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Respiratory water loss in free-flying pigeons
Abstract
We assessed respiratory and cutaneous water loss in trained tippler pigeons (Columba livia) both at rest and in free flight. In resting pigeons, exhaled air temperature T(ex) increased with ambient air temperature T(a) (T(ex)=16.3+0.705T(a)) between 15 degrees C and 30 degrees C, while tidal volume V(T) (V(T)=4.7+/-1.0 ml, mean +/- S.D. at standard temperature and pressure dry) and breathing frequency f(R) (f(R)=0.46+/-0.06 breaths s(-1)) were independent of T(a). Respiratory water loss, RWL, was constant over the range of T(a) (RWL=1.2+/-0.4 mg g(-1) h(-1)) used. In flying pigeons, T(ex) increased with T(a) (T(ex)=25.8+0.34T(a)), while f(R) was independent of T(a) (f(R)=5.6+/-1.4 breaths s(-1)) between 8.8 degrees C and 27 degrees C. Breathing frequency varied intermittently between 2 and 8 breaths s(-1) during flight and was not always synchronized with wing-beat frequency. RWL was independent of air temperature (RWL=9.2+/-2.9 mg g(-1) h(-1)), but decreased with increasing inspired air water vapor density (rho(in)) (RWL=12.5-0.362rho(in)), whereas cutaneous water loss, CWL, increased with air temperature (CWL=10.122+0.898T(a)), but was independent of rho(in). RWL was 25.7-32.2 %, while CWL was 67.8-74.3 % of the total evaporative water loss. The data indicate that pigeons have more efficient countercurrent heat exchange in their anterior respiratory passages when at rest than in flight, allowing them to recover more water at rest at lower air temperatures. When evaporative water loss increases in flight, especially at high T(a), the major component is cutaneous rather than respiratory, possibly brought about by reducing the skin water vapor diffusion resistance. Because of the tight restrictions imposed by gas exchange in flight, the amount of water potentially lost through respiration is limited.
... In addition to energy, birds need to balance their water budget, and this might be difficult during migratory endurance flights. Although metabolically produced water from fat and protein catabolism might counterbalance water loss due to evaporative cooling (Dawson, 1982;Michaeli & Pinshow, 2001) and in faeces (Giladi & Pinshow, 1999), long flights could potentially lead to dehydration (Yapp, 1956;Carmi et al., 1992;Klaassen, 1995Klaassen, , 1996Klaassen, , 2004. If so, migrants could seek stopovers for rehydration (Leberg, Spengler & Barrow Jr, 1996). ...
... Most energy metabolised for flapping flight is transferred as heat to the body and therefore may increase body temperature. To avoid detrimental levels of hyperthermia, birds cool their body through evaporation/respiration (Salt, 1964;Dawson, 1982;Michaeli & Pinshow, 2001) and/or heat transfer from the body to the surrounding air layers (Ward et al., 1999;Schraft, Whelan & Elliott, 2019). If these mechanisms are not sufficient, birds may interrupt the migratory endurance flight to prevent body temperature from rising above the normothermic zone (Guillemette et al., 2016(Guillemette et al., , 2017. ...
... In flying animals, water loss increases with increasing temperature and decreasing humidity (Torre-Bueno, 1976;Biesel & Nachtigall, 1987;Adams, Pinshow & Gannes, 1997;Michaeli & Pinshow, 2001;Engel, Biebach & Visser, 2006). It has, therefore, been suggested that migrants interrupt their endurance flight in warm and dry air to prevent dehydration (see Section III.2d; reviewed in Schmaljohann et al., 2008). ...
Global movement patterns of migratory birds illustrate their fascinating physical and physiological abilities to cross continents and oceans. During their voyages, most birds land multiple times to make so‐called ‘stopovers’. Our current knowledge on the functions of stopover is mainly based on the proximate study of departure decisions. However, such studies are insufficient to gauge fully the ecological and evolutionary functions of stopover. If we study how a focal trait, e.g. changes in energy stores, affects the decision to depart from a stopover without considering the trait(s) that actually caused the bird to land, e.g. unfavourable environmental conditions for flight, we misinterpret the function of the stopover. It is thus important to realise and acknowledge that stopovers have many different functions, and that not every migrant has the same (set of) reasons to stop‐over. Additionally, we may obtain contradictory results because the significance of different traits to a migrant is context dependent. For instance, late spring migrants may be more prone to risk‐taking and depart from a stopover with lower energy stores than early spring migrants. Thus, we neglect that departure decisions are subject to selection to minimise immediate (mortality risk) and/or delayed (low future reproductive output) fitness costs. To alleviate these issues, we first define stopover as an interruption of migratory endurance flight to minimise immediate and/or delayed fitness costs. Second, we review all probable functions of stopover, which include accumulating energy, various forms of physiological recovery and avoiding adverse environmental conditions for flight, and list potential other functions that are less well studied, such as minimising predation, recovery from physical exhaustion and spatiotemporal adjustments to migration. Third, derived from these aspects, we argue for a paradigm shift in stopover ecology research. This includes focusing on why an individual interrupts its migratory flight, which is more likely to identify the individual‐specific function(s) of the stopover correctly than departure‐decision studies. Moreover, we highlight that the selective forces acting on stopover decisions are context dependent and are expected to differ between, e.g. K−/r‐selected species, the sexes and migration strategies. For example, all else being equal, r‐selected species (low survival rate, high reproductive rate) should have a stronger urge to continue the migratory endurance flight or resume migration from a stopover because the potential increase in immediate fitness costs suffered from a flight is offset by the expected higher reproductive success in the subsequent breeding season. Finally, we propose to focus less on proximate mechanisms controlling landing and departure decisions, and more on ultimate mechanisms to identify the selective forces shaping stopover decisions. Our ideas are not limited to birds but can be applied to any migratory species. Our revised definition of stopover and the proposed paradigm shift has the potential to stimulate a fruitful discussion towards a better evolutionary ecological understanding of the functions of stopover. Furthermore, identifying the functions of stopover will support targeted measures to conserve and restore the functionality of stopover sites threatened by anthropogenic environmental changes. This is especially important for long‐distance migrants, which currently are in alarming decline.
... However, the functional significance of such controls has not been studied in flight. Measurements of EWL in flying birds are few, and most that do exist were made at relatively low ambient temperature and on birds greater than 75 g [12][13][14][15]. Smaller species, including hummingbirds, are sensitive to environmental temperature [16][17][18] and therefore at high temperature must have the ability to increase EWL during flight if they are to engage in flight. ...
... Although we had relatively few measurements of BLUH (n = 17), it was interesting that data were absent from 12.00 to 18.00, which includes periods of the day when T was unfavourable. Unlike BLUH, RIHU were more active midday (12.00- 15.00) even though T e was near T 0 (figure 6d). ...
At high temperature (greater than 40°C) endotherms experience reduced passive heat dissipation (radiation, conduction and convection) and increased reliance on evaporative heat loss. High temperatures challenge flying birds due to heat produced by wing muscles. Hummingbirds depend on flight for foraging, yet inhabit hot regions. We used infrared thermography to explore how lower passive heat dissipation during flight impacts body-heat management in broad-billed (Cynanthus latirostris, 3.0 g), black-chinned (Archilochus alexandri, 3.0 g), Rivoli’s (Eugenes fulgens, 7.5 g) and blue-throated (Lampornis clemenciae, 8.0 g) hummingbirds in southeastern Arizona and calliope hummingbirds (Selasphorus calliope, 2.6 g) in Montana. Thermal gradients driving passive heat dissipation through eye, shoulder and feet dissipation areas are eliminated between 36 and 40°C. Thermal gradients persisted at higher temperatures in smaller species, possibly allowing them to inhabit warmer sites. All species experienced extended daytime periods lacking thermal gradients. Broad-billed hummingbirds lacking thermal gradients regulated the mean total-body surface temperature at approximately 38°C, suggesting behavioural thermoregulation. Blue-throated hummingbirds were inactive when lacking passive heat dissipation and hence might have the lowest temperature tolerance of the four species. Use of thermal refugia permitted hummingbirds to tolerate higher temperatures, but climate change could eliminate refugia, forcing distributional shifts in hummingbird populations.
... As these meteorological factors vary in time and space, migratory birds are expected to be selective for time periods and flight altitudes to minimize energy costs or water loss or, if possible, both. Energetic flight costs and the environmental factors affecting the energy consumption are in general well understood (Masman & Klaassen 1987;Pennycuick 1989;Rayner 1990;Weber & Houston 1997;Pennycuick 1998;Thomas & Hedenström 1998;Wikelski et al. 2003;McWilliams et al. 2004;Hedenström et al. 2005); on the contrary the water budget of migrating birds is poorly understood (Michaeli & Pinshow 2001), though intensive wind tunnel experiments have been performed, e.g. , Rothe et al. (1987), and . Klaassen et al. (1999) introduced a physiological model based mainly on the water expenditure model by Carmi et al. (1993) and the flight power model from Pennycuick (1989). ...
... estimated that Thrush Nightingales (Luscinia luscinia) flying for 12 hours in a wind tunnel at temperatures between 16 and 23°C did not dehydrate, see also Kvist et al. (1998), whereas according to pigeons remain flying only for 2 hours at 25°C due to dehydration. In outdoor experiments, pigeons flew freely for more than 2 hours at temperatures around of 27°C (Michaeli & Pinshow 2001), indicating that results of wind tunnel experiments cannot so easily be applied to free flying birds, probably because a wind tunnel-flight is more stressful VI-8 WIND GOVERNS SONGBIRD'S FLIGHT ALTITUDE than a free-flight (Ward et al. 1999;. Only little is known about flight duration of freely migrating songbirds, e.g. ...
... Energetic flight costs and the environmental factors affecting the energy expenditure are in general well understood (e.g., Masman and Klaassen 1987; Pennycuick 1989; Rayner 1990; Hedenström and Alerstam 1995; Klaassen 1996; Weber and Houston 1997; Pennycuick 1998; Thomas and Hedenström 1998; Rayner 2001; Wikelski et al. 2003; McWilliams et al. 2004; Hedenström et al. 2005; Engel et al. 2006a). On the contrary, we have only started to understand the water budget of flying birds despite intensive research, e.g., Biesel and Nachtigall (1987); Rothe et al. (1987); Adams et al. (1997); Giladi and Pinshow (1999); Pennycuick et al. (1999);; Michaeli and Pinshow (2001); Engel (2005); and Engel et al. (2006b,c,d). Carmi et al. (1992) developed a model to estimate birds' water loss during flight. ...
