American flamingo

American flamingo
Galapagos Islands
Scientific classification
Kingdom: Animalia
Phylum: Chordata
Class: Aves
Order: Phoenicopteriformes
Family: Phoenicopteridae
Genus: Phoenicopterus
Species: P. ruber
Binomial name
Phoenicopterus ruber
Linnaeus, 1758

The American flamingo (Phoenicopterus ruber) is a large species of flamingo closely related to the greater flamingo and Chilean flamingo. It was formerly considered conspecific with the greater flamingo, but that treatment is now widely viewed (e.g. by the American and British Ornithologists' Unions) as incorrect due to a lack of evidence. It is also known as the Caribbean flamingo although it is present in the Galápagos Islands. In Cuba it is also known as the Greater Flamingo. It is the only flamingo that naturally inhabits North America.

Distribution

Skull MHNT

The American flamingo breeds in the Galápagos, coastal Colombia, Venezuela and nearby islands, Trinidad and Tobago, along the northern coast of the Yucatán Peninsula, Cuba, Hispaniola, The Bahamas, and the Turks and Caicos Islands.[1] The population in Galapagos differs genetically from that in the Caribbean, and the Galapagos flamingos are statistically smaller, exhibit differences in body shape sexual dimorphism, and lay smaller eggs.[2] The American flamingo was also found in southern Florida, but since the arrival of Europeans it has been all but eradicated there, sightings today are usually considered to be escapees, although at least one bird banded as a chick in the Yucatán Peninsula has been sighted in Everglades National Park,[3] and others may be vagrant birds from Cuba . From a distance, untrained eyes can also confuse it with the roseate spoonbill.[4][5]


Its preferred habitats are similar to that of its relatives: saline lagoons, mudflats, and shallow brackish coastal or inland lakes. An example habitat is the Petenes mangroves ecoregion of the Yucatán.[6]

Description

The American flamingo is a large wading bird with reddish-pink plumage. Like all flamingos, it lays a single chalky white egg on a mud mound, between May and August; incubation until hatching takes from 28 to 32 days; both parents brood the young for a period of up to 6 years when they reach sexual maturity. Their life expectancy of 40 years is one of the longest in birds.

Adult American flamingos are smaller on average than greater flamingos but are the largest flamingos in the Americas. They measure from 120 to 145 cm (47 to 57 in) tall. The males weigh an average of 2.8 kg (6.2 lb), while females average 2.2 kg (4.9 lb). Most of its plumage is pink, giving rise to its earlier name of rosy flamingo and differentiating adults from the much paler greater flamingo. The wing coverts are red, and the primary and secondary flight feathers are black. The bill is pink and white with an extensive black tip. The legs are entirely pink. The call is a goose-like honking.

It is one of the species to which the Agreement on the Conservation of African-Eurasian Migratory Waterbirds (AEWA) applies.

Mating and bonding behaviors

Mating and bonding behaviors of "Phoenicopterus ruber" individuals have been extensively studied in captivity. The American flamingo is usually monogamous when selecting a nest site, incubating and raising young; however, extra-pair copulations are frequent. While males usually initiate courtship, females control the process. If there is mutual interest, a female will walk by the male, and if the male is receptive he will walk with her. Both parties will make synchronized movements until one member aborts this process. For low-intensity courtships, males and females will walk in unison with their heads raised. In high-intensity courtships, males and females will walk at a quick pace with their heads dropped in a false feeding posture. This high-intensity courtship will stop at any point if either bird turns and the other does not follow, the heads are raised, unison movements are stopped, or the pace of movement is slowed. If the female is ultimately receptive to copulation, she will stop walking and present for the male. Long-term pairs do not frequently engage in courtship behaviors or in-group display. Pairs often stand, sleep, and eat in close proximity. Courtship is most often seen among individuals that change partners often or are promiscuous. There is a spectrum of pairing relationships. Some birds have a long-term partner throughout the year; others form pairs during periods of courtship and nest attendance. How long a relationship lasts is affected by many factors, including addition and removal of adults, maturation of juveniles, and occurrence of trios and quartets. In most pairs, both individuals usually construct and defend the nest site. In rare cases, one individual will undertake both duties. Within trios, the dominant pair begins the nesting process by choosing and then defending the site. For trios with one male and two females, the subordinate female is tolerated by the male, but often fights with the dominant female. If two females share a nest and both lay an egg, one female will try to destroy the other egg or roll it out of the nest. For trios with 2 males and 1 female, the subordinate male is tolerated by both individuals and will often become the primary incubator and caregiver of the chicks. For quartets, the dominant male and two females take care of the nest, while the subordinate male remains around the periphery, never gaining access to the nest. Less animosity is observed between the dominant and subordinate females in quartets compared to trios.[7]

