Osmoregulation in an avian nectarivore, the whitebellied sunbird Nectarinia talatala: response to extremes of diet concentration
Department of Zoology and Entomology, University of Pretoria, Pretoria 0002, South Africa
* Author for correspondence (e-mail: tfleming{at}zoology.up.ac.za)
Accepted 5 March 2003
![]() |
Summary |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Key words: African sunbird, Nectarinia talatala, cloacal fluid, electrolyte balance, nectar concentration, osmolality, urine, water balance.
![]() |
Introduction |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Of necessity, when fed dilute sugar solutions, avian nectarivores have to
drink up to four or five times their body mass over just 12 h to ingest their
requisite energy (Collins,
1981; McWhorter and
Martínez del Rio, 1999
;
Nicolson and Fleming, 2003
).
In addition to the high preformed water load, nectar is low in electrolytes
(Hiebert and Calder, 1983
).
For nectarivores, the problem may be conservation of electrolytes, rather than
electrolyte excess (as examined in most avian osmoregulation studies). On the
other hand, when only concentrated nectars are available, nectarivores may
struggle to maintain water intake sufficient for physiological requirements.
Evaporative losses at high ambient temperatures may outstrip water gain on
concentrated nectars (Beuchat et al.,
1990
; Powers,
1992
), requiring birds to resort to water conserving strategies
such as torpor (Lasiewski,
1964
). Only a handful of studies have examined the water flux and
osmoregulation of nectarivorous birds
(Beuchat et al., 1990
;
Collins, 1981
; Goldstein and
Bradshaw,
1998a
,b
;
Lotz and Nicolson, 1999
;
McWhorter and Martínez del Rio,
1999
; McWhorter et al.,
2003
). The aim of this study was to examine the osmoregulatory
capacity of the whitebellied sunbird Nectarinia talatala fed extremes
of diet concentration in the presence and absence of supplementary drinking
water.
![]() |
Materials and methods |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Osmoregulation experiments were run over 2 days. Shortly after lights-on on the first day (07:0007:30 h), birds were weighed (±0.001 g) and feeders containing maintenance diet were replaced by others containing experimental diets. Feeders of supplementary water were provided where appropriate. Voided cloacal fluid (CF) was collected over the second 24 h (the test day) in trays under the cages; the trays contained liquid paraffin to prevent evaporation of CF. Trays were covered by plastic gauze (vegetable bagging) stretched tightly over the entire tray. Mesh thickness measured 0.13±0.03 mm and mesh size was 6.61±0.57 mm. This prevented birds from touching the paraffin, but was fine enough to offer minimal interference with CF collection. Trays were tipped up and left to stand so that CF droplets coalesced and could be drawn up with Pasteur pipettes. Accuracy of the paraffin collection method was determined by placing collection trays above a larger paraffin-filled tray; waxproof paper was suspended next to the cage sides to direct any CF droplets into the larger tray. Birds were maintained on a dilute diet (0.07 mol l1 sucrose) for 24 h and then placed in the cage for 1 h without any supply of food. Less than 1% of CF volume was missed with this collection method.
The experimental diets were sucrose solutions of eight concentrations,
ranging from 0.07 to 2.5 mol l1. Osmolalities of these diets
ranged from 70 mosm kg1 H2O up to an estimated
5,800 mosm kg1 (Table
1). For sucrose concentrations 0.25 mol l1,
separate trials were run with and without supplementary water. Trials at 0.07
and 0.1 mol l1 were not repeated with and without water
since birds lost considerable mass on these diets and very little of the water
provided was consumed. Each of the seven birds received every test diet in
random order (a total of 14 trials per bird).
|
Birds and feeders were weighed at the start and end of the test day to
assess any change in body mass and consumption of diet and supplementary
water. Evaporation from the 1 mm diameter holes through which the birds fed
was assumed to be negligible. Dripping was a greater problem, and was
controlled by placing paraffin collection jars directly under the feeders and
making appropriate corrections (Nicolson
and Fleming, 2003). Water gain (ml day1) was
calculated as the sum of preformed + metabolic + supplementary water volumes.