... According to Biesel and Nachtigall (1987), pigeons remain flying only for 2 h at 25°C due to dehydration. In outdoor experiments, pigeons flew freely for more than 2 h at temperatures around of 27°C (Michaeli and Pinshow 2001), indicating that birds in wind tunnel experiments might behave differently to free flying birds. Wind tunnelflights may be more stressful than free-flights (Ward et al. 1999; Liechti and Bruderer 2002; Engel 2005) because birds have only little space available in the flight chamber, which may be especially for bounding flyers a constraint. ...
Meteorological conditions influence strongly the energy and water budget of birds. By adjusting their flights spatially and
temporally with respect to these conditions, birds can reduce their energy expenditure and water loss considerably. By radar,
we quantified songbird migration across the western Sahara in spring and autumn. There autumn migrants face the trade-off
between (a) favorable winds combined with hot and dry air at low altitudes and (b) unfavorable winds combined with humid and
cold air higher up. Thus, it can be tested whether birds may chose altitudes to minimize water loss instead of energy expenditure.
We predicted optimal flight altitudes with respect to water loss and energy expenditure based on a physiological flight model
when crossing the western Sahara and compared these model predictions spatially and temporally with measured songbird densities.
The model aiming for minimal water consumption predicted a mean flight altitude of 3,400m under autumn conditions. However,
64% of the nocturnal songbird migration flew at altitudes below 1,000m above ground level profiting from tailwind. This preference
for tailwind in autumn, despite the hot and dry air, emphasizes the importance of energy savings and diminishes the significance
of possible water stress for the selection of flight altitude. Nevertheless, during daytime, high energy expenditure due to
air turbulences and water loss due to warmer air and direct solar radiation prevent songbirds from prolonging their nocturnal
flights regularly into the day. Birds crossing the Sahara save water by nocturnal flights and diurnal rests.
... Most investigators have indirectly estimated RWL by measuring the temperature of exhaled air and minute volume during respiration, and then calculating RWL as a product of minute volume and the saturated water vapor density at the temperature of exhaled air (Withers and Williams, 1990;Geist, 2000). CWL has also been indirectly estimated by using whole body plethsesmography (Withers and Williams, 1990), or by evaluating resistance of sites on the skin and calculating whole organism CWL from Fick's law of diffusion and estimates of skin surface area (Michaeli and Pinshow, 2001;Marder et al., 2003;Larcombe et al., 2003). Direct measurements of RWL and CWL of birds are few, mostly from desert species; RWL and CWL has been measured in only four non-desert species of birds (Tieleman and Williams, 2002;Williams, 2005b, 2007). ...
... Traditionally respiratory variables were used to indirectly estimate RWL in birds (Jackson and Schmidt-Nielsen, 1964;, but the accuracy of such estimates remains untested. We have compared indirect estimates of RWL Michaeli and Pinshow, 2001;Larcombe et al., 2003) with values that were directly measured (Bernstein, 1971;Wolf and Walsberg, 1996;Tieleman and Williams, 2002;Muñoz-Garcia and Williams, 2005b; this study) and found no Fig. 4. The relationship between amount of ceramide 3 and whole organism cutaneous water loss (g H 2 O/d). Unfilled circles represent mean values of each species and vertical lines represent ±1 S.E. ...
We measured respiratory water loss (RWL) and cutaneous water loss (CWL) of 12 species of passerine birds, all from a temperate environment, and related their CWL to classes of lipids within the stratum corneum (SC). We purposed to gain insight into the generality of patterns of CWL in birds that have been generated mostly from studies on species from deserts, and we addressed the hypothesis that CWL is a passive diffusion process. Despite taxonomic and ecological differences among 12 species of temperate birds, mass-specific RWL and surface-specific CWL were statistically indistinguishable across species. When the birds were dead, CWL was reduced by 16.3% suggesting that CWL is, in part, under physiological control. We found that ceramides, cerebrosides, dioscylceramides, cholesterol, cholesterol sulfate, fatty acid methyl esters, free fatty acid, sterol esters, and triacylglycerol constituted the intercellular lipids of the avian SC. CWL was positively associated with amount of ceramide 3, but this lipid class represented less than 2% of the total SC lipids. Combining direct measurements (n=24) of RWL with indirect estimates (n=25) yielded the equation log RWL (g H(2)O/d)=-0.86+0.73 (log body mass, g).
... As predicted, airflow rate did have a noticeable effect on heat transfer efficiency, with lower flow rates resulting in more effective heat transfer (11-14% and 6-9% greater efficiency for Panoplosaurus and Euoplocephalus, respectively; Fig 13). These results agree with previous measurements and simulations [69,70] that indicate flow rate is one of the most important contributing factors affecting heat transfer between air and the nasal passage. ...
Convoluted nasal passages are an enigmatic hallmark of Ankylosauria. Previous research suggested that these convoluted nasal passages functioned as heat exchangers analogous to the respiratory turbinates of mammals and birds. We tested this hypothesis by performing a computational fluid dynamic analysis on the nasal passages of two ankylosaurs: Panoplosaurus mirus and Euoplocephalus tutus. Our models predicted that Panoplosaurus and Euoplocephalus would have required 833 and 1568 thermal calories, respectively, to warm a single breath of air by 20°C. Heat recovery during exhalation resulted in energy savings of 65% for Panoplosaurus and 84% for Euoplocephalus. Our results fell well within the range of values for heat and water savings observed in extant terrestrial amniotes. We further tested alternate airway reconstructions that removed nasal passage convolutions or reduced nasal vestibule length. Our results revealed that the extensive elaboration observed in the nasal vestibules of ankylosaurs was a viable alternative to respiratory turbinates with regards to air conditioning. Of the two dinosaurs tested, Euoplocephalus repeatedly exhibited a more efficient nasal passage than Panoplosaurus. We suggest that the higher heat loads associated with the larger body mass of Euoplocephalus necessitated these more efficient nasal passages. Our findings further indicate that the evolution of complicated airways in dinosaurs may have been driven by the thermal requirements of maintaining cerebral thermal homeostasis.
... In contrast to scenario 1, birds have a strong urge to accumulate large amounts of energy in preparation for the upcoming high-energy demanding flight period. 3. Upon arrival at the "first" stopover landscapes after an energetically highly demanding flight migrants have lost a large fraction of their energy stores (Loria and Moore 1990;Moore and Yong 1991;Pilastro and Spina 1997;Yong and Moore 1997;Spina and Pilastro 1999;Battley et al. 2000;Ottosson et al. 2002;Yohannes et al. 2008;Maggini and Bairlein 2010a), might be physically exhausted (Schwilch et al. 2002), and may experience water stress when migrated at high temperatures (Biesel and Nachtigall 1987;Carmi et al. 1992;Giladi and Pinshow 1999;Ward et al. 1999;Michaeli and Pinshow 2001), but see Schmaljohann et al. (2008). Birds with fully depleted of energy (Maggini and Bairlein 2010a), while others with some remaining energy stores might search for a specific stopover site. ...
In birds, accumulating energy is far slower than spending energy during flight. During migration, birds spend, therefore, most of the time at stopover refueling energy used during the previous flight. This elucidates why current energy stores and actual rate of accumulating energy are likely crucial factors influencing bird’s decision when to resume migration in addition to other intrinsic (sex, age) and extrinsic (predation, weather) factors modulating the decision within the innate migration program. After first summarizing how energy stores and stopover durations are generally determined, we critically review that high-energy stores and low rates of accumulating energy were significantly related to high departure probabilities in several bird groups. There are, however, also many studies showing no effect at all. Recent radio-tracking studies highlighted that migrants leave a site either to resume migration or to search for a better stopover location, so-called “landscape movements”. Erroneously treating such movements as departures increases the likelihood of type II errors which might mistakenly suggest no effect of either trait on departure. Furthermore, we propose that energy loss during the previous migratory flight in relation to bird’s current energy stores and migration strategy significantly affects its urge to refuel and hence its departure decision.
... Long-distance bird migrants seem to be able to achieve the impossible, spending energy at an unmatched rate among vertebrates and dumping large amounts of heat produced while flying, all without dehydrating. Numerous wind-tunnel studies, laboratory and aviary experiments have shown that convection is the main mechanism by which a flying bird maintains heat balance, followed by radiation and evaporation [1][2][3][4][5][6][7][8][9]. Hyperthermia, a condition that develops when those mechanisms of heat dissipation are not sufficient to maintain heat balance, is barely mentioned as a potential constraint of performance in migrating birds (but see [4] and [10]). ...
While some migratory birds perform non-stop flights of over 11 000 km, many species only spend around 15% of the day in flight during migration, posing a question as to why flight times for many species are so short. Here, we test the idea that hyperthermia might constrain flight duration (FD) in a short-distance migrant using remote biologging technology to measure heart rate, hydrostatic pressure and body temperature in 19 migrating eider ducks ( Somateria mollissima ), a short-distance migrant. Our results reveal a stop-and-go migration strategy where migratory flights were frequent (14 flights day ⁻¹ ) and short (15.7 min), together with the fact that body temperature increases by 1°C, on average, during such flights, which equates to a rate of heat storage index (HSI) of 4°C h ⁻¹ . Furthermore, we could not find any evidence that short flights were limited by heart rate, together with the fact that the numerous stops could not be explained by the need to feed, as the frequency of dives and the time spent feeding were comparatively small during the migratory period. We thus conclude that hyperthermia appears to be the predominant determinant of the observed migration strategy, and suggest that such a physiological limitation to FD may also occur in other species.
This article is part of the themed issue ‘Moving in a moving medium: new perspectives on flight’.
... The hypothesis we investigate here is that physiological costs and cost accumulation can be compensated for during long flights. If this is so, then migratory birds may simply fly as far as their ecology dictates and their fuel reserves and body water requirements allow [16,[47][48][49][50][51][52][53][54]. ...
Many migrating birds undertake extraordinary long flights. How birds are able to perform such endurance flights of over 100-hour durations is still poorly understood. We examined energy expenditure and physiological changes in Northern Bald Ibis Geronticus eremite during natural flights using birds trained to follow an ultra-light aircraft. Because these birds were tame, with foster parents, we were able to bleed them immediately prior to and after each flight. Flight duration was experimentally designed ranging between one and almost four hours continuous flights. Energy expenditure during flight was estimated using doubly-labelled-water while physiological properties were assessed through blood chemistry including plasma metabolites, enzymes, electrolytes, blood gases, and reactive oxygen compounds. Instantaneous energy expenditure decreased with flight duration, and the birds appeared to balance aerobic and anaerobic metabolism, using fat, carbohydrate and protein as fuel. This made flight both economic and tolerable. The observed effects resemble classical exercise adaptations that can limit duration of exercise while reducing energetic output. There were also in-flight benefits that enable power output variation from cruising to manoeuvring. These adaptations share characteristics with physiological processes that have facilitated other athletic feats in nature and might enable the extraordinary long flights of migratory birds as well.