Adaptations

The American flamingo has adapted to its shallow water environment in several ways. It has evolved long legs and large webbed feet in order to wade and stir up the bottom of the water bed to bring up their food source to then be retrieved. In order to feed, it has evolved a specialized beak which is hooked downward and features marginal lamellae on the upper mandible, and inner and outer lamellae on both the upper and lower mandibles. These are adapted for filtering out different sized food from water.[8] Depending on the food source in their area, will depend on the exact morphology of their beaks on what can and cannot be strained out of them. It submerges its head under water to retrieve its food, and may have its head under water for large amounts of time, which requires it to hold its breath. Factors which affect the habitat choice of American flamingos are environmental temperatures, water depth, food source, accessibility of an area and the presence of vegetation beds in feeding areas. If available food items don't meet the needs of the flamingo or the temperature is not appropriate to their requirements, they will move to a better feeding or more temperate area.

Osmoregulation

Further information: Avian anatomy#Kidney

The role of osmoregulation—the maintenance of a precise balance of solute and water concentrations within the body—is performed by a number of bodily functions working together. In Phoenicopterus ruber, the kidney, the lower gastrointestinal tract and the salt glands work together to maintain the homeostasis between ions and fluids. In mammals, the kidneys and urinary bladder are the primary organs used in osmoregulation. Birds, however, lack a urinary bladder and must compensate using these three organs.

Phoenicopterus ruber are salt water birds that ingest food with a high salt content and mostly drink salt water (with an osmolarity of usually 1000), hyperosmotic to the bodies cells . As well, though not commonly, they can drink fresh water at near boiling temperatures from geysers. From their high salt diet, they would lose more water and have a greater salt uptake. One way in which they have adapted to osmoregulate is through the use of a salt gland, which is found in their beaks.[9] This salt gland helps emit excess salt from the body through the nasal openings in the flamingo's beaks. When these birds consume salt, the osmolarity increases in the blood plasma through the gut. This causes water to move out of the cells, increasing extracellular fluids. Both these changes in turn activate the salt glands of the bird,[10] but before any activity occurs in the salt glands the kidney has to reabsorb the ingested sodium from the small intestine. As seen in other saltwater birds, the fluid that is excreted has been seen to have an osmolarity greater than that of the salt water, but this varies with salt consumption and body size.[11]

As food and saltwater is ingested, sodium and water absorption begins in the gut. It is absorbed through the walls of the gut and into the extracellular fluid. Sodium is then circulated to the kidney where the plasma undergoes filtration by the renal glomerulus. Although bird's kidneys tend to be larger in size they are inefficient in producing concentrated urine that is significantly hyperosmotic to their blood plasma. This form of secretion would cause dehydration from water loss. Therefore, sodium and water are reabsorbed into the plasma by renal tubules. This increase in osmotic plasma levels causes extracellular fluid volume to increase which triggers receptors in both the brain and heart. These receptors then stimulate salt gland secretion and sodium is able to efficiently leave the body through the nares while maintaining a high body water level.[10]

Flamingos, like many other marine birds, have a high saline intake, yet even with this in mind, the glomular filtration rate (GFR) remains unchanged. This is because of the salt glands; high concentrations of sodium are present in the renal filtrate but can be reabsorbed almost completely where it is excreted in high concentrations in the salt glands.[10] Renal reabsorption can be increased through the output of the antidiuretic hormone called arginine vasotacin (AVT). AVT opens protein channels in the collection ducts of the kidney called aquaporins. Aquaporins increase the membrane permeability to water, as well as causes less water to move from the blood and into the kidney tubules.

Specialized osmoregulatory cells and transport mechanisms

The salt gland used by the American flamingo has two segments, a medial and lateral segment. These segments are tube shaped glands that consist of two cell types. The first is the cuboidal – peripheral cells which are small, triangular shaped cells which have only a few mitochondria. The second specialized cells are the principal cells which are found down the length of the secretory tubules, and are rich in mitochondria.[12] These cells are similar to the mitochondria rich cells found in teleost fish.

