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Lifespan, longevity, and ageing

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Maximum longevity: 44 years (captivity) Observations: One captive specimen reportedly lived to the age of 44 (http://www.demogr.mpg.de/longevityrecords).
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Associations

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Flamingos have very few predators. This is probably largely due to their choice of habitat. Hypersaline estuaries are not favorable for other species, and oftentimes the colonial sites are on islands or other areas only easily accessible by flight. However, various species have been noted to prey on flamingos or their eggs. This short list includes turkey vultures, foxes, badgers, and wild boars. Yellow-legged gulls will prey on eggs and flightless young. Humans will also hunt flamingos for meat or for their eggs.

Known Predators:

  • Turkey vultures (Cathartes aura)
  • Foxes (Vulpes)
  • Badgers
  • Wild boars (Sus scrofa)
  • Yellow-legged gulls (Larus michahellis)
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Meziani, A. 2011. "Phoenicopterus ruber" (On-line), Animal Diversity Web. Accessed April 27, 2013 at http://animaldiversity.ummz.umich.edu/site/accounts/information/Phoenicopterus_ruber.html
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Adam Meziani, University of Michigan-Ann Arbor
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Phil Myers, University of Michigan-Ann Arbor
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Morphology

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Greater flamingos are one of the larger members of the Aves class with a wingspan measuring 1.5 m wide, standing 1.2 m tall, and weighing 2.1 to 4.1 kg. They are most well-known for their bright pink coloration and in fact, the word "flamingo" derives from old Spanish for "flaming" or "red feather." Individuals have long, graceful necks and legs which in proportion to body size are the longest of any bird. Flamingos will often rest their head on their body in order to avoid fatigue in the neck muscles.

The bill is uniquely adapted for filter-feeding, and its shape is not shared among any other family of birds. Their large bills consist of layers of horny plates used to filter out prey from the water. In contrast to other birds, flamingo's bills are essentially reversed. Flamingo's lower mandibles are larger than the upper, which is not rigidly attached to the skull. Thus when it eats, the upper mandible moves as opposed to the lower, which is completely reversed from all birds and mammals. This reversal is largely attributed to flamingos' method of feeding by submerging their heads upside-down.

Sexual dimorphism is present in that males are slightly larger than females, and females obtain their adult color slightly earlier than males. Otherwise both sexes are uniformly colored. Adults have primarily pink plumage with black flight feathers only visible in flight. They feature pale irises and a pale bill with pink and black on the tip. The legs are bright pink as well and end with pink, webbed feet. Because there is no difference in coloration between the sexes, the bright pink coloration is not likely to be any type of sexual signal, though some researchers suggest it may function equally for both sexes in selecting a mate as a sign of fitness due to overall nutrition status.

Young birds are covered with a downy-type feather when they first hatch. Both their legs and bill are dark gray in color, and only become pink as the bird matures. The feathers are also initially gray, but will gradually be replaced by the pink, adult plumage as the flamingo ages and incorporates carotenoid compounds from its diet into new growth. Maturity generally takes about three years, though some have been seen with juvenile plumage at up to five years of age.

Range mass: 2.1 to 4.1 kg.

Range length: 120 to 145 cm.

Range wingspan: 140 to 165 cm.

Other Physical Features: endothermic ; homoiothermic; bilateral symmetry

Sexual Dimorphism: sexes alike; male larger

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Meziani, A. 2011. "Phoenicopterus ruber" (On-line), Animal Diversity Web. Accessed April 27, 2013 at http://animaldiversity.ummz.umich.edu/site/accounts/information/Phoenicopterus_ruber.html
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Adam Meziani, University of Michigan-Ann Arbor
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Life Expectancy

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Chicks generally have a higher mortality rate than adults. At birth, they are unable to fend for themselves and are fully dependent upon their parents. However, if they are able to survive into adulthood, flamingos live an average lifespan of 25 years in the wild with a maximum of 44 years. In captivity, flamingos live an average of 30 years. The oldest flamingo in the world is over 75 years old and resides at the Adelaide Zoo in Australia.

Range lifespan
Status: wild:
44 (high) years.

Range lifespan
Status: captivity:
75 (high) years.

Average lifespan
Status: wild:
25 years.

Typical lifespan
Status: captivity:
30 (high) years.