... Combing our data with data in the literature, I compared predictions of the T & W model with our direct measurements of RWL. I included data on RWL for birds that were directly measured (Bernstein, 1979;Wolf and Walsberg, 1996b;Tieleman and Williams, 2002;Mekechnie and Wolf, 2004;Munoz-Garcia and Williams, 2005) or calculated from respiratory parameters (Withers and Williams, 1990;Michaeli and Pinshow 2001;Larcombe et al., 2003). For temperate birds, RWL (g/day) as a function of body mass was described as log RWL normothermic = -0.78 ...
... Although comparable respiratory data are relatively few for reptiles, these low respiratory frequencies for birds are not that different from those of similarly sized-continuously breathing-lizards (Bennett 1973) and alligators (see Methods above). These disparate respiratory parameters call into question how important respiratory conchae are for endothermy in birds, and are reflected in the conflicting results of empirical studies on avian respiratory conchae (Tieleman et al., 1999;Geist, 2000;Michaeli and Pinshow, 2001). ...
The nasal region plays a key role in sensory, thermal, and respiratory physiology, but exploring its evolution is hampered by a lack of preservation of soft-tissue structures in extinct vertebrates. As a test case, we investi-gated members of the "bony-headed" ornithischian dinosaur clade Pachyce-phalosauridae (particularly Stegoceras validum) because of their small body size (which mitigated allometric concerns) and their tendency to preserve nasal soft tissues within their hypermineralized skulls. Hypermineralization directly preserved portions of the olfactory turbinates along with an internal nasal ridge that we regard as potentially an osteological correlate for respi-ratory conchae. Fossil specimens were CT-scanned, and nasal cavities were segmented and restored. Soft-tissue reconstruction of the nasal capsule was functionally tested in a virtual environment using computational fluid dynamics by running air through multiple models differing in nasal soft-tissue conformation: a bony-bounded model (i.e., skull without soft tissue) Abbreviations used: acPM 5 anastomotic canal in premaxilla; aEth 5 ethmoid artery; air 5 airway; anas 5 anastomosis between pal-atine, lateral nasal, and dorsal alveolar vessels; aSO 1 LN 5 anastomo-sis between supraorbital and lateral nasal vessels; aSph 5 sphenopalatine artery; at 5 potential accessory turbinate; bch 5 bony choana (fenestra exochoanalis); bLN 5 branches of lateral nasal vessels; bMN 5 branches of medial nasal vessels; cap 5 cartilaginous nasal cap-sule; caud co 5 caudal concha; cDA 5 dorsal alveolar canal; ch 5 choana (fenestra endochoanalis); cLN 5 canal for lateral nasal vessels; cMN 5 canal for medial nasal vessels; co 5 concha; cPM 5 canal in pre-maxilla; cSO 1 LN 5 canal for anastomosis between supraorbital and lateral nasal vessels; cSO 5 canal for supraorbital vessels; DA 5 dorsal alveolar vessels; f 5 frontal; fSO 5 suborbital fenestra; gLN 5 groove for lateral nasal vessels; j 5 jugal; lac 5 lacrimal; Lc 5 lacrimal canal; LN 5 lateral nasal vessels; max 5 maxilla; mid co 5 middle concha; MN 5 medial nasal vessels; mu 5 mucosa; nar 5 naris; nas 5 nasal; nc 5 nasal capsule; ng 5 nasal gland; npd 5 ductus nasopharyngeus; ns 5 nasal septum; ob 5 olfactory bulb; OfC 5 olfactory conchal vessels; olf e 5 olfactory epithelium; om 5 olfactory meatus; ot 5 olfactory turbi-nate; p 5 parietal; PA 5 palatine vessels; pl 5 palatine; pm 5 premax-illa; po 5 postorbital; post 5 postvestibular ridge; preco 5 preconcha; preco rec 5 preconchal recess; prf 5 prefrontal; ps 5 parasphenoid ros-trum; pt 5 pterygoid; q 5 quadrate; qj 5 quadratojugal; RC 5
... Field observations on birds exposed to actual T a s above 50 ºC that employ neither panting nor gular fluttering are also well documented (Thomas and Robin, 1977;Thomas and Maclean, 1981;Thomas, 1984;Ophir, personal observations). Additionally, many laboratory studies have established the foundation for the recognition that CWE as an adaptation to diurnal active life in hot environments does occur in pigeons and other birds (Smith, 1969;Smith and Suthers, 1969;Bernstein, 1971a,b;Lasiewski et al., 1971;Appleyard, 1979;Hudson and Bernstein, 1981;Marder, 1983;Marder and Ben Asher, 1983;Marder and Gavrieli-Levin, 1987;Withers and Williams, 1990;Wolf andWalsberg, 1996, Michaeli andPinshow, 2001). It should be emphasized, however, that although CWE in many species increases with T a , its relative importance as a proportion of total evaporation decreases (Wolf and Walsberg, 1996). ...
The most conspicuous phenomenon in the process of heat acclimation of the rock pigeon (Columba livia) is the remarkable increase in its capacity to evaporate water from its skin. This cooling route becomes the chief thermoregulatory means in the heat-acclimated (HAc) pigeon and is responsible for its ability to maintain normal body temperatures even at extremely high ambient temperatures of 60 ºC. Since the avian skin lacks sweat glands or any other homologous functional structure, cutaneous water evaporation (CWE) must occur along a different pathway than that known in mammals. The aim of this review is to characterize the CWE mechanism in the rock pigeon from three aspects: the regulatory pathway, the driving force, and the water passageway to the skin surface. CWE is controlled by the adrenergic system at various levels, both peripherally and at higher levels. It was found that nonspecific b-adrenergic inhibition (by propranolol) increases CWE in the HAc pigeon, but not in the non-acclimated (NAc) pigeon. This effect was found to be mainly peripheral, b2-related. Systemic a2-adrenergic stimulation (by clonidine) also increased CWE. However, this response showed no local effect. Skin blood flow (SkBF) was measured at various ambient temperatures and during CWE-stimulating adrenergic manipulations in the effort to understand the possible role of the cardiovascular system as the driving force in the mechanism. Two different methods were integrated--laser-Doppler flowmetry and ultrasonic flowmetry. As expected, heat exposure (50 ºC) significantly increased SkBF. This increase was found to be stronger in HAc pigeons. Injection of propranolol increased SkBF in HAc pigeons, but decreased SkBF in NAc pigeons. Injection of clonidine decreased SkBF in both acclimation states. Based on these results, we concluded that SkBF by itself plays no crucial role in the CWE mechanism. Therefore, apparently other vaso-dynamic changes, apart from SkBF, are involved in CWE. Ultrasonic measurements showed that pharmacologically-induced CWE (propranolol or clonidine) in HAc pigeons is accompanied by an increase in arterial flow, and by a decrease in venous flow. No significant changes (arterial or venous) were found in NAc pigeons. The above results suggest a reduction in arterial resistance along with an increase in venous resistance. This would lead to an increase in capillary hydrostatic pressure, and may therefore serve as the main driving force in the process of CWE. We also hypothesize that in addition to the driving force, there is another component--an adjustable gating mechanism--which functions as a resistance modulator for water movement towards the skin surface.
... EWL was different in different temperatures. There were many reports about the relation between EWL and temperature (Greogry, 1975;Williams, 1980;Chessman, 1984;Ganey et al., 1993;Amey and Grigg, 1995;Wolf and Walsberg, 1996;Gilead and Berry, 2001;Buttermer and Thomas, 2003;Tirado et al., 2007). EWL in E. miletus and A. chevrieri increased when the temperature increased, the maximal EWL at 35 1C was 4.78 mg H 2 O/g h in E. miletus and 5.92 mg H 2 O/g h in A. chevrieri. ...
Evaporative water loss (EWL) and energy metabolism were measured at different temperatures in Eothenomys miletus and Apodemus chevrieri in dry air. The thermal neutral zone (TNZ) of E. miletus was 22.5–30°C and that of A. chevrieri was 20–27.5°C. Mean body temperatures of the two species were 35.75±0.5 and 36.54±0.61°C. Basal metabolic rates (BMR) were 1.92±0.17 and 2.7±0.5mlO2/gh, respectively. Average minimum thermal conductance (Cm) were 0.23±0.08 and 0.25±0.06mlO2/gh°C. EWL in E. miletus and A. chevrieri increased with the increase in temperature; the maximal EWL at 35°C was 4.78±0.6mgH2O/gh in E. miletus, and 5.92±0.43mgH2O/gh in A. chevrieri. Percentage of evaporative heat loss to total heat production (EHL/HP) increased with the increase in temperature; the maximal EHL/HP was 22.45% at 30°C in E. miletus, and in A. chevrieri it was 19.96% at 27.5°C. The results may reflect features of small rodents in the Hengduan mountains region: both E. miletus and A. chevrieri have high levels of BMR and high levels of total thermal conductance, compared with the predicted values based on their body masses, while their body temperatures are relatively low. EWL plays an important role in temperature regulation.
... Furthermore, data can now be transmitted from an animal to an orbiting satellite, thereby allowing data capture over periods of months while the animals traverse thousands of miles (see Fedak, in this symposium for a discussion of the opportunities and constraints of such systems). Miniaturization of transmitters and data loggers also permits investigation of previously unex-plored variables, such as the patterns of exhaled temperature and respiratory and cutaneous evaporative water loss in free-flying pigeons (Michaeli and Pinshow, 2001). These measures can be integrated with more ''traditional'' methodologies such as careful mass balance studies (Giladi and Pinshow, 1999) to provide a detailed evaluation of homeostatic regulation in the field. ...
Over the past decades, comparative and ecological physiologists have successfully described many won- drous ways in which organisms are specialized for life in a variety of habitats. However, most of these inves- tigations were done in the laboratory, where both an- imals and their environments are under control and manipulable. An important focus of contemporary comparative and ecological physiology is to explore physiological function under natural conditions with ecological con- text in mind. The impetus for this has come from two directions. First, advances in technology and method- ology have provided opportunities for addressing an ever-expanding array of physiological questions in wild animals. Second, conceptual advances have in- spired new sorts of questions, and an understanding of physiology in the field continues to contribute to the deepening interplay between physiologists, ecologists, and evolutionary biologists. ETHODOLOGICAL ADVANCES Methodological advances include both the develop- ment of new technologies and the application of exist- ing approaches to new questions. Implanted transmitters that relay information about body temperature and heart rate have been used for many years in free-living ani- mals. However, these approaches continue to be refined
Turbinals are bony or cartilaginous structures that are present in the nasal cavity of most tetrapods. They are involved in key functions such as olfaction, heat, and moisture conservation, as well as protection of the respiratory tract. Despite recent studies that challenged long‐standing hypotheses about their physiological and genomic correlation, turbinals remain largely unexplored, particularly for non‐mammalian species. Herein, we review and synthesise the current knowledge of turbinals using an integrative approach that includes comparative anatomy, physiology, histology and genomics. In addition, we provide synonyms and correspondences of tetrapod turbinals from about 80 publications. This work represents a first step towards drawing hypotheses of homology for the whole clade, and provides a strong basis to develop new research avenues.