These cells within the salt gland employ several types of transport mechanisms that respond to osmoregulatory loads.[13] Sodium-Potassium ATPase works with a Sodium-Chloride cotransporter (also known as the NKCC), and a basal potassium channel to secrete salt (NaCl) into secretory tubes.[14] The ATPase uses energy from ATP to pump three sodium ions out of the cell and two potassium ions into the cell. The potassium channel allows potassium ions to diffuse out of the cell. The cotransporter pumps one sodium, potassium and two chloride ions into the cell. The chloride ion diffuses through the apical membrane into the secretory tube and the sodium follows via a paracellular route.[12] This is what forms the hyperosmotic solution within the salt glands.

Circulatory system

Although there has been little investigation on the specific circulatory and cardiovascular system of the phoenicopteridae, they possess the typical features of an avian circulatory system. As is seen in other aves, the flamingo's circulatory system is closed maintaining a separation of oxygenated and deoxygenated blood. This maximizes their efficiency to meet their high metabolic needs during flight. Due to this need for increased cardiac output, the avian heart tends to be larger in relation to body mass than what is seen in most mammals.

Heart type and features

The avian circulatory system is driven by a four-chambered, myogenic heart contained in a fibrous pericardial sac. This pericardial sac is filled with a serous fluid for lubrication.[15] The heart itself is divided into a right and left half, each with an atrium and ventricle. The atrium and ventricles of each side are separated by atrioventricular valves which prevent back flow from one chamber to the next during contraction. Being myogenic, the hearts pace is maintained by pacemaker cells found in the sinoatrial node, located on the right atrium. The sinoatrial node uses calcium to cause a depolarizing signal transduction pathway from the atrium through right and left atrioventricular bundle which communicates contraction to the ventricles. The avian heart also consists of muscular arches that are made up of thick bundles of muscular layers. Much like a mammalian heart, the avian heart is composed of endocardial, myocardial and epicardial layers.[15] The atrium walls tend to be thinner than the ventricle walls, due to the intense ventricular contraction used to pump oxygenated blood throughout the body.

Organization of circulatory system

Similar to the atrium, the arteries are composed of thick elastic muscles to withstand the pressure of the ventricular constriction, and become more rigid as they move away from the heart. Blood moves through the arteries, which undergo vasoconstriction, and into arterioles which act as a transportation system to distribute primarily oxygen as well as nutrients to all tissues of the body.[16] As the arterioles move away from the heart and into individual organs and tissues they are further divided to increase surface area and slow blood flow. Travelling through the arterioles blood moves into the capillaries where gas exchange can occur. Capillaries are organized into capillary beds in tissues, it is here that blood exchanges oxygen for carbon dioxide waste. In the capillary beds blood flow is slowed to allow maximum diffusion of oxygen into the tissues. Once the blood has become deoxygenated it travels through venules then veins and back to the heart. Veins, unlike arteries, are thin and rigid as they do not need to withstand extreme pressure. As blood travels through the venules to the veins a funneling occurs called vasodilation bringing blood back to the heart.[16] Once the blood reaches the heart it moves first into the right atrium, then the left ventricle to be pumped through the lungs for further gas exchange of carbon dioxide waste for oxygen. Oxygenated blood then flows from the lungs through the left atrium to the left ventricle where it is pumped out to the body. With respect to thermoregulation, the American flamingo has highly vascularized feet that use a countercurrent exchange system in there legs and feet. This method of thermoregulation keeps a constant gradient between the veins and arteries that are in close proximity in order to maintain heat within the core and minimize heat loss or gain in the extremities. Heat loss is minimized while wading in cold water, while heat gain is minimized in the hot temperatures during rest and flight.[17]

Physical and chemical properties of pumping blood

Avian hearts are generally larger than mammalian hearts when compared to body mass. This adaptation allows more blood to be pumped to meet the high metabolic need associated with flight. Birds, like the flamingo, have a very efficient system for diffusing oxygen into the blood; birds have a ten times greater surface area to gas exchange volume than mammals. As a result, birds have more blood in their capillaries per unit of volume of lung than a mammal.[18] The American flamingo's four-chambered heart is myogenic, meaning that all the muscle cells and fibers have the ability to contract rhythmically.[18] The rhythm of contraction is controlled by the pace maker cells which have a lower threshold for depolarization. The wave of electrical depolarization initiated here is what physically starts the heart's contractions and begins pumping blood. Pumping blood creates variations in blood pressure and as a result, creates different thicknesses of blood vessels. The Law of LaPlace can be used to explain why arteries are relatively thick and veins are thin.