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Meziani, A. 2011. "Phoenicopterus ruber" (On-line), Animal Diversity Web. Accessed April 27, 2013 at http://animaldiversity.ummz.umich.edu/site/accounts/information/Phoenicopterus_ruber.html
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Adam Meziani, University of Michigan-Ann Arbor
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Phil Myers, University of Michigan-Ann Arbor
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Rachelle Sterling, Special Projects
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Habitat

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Flamingos live in large colonies, oftentimes numbering into the thousands of individuals. They tend to occupy large mud flats where the loose mud can be easily formed into the mounds that they use as nests. These large mud flats are usually located near a food supply.

Hyper-saline estuaries are the preferred habitat. They are harsh environments where filter feeders benefit from reduced competition and predation while at the same time being able to take advantage of the abundant food sources. These habitats are often located near larger bodies of water such as coastal areas, sea inlets, rivers, and open lakes. Habitats are nearly always coastal, but they have been known to move inland to lagoons or volcanic lakes.

In colonies of such high density, occasional food shortages arise and flocks will perform short migrations in search of greater food resources. Flamingos show little to no site-tenacity and don't often return to previous flocking sites, or to their birth locations.

Average elevation: sea level m.

Habitat Regions: tropical ; saltwater or marine ; freshwater

Aquatic Biomes: lakes and ponds; rivers and streams; temporary pools; coastal

Other Habitat Features: riparian ; estuarine

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Meziani, A. 2011. "Phoenicopterus ruber" (On-line), Animal Diversity Web. Accessed April 27, 2013 at http://animaldiversity.ummz.umich.edu/site/accounts/information/Phoenicopterus_ruber.html
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Adam Meziani, University of Michigan-Ann Arbor
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Distribution

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Flamingos are found on all continents except Antarctica and Australia. Depending on the authority involved, there are up to six distinct species, each with its own range and geographic dispersion.

Specifically, the range of greater flamingos extends across the entire shoreline of Africa, the Mediterranean Sea, parts of Asia and India as well as southern United States, the Caribbean, and Yucatan Peninsula where there are warm coastal habitats.

The range of Caribbean flamingos, a subspecies of Phoenicopterus ruber, covers the northern shore of South America, most shoreline around the Caribbean Sea, as well as nearby islands in the Caribbean and Eastern Pacific. Flamingos have been seen in the southern United States, though they are not as prolific as in the more southern latitudes.

Biogeographic Regions: palearctic (Native ); ethiopian (Native ); neotropical (Native )

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Meziani, A. 2011. "Phoenicopterus ruber" (On-line), Animal Diversity Web. Accessed April 27, 2013 at http://animaldiversity.ummz.umich.edu/site/accounts/information/Phoenicopterus_ruber.html
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Adam Meziani, University of Michigan-Ann Arbor
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Phil Myers, University of Michigan-Ann Arbor
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Untitled

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Flamingo specimens in the fossil record have been found that are remarkably similar to modern day species dating as far back as 30 million years ago, with evidence of more primitive forms dating back to the tertiary period. Depending on the authority, there are up to 6 different species of flamingos: greater flamingos (Phoenicopterus roseus), Caribbean flamingos (Phoenicopterus ruber), Chilean flamingos (Phoenicopterus chilensis), lesser flamingos (Phoeniconaias minor), Andean flamingos (Phoenicoparrus andinus), and James's flamingos (Phoenicoparrus jamesi).

However, Caribbean flamingos are often classified as a subspecies of greater flamingos. When this convention is followed, they are referred to as Phoenicopterus ruber ruber and Phoenicopterus ruber roseus respectively. While this issue is not yet settled, there are certain strong morphological characteristics shared between the two, most notably in the bill morphology. For the purposes of this article, the two were considered to be members of the same species.

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Meziani, A. 2011. "Phoenicopterus ruber" (On-line), Animal Diversity Web. Accessed April 27, 2013 at http://animaldiversity.ummz.umich.edu/site/accounts/information/Phoenicopterus_ruber.html
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Adam Meziani, University of Michigan-Ann Arbor
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Phil Myers, University of Michigan-Ann Arbor
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Behavior

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As a social species living in large groups, intraspecific communication can be essential. For instance, parents returning to feed their young after foraging must find their own mate and offspring. In a group with potentially tens of thousands of members, communication serves a vital role in maintaining colony cohesion and interactions among other members.

Flamingos will communicate with other members mainly by vocalizations. While in flight, they will call with loud honking noises, which has been compared to the familiar sound of geese. While on land, the vocalizations are softer in volume. As part of imprinting, chicks begin making vocalizations while still in the egg. Parents learn to recognize their offspring's unique voice before it even hatches, and will recognize their offspring afterward based on such calls.