Osmoregulation refers to the mechanism by which birds regulate water and electrolyte levels in their bodies. In this chapter, I explain the various ways that birds obtain water, including drinking water, water in foods they ingest, and water produced by metabolic process. Birds also continuously lose water, and those processes, including respiration, cutaneous water loss, and excretion, are also explained. Birds can alter the amount of water lost in those different ways, and I explain how that occurs. The anatomy of the avian kidney is described in detail, including how avian kidneys differ from mammalian kidneys and the anatomy of the functional unit of the kidney—the nephron. The various functions of the kidneys are described, including filtration, excretion, secretion, and absorption. The process by which avian kidneys can increase or decrease the amount of water lost as urine is explained, including the roles of arginine vasotocin and proteins called aquaporins. Also explained are the roles of the cloaca and lower intestine in avian osmoregulation. Nectar-feeding birds ingest large amounts of water, and the ways by which they eliminate excess water are described. How and why birds excrete nitrogenous wastes as uric acid is explained, and the chapter closes with a description of the structure and function of avian salt glands.
The nasal passage performs multiple functions in amniotes, including olfaction and thermoregulation. These functions would have been present in extinct animals as well. However, fossils preserve only low‐resolution versions of the nasal passage due to loss of soft‐tissue structures after death. To test the effects of these lower resolution models on interpretations of nasal physiology, we performed a broadly comparative analysis of the nasal passages in extant diapsid representatives, e.g., alligator, turkey, ostrich, iguana, and a monitor lizard. Using computational fluid dynamics, we simulated airflow through 3D reconstructed models of the different nasal passages and compared these soft‐tissue‐bounded results to similar analyses of the same airways under the lower‐resolution limits imposed by fossilization. Airflow patterns in these bony‐bounded airways were more homogeneous and slower flowing than those of their soft‐tissue counterparts. These data indicate that bony‐bounded airway reconstructions of extinct animal nasal passages are far too conservative and place overly restrictive physiological limitations on extinct species. In spite of the diverse array of nasal passage shapes, distinct similarities in airflow were observed, including consistent areas of nasal passage constriction such as the junction of the olfactory region and main airway. These nasal constrictions can reasonably be inferred to have been present in extinct taxa such as dinosaurs.
Turbinals are bony or cartilaginous structures that are present in the nasal cavity of most tetrapods. They are involved in key functions such as olfaction, heat, and moisture conservation, as well as protection of the respiratory tract. Despite recent studies that challenged long standing hypotheses about their physiological and genomics correlation, turbinals remain largely unexplored. This is especially true for non-mammalian species. We reviewed and synthesized the current knowledge of turbinals by an integrative approach that includes comparative anatomy, physiology, histology and genomics. This provides a strong basis to develop new research avenues. In addition, we provide synonyms and correspondences of turbinals at the scale of tetrapods from about 80 publications. This work represents a first step towards drawing hypotheses of homology for the whole clade.
We tested the aerodynamic function of nasal conchae in birds using CT data from an adult male wild turkey (Meleagris gallopavo) to construct 3D models of its nasal passage. A series of digital "turbinectomies" were performed on these models and computational fluid dynamic analyses were performed to simulate resting inspiration. Models with turbinates removed were compared to the original, unmodified control airway. Results revealed that the four conchae found in turkeys, along with the crista nasalis, alter the flow of inspired air in ways that can be considered baffle-like. However, these baffle-like functions were remarkably limited in their areal extent, indicating that avian conchae are more functionally independent than originally hypothesized. Our analysis revealed that the conchae of birds are efficient baffles that-along with potential heat and moisture transfer-serve to efficiently move air to specific regions of the nasal passage. This alternate function of conchae has implications for their evolution in birds and other amniotes.
The evaporative water loss (WEL) and energy metabolism were measured in different temperatures in Eothenomys miletus and Apodemus chevrieri in laboratory. The thermal neutral zone (TNZ) of Eothenomys miktus was 22.5 - 30°C and of Apodemus chevrkri was 25 -30°C. Mean body temperature were for two species were 36.12°C and 36.17°C. Basal metabolic rates (BMR) were 2. 99 ±0.48ml O 2/g· h and 4.24 ±0.50ml O 2/g ·h, respectively. Average minimum thermal conductance (C m) was 0.26 ±0.038 ml O 2/g· h· t and 0.32 ±0.034 ml O 2/g ·h· °C. Evaporative water loss in E. miletus and A. chevrieri increased when the temperature enhanced, the maximal evaporative water loss was 10.32 mg H 2O/ g· h in 30°C in E. miletus, and was 14.57mg H 2O/g· h in 35 tin A. chevrkri. Percentage of evaporative heat loss to total heat production (EHL/HP) increased when the temperature enhanced, the maximal EHL/HP was 34. 6% in 30°C in E. miktus, and in A. chevrkri was 37. 5% in 35°C. The results may reflect features of small rodents in the Hengduan mountains region; both Eothenomys miktus and Apodemus chevrieri have high levels of basal metabolic rate and high levels of total thermal conductance, compared with the predicted values based on their body masses while their body temperatures are relatively low. Evaporative water loss plays an important role in temperature regulation.
A common perception is that desert birds experience greater extremes of heat and aridity than their mammalian counterparts, in part, because birds do not use burrows as a refuge from the desert envi- ronment. We report observations of Dunn's Larks (Er- emalauda dunni), Bar-tailed Desert Larks (Ammo- manes cincturus), Black-crowned Finch Larks (Ere- mopterix nigriceps), and Hoopoe Larks (Alaemon alaudipes) using burrows of the large herbivorous liz- ard Uromastyx aegypticus as thermal refugia during hot summer days in the Arabian Desert. Continuous recordings of shade air temperature (T,), soil surface temperature (T,,,,), burrow air temperature (Ta_burrow), and burrow substrate temperature (TsubsVate) showed that T surface exceeded 60°C on most days. T, typically ex- ceeded 45°C whereas Ta_burrow was around 41°C during midday. Calculations of total evaporative water loss at different temperatures indicated that Hoopoe Larks can potentially reduce their water loss by as much as 81% by sheltering in Uromastyx burrows during the hottest periods of the summer day.
Migratory birds deposit fat and protein before passing ecological barriers and must economize these during such crossings. Birds crossing the western Sahara during autumn face a trade-off between cold and humid air along with head winds at high altitudes versus warm and dry air along with tail winds at low altitudes. Since water loss rate increases with temperature, migrants should avoid warm and dry air to save water and hence fly at high altitudes. By quantifying nocturnal songbird migration across the western Sahara with radar, we found that more than 60% of the songbirds migrated below 1000 m above ground level. Thus, the majority of songbirds performed sustained migratory flights in much warmer and drier conditions than predicted (weighted means: 30 °C; relative humidity: 27%; water vapour density: 7.8 g/m3). Based on the metabolically available water from fat and protein catabolism, we estimated the maximum possible overall water loss rate of a flying model bird, the garden warbler, Sylvia borin, for the entire Sahara crossing at 0.29 g/h. This is considerably lower than water loss rates for the same model bird passing our study site, 0.62 g/h at 30 °C, based on applied calculations of physiological studies. Our results clearly show that migrating songbirds can fly at much higher temperatures, and have considerably lower water loss rates, than predicted. This new insight based on observations under natural conditions will have substantial impact on the development of new physiological models for birds and other animals with restricted access to water.
Birds from deserts generally have lower total evaporative water loss (TEWL), the sum of cutaneous (CWL) and respiratory water loss (RWL), than species from mesic areas. We investigated the role of CWL and RWL as a function of air temperature (T(a)) in hoopoe larks (Alaemon alaudipes) and Dunn's larks (Eremalauda dunni) from the Arabian Desert and skylarks (Alauda arvensis) and woodlarks (Lullula arborea) from temperate mesic grasslands. The proportional contribution of CWL to TEWL in all larks at moderate T(a) ranged from 50% to 70%. At high T(a) (40 degrees -45 degrees C), larks enhanced CWL by only 45%-78% and relied on an increase in RWL by 676%-2,733% for evaporative cooling. Surface-specific CWL at 25 degrees C was 29% lower in the arid-zone species than in the mesic larks. When acclimated to constant T(a), 15 degrees C-acclimated hoopoe larks increased CWL by 22% compared with 35 degrees C-acclimated birds, but the other species did not change CWL. This study is consistent with the hypothesis that larks from deserts have a reduced CWL at moderate and low T(a) but provided no support for the hypothesis that at high T(a) larks from arid regions rely more on CWL than larks from mesic environments. Interspecific differences in CWL cannot be attributed to acclimation to environmental temperature and are possibly the result of genetic differences due to natural selection or of phenotypically plastic responses to divergent environments during ontogeny.
Exhaled air temperature (T (exh)) has a paramount effect on respiratory water loss during flight. For migratory birds, low T (exh) potentially reduces water loss and increases flight range. However, only three studies provide empirical data on T (exh) during flight. The aim of this study was to record T (exh) of birds during rest and flight at a range of controlled ambient temperatures (T (amb)). One wigeon and two teal flew a total of 20 times in a wind tunnel at T (amb) ranging from 1 degrees to 24 degrees C. T (exh) during flight did not differ between the two species and was strongly correlated with T (amb) (T (exh)=1.036 T (amb) + 13.426; R2=0.58). In addition, body temperature had a weak positive effect on T (exh). At a given T (amb), T (exh )was about 5 degrees C. higher during flight than at rest.
Water imbalance during flight is considered to be a potentially limiting factor for flight ranges in migrating birds, but empirical data are scarce. We studied flights under controlled ambient conditions with rose-colored starlings in a wind tunnel. In one experiment, we measured water fluxes with stable isotopes at a range of flight speeds (9-14 m s(-1)) at constant temperature (15 degrees C). In a second experiment, we measured evaporation rates at variable ambient temperatures (Ta = 5 deg -27 deg C) but constant speed (12 m s(-1)). During all flights, the birds experienced a net water loss. On average, water influx was 0.98 g h(-1) (SD = 0.16; n = 8), and water efflux was 1.29 g h(-1) (SD = 0.14; n = 8), irrespective of flight speed. Evaporation was related to temperature in a biphasic pattern. At temperatures below 18.2 degrees C, net evaporation was constant at 0.36 g h(-1) (SD = 0.18; n = 10), rising at higher temperatures with a slope of 0.11 per degree to about 1.5 g h(-1) at 27 degrees C. We calculated the relative proportion of dry and evaporative heat loss during flight. Evaporative heat loss at Ta < 18.2 deg C was 14% of total heat production during flight, and dry heat loss accounted for 84%. At higher temperatures, evaporative heat loss increased linearly with T(a) to about 25% at 27 degrees C. Our data suggest that for prolonged flights, rose-colored starlings should adopt behavioral water-saving strategies and that they cannot complete their annual migration without stopovers to replenish their water reserves.
