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Functional anatomy of the footpad vasculature of dogs: Scanning electron microscopy of vascular corrosion casts
Abstract
Dogs are well adapted to cold climates and they can stand, walk and run on snow and ice for long periods of time. In contrast to the body trunk, which has, dense fur, the paws are more exposed to the cold due to the lack of fur insulation. The extremities have a high surface area-to-volume ratio, so they lose heat very easily. We offer anatomical evidence for a heat-conserving structure associated with dog footpad vasculature. Methylmethacrylate vascular corrosion casts for scanning electron microscopy, Indian ink-injected whole-mount and histological specimens were each prepared, in a series of 16 limbs from four adult dogs. Vascular casts and Indian ink studies showed that abundant venules were arranged around the arteries supplying the pad surface and formed a vein-artery-vein triad, with the peri-arterial venous network intimately related to the arteries. In addition, numerous arteriovenous anastomoses and well-developed venous plexuses were found throughout the dermal vasculature. The triad forms a counter-current heat exchanger. When the footpad is exposed to a cold environment, the counter-current heat exchanger serves to prevent heat loss by recirculating heat back to the body core. Furthermore, the arteriovenous anastomoses shift blood flow, draining blood to the skin surface, and the venous plexuses retain warm blood in the pad surface. Hence, the appropriate temperature for the footpad can be maintained in cold environments. © 2011 The Authors. Veterinary Dermatology.
... Frostbite seems likely to occur in dogs and cats because their paws lack insulation [3,31]. Distal limbs are also more likely to lose heat because, like neonates, they, too, have a large surface area to volume ratio [31]. ...
... Frostbite seems likely to occur in dogs and cats because their paws lack insulation [3,31]. Distal limbs are also more likely to lose heat because, like neonates, they, too, have a large surface area to volume ratio [31]. ...
... Why this is the case has only recently been explored. However, the veterinary literature is rich with reports that document how other species make use of counter-current heat exchange to maintain temperatures at one or more extremities, including the following [31][32][33][34][35][36][37][38][39][40]: ...
The body's ability to maintain a near‐constant thermal set point is critical for survival. Thermoregulation requires coordinated efforts between the hypothalamus, as the body's central control, and the periphery. Peripheral body temperature may be sacrificed at the expense of core body temperature for the good of the whole. When this occurs, the patient may present with palpably cool extremities. Cool extremities are common findings on physical examination when patients have been exposed to hypothermic conditions. The footpad vasculature of dogs provides counter‐current heat exchange that warms cool venous blood that is returning from the limbs to the heart. This is a protective mechanism akin to that which is seen in the ears of rabbits, and the fins, flukes, and tongues of sea life. Pathological conditions may also cause poikilothermy. This chapter discusses three of these: feline arterial thromboembolism (ATE), reversed patent ductus arteriosus (PDA), and shock. All three conditions have the potential to create cooler extremities that may or may not be cyanotic. These findings on physical examination facilitate diagnosis and are logical reflections of the underlying pathophysiology.
... In this study, we found that the dermis layer is composed of two parts: dermal papillae, and another part that is rich in collagen fibres. The dermal papillae and the stratified epithelium layer, which have distinctive honeycomb-like structures at the micro-scale level, make up the epidermis layer; this structure is also found in the paw pad of the Beagle dog (Ninomiya et al., 2011) and in the paw pad of the Clouded leopard (Hubbard et al., 2009). Therefore, it appears that this special micro-structured layer is common in the paw pads of digitigrades, and to the best of our knowledge, has not been studied previously. ...
... Moreover, the cushioning capacity of the epidermis layer plateaued when the Young's modulus of the dermal papillae was lower than 0.04 MPa, as indicated by the material property sensitivity analyses. Indeed, these honeycomblike micro-structures, consisting of stratified epithelium and dermal papillae, have also been found in the paw pads of other digitigrade mammals, such as cats and leopards (Hubbard et al., 2009;Ninomiya et al., 2011), suggesting that this characteristic structure may be desirable for quieter and faster locomotion patterns. ...
... The 1.5-mm-thick slices were washed in distilled water, dehydrated with alcohol and embedded in paraffin for 3 h at 60°C. The paraffin tissue blocks were cut into 5-μm-thick slices and then stained with haematoxylin and eosin and Masson's trichrome stain for histological examination (Ninomiya et al., 2011). The cubes and cuboids were washed in distilled water and air-dried. ...
Macroscopic mechanical properties of digitigrade paw pads, such as non-linear elastic and variable stiffness, have been investigated in previous studies. However, little is known about the micro-scale structural characteristics of digitigrade paw pads or the relationship between these characteristics and the exceptional cushioning of the pads. The digitigrade paw pad consists of a multi-layered structure, which is mainly comprised of a stratified epithelium layer, a dermis layer and a subcutaneous layer. The stratified epithelium layer and dermal papillae constitute the epidermis layer. Finite element analyses were carried out and showed that the epidermis layer effectively attenuated the ground impact across impact velocities of 0.05-0.4 m/s, and that the von Mises stresses were uniformly distributed in this layer. The dermis layer encompassing the subcutaneous layer can be viewed as a hydrostatic system, which can store, release and dissipate impact energy. All three layers in the paw pad work as a whole to meet the biomechanical requirements of animal locomotion. These findings provide insights into the biomechanical functioning of digitigrade paw pads and could be used to facilitate bio-inspired, ground-contacting component development for robots and machines, as well as contribute to footwear design.