Preformed water was calculated by subtracting the mass of sugar from the mass
of solution consumed. Metabolic water was calculated as 198 g water for every
mole (342 g) of sucrose consumed (=0.58 ml H2O for every g sucrose;
from the equation of Schmidt-Nielsen,
1997
). For this calculation we assumed that sugars ingested were
completely assimilated (Jackson et al.,
1998
; Lotz and Nicolson,
1996
), that all sugar assimilated was catabolised (i.e.
respiratory quotient=1.0; Collins et al.,
1980
; Prinzinger et al.,
1992
) and that birds are approximately in mass balance.
Evaporative water loss (EWL, ml day1) was estimated from the
difference between water gain and CF output.
Processing and analysis
After collection of CF from under liquid paraffin, volumes (ml
day1) were measured in a graduated cylinder, and a portion
frozen for later analysis of osmolality and Na+ and K+
concentrations.
Osmolality of CF (mosm kg1) was measured using a vapour
pressure osmometer (Vapro® 5520, Wescor Inc., Utah, USA),
fitted with a specially selected thermocouple head that gave a range of
03200 mosm kg1. Regular and thorough cleaning ensured
that deionised water registered an osmolality of 0 mosm kg1
with reasonable reliability. Deionised water was processed after approximately
every ten samples, and the thermocouple head was cleaned if the reading
exceeded 5 mosm kg1 (approximately every 20 samples). Since
the greatest variability was observed between calibration runs, we did not
measure osmolality of each sample in sequential triplicate, like some other
authors. Rather, samples were sorted into groups of approximately similar
expected concentrations, centrifuged and the supernatant measured blind (with
no knowledge of the diet during that trial). All samples were thus measured in
a random order twice, being refrozen and centrifuged between measurements. If
values differed substantially between the two analyses, a third reading was
taken. This method of analysis yielded coefficients of variation of 36, 25 and
16% for dilute (0.07 to 0.25 mol l1 sucrose), average (0.5
and 1 mol l1) and concentrated (1.5 to 2.5 mol
l1) sugar solutions, respectively; these equate to
osmolality readings differing by an average of 4.9, 13.5 and 32.4 mosm
kg1. Sodium and potassium ions in CF (mol
l1) were measured by flame photometry (Model 420, Sherwood
Scientific Ltd., Cambridge, UK) in random order and in duplicate (or
triplicate where values differed substantially). We assumed that solutes were
a negligible component of CF volume and that CF approximated water
(Lotz and Nicolson, 1999),
enabling calculation of total osmotic excretion (osmolality x CF volume;
mosm day1) as well as electrolyte output (ion concentration
x CF volume; mmol day1).
Statistical procedures
Water gain, CF volumes, osmolalities and osmotic excretion, as well as EWL
(expressed as volume or proportion of total water gain) were tested for the
effects of diet concentration and the provision of supplementary water by
repeated-measures analysis of variance (RM-ANOVA). Post-hoc
comparisons were carried out by Tukey's Honest Significant Difference test.
These analyses were conducted for diet concentrations of 0.252.5 mol
l1, since these diet trials were performed both with and
without supplementary water (experiments using 0.07 and 0.1 mol
l1 sucrose diet were performed with water only). Regression
analyses were carried out for CF volume compared with osmolality, as well as
osmotic excretion and electrolyte outputs. Regression lines were fitted to
data from all individuals on all diet trials.
For all tests, the level of significance was P0.05. Values are
means ± 1 S.D.
![]() |
Results |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
On the lowest sucrose concentrations (0.07 and 0.1 mol
l1), birds were subject to massive water flux and did not
maintain energy balance, losing mass
(Nicolson and Fleming, 2003).