Respiratory water loss in Starlings (Sturnus vulgaris) at rest and during flight at ambient temperatures (T(amb)) between 6 and 25 degrees C was calculated from respiratory airflow and exhaled air temperature. At rest, breathing frequency f (1.4+/-0.3 Hz) and tidal volume Vt (1.9+/-0.4 ml) were independent of T(amb), but negatively correlated with each other. Mean ventilation at rest was 156+/-28 ml min(-1) at all T(amb). Exhaled air temperature (T(exh)) at rest increased with T(amb) (T(exh) = 0.92.T(amb)+12.45). Respiratory water loss at rest averaged 0.18+/-0.09 ml h(-1) irrespective of T(amb). In flying Starlings f was 4.0+/-0.4 Hz and independent of T(amb). Vt during flight averaged 3.6+/-0.4 ml and increased with T(amb) (Vt = 0.06.T(amb)+2.83) as, correspondingly, did ventilation. T(exh) during flight increased with T(amb) (T(exh) = 0.85.T(amb)+17.29). Respiratory water loss during flight (average REWL(f) = 0.74+/-0.22 ml h(-1)) was significantly higher than at rest and increased with T(amb). Our measurements suggest that respiratory evaporation accounts for most water loss in flying Starlings and increases more than cutaneous evaporation with rising ambient temperature.
During level flight at 10 m.s−1 in a wind tunnel, white-necked ravens (Corvus cryptoleucus, mass 0·48 kg) exhibited an increase in body temperature to steady-state levels as high as 45 °C, exceeding resting levels by nearly 3 °C. This reflects the storage of up to half of the metabolic heat produced (Hp) during 5 min of flight. During steady-state flight, body heat was dissipated in part by respiratory evaporation and convection (13–40% of Hp) evoked by increases in ventilation proportional to body temperature. Remaining heat was lost by cutaneous evaporation (10 % of Hp) as well as by radiation and convection from the external body surface. The results suggest strategies that might be used by ravens during flight under desert conditions.
Direct measurements of ventilatory parameters have been employed in a study of ventilatory adjustments and changes in expired gas composition during heat stress in the greater flamingo, Phoenicopterus ruber. At thermoneutrality = 39.5 C) average resting values were breathing rate (f) 9.6∙ min⁻¹, tidal volume 40.4∙ ml∙ kg⁻¹, ventilation 382.6 ∙ ml ∙ min ⁻¹ ∙ kg⁻¹, oxygen uptake 1.03∙ml O₂STP. g⁻¹∙ h⁻¹. The f is lower and all other parameters higher than values predicted from allometric equations, and averaged 40.3 mm Hg and 108.3 mm Hg. During rapid shallow panting at 40 C < < 42 C, f increased 23 times, was reduced to 15% of normal and closely matched the tracheal dead space, and VI increased 3-3.5 times. The rapid shallow breathing during panting was interrupted at regular intervals by brief sequences of deeper breaths (flush outs). The importance of the described panting pattern for thermal and respiratory homeostasis is discussed.
This study examines metabolic changes occurring during short to endurance flights and during subsequent recovery in free-flying pigeons, in particular the change towards lipid utilization with increasing flight duration, lipid supply to the flight muscles, protein utilization and the time needed to metabolically recover. Eight plasma metabolite concentrations were measured in homing pigeons released from sites 20–200 km from the loft (0.3–4.8 h flight duration) just after landing and after keeping birds fasting at rest for 30 and 60 min, respectively, after their return. Birds kept in the loft fasting at rest were used as controls. Plasma free fatty acid and glycerol concentrations increased rapidly with flight duration and leveled off after about 1.5 h. This indicates a marked change towards a high and stable lipid utilization from adipose tissues within 1–2 h of flight. Plasma triglyceride levels and very-low-density lipoproteins were decreased after short flights, but subsequently regained or surpassed fasting levels at rest. This indicates that re-esterification of free fatty acids and delivery as very-low-density lipoproteins to the flight muscles to circumvent constraints of fatty acid supply, as described previously for small passerines, is not as significant in the pigeon which has a much lower mass-specific energy rate. An initial increase in plasma glucose levels and a transient decrease to fasting levels at rest was observed and may reflect the initial use and subsequent exhaustion of glycogen stores. Contrary to other birds and mammals, -hydroxy-butyrate levels increased markedly with flight duration. This may suggest a more important sparing of carbohydrates and protein as gluconeogenic precursors in the pigeon than in other species. Plasma uric acid levels increased linearly up to about 4 h flight duration. This indicates an accelerated protein breakdown during flight which may primarily serve to deliver amino acids as glucogenic precursors and citrate cycle intermediates. With increasing flight duration, the energy sources change from an initial phase based primarily on carbohydrates to a lipid-based endurance phase. It is discussed whether this metabolic change depends on the level of power output or the performed work (energy spent) since the start of flight. During the first hour of recovery, most metabolites reached or approached fasting levels at rest, indicating a marked reduction in lipolysis and protein breakdown. -hydroxy-butyrate levels remained at flight levels and glucose levels increased slightly, indicating a restoration of glycogen stores.
The temperature of expired air at the external nares of black-tailed prairie dogs (Cynomys ludovicianus) was measured at inspired (ambient) air temperatures of 25, 30, 35, and 40 C, and over a broad range of humidities at each temperature. Expired air temperature was positively related to inspired air temperature and humidity; comparisons with published data for banner-tail kangaroo rats (Dipodomys spectabilis), deer mice (Peromyscus maniculatus), house mice (Mus musculus), and Australian hopping mice (Notomys alexis) showed similarities and differences among coefficients of multiple linear regressions describing analogous relationships. Simulations for a hypothetical mammal suggested how differences in the recovery of respiratory heat and water in nasal passages, and the loss of respiratory heat and water from the nose, should be affected by different relationships between the temperature of expired air and the temperature and humidity of inspired air.
The reversed sexual size dimorphism of prairie falcons is near the extreme found among raptorial birds. Mean basal metabolic rate (BMR) for males (390.2 ± 15.0 ml O₂/h) and females (504.8 ± 23.3 ml O₂/h) and mass-specific metabolism (0.79 ± 0.05 ml O₂/g h and 0.67 ± 0.03 ml O₂/g h, respectively) differ significantly between sexes. Females have a slightly broader thermal neutral zone (TNZ) than males; the upper critical temperature () is ∼ 35 C for both sexes, and the lower critical temperature () is 19 and 22 C, respectively. Below the mass-specific rate of heat loss is the same in both sexes; the males' mean mass-specific conductance is 81% of the allometrically predicted value, and the females' is 86%. Mass-specific conductance of males diminishes more than that of females as ambient temperature () decreases. Mean tidal volumes and mean minute volumes () are smaller in males than in females, but ventilatory patterns are similar for the sexes. Mean frequency and mean are minimal near and increase sharply within the TNZ as increases. Total evaporative water loss also increases sharply within the TNZ. Both respiratory and cutaneous evaporative water loss contribute to the increase, with cutaneous water loss accounting for 60%-75% of the total water loss in both sexes. At high ventilation frequencies, exhaled air is not saturated with water vapor.
Complex nasal turbinal bones are associated with reduction of respiratory water loss in desert mammals and have previously been described as an adaptation to xeric conditions. However, complex turbinates are found in vertually all mammals. Experimental data presented here indicate that turbinates also substantially reduce respiratory water loss in five species of small mammals from relatively mesic environments. The data support the conclusion that turbinates did not evolve primarily as an adaptation to particular environmental conditions, but in relation to high ventilation rates, typical of all mammals. Complex turbinates appear to be an ancient attribute of mammals and may have originated among the therapsid ancestors of mammals, in relation to elevated ventilation rates and the evolution of endothermy. -Author
The thermal and respiratory physiology of the Spinifex Pigeon (Geophaps plumifera) is generally similar to that expected for a 90-g nonpasserine bird. The body temperature is 40.5 to 41.8°C except during thermal stress. The thermoneutral zone extends from about 35 to 45°C. The basal metabolic rate (0.85 ml O2 g-1 hr-1) is about 68% of the predicted nonpasserine value and 75% of the rate expected for a pigeon. Metabolic rate increases at and . Dry thermal conductance is constant at 1.5 J g-1 hr-1 ⚬C-1 for . Evaporative water loss increases exponentially with Ta from <1 mg g-1 hr-1 at 0°C to >20 mg g-1 hr-1 at . A number of physiological characteristics contribute to the remarkable thermal tolerance by Spinifex Pigeons of high ambient temperatures. (1) The metabolic heat production is low. (2) The pigeons become hyperthermic (Tb=43.4⚬C at , and this facilitates nonevaporative heat loss. (3) The dry thermal conductance increases three- to fivefold at elevated Ta (>30°C), facilitating nonevaporative heat loss. (4) Evaporative heat loss dissipates more than 100% of the metabolic heat production at . Expired air temperatures are substantially lower than Tb at low Ta's; this reduces the respiratory evaporative water loss (REWL). The REWL increases exponentially with Ta, from about 0.30 mg g-1 hr-1 (0°C) to 1.0 (40°C). REWL is about 20% of total EWL, at all Ta's. Cutaneous EWL is about 80% of the total evaporative water loss. It increases from about 0.75 mg g-1 hr-1 (0°C) to 3.5 (40°C). The mechanism for increasing cutaneous evaporative water loss at high Ta is not clear.
Eight homing pigeons (Columba livia) were flown distances of 90 and 320 km with and without transmitters (weighing either 2.5% or 5.0% of the pigeon's body mass, MB) mounted on a back harness. Flight times in April through June for the 90-km distance were 60 min without a transmitter or harness, 69 min with a harness alone and about 76 min with a harness and transmitter (weighing either 2.5% or 5.0% of MB). Flight times for the 320-km distance were 4 hr 16 min for the controls and 5 hr 35 min for the two fastest pigeons wearing a harness and transmitter weighing 2.5% of MB. The results show that on 90-km flights harnesses alone slow birds by 15% and harnesses and transmitters (≤ 5%MB) slow birds 25 to 28%; on 320-km flights harnesses and transmitters slow birds >31%. Moreover, on the 320-km flights, CO2 production of the pigeons (measured with the doubly-labeled water method) was 41 to 52% higher per hour when encumbered with a transmitter and harness. Thus, encumbered pigeons produced 85 to 100% more total CO2 covering the 320-km distance. Therefore, high performance homing pigeons work substantially harder and longer during a long distance flight when wearing harnesses and transmitters.