Adults also rely on physical positions. Visual cues can be used for establishing dominance within the flock. For instance, the choice of which side the head rests on can determine aggressiveness with others. Body language is also communicated by the extent to which feathers are ruffled, similar to the way a cat may raise the hair along its back when threatened - a bird which makes itself appear larger is more threatening to a potential opponent. In such aggressive meetings, birds will also adopt a ritual which involves maneuvering the head and neck in a threatening fashion and producing a clicking sound with the beak by snapping it open and shut quickly. If this warning is ignored, birds may snap their bills at each other in "bill fencing" until one backs down.

Greater flamingos also engage in physical courtship displays, in which males attract females through specific movements and postures. Females will communicate interest by mimicking these movements back to the male.

It is unclear if flamingos utilize any type of chemical or pheromone signaling mechanism. Adult flamingos will often delay mating even after reaching sexual maturity. Whether this unusual behavior is a response to pheromone signaling is not known.

Like all birds, greater flamingos perceive their environments through auditory, tactile, visual and chemical stimuli.

Communication Channels: visual ; tactile ; acoustic

Perception Channels: visual ; tactile ; acoustic ; chemical

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Meziani, A. 2011. "Phoenicopterus ruber" (On-line), Animal Diversity Web. Accessed April 27, 2013 at http://animaldiversity.ummz.umich.edu/site/accounts/information/Phoenicopterus_ruber.html
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Adam Meziani, University of Michigan-Ann Arbor
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Phil Myers, University of Michigan-Ann Arbor
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Rachelle Sterling, Special Projects
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Conservation Status

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Greater flamingos are currently considered to be non-threatened. Their large range allows them to be more resistant to local changes of habitat that could be more critical for shorter-ranged animals. Greater flamingos readily migrate in response to decreases in habitat quality. Furthermore, the wild population is quite large and both the range and population numbers of greater flamingos appear to be increasing.

Nevertheless, due to the preferred habitat and nesting behaviors of the flamingo, there are areas that conservationists could focus on. Because the colony feeds as a large group, they are susceptible to contaminated food sources. Though this poses no danger for the species as a whole, individual colonies can be affected by local contaminants in their food supply. A flock in Spain, for instance, was afflicted by a toxic strain of cyanobacteria in their food supply, from which many adults in a mature flock perished. Because their feeding locations are often downstream of human activity in less industrialized nations, habitat limitation may be a risk in flamingo conservation.

Likewise, human excursion into the preferred shoreline habitats of these birds may interrupt their nesting and breeding success. For instance, activities as innocuous as photography have been known to disrupt breeding colonies when the birds have considered it a threat and left the region. The isolated nature of their preferred roosts mitigates contact with humans, and at present human activity does not appear to be affecting flamingos to any great extent.

Greater flamingos are also quite easily maintained in captivity, and as popular zoo animals there are large captive populations across the globe. Greater flamingos are thus likely to survive in the rare event that their natural habitat should face an unforeseen calamity.

US Migratory Bird Act: no special status

US Federal List: no special status

CITES: appendix i

IUCN Red List of Threatened Species: least concern

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Meziani, A. 2011. "Phoenicopterus ruber" (On-line), Animal Diversity Web. Accessed April 27, 2013 at http://animaldiversity.ummz.umich.edu/site/accounts/information/Phoenicopterus_ruber.html
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Adam Meziani, University of Michigan-Ann Arbor
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Phil Myers, University of Michigan-Ann Arbor
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Rachelle Sterling, Special Projects
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Benefits

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There is no significant negative impact of greater flamingos on humans. Their preference for isolation has kept them largely apart from human areas.

If there is a risk, it is the potential for disease transmission. Large colonies are susceptible to rapid spread of disease and tuberculosis and avian flu, both human respiratory diseases, are common in flamingos. However, since flamingos prefer isolation and will readily flee humans, the risk for transmission is decreased to only when hunted for human consumption. However, this risk remains low and no serious outbreak of human disease has been traced to flamingo populations.

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Meziani, A. 2011. "Phoenicopterus ruber" (On-line), Animal Diversity Web. Accessed April 27, 2013 at http://animaldiversity.ummz.umich.edu/site/accounts/information/Phoenicopterus_ruber.html
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Adam Meziani, University of Michigan-Ann Arbor
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Phil Myers, University of Michigan-Ann Arbor
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Benefits

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Flamingos are occasionally hunted by local people for food in some areas. Flamingo meat and eggs are sold at markets, but otherwise there is no economic impact towards humans. Their bright pink coloration fades with time, so greater flamingo feathers have not become an animal trade commodity.

