and Sassone-Corsi,
P. (2001). A cell-based system that recapitulates the dynamic
light-dependent regulation of the vertebrate clock. Proc. Natl.
Acad. Sci. USA 98,10178
-10183.
Pohl, H. (1978). Comparative aspects of circadian rhythms in homeotherms, re-entrainment after phase shifts of the zeitgeber. Int. J. Chronobiol. 5, 493-517.[Medline]
Rahmatullah, M. and Boyde, T. R. C. (1980). Improvements in the determination of urea using diacetyl monoxime; methods with and without deproteinisation. Clin. Chem. Acta 107, 3-9.[CrossRef][Medline]
Ramaswamy, M. and Gopalakrishna Reddy, T. (1983). Ammonia and urea excretion in three species of air-breathing fish subjected to aerial exposure. Proc. Indian Acad. Sci. 92,293 -297.
Rodela, T. M. and Wright, P. A. (2006). Metabolic and neuroendocrine effects on diurnal urea excretion in the mangrove killifish Rivulus marmoratus. J. Exp. Biol. 209,2704 -2712.
Saha, N. and Ratha, B. K. (1990). Alterations in excretion pattern of ammonia and urea in a freshwater air-breathing teleost, Heteropneustes fossilis (Bloch) during hyper-ammonia stress. Indian J. Exp. Biol. 28,597 -599.
Sanchez-Vázquez, F. J., Zamora, S. and Madrid, J. A. (1995). Light-dark and food restriction cycles in sea bass: effect of conflicting zeitgebers on demand-feeding rhythms. Physiol. Behav. 58,705 -714.[CrossRef][Medline]
Sánchez-Vázquez, F. J., Madrid, J. A., Zamora, S., Iigo, M. and Tabata, M. (1996). Demand feeding and locomotor circadian rhythms in the goldfish, Carassius aurutus: dual and independent phasing. Physiol. Behav. 60,665 -674.[Medline]
Stokkan, K. A., Yamazaki, S., Tei, H., Sakaki, Y. and Menaker,
M. (2001). Entrainment of the circadian clock in the liver by
feeding. Science 291,490
-493.
Talwar, P. K. and Jhingran, A. G. (1991). Inland Fishes of India and Adjacent Countries, Vol.I . New Delhi: Oxford and IBH Publishing Co.
Taylor, D. S. (1988). Observation on the ecology of the killifish Rivulus marmoratus (Cyprinodontidae) in an infrequently flooded mangrove swamp. Northeast Gulf Sci. 10,63 -68.
Verbeeten, B. E., Carter, C. G. and Purser, G. J. (1999). The combined effect of feeding time and ration on growth performance and nitrogen metabolism of greenback flounder. J. Fish Biol. 55,1328 -1343.[CrossRef]
Verdouw, H., van Echteld, C. J. A. and Dekkers, E. M. J. (1978). Ammonia determinations based on indophenol formation with sodium salicylate. Water Res. 12,399 -402.[CrossRef]
Walsh, P. J. and Milligan, C. L. (1995). Effects of feeding and confinement on nitrogen metabolism and excretion in the gulf toadfish Opsanus beta. J. Exp. Biol. 198,1559 -1566.
Whitmore, D., Foulkes, N. S., Strahle, U. and Sassone-Corsi, P. (1998). Zebrafish Clock rhythmic expression reveals independent peripheral circadian oscillators. Nat. Neurosci. 1,701 -706.[CrossRef][Medline]
Whitmore, D., Foulkes, N. S. and Sassone-Corsi, P. (2000). Light acts directly on organs and cells in culture to set the vertebrate circadian clock. Nature 404, 87-91.[CrossRef][Medline]
Wood, C. M. (1993). Ammonia and urea metabolism and excretion. In The Physiology of Fishes (ed. D. Evans), pp. 379-425. Boca Raton: CRC Press.
Wood, C. M., Gilmour, K. M., Perry, S. F., Part, P., Laurent, P. and Walsh, P. J. (1998). Pulsatile urea excretion in gulf toadfish (Opsanus beta): evidence for activation of a specific facilitated diffusion transport system. J. Exp. Biol. 201,805 -817.[Abstract]
Wright, P. A. (1993). Nitrogen excretion and enzyme pathways for ureagenesis in freshwater tilapia (Oreochromis niloticus). Physiol. Zool. 66,881 -901.
Wright, P. A. and Wood, C. M. (1985). An
analysis of branchial ammonia excretion in the freshwater rainbow trout.
Effects of environmental pH change and sodium uptake blockade. J.
Exp. Biol. 114,329
-353.
Yanelli, P. and Harrington, M. E. (2004). Let there be `more' light: enhancement of light actions on the circadian system through non-photic pathways. Prog. Neurobiol. 74, 59-76.[CrossRef][Medline]
CiteULike 
Complore 
Connotea 
Del.icio.us 
Digg 
Reddit 
Technorati 
Twitter What's this?
| |||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