Dehydration tolerance in mammals is associated with the degree to which an animal is able to maintain plasma volume. During thermal dehydration, rock pigeons (Columba livia), quail (Coturnix coturnix japonica), and white-necked ravens (Corvus cryptoleucus) maintained nearly constant volumes despite mean body mass losses of 17%, 15%, and 13%, respectively. During flight-incurred dehydration in tippler pigeons (C. livia), no changes occurred in plasma volume although the birds lost 6%-10% of their preflight body mass. Thus, dehydrated birds were found to be excellent plasma volume conservers, like the most xericadapted mammal species. We suggest that plasma volume conservation in birds is an adaptation associated with high heat loads incurred during flight. In contrast, plasma conservation in mammals is associated with their ability to inhabit arid environments.
SUMMARY 1. Five pigeons were trained to fly in a boundary-layer wind-tunnel at a velocity of 10 m s"1 for at least 10 min, and a number of respiratory and cardiovascular variables were recorded. For comparison, heart rate, respira- tory frequency and E.M.G. from the pectoralis major muscles were also recorded, using radio-telemetry, from free-flying pigeons. 2. For the flights in the wind tunnel there were immediate increases in respiratory frequency and heart rate upon take-off; these variables con- tinued to increase during the flight, eventually becoming on average 411 breaths min"1 (20 x resting) and 670 beats min"1 (6 x resting) respectively. There was a 1:1 relationship between ventilation and wing beat. Oxygen uptake and carbon dioxide production reached their highest values of 12-5 x and 14-4 x resting respectively within 1 min of take-off and then declined to steady levels of 200 ml kg"1 min S.T.P.D. (10 x resting) and 184 ml kg"1 min S.T.P.D. (10-7 x resting) 4 min after take-off. If allowances are made for the weight and drag of the KOi mask and tubes, these stable values are at least 12% higher than would occur in an unloaded bird. Body temperature rose steadily after take-off, reaching a stable value of 43-3 °C, which was 2 °C above resting, after 6 min of flight. There was a i-8 x rise in a — v0 content difference and little change in cardiac stroke volume during flight, so that the rise in heart rate was the major factor in transporting the extra O2 to the active muscles. Respiratory quotient rose from 0-85 at rest to 099, 30 s after take off, and then fell to 0-92 after 7 min of flight. Blood lactate rose to 59-8 mg% (6-5 x its resting value). 3. Comparisons with the free-flying birds indicated that the pattern of flight in the wind tunnel was somewhat abnormal, especially at the beginning of a flight, and this may account for the value of VQ being higher at the start of a flight and then declining to a steady value as the flight progressed. 4. Upon landing, heart rate, T^, T^X)i and body temperature began to fall immediately, and within 2 min, heart rate, V'Oi and T^ot had returned to the 'tunnel on' resting values. Respiratory frequency increased upon landing and its decline closely matched the fall in body temperature. R.Q. rose above unity immediately upon landing as CO2 was removed in excess of its
We measured carbon dioxide production and water efflux of 12 tippler pigeons (Columba spp.) during seven experimental flights using the doubly labeled water (DLW) method. Prior to the experiment birds were randomly assigned to one of two groups. One group flew as controls (no load or harness) on all seven flights. The other group wore a harness on two flights, a dorsal load/harness package (weighing about 5% of a bird's mass) on two flights, and they were without a load in three flights. Plight duration of pigeons with only a harness and with a dorsal load/harness package was 21 and 26% less, respectively, than the controls. Pigeons wearing a harness, or wearing a dorsal load/harness package lost water 50-90%, and 57-100% faster, respectively, than control pigeons. The mean CO, production of pigeons wearing a harness or a load/harness package was not significantly different than pigeons without a harness or load. The small sample sizes and large variability in DLW measurements precluded a good test of the energetic cost of flying with a harness and dorsal load.
Oxygen consumption of 2 budgerigars (Melopsittacus undulatus) was measured during level, ascending and descending flights lasting 5–20 min. in a wind-tunnel at speeds between 19 and 48 km./hr. In level flight oxygen consumption was lowest at 35 km./hr. with a mean value of 21·9 ml. (g. hr.)−1 or 12·8 times the standard value calculated for these birds (weight = 35 g.). At a given speed oxygen consumption was highest for ascending flight and lowest for descending flight. Carbon dioxide production was measured on one bird flying level at 35 km./hr. for 20 min. The ratio of carbon dioxide production to oxygen consumption was 0·780, indicating that the bird was oxidizing primarily fat. The efficiencies of level, ascending and descending flight are discussed. The measurements indicate that for the budgerigar 42 km./hr. is the most economical speed for covering distance, and below 27 km./hr. undulating flight is more economical than flight at a constant altitude. Evaporative water loss in level flight was measured in two birds for 20 min. at 35 km./hr. at temperatures of 18–20° and 29–31° C. At 36–37° C. the birds became overheated and would not fly for as long as 20 min. Evaporative water loss at 18–20° C. was 20·4 mg. (g. hr.)−1. It increased to 63·9 mg. (g. hr.)−1 at 36–37° C. After accounting for metabolic water production and faecal water loss, budgerigars flying at 18–20° C. had a net water loss of 11 mg. (g. hr.)−1. At this temperature 15 % of the estimated heat production in flight was lost by evaporation of water, while 47% was lost by evaporation of water at 36–37° C. Lung ventilation, tidal volume and partial pressure of carbon dioxide in expired air were estimated for flying budgerigars from evaporative water-loss data. In level flight at 18–20° C and 35 km./hr. these quantities had values of 398 ml. (g. hr.)−1, 0·033 ml. (g. breath)−1 and 37 mm. Hg. respectively. Respiratory rate in level flight was measured in 2 birds at speeds between 19 and 48 km./hr. Respiratory rate depended on speed and was lowest at 35 km./hr. Since wing-beat frequency was constant at 840 beats/min. at all speeds, respiratory rate and wing-beat frequency were not synchronized. Published data and analysis of dimensional relations of birds suggest that in birds the size of a budgerigar or smaller a respiratory rate equal to the wing-beat frequency would be too high for efficient ventilation of the lungs. Birds the size of a pigeon or larger probably have synchronous wing beats and respirations.
Data pooling is an analytic procedure in which multiple samples of an individual's behaviour are treated as independent events. Although common in animal behaviour research, data pooling has been discredited because it may violate statistical assumptions. Four data sets were analysed in both their pooled and unpooled forms. Pooling did not bias results provided that either intra-subject variance exceeded between-subject variance or Ns were equal. Between-groups tests of significance were affected in the same way as descriptive statistics, and as long as intra-subject variance exceeded between-subject variance, pooling did not increase the probability of a type 1 error. Utmost care must be taken to sample individuals from populations and behaviour from those individuals in an unbiased manner.
1.1. Virtually all of our knowledgeof avian evaporative water loss is based on open flow determinations, and several generalizations concerned with water loss are based on insufficient information because of limitations in this technique.2.2. Some characteristics of the open flow system as they relate to measurement of avian evaporative water loss are examined, and a new formula for predicting relative humidity in the respiratory chamber is presented and tested.3.3. Air flow rate (and the resultant humidity in the chamber) influences the effectiveness of evaporative cooling in open flow determinations. Higher air flow rates (lower humidities) permit many avain species to dissipate all of their metabolic heat through evaporative cooling.4.4. A wide variety of birds were capable of maintaining their body temperatures below environmental temperatures of 44°–46°C for periods ranging from 1 to 4 hr through evaporative cooling.
Core temperatureT
c, breast temperatureT
s–br and leg temperatureT
s–1 were measured simultaneously in pigeons during rest and flight in a wind tunnel, using thermistors.MeanT
c at rest is 39.80.7C and is independent of ambient temperatureT
a (10–30C). In the first minutes of flight,T
c increases to 1.5–3.0C above resting level and remains at this higher level. This hyperthermia increases withT
a (v=const.). It isconstant in the lowT
a range (10.6–13.9C) at flight speeds v ranging from 10–18 m s–1 and normal body mass, but increases with v and elevated body mass in the highT
a range (23.7–28.8C).
T
s–1 is adapted toT
a at rest and increases in flight up to 3–4C belowT
c. This increase inT
s–1 is linear toT
a.
T
s–br is always lower thanT
c, in extreme cases reaching restingT
c in flight.
Body water conservation is important in flying birds because the very high metabolic demands and heat dissipation requirements during flight depend on plasma-volume integrity. Wind tunnel experiments and theoretical model predictions show that evaporative water loss (EWL) depends on air temperature (T
a) and water vapor density (ρa), but these relationships have not been examined in free-flying birds. The contribution of excretory water loss to the total water loss of a flying bird is thought to be negligible but this assumption is untested. To study the dependence of water losses on environmental conditions in free-flying birds and to quantify the contribution of excretory water loss to total water loss, we estimated evaporative and excretory water losses in 16 trained, free-flying tippler pigeons (Columba livia, 250–340 g). We collected excreta by attaching a light latex, water-impermeable receptacle around each bird's vent. By gravimetry, we measured evaporative and excretory water losses of birds for eight flights at different T
as and compared flying to resting (control) birds for two of these flights. EWL was constant with respect to T
a when less than 15 °C, and increased with increasing T
a above 19 °C, indicating that evaporative cooling was invoked when the heat load increased. EWL increased with increasing ρa, possibly due to the strong correlation between ρa and T
a. Excretory water loss was independent of ρa or T
a and averaged almost 10% of the total water loss. Measurements of EWL made on pigeons during wind tunnel experiments and previous free-flight studies are consistent with our free-flight measurements made at similar T
as.
The influence of flight and flight duration on 13 blood parameters was studied in homing pigeons which returned after 2–22 h of flight from release sites 113–620 km away. The haematocrit value decreased from 54.4% in controls to 51.0% in the flown birds. A lowered haematocrit overproportionately improves blood flow. The plasma concentrations of glucose and l(+)-lactate did not differ between experimental and control birds. This is compatible with the idea that carbohydrates are utilized as fuel mainly in the initial phase of flight. Plasma free fatty acid levels were significantly increased during flight and triglyceride concentrations gradually decreased with progressive flight duration. These findings support the view that lipids are the main energy source during flight. Plasma uric acid concentrations were increased two- to fourfold in flown birds. Urea levels gradually rose with flight duration to 400% of controls. Plasma protein concentration was lowered in flown pigeons. These results hint to an increased protein degradation during flight. Na+, K+, Ca2+, and Mg2+ levels in the plasma of the flown pigeons were not significantly different from control values. This finding together with the urea/uric acid ratio indicates that no severe dehydration occurred in our pigeons during free-range flight.