Positive Impacts: food

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Meziani, A. 2011. "Phoenicopterus ruber" (On-line), Animal Diversity Web. Accessed April 27, 2013 at http://animaldiversity.ummz.umich.edu/site/accounts/information/Phoenicopterus_ruber.html
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Adam Meziani, University of Michigan-Ann Arbor
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Phil Myers, University of Michigan-Ann Arbor
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Associations

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Greater flamingos consume large amounts of aquatic invertebrates, crustaceans, and algae and likely has a large impact on those populations. Flamingos feed in shallow bodies of water, and often use their large feet to stir organisms from the bottom up into the water column. This activity likely contributes to sufficient oxygenation and mixing of organic material within these bodies of water and aids in avoiding anoxic conditions. Greater flamingo eggs and young fall prey to local predators, thus supporting these populations.

Flamingos are also susceptible to pathogens, most notably tuberculosis and avian flu. Large colonies are prime conditions for spread of disease if introduced.

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Meziani, A. 2011. "Phoenicopterus ruber" (On-line), Animal Diversity Web. Accessed April 27, 2013 at http://animaldiversity.ummz.umich.edu/site/accounts/information/Phoenicopterus_ruber.html
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Adam Meziani, University of Michigan-Ann Arbor
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Phil Myers, University of Michigan-Ann Arbor
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Rachelle Sterling, Special Projects
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Trophic Strategy

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The feeding behaviors of flamingos are one of their most distinctive characteristics. The flamingo's long legs are used to stir up sediment at the bottom of shallow water. The flamingo's bill is equipped with rows of bony projections lining the edges of the interior of their beaks, which function as a sieve. The bird will take a mouthful of water and move its beak to pump water out, using this uniquely curved bill to filter out tiny organisms to eat. Since the flamingo dips its head down into the water to eat, it effectively feeds "upside down," and the beak reflects this in its morphology - both in the spoon-like shape of the bill and the articulation of the joint of the upper jaw. In contrast to mammals and other vertebrates, the upper jaw is able to move during feeding. To picture this evolutionary accomplishment, consider that since flamingos feed with their heads upside down, the bill appears right side up when the head is inverted, an adaptation where a flamingo's upper bill is like another bird's lower bill. The physical top half is the functional bottom half.

Flamingos are not selective in their diet. Anything that can be captured by their filtration feeding method appears to be consumed. Stomachs of wild flamingos have been examined, and flamingos appear to eat organic ooze (bacteria and microscopic organisms), worms, nematodes, molluscs, crustaceans, insects and larvae, and even vertebrates such as small fish. They will also consume vegetable matter. Though they can subsist on a wide variety of foods, small crustaceans are responsible for the bright pink pigment that flamingos are famous for. Carotenoid compounds from the crustaceans is incorporated into the plumage and skin around the legs, and animals become pale which do not receive this nutrient. For instance, individuals kept in zoos that are not fed a supplemented diet will not have the same coloration as wild birds. The sun will cause this coloration to fade over time, so it must be continually supplied to keep the bird's color.

Flamingos' tongues have evolved to be quite muscular in comparison to other birds as they are critical to the pumping mechanism required to pump food through filter system. The tongue was savored as a delicacy in ancient Rome.

Animal Foods: fish; insects; mollusks; aquatic or marine worms; aquatic crustaceans; other marine invertebrates; zooplankton

Plant Foods: algae; phytoplankton

Foraging Behavior: filter-feeding

Primary Diet: carnivore (Eats non-insect arthropods)

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Meziani, A. 2011. "Phoenicopterus ruber" (On-line), Animal Diversity Web. Accessed April 27, 2013 at http://animaldiversity.ummz.umich.edu/site/accounts/information/Phoenicopterus_ruber.html
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Adam Meziani, University of Michigan-Ann Arbor
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Phil Myers, University of Michigan-Ann Arbor
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Rachelle Sterling, Special Projects
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Reproduction

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Males and females are generally monogamous, remaining together during incubation and nurturing of the young. Mates will often remain together for many years, only choosing a new mate after the death of another.