... It has been well established that dogs possess footpad particularly consisting of two components: venous and arterial vessels enmeshed with one another [4], which is the functional analogue of the tongue, fins and flukes of whales, dolphins [5] and manatees [6 ], serving to conserve core body temperature. As the foot pad is highly vascularized and relatively uninsulated, representing a surface for heat loss and many breeds of dogs can be traced back to the arctic, in some ways these breeds are going to be better equipped to handle the cold weather as in the arctic animal [4]. ...
... It has been well established that dogs possess footpad particularly consisting of two components: venous and arterial vessels enmeshed with one another [4], which is the functional analogue of the tongue, fins and flukes of whales, dolphins [5] and manatees [6 ], serving to conserve core body temperature. As the foot pad is highly vascularized and relatively uninsulated, representing a surface for heat loss and many breeds of dogs can be traced back to the arctic, in some ways these breeds are going to be better equipped to handle the cold weather as in the arctic animal [4]. ...
The microvasculature of footpads in the dog and domestic cat was investigated using histology and scanning electron microscopy of corrosion casts. Methylmethacrylate resin vascular casts for scanning electron microscopy, Indian ink injected whole mount and histological specimens were each prepared, in a series of 16 limbs of 4 adult dogs and 12 limbs of 3 adult domestic cats. The network of blood vessels in the dog paw pad appears to have an intricate pattern, especially with regard to venous outflow forming a peri-arterial venous network. Numerous arteriovenous anastomoses (AVAs) were found in the canine dermis. While, that of the domestic cat had less complex vascular pattern in the foot-pad without the peri-arterial venous network. AVAs were observed sporadically in the feline dermis. The peri-arterial venous network in the paw pad formed a countercurrent heat exchanger in dogs. When the foot pad is exposed to a cold environment in dogs, the countercurrent heat exchanger serves to prevent heat loss by re-circulating heat back to the body core, adopting an inhospitable environment. AVAs also play a role in regulating the body temperature. A lack of the peri-arterial venous network and few AVAs appear to make felines more prone to suffer from a cold condition than canines.
... where D s = k s ρ s c s is the thermal diffusivity coefficient for the shell. Since we assume a homogeneity for the shell, then D s is a function neither of time, nor of coordinates, then (22) can be transformed into: ...
... There are researches which demonstrate that vasculature could be built in a sophisticated way to relax these limitations. See [22,28,9]. ...
A novel model of thermal regulation of homoeothermic animals has been
implemented. The model is based on a non-equilibrium thermodynamic approach
which introduces entropy balance and the rate of entropy generation as a
formulation of The Second Law. The model explains linear correlation between an
animals skin and environment temperatures using the first principles and
demonstrates the role of blood circulation in the thermoregulation of
homoeothermic animals.
... The central region of the metacarpal torus presented loose and remarkably vascularized surface dermis. The largest amount of vessels in comparison to the other assessed regions is likely justified by the large amount of arteriovenous anastomoses observed in this region, since it allows blood deviation to the tips of the limbs that get in touch with the ground -this is an important thermoregulation mechanism (NINOMIYA et al., 2011). ...
The aim of the present study is to describe the skin morphology and morphometry of the giant anteater (M. tridactyla), based on comparative analysis applied to skin segments from central metacarpal torus (palmar pad), dorsal thorax, ventral cervical, ventral abdomen, medial carpal and nasal regions. In order to do so, eight adult specimens of M. tridactyla were used for macroscopic studies and four for microscopic assessments. Microscopy was used to assess fur general features that were macroscopically assessed through visual analysis. Fragments (2.0cm²) were collected from the selected regions for microscopic studies. Samples were fixed on McDowell solution, processed through routine histology techniques and subjected to semi-serial cuts (5 μm). The cuts were stained in HE, Alcian blue and periodic acid Schiff. General morphology of different skin layers was described, as well as their architecture and composition; mesoscopy of the epidermis, dermis and stratum corneum was also carried out. There was difference in skin morphometry between males and females, and between different skin regions in the same animal, based on the statistical evaluation of the recorded values. All epidermis layers were assessed for the selected regions. Dermis encompassed surface and deep layers; it presented sweat and sebaceous glands, as well as hair follicles. Findings also allowed reporting that epidermis components are easily identified given its thickness, and the large amount of sweat glands in it – it contrasts its physiological features.