Their mean daily water gain was 47.8±8.3 ml day1
(Fig. 1A, Table 2), or 5.15 times body
mass. Mean voided CF volumes were 29.6±7.0 ml day1
(Fig. 1B,
Table 2), or 3.18 times body
mass.
|
|
In contrast, on the most concentrated sucrose solutions (2 and 2.5 mol l1) and when no supplementary water was provided, birds ingested only 1.92±0.50 ml day1 of preformed water, while metabolic water contributed a further 1.62±0.22 ml day1 (total water gain = 3.91±0.56 and 3.05±0.37 ml day1, Fig. 1A). Consequently, volumes of CF fell away sharply with increasing dietary sucrose concentration, so that when birds were not provided with supplementary drinking water, CF volumes were only 0.26 and 0.04 ml day1 (2 and 2.5 mol l1, respectively; Fig. 1B). Most waste material was solid for birds on these very concentrated diets.
In addition to altering water excretion through CF, the evaporative component of water loss was affected by diet. A smaller volume of water was lost through evaporation on more concentrated diets, and there were greater evaporative losses when the birds were provided with supplementary water (Fig. 2A; diet, F5,30=23.72, P<0.001; water, F1,6=10.54, P=0.017; interaction, F5,30=4.66, P=0.003). As a percentage of water gain, EWL was also significantly affected by diet concentration and the provision of supplementary water (Fig. 2B): a greater proportion of water gain was lost through EWL on trials without water and on more concentrated diets (diet, F5,30=66.53, P<0.001; water, F1,6=24.42, P=0.003; interaction, F5,30=9.41, P<0.001). For example, on the most dilute diets (0.07 and 0.1 mol l1 sucrose), 18.2±5.3 ml day1 of water was not accounted for in CF and was presumably lost largely through evaporation (38±9% of water gain), while on 2 and 2.5 mol l1 sucrose diets without supplementary water, 96±3% of ingested water was unaccounted for. Presumably most of this was lost through evaporation (although the small volumes of voided CF made collection error more likely).
|
Cloacal fluid osmolality increased significantly with diet concentration, even when supplementary water was provided (Fig. 3A, Table 2; diet, F5,30=4.81, P=0.002; water, F1,6=6.32, P=0.046; interaction, F5,30=4.03, P=0.006) and was tightly correlated with CF volume, reflecting water flux of the birds (Fig. 3B, r296=0.762, P<0.001). A remarkably low osmolality was recorded for CF from birds fed 0.25 mol l1 sucrose with supplementary water (6.2±2.6 mosm kg1, N=7), while the most concentrated CF measured was 461±253 mosm kg1 (for birds fed 2.5 mol l1 sucrose without supplementary water; N=6 birds that yielded sufficient volumes to measure accurately). Even though only small volumes of supplementary water were consumed, drinking had a significant effect on CF osmolality (Table 2).
|
Interestingly, total solute output (osmotic excretion) was also correlated with diet concentration, being highest for the most dilute diets where birds showed the highest water flux (Fig. 4A, Table 2; diet, F5,30=5.36, P=0.001; water, F1,6=0.01, P=0.918; interaction, NS). This was also reflected in a positive correlation between osmotic excretion and CF volume, total osmotic excretion being significantly higher for dilute diets where birds had higher water fluxes (Fig. 4B; r296=0.581, P<0.001).
|
Diet concentration as well as the provision of drinking water affected electrolyte (Na+ and K+) concentrations in CF (Table 2). Minimum electrolyte concentrations were 0.34±0.16 and 0.37±0.09 mmol l1 for Na+ and K+, respectively, on 0.25 mol l1 sucrose diets with supplementary drinking water provided; maximum values were 12.67±8.14 and 21.79±7.92 on 2.5 mol l1 sucrose diets without water. Almost without exception, K+ excretion exceeded Na+ excretion. As for total osmotic excretion, electrolyte outputs were highest for the most dilute diets, with high water fluxes, and lowest for concentrated diets without supplementary water provided (Fig. 5A), so that electrolyte output was significantly correlated with volume of CF (Fig. 5B; r296=0.514, P<0.001). Na+ and K+ in CF together accounted for 9.1±7.3% of total osmolality over all diets, and reached a maximum of 16.7±10.7% on the 0.25 mol l1 sucrose diet. The composition of the remainder of excreted osmolytes is not known.
|
![]() |
Discussion |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
|
How do sunbirds cope with LOW concentration nectars?