Mating in P. ruber is a complex affair. Their highly gregarious nature leads to distinct behaviors for selecting a mate and rearing the young afterward. The entire adult colony prepares for mating. When a colony has found a suitable location, adults will gather near the drinking area. Though birds over one year of age can breed, only fully colored adults will take part in the breeding ritual. The birds will gather and begin displays of their size and coloration. They will elongate their necks, extend their wings, and touch nearby individuals with their beaks and wings. Though it is difficult to determine due to the similar appearance between males and females, it appears that groups of males congregate while displaying. Regardless, the entire flock performs similar displays, oftentimes for months before the breeding itself begins.

This breeding display has various positions which the flamingos adopt, and have been named by researchers. The head is first held extended in the "head flagging," and waved rapidly back and forth while calling loudly. This is followed by a "wing salute," where the dark flight feathers are displayed. The bird will then perform a "twist preen," dipping the head beneath a wing. The wings are again displayed in an "inverted wing salute," followed by stretching a wing and a leg on one side of the body backwards while dipping the head downwards. The entire dance takes only seconds, and is repeated constantly throughout the pre-pairing phase. This usually takes place in shallow water.

A female will usually move farther from the main group when she has found a suitable mate and the male will follow her. Both will continue making various display positions. Females will signal their readiness by keeping their head down near the water level. Males will add a head bobbing display, inverting their neck backward and resting their head on their back. When the female is ready for copulation, she will move to deeper water, and spread her wings to signal the male.

Mating System: monogamous

There is no set breeding season for flamingos, with young being born at any time of year. However, the colonies as a whole will usually breed concurrently over the warmer seasons following the rains, with most breeding in late spring or early summer. This timing is due more to availability of food supplies than any limitations on seasonal fertility. The main factors which are preliminary to mating appear to be an abundant food supply, suitable mudflats for nesting and creating the creche, and availability of fresh water.

When the mating is complete, both birds will build a nest from the mud. The nest is a small mound approximately twelve inches high, circular, and with a depressed center for the egg to be laid. When available, bits of vegetation, twigs, or feathers are incorporated into the nest. The male will usually begin building, with both partners eventually working on the nest until the egg is laid.

The eggs are large and milky white, about the size of a large orange or grapefruit. A pair of flamingos will usually lay a single egg once per breeding cycle. In the rare cases where two eggs are laid, usually only one will hatch. The egg is incubated by both parents, who take turns as the partner forages away from the nest. Incubation lasts 28 to 32 days, after which the chicks hatch weighing 85 to 102 grams. Hatchlings are semiprecocial with downy feathers and eyes open, but are initially unable to feed themselves. Greater flamingos' specialized beaks do not begin to develop until the young are 2 weeks old. Newly hatched chicks will remain in the nest for the first five to eight days, at which time they gather with other chicks in groups called "creches." Chicks are reared by both parents until ready to fly at 65 to 90 days old. Parents are able to call and locate their young within the creche and continue to provide care until the young fledges.

Breeding interval: Greater flamingos breed once yearly.

Breeding season: Greater flamingos breed after the rainy season, usually in spring or summer.

Range eggs per season: 1 to 2.

Average eggs per season: 1.

Range time to hatching: 28 to 32 days.

Range fledging age: 65 to 90 days.

Range age at sexual or reproductive maturity (female): 3 to 5 years.

Average age at sexual or reproductive maturity (female): 3 years.

Range age at sexual or reproductive maturity (male): 3 to 5 years.

Average age at sexual or reproductive maturity (male): 3 years.

Key Reproductive Features: iteroparous ; seasonal breeding ; gonochoric/gonochoristic/dioecious (sexes separate); sexual ; oviparous

Both male and female parents provide significant resources for their young. Both participate in building the nest and incubation. A few days before hatching, the chick will begin to produce vocalizations. Imprinting to the parents initially starts through this vocalization while still in the egg. Once newly hatched, a chick recognizes its parents and the parents recognize the chick. Parents provide food for the young hatchling until the chick is ready to forage for itself. This nourishment is called "crop milk," a nutritious secretion from the oral crop of the parents. The milk is similar to human milk, both in composition and because it is stimulated by the same hormone, prolactin. The crop milk of flamingos, however, is red in color due to the pigments present in the diet. This pigment will eventually be incorporated into the chick's feathers, the first step towards the characteristic coloration of flamingos.