Blood composition

It was widely thought that avian blood had special properties which attributed to a very efficient extraction and transportation of oxygen in comparison to mammalian blood. This of course is not true; there is no real difference in the efficiency of the blood, and both mammals and birds use a hemoglobin molecule as the primary oxygen carrier with little to no difference in oxygen carrying capacity.[19] Captivity and age have been seen to have an effect on the blood composition of the American flamingo. A decrease in white blood cell numbers was predominate with age in both captive and free living flamingos, but captive flamingos showed a higher white blood cell count than free living flamingos. One exception occurs in free living flamingos with regards to white blood cell count. The number of eosinophils in free living birds are higher because these cells are the ones that fight off parasites with which a free living bird may have more contact than a captive one. Captive birds showed higher hematocrit and red blood cell numbers than the free living flamingos, and a blood hemoglobin increase was seen with age. An increase in hemoglobin would correspond with an adults increase in metabolic needs. A smaller mean cellular volume recorded in free living flamingos coupled with similar mean hemoglobin content between captive and free living flamingos could show different oxygen diffusion characteristics between these two groups. Plasma chemistry remains relatively stable with age but lower values of protein content, uric acid, cholesterol, triglycerides, and phospholipids were seen in free living flamingos. This trend can be attributed to shortages and variances in food intake in free living flamingos.[20]

Blood composition and osmoregulation

Avian erythrocytes (red blood cells) have been shown to contain approximately ten times the amount of taurine (an amino acid) than mammal erythrocytes. Taurine has a fairly large list of physiological functions; but in birds, it can have an important influence on osmoregulation. It helps the movement of ions in erythrocytes by altering the permeability of the membrane and regulating osmotic pressure within the cell. The regulation of osmotic pressure is achieved by the influx or efflux of taurine relative to changes in the osmolarity of the blood. In a hypotonic environment, cells will swell and eventually shrink; this shrinkage is due to efflux of taurine. This process also works in the opposite way in hypertonic environments. In hypertonic environments cells tend to shrink and then enlarge; this enlargement is due to an influx in taurine, affectively changing the osmotic pressure.[21] This adaptation allows the flamingo to regulate between differences in salinity.

Respiratory system

Relatively few studies have focused on the flamingo respiratory system, however little to no divergences from the standard avian anatomical design have occurred in their evolutionary history. Nevertheless, some physiological differences do occur in the flamingo and structurally similar species.

The respiratory system is not only important for efficient gas exchange, but for thermoregulation and vocalization.[15] Thermoregulation is important for flamingos as they generally live in warm habitats and their plush plumage increases body temperature. Heat loss is accomplished through thermal polypnea (panting), that is an increase in respiratory rate. It has been seen that the medulla, hypothalamus and mid-brain are involved in the control of panting, as well through the Hering-Breuer reflex that uses stretch receptors in the lungs, and the vagus nerve.[22] This effect of the panting is accelerated by a process called gular fluttering;[23] rapid flapping of membranes in the throat which is synchronized with the movements of the thorax. Both of these mechanisms promote evaporative heat loss, which allows for the bird to push out warm air and water from the body. Increases in respiratory rate would normally cause respiratory alkalosis because carbon dioxide levels are rapidly dropping in the body, but the flamingo is able to bypass this, most likely through a shunt mechanism,[24] which allow it to still maintain a sustainable partial pressure of carbon dioxide in the blood. Since the avian integument is not equipped with sweat glands, cutaneous cooling is minimal. Because the flamingo's respiratory system is shared with multiple functions, panting must be controlled to prevent hypoxia.