... It is found in many mammals such as rodents, bears, hedgehogs, bats, marsupials Geiser et al., 2014) and even primates (Dausmann et al., 2004;Blanco et al., 2021). Other strategies used by endothermic mammals for coping with low temperature include increased heat production via shivering and non-shivering thermogenesis, reduction of heat loss from the body surface with the help of fur (Hart, 1956) and/or subcutaneous adipose tissue (Tattersall et al., 2012), or modifications of the blood system such as sequence changes of haemoglobin genes (Campbell et al., 2010), counter-current heat exchange (Ninomiya et al., 2011) or the heart's pumping ability mediated by a missense mutation in the NRAP gene (Buggiotti et al., 2021). Mitogenome adaptations include polymorphisms in mitochondrial genes encoding subunits of the respiratory chain (Balloux et al., 2009;Awadi et al., 2021) and stem-loop formation(s) in the major NCR (Melo-Ferreira et al., 2014). ...
Enriching mitochondrial DNA (mtDNA) for sequencing entire mitochondrial genomes (mitogenomes) can be achieved by single long-range PCR. This avoids interference from the omnipresent nuclear mtDNA sequences (NUMTs). The approach is currently restricted to the use of samples collected from humans and ray-finned fishes. Here, we extended the use of single long-range PCR by introducing back-to-back oligonucleotides that target a sequence of extraordinary homology across vertebrates. The assay was applied to five hibernating rodents, namely alpine marmot, Arctic and European ground squirrels, and common and garden dormice, four of which have not been fully sequenced before. Analysis of the novel mitogenomes focussed on the prediction of mitochondrial-derived peptides (MDPs) providing another level of information encoded by mtDNA. The comparison of MOTS-c, SHLP4 and SHLP6 sequences across vertebrate species identified segments of high homology that argue for future experimentation. In addition, we evaluated four candidate polymorphisms replacing an amino acid in mitochondrially encoded subunits of the oxidative phosphorylation (OXPHOS) system that were reported in relation to cold-adaptation. No obvious pattern was found for the diverse sets of mammalian species that either apply daily or multiday torpor or otherwise cope with cold. In summary, our single long-range PCR assay applying a pair of back-to-back primers that target a consensus sequence motif of Vertebrata has potential to amplify (intact) mitochondrial rings present in templates from a taxonomically diverse range of vertebrates. It could be promising for studying novel mitogenomes, mitotypes of a population and mitochondrial heteroplasmy in a sensitive, straightforward and flexible manner.
... The countercurrent heat exchanger is not limited to the brain; it is found in other parts of the body throughout the animal kingdom. The heat transfer system is found in the testes in terrestrial mammals [9] and dolphins [10], penguin flippers [11], whale fins [12], rabbit ears [13], canine paw pads [14], manatee tails [15], and the ophthalmic rete of birds [16]. Magilton et al suggested that the ventral petrosal sinus, which drains cooled blood from the parietofrontal region and lies extracranially adjacent to the base of the brain, allows significant direct conduction of heat to cool the rostral brainstem directly [17], as in dogs [18]. ...
The objectives of this study were to describe the microvasculature of the guttural pouch and consider its provable function. We suggest a working hypothesis that the guttural pouch is an additional organ of thermoregulation. Vascular corrosion casts were prepared for scanning electron microscopy by injecting acrylic resin via the common carotid artery, and tissue sections were prepared for histologic examination in 10 equine cadavers. The arteries supplying the guttural pouch originated from the external carotid artery and its branches, and the arteries formed a capillary network in the pouch mucosa. Some of the superficial arterioles and capillaries extended toward the internal carotid artery (ICA) after supplying the pouch mucosa and formed a fine, compact network in the tunica adventitia of the ICA. The capillaries formed two types of vascular plexuses surrounding the ICA: one with capillary bundles parallel to the ICA in the outer layer of the tunica adventitia (outer periarterial plexus) and the other with vein–artery–vein triads in the inner layer of the tunica adventitia (inner periarterial plexus). The microvascular arrangement and the ICA in the guttural pouch were closely related and consisted of a countercurrent heat exchanger. Such an arrangement supports the hypothesis that the guttural pouch participates in selective brain cooling. Results of the present study help provide a better understanding of the function of the guttural pouch in horses.
... There are researches which demonstrated that vasculature could be build in a sophisticated way to relax this limitation. See [9,23,29]. ...
A novel model of thermal regulation of homoeothermic animals.
... In addition, most of the peripheral arteries in the head of beaked whales are accompanied on either side by paired, anastomosing veins, forming counter-current triads. Similar peripheral triads have been noted in numerous mammalian species, including manatees and dogs (Murie, 1872;Fawcett, 1942;Ninomiya et al., 2011). All of the aforementioned vascular structures are strikingly similar to heat-exchange structures described in the extremities (e.g., fins and flukes) of cetaceans (Scholander and Schevill, 1955;Elsner et al., 1974). ...