Nectar usually includes excess water even in the desert,
hummingbirds flying at ambient temperatures of 2337°C produce CF
that is still chronically hypo-osmotic to plasma
(Hiebert and Calder, 1986). As
a consequence, nectarivores may be faced with excess water more often than
water deficits. Flowers pollinated by passerine birds tend to produce more
dilute nectars than hummingbird-pollinated flowers, a good example being the
genus Aloe in southern Africa, in which nectar concentrations can be
lower than the 0.25 mol l1 diet used in this study
(Nicolson, 2002
).
On dilute diets, our sunbirds voided some of the most dilute CF recorded to
date (lowest values averaging 6.2±2.6 mosm kg1,
N=7). Tapwater often gives higher osmolality values than this. A
minimum field-collected value of 10 mosm kg1 has been
recorded for broadtailed hummingbirds Selasphorus platycercus,
feeding at artificial feeders (Calder and
Hiebert, 1983), while under laboratory conditions, ruby-throated
hummingbirds Archilochus colubris, feeding on 0.2 mol
l1 sugar solutions, produced CF with an average osmolality
of 10 mosm kg1 (Beuchat,
1998
). Measurement of extremely dilute osmolalities in the present
study was made possible by selection of a special thermocouple head for the
osmometer and thorough and frequent cleaning. The use of such a thermocouple
head was also noted by Beuchat
(1998
), but other authors have
been unable to measure such low osmolalities
(Lotz and Martínez del Rio,
2003
).
Our minimum values for electrolyte excretion are comparable with the lowest
figures recorded for rufous hummingbirds, S. rufus (<0.5 mmol
l1 for Na+ and K+;
Lotz and Martínez del Rio,
2003), and lesser doublecollared sunbirds, N. chalybea
(0.6 mmol l1 for Na+ and 1.5 mmol
l1 for K+;
Lotz and Nicolson, 1999
), fed
electrolyte-free diets. These nectarivorous birds have all demonstrated a
remarkable ability to produce extremely dilute urine, reabsorbing most
electrolytes from excreted fluid. The increase in total Na+ and
K+ excretion with increasing water flux on dilute diets is an
interesting result and may pose a problem for birds dealing with dilute nectar
diets that are low in electrolytes, particularly Na+
(Goldstein and Bradshaw,
1998b
). However, means of 3.4 mmol l1
Na+ and 24.7 mmol l1 K+ were measured
in nectar of 19 hummingbird-pollinated plant species by Hiebert and Calder
(1983
) and, in conjunction
with arthropod feeding, even these low values may provide adequate electrolyte
replacement for birds feeding on natural diets
(Lotz and Martínez del Rio,
2003
).
Nectarivore kidneys examined to date lack the morphology associated with
the concentrating abilities of other birds
(Goldstein and Braun, 1989;
Johnson and Mugaas, 1970
).
Kidneys of hummingbirds and honeyeaters contain few mammalian-type
concentrating nephrons and a small medullary component
(Casotti et al., 1998
). They
appear to be designed to recover valuable solutes from large quantities of
plasma rather than to concentrate urine
(Beuchat et al., 1990
;
Goldstein and Skadhauge,
2000
). Sunbird renal morphology is yet to be described. Sunbirds,
unlike hummingbirds (McWhorter and
Martínez del Rio, 1999
), are able to modulate water
absorption by the intestine so that excess preformed water is shunted through
the gut, and the water load to be processed by the kidneys is correspondingly
reduced (McWhorter et al.,
2003
). A similar modulation of water absorption may exist in
honeyeaters (Goldstein and Bradshaw,
1998b
). This ability serves to resolve the potential conflict
between filtering excess water and retaining solutes. Post-renal modification
also plays a significant role in both sunbird and hummingbird osmoregulation
(Lotz and Martínez del Rio,
2003
; Roxburgh and Pinshow,
2002
).