For a flamingo, having such a long neck means adapting to an unusually long trachea. Tracheas are an important area of the respiratory tract; aside from directing air in and out of the lungs, it has the largest volume of dead space in the tract. Dead space in avians is around 4.5 times higher in mammals of roughly the same size.[15] In particular, flamingos have a trachea that is longer than its body length[25] with 330 cartilaginous rings.[26] As a result, they have a calculated dead space twice as high as another bird of the same size.[27] To compensate for the elongation, they usually breathe in deep, slow patterns.[15]

One hypothesis for the bird's adaptation to respiratory alkalosis is tracheal coiling. Tracheal coiling is an overly long extension of the trachea and can often wrap around the bird's body. When faced with a heat load, birds often use thermal panting and this adaptation of tracheal coiling allows ventilation of non-exchange surfaces which can enable the bird to avoid respiratory alkalosis. The flamingo uses a "flushout" pattern of ventilation where deeper breaths are essentially mixed in with shallow panting to flush out carbon dioxide and avoid alkalosis. The increased length of the trachea provides a greater ability for respiratory evaporation and cooling off without hyperventilation.[28]

Thermoregulation

Further reading: Thermoregulation in birds and mammals

Thermoregulation is a matter of keeping a consistent body temperature regardless of the surrounding ambient temperature. Flamingos require both methods of efficient heat retention and release. Even though the American flamingo resides mainly close to the equator where there is relatively little fluctuation in temperature, seasonal and circadian variations in temperature must be accounted for.

Like all animals, flamingos maintain a relatively constant basal metabolic rate (BMR); the metabolic rate of an animal in its thermoneutral zone (TNZ) while at rest. The BMR is a static rate which changes depending on factors such as the time of day or seasonal activity. Like most other birds, basic physiological adaptations control both heat loss in warm conditions and heat retention in cooler conditions. Using a system of countercurrent blood flow, heat is efficiently recycled through the body rather than being lost through extremities such as the legs and feet.

Living in the equatorial region of the world, the American flamingo has little variation in seasonal temperature changes. However, as a homeothermic endotherm it is still faced with the challenge of maintaining a constant body temperature while being exposed to both the day (light period) and night (dark period) temperatures of its environments. Phoenicopterus ruber have evolved a number of thermoregulatory mechanisms to keep itself cool during the light period and warm during the dark period without expending too much energy. The American flamingo has been observed in a temperature niche between 17.8–35.2 °C (64.0–95.4 °F).[29] In order to prevent water loss through evaporation when temperatures are elevated the flamingo will employ hyperthermia as a nonevaporative heat loss method keeping its body temperature between 40–42 °C (104–108 °F).[23] This allows heat to leave the body by moving from an area of high body temperature to an area of a lower ambient temperature. Flamingos are also able to use evaporative heat loss methods such as, cutaneous evaporative heat loss and respiratory evaporative heat loss. During cutaneous heat loss, Phoenicopterus ruber relies on evaporation off of the skin to reduce its body temperature. This method is not very efficient as it requires evaporation to pass through the plumage. A more efficient way to reduce its body temperature is through respiratory evaporative heat loss, where the flamingo engages in panting to expel excessive body heat. During the dark period the flamingos tend to tuck their heads beneath their wing to conserve body heat. They may also elicit shivering as a means of muscular energy consumption to produce heat as needed.[15]

P. ruber stands on one leg in order to retain body heat

One of the most distinctive attribute of P. ruber is its unipedal stance, or the tendency to stand on one leg. While the purpose of this iconic posture remains ultimately unanswered, strong evidence supports its function in regulating body temperature.[30] Like most birds, the largest amount of heat is lost through the legs and feet;[30] having long legs can be a major disadvantage when temperatures fall and heat retention is most important. By holding one leg up against the ventral surface of the body, the flamingo lowers the surface area by which heat exits the body.[29] Moreover, it has been observed that during periods of increased temperatures such as mid-day, flamingos will stand on both legs. Holding a bipedal stance multiplies the amount of heat lost from the legs and further regulates body temperature.[30]

Migration

Like other flamingo species, American flamingos will migrate short distances to ensure that they get enough food or because their current habitat has been disturbed in some way. One habitat disturbance that has been observed to cause flamingos to leave their feeding grounds is elevated water levels. These conditions make it difficult for Phoenicopterus ruber to wade, hindering their ability to access food. The flamingos will then abandon their feeding grounds in search of an alternate food source.[31] While the flights are not as long as other migratory birds, flamingos still fly for periods without eating.