Beaked whales are medium-sized toothed whales that inhabit depths beyond the continental shelf; thus beaked whale strandings are relatively infrequent compared to those of other cetaceans. Beaked whales have been catapulted into the spotlight by their tendency to strand in association with naval sonar deployment. Studies have shown the presence of gas and fat emboli within the tissues and analysis of gas emboli is suggestive of nitrogen as the primary component. These findings are consistent with human decompression sickness (DCS) previously not thought possible in cetaceans. Because, tissue loading with nitrogen gas is paramount for the manifestation of DCS and nitrogen loading depends largely on the vascular perfusion of the tissues, we examined the anatomy of the extracranial arterial system using stranded carcasses of 16 beaked whales from five different species. Anatomic regions containing lipid and/or air spaces were prioritized as potential locations of nitrogen gas absorption due to the known solubility of nitrogen in adipose tissue and the nitrogen content of air, respectively. Attention was focused on the acoustic fat bodies and accessory sinus system on the ventral head. We found much of the arterial system of the head to contain arteries homologous to those found in domestic mammals. Robust arterial associations with lipid depots and air spaces occurred within the acoustic fat bodies of the lower jaw and pterygoid air sacs of the ventral head, respectively. Both regions contained extensive trabecular geometry with small arteries investing the trabeculae. Our findings suggest the presence of considerable surface area between the arterial system, and the intramandibular fat bodies and pterygoid air sacs. Our observations may provide support for the hypothesis that these structures play an important role in the exchange of nitrogen gas during diving. J. Morphol., 2015. © 2015 Wiley Periodicals, Inc.
... In addition, most of the peripheral arteries in the head of beaked whales are accompanied on either side by paired, anastomosing veins, forming counter-current triads. Similar peripheral triads have been noted in numerous mammalian species, including manatees and dogs (Murie, 1872;Fawcett, 1942;Ninomiya et al., 2011). All of the aforementioned vascular structures are strikingly similar to heat-exchange structures described in the extremities (e.g., fins and flukes) of cetaceans (Scholander and Schevill, 1955;Elsner et al., 1974). ...
Beaked whales are a poorly known but diverse group of whales that have received considerable attention due to strandings that have been temporally and spatially associated with naval sonar deployment. Postmortem studies on stranded carcasses have revealed lesions consistent with decompression sickness, including intravascular gas and fat emboli. These findings have been supported by analyses of intravascular gas emboli showing composition dominated by nitrogen gas. To increase our understanding of the pathophysiology of nitrogen bubble formation and intravascular embolization, we examined the gross and microscopic anatomy of the venous system in the head of beaked whales. Since the potential sources of intravascular fat and gas emboli were of greatest interest, focus was placed on the acoustic fat bodies and pneumatic accessory sinus system. Herein, we describe intimate arteriovenous associations with specialized adipose depots and air sinuses in beaked whales. These vascular structures comprise an extensive network of thin-walled vessels with a large surface area, which is likely to facilitate exchange of nitrogen gas and may, therefore, form anatomic regions that may be important in physiological management of diving gases. These structures may also be vulnerable to pathologic introduction of emboli into the vascular system. Expansive, thin-walled venous lakes are found within the pterygoid region, which suggest the potential for nitrogen exchange as well as for compensation of middle-ear pressures during descent on a dive. These findings warrant further research into the structure and function of this morphology as it relates to normal and pathologic physiology. J. Morphol., 2015. © 2015 Wiley Periodicals, Inc.
... India ink may be combined with gelatin (Kolts et al., 1994;Ninomiya et al., 2011). This can be achieved by mixing 300 mL of 5% gelatin and 0.5% (v/v) India ink solution and injecting into arteries (Kolts et al., 1994). ...
From a biological point of view, casting refers to filling of anatomical and/or pathological spaces with extraneous material that reproduces a three-dimensional replica of the space. Casting may be accompanied by additional procedures such as corrosion, in which the soft tissue is digested out, leaving a clean cast, or the material may be mixed with radiopaque substances to allow x-ray photography or micro computed topography (µCT) scanning. Alternatively, clearing of the surrounding soft tissue increases transparency and allows visualization of the casted cavities. Combination of casting with tissue fixation allows anatomical dissection and didactic surgical procedures on the tissue. Casting materials fall into three categories namely, aqueous substances (India ink, Prussian blue ink), pliable materials (gelatins, latex, and silicone rubber), or hard materials (methyl methacrylates, polyurethanes, polyesters, and epoxy resins). Casting has proved invaluable in both teaching and research and many phenomenal biological processes have been discovered through casting. The choice of a particular material depends inter alia on the targeted use and the intended subsequent investigative procedures, such as dissection, microscopy, or µCT. The casting material needs to be pliable where anatomical and surgical manipulations are intended, and capillary-passable for ultrastructural investigations.
It is generally known that forelimbs and hindlimbs play different roles during locomotion, but the possible differences in the biomechanical functions of the metacarpal pad and metatarsal pad remain unknown. This study combined kinematic and pressure data from dogs to investigate the key roles of the metacarpal and metatarsal pads. The peak vertical ground reaction force of the metacarpal pad was found to be larger than that of the metatarsal pad, whereas the peak vertical ground reaction force of the fore toes was equal to that of hind toes, and the vertical deformations of the metacarpal and metatarsal pads were almost equal; moreover, the obtained stiffness of the metacarpal pad was several times greater than that of metatarsal pad based on in vivo measurement data. The results showed that the metacarpal pad demonstrated the biomechanical characteristics of cushion and support; however, the support characteristics of the metatarsal pad were weak. Furthermore, magnetic resonance imaging was performed to gather evidence to interpret the various roles played by the metacarpal pad and the metatarsal pad. It was found that the morphology and volumes of internal adipose tissues were closely related to the functions played by the metapodial pad during movement.