Pulmonary ventilation (tidal volume, frequency) and oxygen content of expired air were measured in separate flights for 3 species of birds — Evening Grosbeak (Hesperiphona vespertina), Ring-billed Gull (Larus delawarensis), and Black Duck (Anas rubripes). Heart rate was measured in flight or immediately after landing in 12 species.
Respiratory frequency and tidal volume were greater in flight than during rest. As the O2 content of expired air did not change appreciably, the increase in O2 consumption was similar to the increase in ventilation and averaged more than 10 times basal. The influence of body weight on metabolism during flight was similar to that previously observed under basal conditions.
Heart rates during flight (10 species), immediately after landing (12 species), and maximal rates from various authors (15 species) were in close agreement, and were 2–4 times as high as during rest. The heart rate decreased with increasing body weight according to the equation HRf=25.1 BW−0.16 (HR per sec, BW in g). In flight there was much less variation and there was a smaller decrease with increasing weight than during rest. Although the estimated stroke volume and heart size appear larger in birds, the ratio of these functions was similar to that in mammals.
The BMR (6.00 ml O2min–1) and thermal conductance (0.235 ml O2min–1C–1) ofAmazona viridigenalis, a medium sized parrot, are close to allometrically predicted values for nonpasserine birds, but theT
1c of 26.5 C is 8.5 C higher than predicted (Fig. 1). Minimal respiratory frequencies measured in four species of birds average 60% of the rate predicted by a previous equation and yield the relationship, breathsmin–1= 10.3 kg–0.32. Frequencies are very dependent upon the methods used to obtain the data (Fig. 3). Resting values of respiratory parameters are poorly defined in the existing literature, and there are no single resting values within the TNZ analogous to a BMR. Rather values change within, as well as below and above, the TNZ. Minimal values of different parameters occur at differentT
a's, not necessarily within the TNZ (Figs. 2, 4, 5). For clarity, resting respiratory parameters should be reported as standard values, analogous to standard metabolic rates, withT
a specified. In birds the pattern of ventilation (f andV
T) changes asT
a changes resulting in different extraction efficiencies at a given minute volume (Figs. 6, 7). This facilitates adjustment to both changing oxygen demands and changing thermoregulatory needs.
We examined the relationship between body temperature (Tb) of free flying pigeons and ambient water vapor pressure and temperature. Core or near core Tb of pigeons were measured using thermistors inserted into the cloaca and connected to small transmitters mounted on the tail
feathers of free flying tippler pigeons (Columba livia). Wet and dry bulb temperatures were measured using modified transmitters mounted onto free-flying pigeons. These allowed
calculation of relative humidity and hence water vapor pressure at flight altitudes. Mean Tb during flight was 42.0 ± 1.3 °C (n = 16). Paired comparisons of a subset of this data indicated that average in-flight Tb increased significantly by 1.2 ± 0.7 °C (n = 7) over that of birds at rest (t = −4.22, P < 0.05, n = 7) within the first 15 min of takeoff. In addition, there was a small but significant increase in Tb with increasing ambient air (Ta) when individuals on replicate flights (n = 35) were considered. Inclusion of water vapor pressure into the regression model did not improve the correlation between
body temperature and ambient conditions. Flight Tb also increased a small (0.5 °C) but significant amount (t = 2.827, P < 0.05, n = 8) from the beginning to the end of a flight. The small response of Tb to changing flight conditions presumably reflects the efficiency of convection as a heat loss mechanism during sustained
regular flight. The increase in Tb on landing that occurred in some birds was a probable consequence of a sudden reduction in convective heat loss.
Gas exchange was measured in pigeons flying non-stop for at least 60 min in a wind tunnel and using a flow-through respirometry system similar to that of Tucker (1968).1.
O2 consumption (), CO2 release (), respiratory exchange ratio (R) and metabolic rate (MR) show a characteristic time course independent of age, race, body mass, feeding condition, ambient temperature, flight speed and time of the year. and MR decrease slightly (ca. 10%) within the first 10–15 min of flight before reaching a steady state value. decreases continuously with flight time reaching a constant level earliest after 45 min, resulting in a decrease of R.
2.
The absolute values of and MR are dependent on body mass, flight speed, pigeon race and individual differences in flight behaviour, but are independent of ambient temperature in the range between 5–23°C. Mean MR in the optimal speed range between 11–13 m s−1 lies between 30.5–34.2 W or 100.1±5.0 W kg−1.
3.
R seems to decrease with flight time to the steady state level of R≈0.7 (flight duration was not always long enough to prove this statement), indicating a gradual changeover from a fuel rich in carbohydrate to one consisting nearly exclusively of fat. The initial value of R (ca. 1.1–0.84) as well as the time of decay before reaching the steady state level of R≈0.7 depends on the feeding condition and the time of the year.
The results are interpreted and discussed in comparison to other data available on bird flight.
1.
A method of determining the evaporative water and heat loss of pigeons during flight in a wind tunnel from mass loss and gas exchange measurements is described.
2.
At constant flight speed (v=12 m s–1) evaporativ heat lossH
e accounts for the loss of 10–28.5% of the heat produced (heat productionH
p = 0.75 metabolic rate).H
e increases with rising ambient temperatureT
a (7.5–25C).
3.
At constantT
a of 15C, evaporative heat lossH
e has minimum values within the flight speed range of 10 and 14 m s–1, but increases with both higher and lower flight velocities.
4.
The means for regulatingH
e are summarized and discussed with regard to the peculiarities of the pigeon's respiration.
5.
In all cases studied, evaporative water loss exceeds metabolic water production, thus leading to dehydration. The extent of water loss and its consequences for long distance flights as well as the strategies possible for the bird to avoid excessive water loss, are discussed.
6.
Non-evaporative heat lossH
ne decreases with increasingT
a (v=const.=12 m s–1), whereas the efficiency ofH
ne, characterized as thermal conductanceC, is raised.
7.
At constantT
a of 15C,H
ne andC increase with increased flight speed.
8.
The bird's means of influencingC during flight are discussed.
We used tritium-labeled water to measure total body water, water influx (which approximated oxidative water production) and
water efflux in free-flying tippler pigeons (Columba livia) during flights that lasted on average 4.2 h. At experimental air temperatures ranging from 18 to 27 °C, mean water efflux
by evaporation and excretion [6.3 ± 1.3 (SD) ml · h−1, n = 14] exceeded water influx from oxidative water and inspired air (1.4 ± 0.7 ml · h−1, n = 14), and the birds dehydrated at 4.9 ± 0.9 ml · h−1. This was not significantly different from gravimetrically measured mass loss of 6.2 ± 2.1 g · h−1 (t = 1.902, n = 14, P>0.05). This flight-induced dehydration resulted in an increase in plasma osmolality of 4.3 ± 3.0 mosmol · kg−1 · h−1 during flights of 3–4 h. At 27 °C, the increase in plasma osmolality above pre-flight levels (ΔP
osm = 7.6±4.29 mosmol · kg−1 · h−1, n = 6) was significantly higher than that at 18 °C (ΔP
osm = 0.83±2.23 mosmol · kg−1 · h−1, (t = 3.43, n = 6, P < 0.05). Post-flight haematocrit values were on average 1.1% lower than pre-flight levels, suggesting plasma expansion. Water
efflux values during free flight were within 9% of those in the one published field study (Gessaman et al. 1991), and within
the range of values for net water loss determined from mass balance during wind tunnel experiments (Biesel and Nachtigall
1987). Our net water loss rates were substantially higher than those estimated by a simulation model (Carmi et al. 1992) suggesting
some re-evaluation of the model assumptions is required.
Preliminary allometric equations relating avian respiratory variables to body weight permit a series of tentative statements regarding avian respiration which were hitherto impossible. Comparisons of avian and mammalian equations reveal dimensional similarities and differences in the two distinct respiratory systems. The avian lung is similar in weight but has a proportionately smaller air space than its mammalian counterpart. The total volume of the avian respiratory system is much greater than that of mammals. Avian tidal volumes are larger than those of mammals, but avian respiratory rates are lower, and avian minute volumes are somewhat less than in comparable sized mammals. Each tidal volume in birds provides air equivalent to a complete turnover of the airspace of the lungs plus trachea. Avian respiration provides a more extensive CO2 washout in the tertiary bronchi exchange areas than occurs in the mammalian alveoli. The amount of oxygen removed from respiratory air in birds is independent of body weight, as it is in mammals, and birds may remove a greater proportion of the oxygen than do mammals.
1.1. Hand-reared acclimated (Acc) and nonacclimated (NAcc) rock pigeons Columba livia were exposed to ambient temperatures (Ta) of 30–65°C and low relative humidities (RH) of 5–35%.2.2. Resting heat production of 3.6 ± 0.7 cal g −1 hr−1 (31.7 W/m2) and 4.9 ± 0.8 cal g −1 hr −1 (43.0 W/m2) were measured in Ace and NAcc pigeons, respectively.3.3. The total evaporative water loss (EWL) was significantly lower (P < 0.05) in Acc compared to NAcc; EWL increase of 0.7 mg H2O per 1°C rise in Ta and 1.35 mg H2O/1°C Ta, respectively, were calculated during heat exposure to 35–60°C Ta.4.4. At 60°C Ta, acclimated pigeons dissipated 304% of heat production as latent heat. In Acc birds body temperature was regulated between 41.2 and 42.0°C within the thermoneutral zone (TNZ) (30–60°C).5.5. In NAcc pigeons the TNZ extends only between 30 and 42°C Ta. When Ta was increased from 35–45°C hyperthermia developed at 0.11°C/1°C increase in Ta.6.6. The heat acclimated pigeon effectively uses cutaneous evaporation instead of panting and gular fluttering for dissipation of both metabolic heat and ambient heat influx.7.7. The significance of the skin and the feather coat in the adaptation of birds to life in the hot deserts is discussed.
Temperature measurements were made on exhaled air of various vertebrates at ambient air temperatures from 12 to 30 °C. In birds the temperature of the exhaled air was closer to the ambient air temperature than to body temperature and in small rodents the exhaled air temperature might be even lower than the temperature of the inhaled air. As air is inhaled, it is warmed and humidified in the upper respiratory tract, and the walls of the passageways are thus cooled. Exhaled air passing over these cool surfaces gives up some of its heat and water. The recondensation of water is quantitatively important, e.g.. at 15 °C, 25% r.h., a cactus wren recovered 74% of the water added to the respiratory air on inhalation. In the kangaroo rat, due to the greater degree of cooling of the exhaled air, 83 % of the water is recovered. Of the heat added on inhalation (warming of air plus heat of vaporization) a major fraction is recovered on exhalation. For example, at 15 °C, 25 % r.h., the cactus wren recovers 75% of the heat added on inhalation, and the kangaroo rat recovers 88 %. In terms of the simultaneous metabolic heat production, these amounts constitute a savings of 16.1 % of the total metabolic heat production, heat that would be lost to the exterior if air were exhaled at body temperature and saturated.