Metabolism

For the most part flamingos are not all that different from other salt water wading birds. They will fast when migrating to a new habitat or the chicks may not receive food daily depending on food availability.[32]

References

  1. 1 2 BirdLife International (2012). "Phoenicopterus ruber". IUCN Red List of Threatened Species. Version 2013.2. International Union for Conservation of Nature. Retrieved 26 November 2013.
  2. ↑ Frias-Soler, R.; et al. (2014). "Genetic and Phenotypic evidence supports evolutionary divergence of the American Flamingo (Phoenicopterus ruber) population in the Galapagos Islands". Waterbirds 37: 349-361.
  3. ↑ Silk, Robert (26 September 2012). "Banded flamingo traced back to Yucatan reserve". keynews.com. Key West Citizen. Retrieved 11 November 2015.
  4. ↑ Sizemore, Grant C.; Main, Martin B.; Pearlstine, Elise V. "Florida's Wading Birds". University of Florida. Flamingos may be confused with the Roseate Spoonbill for a variety of reasons. Both species have relatively long legs, long necks, and pinkish plumage. Both also sift through the water with their bills when feeding. Despite these similarities, the two species are unrelated. The easiest ways to tell the two species apart are by the dark outer wing feathers (primaries) on the flamingo and both species' distinctive bill shapes.
  5. ↑ Hill, K. "Ajaia ajaia (Roseate Spoonbill)". Smithsonian Marine Station at Fort Pierce. From a distance, [the roseate spoonbill] can be confused with the [flamingo], due to the similarity of body color in both species. However, the roseate spoonbill is generally smaller than the flamingo, with a shorter neck, and a longer, spoon-shaped bill.
  6. ↑ World Wildlife Fund. 2010. Petenes mangroves. eds. Mark McGinley, C.Michael Hogan & C. Cleveland. Encyclopedia of Earth. National Council for Science and the Environment. Washington DC
  7. ↑ Shannon, Peter W. (2000). "Social and Reproductive Relationships of Captive Caribbean Flamingos". Waterbirds 23: 173–78. doi:10.2307/1522162. JSTOR 1522162.
  8. ↑ Mascitti, V.; Kravetz, F.O. (2002). "Bill morphology of South American flamingos". Condor 104 (1): 73–83. doi:10.1650/0010-5422(2002)104[0073:bmosaf]2.0.co;2.
  9. ↑ Armstrong, Marian (2007). Flamingo. Wildlife and Plants 6 (Marshall Cavendish). pp. 370–371. ISBN 978-0761476931.
  10. 1 2 3 Hughes, M.R. (2003). "Regulation of salt gland, gut and kidney interactions". Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 136 (3): 507–524. doi:10.1016/j.cbpb.2003.09.005.
  11. ↑ Eckhart, Simon (1982). "The osmoregulatory system of birds with salt glands". Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 71 (4): 547–556. doi:10.1016/0300-9629(82)90203-1.
  12. 1 2 Butler, G.D. (2002). "Hypertonic fluids are secreted by medial and lateral segments in duck (Anas Platyrhynchos) nasal salt gland". Journal of Physiology 540 (3): 1039–1046. doi:10.1113/jphysiol.2002.016980.
  13. ↑ Schmidt-Nielson, K. (1960). "The salt-secreting gland of marine birds." (PDF). Circulation - The journal of the American Heart Association 21: 955–967. doi:10.1161/01.CIR.21.5.955.
  14. ↑ Lowy, R.J.; Dawson, D.C.; Ernst, S.A. (1989). "Mechanism of ion transport by avian salt gland primary cell cultures". American Journal of Physiology. Regulatory, Integrative and Comparative Physiology 256 (6): 25–26. PMID 2735444.
  15. 1 2 3 4 5 6 Whittow, G. Causey (2000). Sturkie's Avian Physiology. San Diego, California: Academic Press. pp. 235, 361. ISBN 978-0-12-747605-6.
  16. 1 2 Hill, Richard W.; Wyse, Gordon A.; Anderson, Margaret (2012). Animal Physiology (Third ed.). Sunderland, MA: Sinauer Associates. pp. 647–678. ISBN 978-0-87893-559-8.