Background:
Overheating is a common form of injury in working dogs. The purpose of this study was to evaluate the relative efficacy of three postexercise cooling methods in dogs with exercise-induced heat stress.
Methods:
Nine athletically conditioned dogs were exercised at 10kph for 15 minutes on a treadmill in a hot environmental chamber (30°C) three times on separate days. After exercise, the dogs were cooled using one of three methods: natural cooling, cooling on a 4°C cooling mat, and partial immersion in a 30°C water bath for 5 minutes.
Results:
Time-weighted heat stress was lower for immersion cooling compared with the cooling mat and the control. The mean time required to lower gastrointestinal temperature to 39°C was 16 minutes for immersion cooling, 36 minutes for the cooling mat, and 48 minutes for control cooling.
Conclusion:
Water immersion decreased postexercise, time-weighted heat stress in dogs and provided the most rapid cooling of the three methods evaluated, even with the water being as warm as the ambient conditions. The cooling mat was superior to cooling using only fans, but not as effective as immersion. The placement of simple water troughs in working- dog training areas, along with specific protocols for their use, is recommended to reduce the occurrence of heat injury in dogs and improve the treatment of overheated dogs.
Dermatological conditions are one of the top reasons why pet owners seek veterinary advice. Dermatopathies can cause pain, blood loss, discomfort, pruritus, and in some instances severe critical illness. Initially, some non‐life‐threatening skin lesions can become complicated, resulting in secondary pyoderma and even sepsis. Certain dermatopathies are known to involve multiple organ systems and cause systemic inflammatory response syndrome (SIRS). Examples of dermatological diseases which can become life‐threatening emergencies include methicillin‐resistant staphylococcal infections, cutaneous thermal burns, frostbite, cutaneous drug eruptions, vasculitis, erythema multiforme, and toxic epidermal necrolysis. Early recognition of these disorders is paramount for successful management; however, despite definitive diagnosis, morbidity and mortality can occur. Many life‐threatening dermatopathies have serious underlying etiologies which led to the dermatological manifestation of the disease. For optimal patient outcomes, one must address the skin lesions, secondary infection, and systemic illness or underlying disorder associated with the dermatopathy.
Résumé
Le coussinet du chien est une formation cutanée aux fonctions multiples. Ses particularités anatomiques le prédisposent surtout aux troubles de la cornification ou/et aux altérations vasculaires. La revue des nombreuses maladies dont il peut être la cible montre combien l’examen histologique est instructif dans la plupart des cas.
Extensive arterio‐venous associations occur in the head, axillae and legs of the Jackass penguin Spheniscus demersus. These vascular arrangements appear to facilitate counter‐current heat exchange. The major heat exchange system in the head is the post orbital rete mirabile formed by the superior orbital artery. Blood from this rete supplies the eye, nasal passages and superficial jaw muscles. Other blood vessels supplying the superficial areas of the head and mouth associate closely with their corresponding veins.
In the axilla the brachial artery divides to form a humeral plexus of parallel running arteries each associating with up to three interlinking veins. Only the marginal vein does not associate with an artery. It appears that a shunt mechanism, which bypasses the veins in the humeral plexus, functions to permit heat loss when required; for instance in a heat‐stressed bird breeding or moulting on land.
In both the upper and lower leg all the major arteries and their branches associate closely with corresponding veins.
The development of these arterio‐venous associations indicates that Spheniscus demersus is adapted to a cool aquatic environment in which heat retention is of prime importance.
The thermal characteristics of the mystacial vibrissae of harbour seals (Phoca vitulina) and of the follicle crypts on the rostrum of the dolphin Sotalia fluviatilis guianensis were measured using an infrared imaging system. Thermograms demonstrate that, in both species, single vibrissal follicles are clearly defined units of high thermal radiation, indicating a separate blood supply to these cutaneous structures. It is suggested that the high surface temperatures measured in the area of the mouth of the follicles is a function of the sinus system. In seals and dolphins, surface temperature gradually decreased with increasing distance from the centre of a follicle, indicating heat conduction from the sinus system via the follicle capsule to adjacent tissues. It is suggested that the follicular sinus system is a thermoregulatory structure responsible for the maintenance of high tactile sensitivity at the extremely low ambient temperatures demonstrated for the vibrissal system of seals. The vibrissal follicles of odontocetes have been described as vestigial structures, but the thermograms obtained in the present study provide the first evidence that, in Sotalia fluviatilis, the follicles possess a well-developed sinus system, suggesting that they are part of a functional mechanosensory system.