Oxygen consumption (V̇o2, tidal volume (vt), and respiratory frequency (f) were measured in the passeriform fish crow, Corvus ossifragus (mass 0.274 kg), in dry air at temperatures of 5–25 °C. Ventilation (V̇i) was calculated as f · Vt, and oxygen extraction as the fraction of available oxygen removed from respiratory air.V̇o2, Vt, f, and V̇i tended to increase with decreasing Ta, while oxygen extraction seemed temperature independent.Mean V̇o2, at 20 °C was similar to the value calculated for a passerine bird. but about twice the value for a nonpasserine bird or a mammal of the same mass. Mean V̇i at 20 C was more than twice as great as in a nonpasserine but only 65% greater than in a mammal. Thus mean O2 extraction at 20 °C was about the same as in the nonpasserine. but substantially higher than in the mammal. The highest measured 02 extraction, about 0.31 at 25 °C, was twice as high as the calculated value for a mammal.These observations confirm the expectation of increased effectiveness of gas exchange in the avian lung, made possible by its arrangement as a through-flow system.
Body and exhaled air temperatures of penguins were measured at ambient air temperatures from − 5 to 27°C. Penguins in an air temperature of 5°C decreased the temperature of their exhaled air to 9°C and thereby reclaimed 81.9% of the water and 83.4% of the heat added to the inhaled air. The heat recovered represents 17.0% of the simultaneous metabolic heat production. Penguins in an air temperature of 5°C and subjected to heat loads increased the temperature of their exhaled air to near that of their body and lost 39.1 cal/L air which is equivalent to 20.4% of their total metabolic heat production. The anatomical site where the majority of the heat and water exchange appears to take place is a common air chamber within the nasal passages of these birds. Alpha-adrenergic neural activity modulating blood flow to the mucosal lining of the nasal passages is postulated as the mechanisms which permits heat and water exchange in cold conditions and heat dissipation during heat loads.
1.1. Studies in respiratory physiology and acid-base balance of panting birds exposed to high Ta s show that flying as well as nonflying birds can use the respiratory system simultaneously for gas exchange and evaporative cooling.2.2. The present study proves that well acclimated hand-reared birds can effectively regulate a normal CO2 level and acid-base status in arterial blood, when exposed to extremely high temperatures (50–60°C).3.3. In many birds practising simple or “flush out” anting, the dead space can be reduced to a volume which is estimated to be approx 15% the volume of the respiratory tract.4.4. These two modes of ventilation, shallow and high-rate, restricted to the nonrespiratory surfaces, may ensure the avoidance of CO2-washout and limit lung ventilation to the volumes needed for oxygen consumption.5.5. This view supports earlier theories, suggesting the existence of physiological shunt mechanisms which operate during thermal panting in birds.
Awake domestic pigeons, either maintained at 22 degrees C (series I) or acutely exposed at 2 degrees C (series II), were studied in a hypobaric chamber at 140 m and at various stages during a 4-week exposure to 4000 m. Steady-state pulmonary ventilation (Vg) and breathing pattern (VT, fr), oxygen consumption (MO2), O2 concentrations and pressures in the arterial (a) and mixed venous blood (v), hematocrit (Ht) and acid-base status in arterial blood, systolic blood pressure and heart frequency (fH) were measured. From these data cardiac output (Vb) and stroke volume (Vs), ventilatory and circulatory requirements (Vg/MO2, Vb/MO2), extraction of O2 from inspired air (EgO2) and blood EbO2), and capacitance coefficient of blood for oxygen (betabo2) were calculated. At 140 m, by comparison with predicted values for mammals of same body weight, pigeons at 22 degrees C extracted more O2 from the inspired gas, with lower fR, larger VT, similar Vg; they extracted O2 from the blood like mammals, with lower fH, larger VS, greater Vb, similar betabO2=70 mumol-L-1-torr-1. Acute exposure to 2 degrees C provoked a two-fold increase in MO2 which was achieved by doubling Vg and increasing O2 extraction from the blood. At 4000 m, in both series, pigeons hyperventilated within the first 30 min, with a resultant hypocapnic alkalosis comparable to that in mammals. Further hyperventilation with consequent greater hypocapnia and increase of arterial PO2 was complete beyond 3 hr. After a few weeks, the pH remained 0.07 above control normoxic value, Ht increased from 45 to 52%, betabO2 reached about 172 mumol-L-1-torr-1. At 2 degrees C, Vb also increased, mainly due to tachycardia.
1.Ventilation frequency, cloacal temperature and EMG of the pectoral muscle have been monitored in budgerigars during flight in a windtunnel at different ambient temperatures.2.Two ventilation patterns were observed: low frequency ventilation (300/min) at ambient temperatures below 26°C (cloacal temperatures below 41·1°C) and a high freqency ventilation (960/min) above 34°C (cloacal temperatures above 42·0°C). At temperatures between these the high frequency was present periodically or superimposed on the low frequency.3.The wing beat frequency was 960/min regardless of the temperature. High frequency ventilation is synchronous with the wing beat, the low frequent ventilation appears to have no systematic relationship to wing beats.4.During high frequency ventilation the bird ventilates through its open beak and the legs are kept hanging down. The open beak may reduce resistance to respiratory air flow.
The rate of evaporative cooling was calculated from the rate of mass loss in starlings (Sturnus vulgaris) during 90 min flights in a wind-tunnel. Evaporative heat loss ranged from 5% of the metabolic rate at -5 degrees C to 19% of the metabolic rate at 29 degrees C. Radiation and convection accounted for the balance of the heat loss. On average, starlings dehydrated during flights at all temperatures above 7 degrees C. The comparison of these results with data from field studies, which indicate that long-distance migrants do not dehydrate, suggests that migrants may maintain water balance by ascending to colder air in which convection carries off most of the heat produced.
A steady-state model, based on a combination of empirical and mechanistic relationships, is developed to predict respiratory water loss from terrestrial vertebrates. Model parameters are evaluated from published data for the banner-tail kangaroo rat (Dipodomys spectabilis). A three-dimensional representation of model behavior is presented, emphasizing the interaction of organismal and environmental variables. The model makes possible the calculation of respiratory water and heat losses for animals in both artificial and natural environments.
Tidal volume (VT), respiration frequency (f) and respiratory evaporation (mre) were measured in the passeriform fish crow, Corvus ossifragus (mass 0.28 kg), during steady state, horizontal, wind-tunnel flight, at air speeds of 7.4-11.0 m-sec-1 and air temperatures (TA) of 12-28 degrees C. Ventilation (V1) of the respiratory system was calculated as f-VT. All parameters were independent of speed. Respiration frequency was independent of TA. VT and V1 were independent of TA below 23 degrees C, but above 23 degrees C increased linearly, as did mre. Oxygen extraction (E), the fraction of available oxygen removed from respiratory system air, was calculated using oxygen consumption data (VO2) reported previously, and VI. E was independent of TA below 23 degrees C, where mean E, similar to that in crows resting at 20 degrees C, was substantially higher than in resting mammals of the same mass. E decreased at higher TA, reflecting hyperventilation accompanying elevated mre. mre accounted for the loss of only 17% of total metabolic heat production (Hp), as calculated from VO2, with a partial efficiency of 25%. Thus most heat loss must follow cutaneous evaporative, or nonevaporative routes.
Core and skin temperature were measured by radiotelemetry in starlings (Sturnus vulgaris) during 30 min flights in a wind tunnel. Core temperature was independent of ambient temperature from 0 to 28 degrees C. The temporal mean of the monitored core temperature during flight was 42-7 degrees C in one bird and 44-0 degrees C in another. These temperatures are 2-4 degrees C higher than the resting temperature in starlings, and are among the highest steady-state temperatures observed in any animal. Skin temperature on the breast was within a few degrees of core temperature. In some locations skin temperature was higher at low ambient temperatures than at intermediate ambient temperatures. An analysis of the data shows that a high core temperature does not function as an aid to head dissipation. On the contrary, insulation is adjusted to maintain a high temperature, presumably because it is necessary for flight. The increase in skin temperature at low ambient temperatures is believed to be a result of a decrease in heat flow through the breast feathers brought about by feather adjustments, to compensate for an unavoidable increase in heat flow in unfeathered or poorly feathered parts of the body.
Using a two-compartment metabolism chamber, we measured oxygen consumption simultaneously with evaporative water loss (EWL) separately from the skin and respiratory tract of pigeons exposed to various air temperatures and humidities. Both respiratory (REWL) and cutaneous (CEWL) water loss increased markedly with increasing air temperature, and latent heat loss through both routes dissipated large fractions of internal heat production during mild heat stress. CEWL as a percentage of total EWL significantly exceeded REWL (60 +/- 1.5%) at thermoneutral air temperatures, and was also a substantial fraction of total EWL at lower and higher temperatures. Both REWL and CEWL were inverse functions (apparently linear) of ambient humidity at 20 and 30 degrees C. These observations verify suggestions by other investigators that CEWL in birds plays a greater role in water balance and in counteracting heat stress than was previously believed.
A steady-state model of the heat and water transfer occurring in the upper respiratory tract of the kangaroo rat, Dipodomys spectabilis, is developed and tested. The model is described by a steady-state energy balance equation in which the rate of energy transfer from a liquid stream (representing the flow of heat and blood from the body core to the nasal region) is equated with the rate of energy transfer by thermal conduction from the nose tip to the environment. All of the variables in the equation except the flow rate of the liquid stream can be either measured directly or estimated from physiological measurements, permitting the solution of the equation for the liquid stream flow rate. After solving for the liquid stream flow rate by using data from three animals, the energy balance equation is used to compute values of energy transfer, expired air temperature, rates of water loss, and efficiency of vapor recovery for a variety of ambient conditions. These computed values are compared with values measured or estimated from physiological measurements on the same three animals, and the equation is thus shown to be internally consistent. To evaluate the model's predictive value, calculated expired air temperatures are compared with measured expired air temperatures of eight additional animals. Finally, the model is used to examine the general dependence of expired air temperature, of rates of water loss, and of efficiency of vapor recovery on ambient conditions.
Pulmonary ventilation and temperature of expired air and of the respiratory passages has been measured by telemetry during flight in the black duck (Anas rubripes) and the respiratory water and heat loss has been calculated.During flight, temperature of expired air was higher than at rest and decreased with decreasing ambient temperatures. Accordingly, respiratory water loss as well as evaporative heat loss decreased at low ambient temperatures, whereas heat loss by warming of the inspired air increased. The data indicated respiratory water loss exceeded metabolic water production except at very low ambient temperatures. In the range between −16 °C to +19 °C, the total respiratory heat loss was fairly constant and amounted to 19% of the heat production. Evidence for the independence of total heat loss and production from changes in ambient temperature during flight is discussed.