Evaporative water loss
Our data indicate a significant role for evaporative water loss (EWL) in
sunbird water balance, and evaporation cannot be discounted as a route for
dealing with excess water. While some of the water we ascribe to EWL could be
lost through problems with collection of CF (evaporation from CF droplets
prior to sinking under paraffin, or not all the CF droplets reaching the
collecting tray), the patterns of EWL show a clear trend that seems unlikely
to be produced by methodological errors.
Birds can modulate their EWL in response to heat stress both through
panting and control of cutaneous evaporation: the latter is effected by
changes in cutaneous vasomotor tone, skin temperature and/or alterations to
the disposition of plumage (Hoffman and
Walsberg, 1999; Marder and
Raber, 1989
; Webster and King,
1987
; Wolf and Walsberg,
1996
). Most research on EWL has been carried out in this
thermoregulatory context (reviewed by
Dawson, 1982
;
Dawson and Whittow, 2000
;
Skadhauge, 1981
), while the
role of evaporation in water balance has seldom been considered.
Cutaneous EWL is certainly influenced by hydration state. For example, it
has been clearly demonstrated that a variety of bird species are capable of
reducing EWL through cutaneous or respiratory routes when deprived of drinking
water, often at a cost to thermoregulation (e.g.
Arad et al., 1987;
Maloney and Dawson, 1998
).
Birds from arid areas also have significantly lower EWL than those from mesic
areas (Williams, 1996
).
However, there are few reports that link water loading (rather than
dehydration) with EWL, and the potential interaction between osmoregulation
and thermoregulation in this context.
In nectarivorous honeyeaters, EWL is significantly affected by both
temperature (Collins et al.,
1980) and diet concentration
(Collins, 1981
). EWL (measured
gravimetrically) increased by 21% and 23% for birds fed a dilute (0.4 mol
l1) compared with a more concentrated (1.2 mol
l1) sucrose diet
(Collins, 1981
). Similarly,
Lotz (1999
) found that the
lesser doublecollared sunbird demonstrated a 115% increase in EWL when
switched from a 1.2 to a 0.2 mol l1 sucrose diet at 20°C
(measured with a humidity meter). These changes recorded in flow-through
chambers are comparable to the increases in EWL volumes calculated by
difference in the present study. In hummingbirds, the third main group of
nectarivorous birds, the effect of dilute diet, and therefore waterloading, on
EWL has not been examined, and neither have birds been allowed to drink when
in respiratory chambers. Published EWL rates are therefore much smaller than
the values recorded for feeding sunbirds and honeyeaters. Nevertheless, in
response to increasing ambient temperature, various hummingbird species
increase EWL (Lasiewski, 1964
;
Powers, 1992
). Furthermore,
Lotz and Martínez del Rio
(2003
) indicated that for
rufous hummingbirds fed 0.21 mol l1 sucrose
solutions, 5068% of water intake was lost through EWL.
On the dilute diets, when water-loaded, whitebellied sunbirds were inactive
and maintained a posture somewhat similar to that when exposed to low ambient
temperatures, feathers being completely piloerect. It is possible that this
posture was a response to warming large volumes of cold food to body
temperature (Lotz et al.,
2003), or else the increased water flux, and potentially greater
evaporative losses, increased heat loss in these birds. Alternatively, their
inability to maintain sufficient energy intake
(Nicolson and Fleming, 2003
)
may have affected their thermogenic capacity. Further analysis of the link
between evaporative water loss and water loading is required to address these
possibilities.
How do sunbirds cope with HIGH concentration nectars?
Sucrose at a concentration of 2.5 mol l1 is at the
uppermost limit of possible nectar concentrations. From allometry, it can be
assumed that a 9.3 g bird should consume around 3035% of body mass
(2.83.3 ml) of water daily, most of which is lost through respiration
(Bartholomew and Cade, 1956).