The mako shark (Isurus oxyrinchus) has specialized vascular networks (retia mirabilia) forming counter-current heat exchangers that allow metabolic heat retention in certain regions of the body, including the aerobic, locomotor red muscle and the viscera. Red muscle, white muscle and stomach temperatures were measured in juvenile (5-13.6 kg) makos swimming steadily in a water tunnel and exposed to stepwise square-wave changes in ambient temperature (T(a)) to estimate the rates of heat transfer and to determine their capacity for the activity-independent control of heat balance. The rates of heat gain of red muscle during warming were significantly higher than the rates of heat loss during cooling, and neither the magnitude of the change in T(a) nor the direction of change in T(a) had a significant effect on red muscle latency time. Our findings for mako red muscle are similar to those recorded for tunas and suggest modulation of retial heat-exchange efficiency as the underlying mechanism controlling heat balance. However, the red muscle temperatures measured in swimming makos (0.3-3 degrees C above T(a)) are cooler than those measured previously in larger decked makos. Also, the finding of non-stable stomach temperatures contrasts with the predicted independence from T(a) recorded in telemetry studies of mako and white sharks. Our studies on live makos provide new evidence that, in addition to the unique convergent morphological properties between makos and tunas, there is a strong functional similarity in the mechanisms used to regulate heat transfer.
In their report “Thermoregulation in the mouths of feeding gray whales” (7 Nov., [p. 1138][1]), John E. Heyning and James G. Mead hypothesize that the special array of arteries and veins found in the tongue of baleen whales may act as a countercurrent heat exchanger. In such arrangements of
Arctic homeotherms maintain their feet near O°C while standing on much colder surfaces by blood-borne heat input. At 5°C in vivo blood viscosity increased approximately 5 times in arctic wolves and wolverines, and for comparison, in non-cold acclimated man. Such increase in blood viscosity in vivo would reduce perfusion; however, specialized arteriovenous plexuses have evolved in foot pad cutaneous tissues. These augment heat delivery and protect tissues from frost bite.
In this article physiological, behavioural and morphological adaptations by the arctic fox to low temperatures and food scarcity in winter are discussed. The arctic fox (Alopex lagopus) adapts to the low polar winter temperatures as a result of the excellent insulative properties of its fur. Among mammals, the arctic fox has the best insulative fur of all. The lower critical temperature is below -WC, and consequently increased metabolic rate to maintain,homeothermy, is not needed under natural temperature conditions. Short muzzle, ears and legs, a short, rounded body and probably a counter-current vascular heat exchange in the legs contribute to reduce heat loss. A capillary rete in the skin of the pads prevents freezing when,standing on a cold substratum. By seeking shelter in snow lairs or in dens below the snow cover and by curling up in a rounded position, exposing only the best-insulated parts of the body, the arctic fox reduces heat loss. The arctic fox copes with seasonal fluctuations in food supply by storing fat and caching food items during summer,and fall. Saving energy through decreased activity and decreased basal metabolic rate might also be,an adaptation to food,scarcity in winter. Key words: arctic fox, basal metabolic rate, lower critical temperature, fat deposition, starvation RI~SUMÉ. Dans cet article, on discute des adaptations physiologiques, comportemental es et morphologiques du renard arctique aux tempkratures
1 In chloralose-anaesthetized dogs pretreated with guanethidine and pancuronium, electrical stimulation (0.2 to 5 Hz) of the peripheral end of the cut tibial nerve caused a frequency-dependent increase in femoral blood flow which was restricted to the paw pads. 2 This neurogenic vasodilatation was not attenuated by atropine, mepyramine plus burimamide, indomethacin or propranolol. It was, however, attenuated in a dose-dependent manner by intra-arterial administration of the dopamine receptor antagonist, ergometrine (0.05 to 0.5 mg). 3 The effect of ergometrine could not be explained by non-specific effects on axonal conduction or transmission or by vasospasm of the blood vessels of the paw-pads. 4 In dogs with intact tibial nerves, a pharmacologically similar dilator response localized to the paw-pads could be elicited by electrical stimulation of loci in the ipsilateral diencephalon and midbrain. This response was not due to inhibition of adrenergic vasomotor tone and was abolished by systemic ganglion blockade or by tibial nerve section as well as by femoral arterial administration of ergometrine. 5 It is suggested that the vasculature of the canine paw pads is innervated by a population of autonomic axons which utilize dopamine or a related substance as a transmitter substance and activation of which causes vasodilation.
Using radioactive microsphere and electromagnetic techniques, hindleg vascular responses were studied in 38 conscious, chronically prepared sheep subjected to either exposure to a warm environment, and/or local warming of the hypothalamus, spinal cord, forelegs or hindlegs. The total proportion of cardiac output passing through AVA's was increased by all treatments. AVA flow in hindleg skin was increased but capillary flow was unchanged by warming the hypothalamus, spinal cord or forelegs. AVA flow was unchanged but capillary flow was increased by warming the ambient air or the hindlegs alone. Equivalent cooling treatments resulted in AVA and capillary flow changes converse to warming.
It is concluded that, in sheep, blood flow through cutaneous AVA's is controlled by specific thermoregulatory reflexes, whereas capillary flow is the target of local temperature effects. A significant role for the direction of the thermal gradient across the skin is implicated.
This study investigates the functional anatomy of the flipper of the jackass penguin (Speniscus demersus). The flippers of birds (n = 15) were dissected and described. Several adaptations from the typical avian wing were noted and reasons were proposed for these. The conclusion is that the osteological and myological adaptations of the flipper are designed to enable the penguin to progress very effectively through water, while the vascular adaptations provide a highly efficient mechanism for thermoregulation.