  17. ↑ Loudon, Catherine; Davis-Berg, Elizabeth C.; Botz, Jason T. (2012). "A laboratory exercise using a physical model for demonstrating countercurrent heat exchange". Advances in Physiology Education 36: 58–62. doi:10.1152/advan.00094.2011.
  18. 1 2 Hoagstrom, C.W., ed. (2002). Vertebrate Circulation. Magill's Encyclopedia of Science: Animal Life 1 (Pasadena, California: Salem Press). pp. 217–219. ISBN 978-1587650192.
  19. ↑ Hoagstrom, C.W., ed. (2002). Respiration in Birds. Magill's Encyclopedia of Science: Animal Life 3 (Pasadena, California: Salem Press). pp. 1407–1411. ISBN 978-1587650192.
  20. ↑ Puerta, M.L.; Garcia Del Campo, A.L.; Abelenda, M.; Fernandez, A.; Huecas, V.; Nava, M.P. (1992). "Hematological Trends in Flamingos, Phoenicopterus Ruber". Comparative Biochemistry and Physiology Part A: Physiology (Great Britain: Pergamon Press Ltd.) 102 (4): 683–686. doi:10.1016/0300-9629(92)90723-4.
  21. ↑ Shihabi, Z.K.; Goodman, H.O.; Holmes, R.P.; O'Connor, M.L. (1988). "The Taurine Content of Avian Erythrocytes and its Role in Osmoregulation". Comparative Biochemistry and Physiology Part A: Physiology 92 (4): 545–549. doi:10.1016/0300-9629(89)90363-0.
  22. ↑ Richards, S.A. (1970). "Physiology of Thermal Panting in Birds". Annales de biologie animale, biochimie, biophysique (10): 151–168. doi:10.1051/rnd:19700614.
  23. 1 2 Bech, Claus; Johansen, Kjell; Maloiy, G.M.O. (1979). "Ventilation and expired gas composition in the flamingo, phoenicopterus ruber, during normal respiration and panting". Physiological Zoology (University of Chicago Press) 52 (3): 313–328. JSTOR 30155753.
  24. ↑ Marder, Jacob; Arad, Zeev (1989). "Panting and acid-base regulation in heat stressed birds". Comparative Biochemistry and Physiology Part A: Physiology 94 (3): 395–400. doi:10.1016/0300-9629(89)90112-6.
  25. ↑ Krautwald-Junghanns, Maria-Elisabeth; Pees, Michael; Reese, Sven; Tully, Thomas (2010). Diagnostic Imaging of Exotic Pets: Birds, Small Mammals, Reptiles. Germany: Manson Publishing. ISBN 978-3-89993-049-8.
  26. ↑ Audubon, John James (1861). The birds of America: from drawings made in the United States and their territories 6. California: Roe Lockwood. pp. 169–177.
  27. ↑ Calder, William A. (1996). Size, Function, and Life History. Mineola, New York: Courier Dove Publications. p. 91. ISBN 978-0-486-69191-6.
  28. ↑ Prange, H.D.; Wasser, J.S.; Gaunt, A.S.; Gaunt, S.L.L. (1985). "Respiratory Responses to Acute Heat Stress in Cranes (Gruidae): The Effects of Tracheal Coiling". Respiratory Physiology 62: 95–103. doi:10.1016/0034-5687(85)90053-2. PMID 4070839.
  29. 1 2 Bouchard, Laura C.; Anderson, Matthew J. (April 2011). "Caribbean Flamingo resting behavior and the influence of weather variables". Journal of Ornithology 152 (2): 307–312. doi:10.1007/s10336-010-0586-9.
  30. 1 2 3 Anderson, Matthew J.; Williams, Sarah A. (27 July 2009). "Why do flamingos stand on one leg?". Zoo Biology 29 (3): 365–374. doi:10.1002/zoo.20266. PMID 19637281. Retrieved 2 December 2013.
  31. ↑ Vargas, F.H.; Barlow, S.S.; Hart, T.T.; Jimenez-Uzcátegui, G.G.; Chavez, J.J.; Naranjo, S.S.; Macdonald, D.W. (2008). "Effects of climate variation on the abundance and distribution of flamingos in the Galápagos Islands". Journal of Zoology 276 (3): 252–265. doi:10.1111/j.1469-7998.2008.00485.x.
  32. ↑ Amat, Juan A.; Hortas, Francisco; Arroyo, Gonzalo M.; Rendón, Miguel A.; Ramírez, José M.; Rendón-Martos, Manuel; Pérez-Hurtado, Alejandro; Garrido, Araceli (2007). "Interannual variations in feeding frequencies and food quality of greater flamingo chicks (Phoenicopterus roseus): Evidence from plasma chemistry and effects on body condition" (PDF). Comparative Biochemistry and Physiology A - Molecular & Integrative Physiology 147 (2): 569–576. doi:10.1016/j.cbpa.2007.02.006. PMID 17360212.

Further reading

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