Sunbirds feeding on concentrated sucrose solutions, with water gains of
approximately 3.9 and 3.1 ml day1 (2 and 2.5 mol
l1 sucrose, respectively), therefore may not necessarily be
dehydrated; however, their water gain may be almost entirely lost by
evaporation alone (Calder,
1979
).
Dehydrated birds generally excrete largely solid waste products and switch
from production of urine that is isoosmotic with plasma to a diminished flow
of urine with an osmolality 23 times that of plasma, avian plasma being
320370 mmol kg1 (Goldstein and Braun,
1988,
1989
;
Goldstein and Skadhauge, 2000
;
Skadhauge, 1981
). Our maximum
CF osmolality values, approximately 1.3x estimated plasma osmolality,
are comparable to data obtained from normally hydrated granivorous birds on
solid diets (Table 3) (Calder, 1981
;
Goldstein et al., 1990
), as
well as to maximum values recorded for other nectarivores. For example, field
measurements of CF from yellowthroated miners Manorina flavigula
indicate that these arid-living honeyeaters produce CF with an osmolality of
368±47 mosm kg1 (mean ±
S.E.M.; Goldstein
and Bradshaw, 1998a
), while Hiebert and Calder
(1986
) recorded values of
308426 mosm kg1 for hummingbirds engaged in intense
competition in high-elevation meadows, distant from artificial feeders.
Birds on concentrated diets drank the greatest volumes of supplementary
water, when it was available. As a consequence of drinking as little as
5.8±3.6 ml day1 supplementary water, CF osmolality
was reduced dramatically from 461±253 to 80±119 mosm
kg1 on the 2.5 mol l1 sucrose diets. On
concentrated nectars, free water may therefore be an important part of the
birds' water balance. Although it is often assumed that nectarivorous birds do
not drink free water, field studies in arid Australia have shown that
honeyeaters are highly dependent on drinking water
(Fisher et al., 1972). Water
drinking in the wild may be used to dilute concentrated nectars
(Nicolson and Fleming,
2003
).
Conclusions
For sunbirds feeding on the most dilute artificial diets, a suite of
physiological constraints associated with water loading may limit food intake
and thus energy balance. However, for the tenfold range of concentrations from
0.25 to 2.5 mol l1 sucrose, reflecting natural nectars,
sunbirds are eminently capable of maintaining water balance. The birds respond
to differences in water availability by altering both CF and evaporative
components of water elimination. Most notably, the scope of CF osmolality in
sunbirds is remarkable. Sunbirds are able to produce some of the most dilute
CF recorded their ability to recover electrolytes from CF may be
unparalleled by any non-nectarivorous bird, while on concentrated diets with
subsequent water shortage, their ability to produce concentrated CF is
comparable with that of some granivorous species.
![]() |
Acknowledgments |
---|
![]() |
References |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Arad, Z., Gavrieli-Levin, I., Eylath, U. and Marder, J. (1987). Effect of dehydration on cutaneous water evaporation in heat-exposed pigeons (Columba livia). Physiol. Zool. 60,623 -630.
Bartholomew, G. and Cade, T. J. (1956). Water consumption of house finches. Condor 58,406 -412.
Beuchat, C. A. (1998). Urinary concentrating ability of a nectarivorous bird, the ruby-throated hummingbird. Bull. Mount Desert Island Biol. Lab. 37, 77-78.
Beuchat, C. A., Calder, W. A. and Braun, E. J. (1990). The integration of osmoregulation and energy balance in hummingbirds. Physiol. Zool. 63,1059 -1081.
Calder, W. A. (1979). On the temperature-dependency of optimal nectar concentrations for birds. J. theor. Biol. 78,185 -196.[Medline]
Calder, W. A. (1981). Diuresis on the desert? Effects of fruit- and nectar-feeding on the house finch and other species. Condor 83,267 -268.
Calder, W. A. and Hiebert, S. M. (1983). Nectar feeding, diuresis, and electrolyte replacement of hummingbirds. Physiol. Zool. 56,325 -334.