To determine the potential role of the skin vasculature as a blood reservoir, we measured venous compliance (Cv), resistance (Rv), and their product, the time constant of venous drainage (tau sk = RvCv), in skin flaps from the hindlimbs of 15 dogs anesthetized with pentobarbital sodium at different core temperatures (Tc, 37-42 degrees C), skin temperature (Ts, 25.3-50.0 degrees C), and during an infusion of papaverine (5%). The vasculature of the flap was isolated, and a double-occlusion technique was used to measure the static pressure in the venous compartment. The blood volume of the flap was altered by changing either flow or outflow pressure (Pv). The change in volume was estimated from the change in weight of the flap with a force transducer. At Tc = 37 degrees C, Rv was 2.27 +/- 0.81 mmHg.min.ml-1.100 g-1 (means +/- SD), Cv was 0.17 +/- 0.06 ml.mmHg-1.100 g-1, and tau sk was 28.0 +/- 8.8 s. Rv decreased with elevated Tc, Ts, and with papaverine. Cv increased with a rise in Tc and Ts. Increasing Tc and Ts did not change tau sk, but the papaverine infusion shortened it. The lowest tau sk (20 s) occurred during maximal vasodilatation. This long tau sk indicates that the skin could serve as a blood reservoir during heat stress.
The brain cooling capacity of the altricial pigeon increases during posthatching growth at a higher rate than that of the precocial duck and chicken. To determine if this difference between the altricial and the precocial modes of development can be related to growth rates of the vascular heat exchanger involved in brain cooling (the ophthalmic rete), we performed a morphometric analysis of this structure during the post-hatching maturation of the three species. The number of vascular units in the rete did not change during development but differed significantly among species. The retia continued to grow in length and diameter in an exponential relation with body mass at similar rates in all species. The surface area of the retial arteries, which reflects the area available for countercurrent heat exchange, also increased exponentially with body mass, but without significant differences among the three species. However, the effectiveness of the rete in brain cooling, as indicated by the degree of brain cooling per unit of heat-exchange area in the rete, was higher in the altricial pigeon than in the precocial chicken and duck. It is concluded that the posthatching morphometric changes in the ophthalmic rete (rete ophthalmicum) are important for the development of brain cooling capacity, but cannot solely explain differences in brain cooling between growing altricial and precocial birds. These differences are most likely related to differences in the maturation of the central thermoregulatory control system and the peripheral effector mechanisms among the two groups of birds.
The microcirculation of the dermal laminae and papillae of the equine foot from seven clinically normal Australian ponies was studied using an improved microvascular casting corrosion technique and scanning electron microscopy. Casts of veins, arteries, capillaries and arteriovenous anastomoses (AVAs) were readily identified by their characteristic surface morphology. Arteries entered the laminar circulation axially, between pairs of axial veins, and were connected to each other by smaller calibre interconnecting arteries. Short abaxial branches of the axial interconnecting arteries gave rise to tufts of predominantly, proximodistally orientated, capillaries arranged abaxially in rows. The laminar veins anastomosed with each other extensively (the axial venous plexus) and formed most of the vascular skeleton of casts of the dermal laminae. AVAs were found throughout the laminar circulation but the largest and longest (40 mu diameter) were found clustered close to the origin of the axial arteries. The density of the laminar AVAs was estimated to be 500 AVAs/cm2. Blood vessels of the dermal papillae of the periople, coronary band, distal laminae, sole and frog shared a basic structural organisation. The cast of each papillary unit consisted of a central artery and vein enmeshed in a sheath of fine capillaries. At intervals along the length of the central artery were short branches which gave rise to tufts of capillaries. The capillaries formed a tortuous anastomosing plexus which encircled the papillary unit and drained into the central vein at intervals along its length. AVAs were always present at the base of the papillary units and anastomoses connected the central artery and vein. AVAs are important components of the dermal microcirculation of the equine foot and their distribution and density is compatible with their proposed role in the pathophysiology of equine laminitis.
Marlins, sailfish, and spearfishes have a heat-producing tissue beneath the brain and adjacent to the eyes. This tissue warms the brain and eyes while the rest of the body remains at water temperature. The heater tissue is derived from the superior rectus eye muscle. Only a portion of this eye muscle contains normal skeletal muscle tissue; the rest consists of the modified muscle tissue that is associated with heat production. The heat-producing portion is supplied with blood through a countercurrent heat exchanger that originates from the carotid artery. The vascular rate prevents the heat being produced by the tissue from being dissipated at the gill. An unusual circulatory supply to the eyes and brain is associated with the presence of the heater tissue in these fishes.
Arctic foxes and gray wolves maintain their foot temperature just above the tissue freezing point (about -1°C)when standing
on extremely cold snow, or when the foot is immersed in a -35°C bath in the laboratory. Proportional thermoregulation stabilized
the subcutaneous temperature of the foot pad to a precision of ± 0.7°C (largest deviations). Selective shunting of blood-borne
body heat through a cutaneous vascular plexus in the foot pad accounted for more than 99 percent of measured heat loss from
the pad surface. Maximum energetic efficiency is achieved because the unit of heat exchange is located in the pad surface
which contacts the cold substrate rather than throughout the pad.