Casotti, G., Braun, E. and Beuchat, C. (1998). Morphology of the kidney in a nectarivorous bird, the Anna's hummingbird Calypte anna. J. Zool. Lond. 244,175 -184.
Collins, B. G. (1981). Nectar intake and water balance for two species of Australian honeyeater, Lichmera indistincta and Acanthorhynchus superciliosis. Physiol. Zool. 54,1 -13.
Collins, B. G., Cary, G. and Packard, G. (1980). Metabolism, thermoregulation and evaporative water loss in two species of Australian nectar-feeding birds (family Meliphagidae). Comp. Biochem. Physiol. 67,629 -635.[CrossRef]
Dawson, W. R. (1982). Evaporative losses of water by birds. Comp. Biochem. Physiol. 71,495 -509.[CrossRef]
Dawson, W. R. and Whittow, G. C. (2000). Heat loss. In Sturkie's Avian Physiology (ed. G. C. Whittow), pp. 343-390. New York: Academic Press.
Fisher, C. D., Lindgren, E. and Dawson, W. R. (1972). Drinking patterns and behaviour of Australian desert birds in relation to their ecology and abundance. Condor 74,111 -136.
Goldstein, D. L. and Bradshaw, S. D. (1998a). Regulation of water and sodium balance in the field by Australian honeyeaters (Aves: Meliphagidae). Physiol. Zool. 71,214 -225.[Medline]
Goldstein, D. L. and Bradshaw, S. D. (1998b). Renal function in red wattlebirds in response to varying fluid intake. J. Comp. Physiol. B 168,265 -272.[CrossRef]
Goldstein, D. L. and Braun, E. J. (1988). Contributions of the kidneys and intestines to water conservation, and plasma levels of antidiuretic hormone, during dehydration in house sparrows (Passer domesticus). J. Comp. Physiol. B 158,353 -361.[Medline]
Goldstein, D. L. and Braun, E. J. (1989). Structure and concentrating ability in the avian kidney. Am. J. Physiol. 256,R501 -R509.[Medline]
Goldstein, D. L. and Skadhauge, E. (2000). Renal and extrarenal regulation of body fluid composition. In Sturkie's Avian Physiology (ed. G. C. Whittow), pp.265 -297. New York: Academic Press.
Goldstein, D. L., Williams, J. B. and Braun, E. J. (1990). Osmoregulation in the field by salt-marsh savannah sparrows, Passerculus sandwichensis beldingi. Physiol. Zool. 63,669 -682.
Hiebert, S. M. and Calder, W. A. (1983). Sodium, potassium, and chloride in floral nectars: energy-free contributions to refractive index and salt balance. Ecology 64,399 -402.
Hiebert, S. M. and Calder, W. A. (1986). The osmoregulatory consequences of nectarivory and frugivory in hummingbirds and other species. In Acta XIX Congressus Internationalis Ornithologici, vol. 2, pp.1498 -1505.
Hoffman, T. C. M. and Walsberg, G. E. (1999).
Inhibiting ventilatory evaporation produces an adaptive increase in cutaneous
evaporation in mourning doves Zenaida macroura. J. Exp.
Biol. 202,3021
-3028.
Jackson, S., Nicolson, S. W. and van Wyk, B.-E. (1998). Apparent absorption efficiencies of nectar sugars in the Cape sugarbird, with a comparison of methods. Physiol. Zool. 71,106 -115.[Medline]
Johnson, O. W. and Mugaas, J. N. (1970). Some histological features of avian kidneys. Am. J. Anat. 127,423 -436.[Medline]
Lasiewski, R. C. (1964). Body temperatures, heart and breathing rate, and evaporative water loss in hummingbirds. Physiol. Zool. 37,212 -223.
Lotz, C. N. (1999). Energy and water balance in the lesser double-collared sunbird, Nectarinia chalybea. PhD thesis, University of Cape Town, South Africa.
Lotz, C. N. and Martínez del Rio, C. (2003). The ability of rufous hummingbirds (Selasphorous rufus) to dilute and concentrate urine. J. Avian Biol. in press.
Lotz, C. N., Martínez del Rio, C. and Nicolson, S. W. (2003). Hummingbirds pay a high cost for a warm drink. J. Comp. Physiol. B. In press.
Lotz, C. N. and Nicolson, S. W. (1996). Sugar preferences of a nectarivorous passerine bird, the lesser double-collared sunbird (Nectarinia chalybea). Funct. Ecol. 10,360 -365.
Lotz, C. N. and Nicolson, S. W. (1999). Energy and water balance in the lesser double-collared sunbird (Nectarinia chalybea) feeding on different nectar concentrations. J. Comp. Physiol. B 169,200 -206.[CrossRef]
Maloney, S. K. and Dawson, T. J. (1998). Changes in pattern of heat loss at high ambient temperatures caused by water deprivation in a large flightless bird, the emu. Physiol. Zool. 71,712 -719.[Medline]
Marder, J. and Raber, P. (1989). Beta-adrenergic control of transcutaneous evaporative cooling mechanisms in birds. J. Comp. Physiol. B 159,97 -103.
McWhorter, T. J. and Martínez del Rio, C.
(1999). Food ingestion and water turnover in hummingbirds: how
much dietary water is absorbed? J. Exp. Biol.
202,2851
-2858.
McWhorter, T. J., Martínez del Rio, C. and Pinshow,
B. (2003). Modulation of ingested water absorption by
Palestine sunbirds: evidence for adaptive regulation. J. Exp.
Biol. 206,659
-666.
Nicolson, S. W. (1998). The importance of osmosis in nectar secretion and its consumption by insects. Am. Zool. 38,418 -425.
Nicolson, S. W. (2002). Pollination by passerine birds: why are the nectars so dilute? Comp. Biochem. Physiol. B 131,645 -652.[CrossRef][Medline]
Nicolson, S. W. and Fleming, P. A. (2003). Energy balance in the whitebellied sunbird, Nectarinia talatala: constraints on compensatory feeding, and consumption of supplementary water. Funct. Ecol. 17,3 -9.[CrossRef]
Poulson, T. L. and Bartholomew, G. A. (1962). Salt utilization in the house finch. Condor 64,245 -252.
Powers, D. R. (1992). Effect of temperature and humidity on evaporative water loss in Anna's hummingbird (Calypte anna). J. Comp. Physiol. B 162, 74-84.
Prinzinger, R., Schafer, T. and Schuchmann, K.-L. (1992). Energy metabolism, respiratory quotient and breathing parameters in two convergent small bird species: the fork-tailed sunbird Aethopyga christinae (Nectariniidae) and the Chilean hummingbird Sephanoides sephanoides (Trochilidae). J. Therm. Biol. 17,71 -79.[CrossRef]
Roxburgh, L. and Pinshow, B. (2002). Ammonotely
in a passerine nectarivore: the influence of renal and post-renal modification
on nitrogenous waste product excretion. J. Exp. Biol.
205,1735
-1745.
Schmidt-Nielsen, K. (1997). Animal Physiology: Adaptation and Environment. Cambridge: Cambridge University Press.
Skadhauge, E. (1981). Osmoregulation in Birds. New York: Springer-Verlag.
Skadhauge, E. and Bradshaw, S. D. (1974).
Saline drinking and cloacal excretion of salt and water in the zebra finch.
Am. J. Physiol. 227,1263
-1267.
Webster, M. and King, J. (1987). Temperature and humidity dynamics of cutaneous and respiratory evaporation in pigeons, Columba livia. J. Comp. Physiol. B 157,253 -260.[Medline]
Williams, J. B. (1996). A phylogenetic perspective of evaporative water loss in birds. Auk 113,457 -472.
Wolf, B. O. and Walsberg, G. E. (1996).
Respiratory and cutaneous evaporative water loss at high environmental
temperatures in a small bird. J. Exp. Biol.
199,451
-457.