The vascular bed of the rabbit ear has been studied with light microscopy, microangiography and scanning electron microscopy of resin casts in a series of 20 ears. The major arteries supplying the ear were the central and rostral auricular branches of the caudal auricular artery. The caudal auricular branch was not observed, except as a small vessel supplying the rostral auricular base. The central auricular branch supplied blood to most of the auricular integument and was surrounded by capillaries extended from those supplying the skin. The periarterial capillaries formed a fine, compact network in the tunica media and were closely related to the central auricular branch. Evidence is presented suggesting that this vascular mechanism has a counter-current heat-exchange function for regulating body temperature. The artery had the well-developed internal elastic lamina and intimal cushions that regulate blood flow at the branching sites. A number of arteriovenous anastomoses were also observed between arterioles and venules, particularly in marginal regions of the ear. The intimal cushions and arteriovenous anastomoses might play an additional role in thermoregulation by regulating local blood flow in the ear.
Although Florida manatees (Trichechus manatus latirostris) have relatively low basal metabolic rates for aquatic mammals of their size, they maintain normal mammalian core temperatures. We describe vascular structures in the manatee tail that permit countercurrent heat exchange (CCHE) to conserve thermal energy. Approximately 1000 arteries juxtaposed to 2000 veins are found at the cranial end of the caudal vascular bundle (CVB); these numbers decrease caudally, but the 1:2 ratio of arteries to veins persists. Arterial walls are relatively thin when compared to those previously described in vascular countercurrent heat exchangers in cetaceans. It is assumed that CCHE in the CVB helps manatees to maintain core temperatures. Activity in warm water, however, mandates a mechanism that prevents elevated core temperatures. The tail could transfer heat to the environment if arterial blood delivered to the skin were warmer than the surrounding water; unfortunately, CCHE prevents this heat transfer. We describe deep caudal veins that provide a collateral venous return from the tail. This return, which is physically outside the CVB, reduces the venous volume within the bundle and allows arterial expansion and increased arterial supply to the skin, and thus helps prevent elevated core temperatures.
Large and powerful ocean predators such as swordfishes, some tunas, and several shark species are unique among fishes in that they are capable of maintaining elevated body temperatures (endothermy) when hunting for prey in deep and cold water . In these animals, warming the central nervous system and the eyes is the one common feature of this energetically costly adaptation . In the swordfish (Xiphias gladius), a highly specialized heating system located in an extraocular muscle specifically warms the eyes and brain up to 10 degrees C-15 degrees C above ambient water temperatures . Although the function of neural warming in fishes has been the subject of considerable speculation , the biological significance of this unusual ability has until now remained unknown. We show here that warming the retina significantly improves temporal resolution, and hence the detection of rapid motion, in fast-swimming predatory fishes such as the swordfish. Depending on diving depth, temporal resolution can be more than ten times greater in these fishes than in fishes with eyes at the same temperature as the surrounding water. The enhanced temporal resolution allowed by heated eyes provides warm-blooded and highly visual oceanic predators, such as swordfishes, tunas, and sharks, with a crucial advantage over their agile, cold-blooded prey.
To examine the functional anatomy of the ocular circulation in four bottlenose dolphins (Tursiops truncatus) and five melon-headed whales (Peponocephala electra).
Eyes were obtained postmortem from whales that died while in captivity and/or were found beached. Specimens from whales were investigated using scanning electron microscopy (SEM) of vascular corrosion casts and histology. The thermal characteristics of live dolphin eyes were measured using an infrared imaging system.
The whale eye receives its primary blood supply from the ophthalmic rete, which extends just behind the eyeball. The ophthalmic rete diverges from the basilar rete and the cervical rete via the posterior thoracic artery. The iris and ciliary processes are supplied by iridic arteries via the major arterial circle that is located around the iris edge. The retinal vessels show the holangiotic type. Choroidal arteries run in parallel arrays so as to interdigitate the densely packed choroidal veins. The venules in the conjunctival fold and palpebral conjunctiva form a well-developed venous plexus. Thermographic examination revealed that the eye shows a substantially higher degree of thermal emission than adjacent skin areas.
The cetacean eye is characterized by a unique vascular pattern and multivessel plexuses, which are quite different from those of terrestrial mammals. This suggests that the ocular vasculature might function as a thermoregulatory system so that the appropriate operating temperature for the photoreceptors can be maintained in a deep and cold aquatic environment. The distinctive plexuses in the orbit might also be for pooling blood in the eye to conserve oxygen during dives. The ophthalmic rete might play a role in a pressure-damping effect on cetacean ocular circulation as well.
Thermal control of blood flow through capillaries and arteriovenous anastomoses in skin of sheep. Pflü gers Archiv
- Hales Jrs Fawcett
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- Bennett
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Hales JRS, Fawcett AA, Bennett JW et al. Thermal control of blood flow through capillaries and arteriovenous anastomoses in skin of sheep. Pflü gers Archiv: European Journal of Physiology 1978; 378: 55–63.