All adults can produce this crop milk, but no parent will feed any chick other than its own. If a chick fails to imprint on its parents, no other birds will provide for it and death will result. Consequently, imprinting is of vital importance. The chick is able to recognize its own parents' calls from up to one hundred meters away. When called, only the intended chick will respond, even with other chicks present within hearing range.

When the chick initially leaves the nest, one of the parents will watch over it as it explores its new environment, keeping other birds away until the young are fully integrated into the creche. The chick leaves the nest to join the creche at 5 to 8 days old, yet it still requires parental care until it fledges at 65 to 90 days of age.

Parental Investment: precocial ; male parental care ; female parental care ; pre-fertilization (Provisioning, Protecting: Female); pre-hatching/birth (Provisioning: Female, Protecting: Male, Female); pre-weaning/fledging (Provisioning: Male, Female, Protecting: Male, Female); pre-independence (Provisioning: Male, Female, Protecting: Male, Female)

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Meziani, A. 2011. "Phoenicopterus ruber" (On-line), Animal Diversity Web. Accessed April 27, 2013 at http://animaldiversity.ummz.umich.edu/site/accounts/information/Phoenicopterus_ruber.html
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Adam Meziani, University of Michigan-Ann Arbor
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Phil Myers, University of Michigan-Ann Arbor
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Rachelle Sterling, Special Projects
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Biology

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Whereas smaller flamingos and other wading birds are restricted to the shallows, the Caribbean flamingo's great size enables it to wade out into relatively deep water. It rarely takes food from the surface, but instead generally feeds with its whole head submerged underwater. With its bill held only slightly open, it filters out food particles by allowing water to pass across rows of tiny comb-like plates on the bill's edges (4). Utilising this specialized technique it is able to obtain huge quantities of the crustaceans, molluscs, aquatic insects, polychaete worms, and algae on which it depends. It is the presence of certain carotenoids in the algae and crustaceans that give the flamingo its distinctively coloured plumage (2) (4). The Caribbean flamingo is a highly social species, with colonies ranging in size from just a few dozen to hundreds of thousands of individual birds during the breeding season (2) (4). Group courtship displays are typical of this flamingo, with thousands of individuals raising their wings, turning their heads, or bowing their necks in spectacular synchrony. Engaging in these displays ensures that all members of the colony are ready to mate at the same time (4). Both sexes are involved in building the nest from bits of mud piled into a smooth cone, and spaced just beyond pecking distance of other pairs' nests. Usually just a single egg is laid, which is incubated by both parents over 27 to 31 days (2). Around six to eight days after hatching, the chicks leave the nests and gather in large crèches, overseen by a small number of adults, and eventually fledge at around 9 to 13 weeks (2) (4). Although the Caribbean flamingo is generally considered to be non-migratory, it is extremely nomadic, and will travel hundreds of kilometres in response to shifting resources (2). Large flocks form long, curving lines in flight, with each bird flying with its neck and legs distinctively outstretched (2) (4).
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Conservation

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In 2007, a network of in-situ and ex-situ conservation initiatives was established by the Caribbean Alliance for Flamingo Research and Conservation, to ensure the protection and conservation of the Caribbean flamingo (10). This includes a range of research and conservation activities coordinated across several countries that fall within the species' range (7).
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Description

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With its brilliant pinkish-red plumage, long slender legs, and remarkably thin, flexible neck, the Caribbean flamingo is one of the most world's most distinctive birds. Together with the greater flamingo, it shares the title for the longest limbs relative to body size of any bird. The legs are pink and, being a wading bird, the front three toes are webbed. The bill has a characteristic downward bend, and is pale-yellow at the base, pink to orange in the middle, and black at the tip (2) (4). Until 2002, the Caribbean flamingo was considered conspecific with the greater flamingo (Phoenicopterus roseus), found in Europe, Africa, and Asia (5) (6). While both species are of a similar size, the greater flamingo has much paler plumage than the Caribbean flamingo (2) (5).
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Habitat

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Found in a wide variety of saline and freshwater habitat such as lagoons, estuaries, mud flats, and coastal or inland lakes (2) (4).
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Range

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The Caribbean flamingo occurs on the north coast of South America, the Yucatan Peninsula in Mexico, and a number of Caribbean islands. In addition, there is a small, isolated population on the Galapagos Islands (2) (7).
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Status

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Classified as Least Concern (LC) on the IUCN Red List (1) and listed on Appendix II of CITES (3).
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Threats

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Development, human disturbance, and habitat loss threatens the coastal Caribbean wetlands on which the Caribbean flamingo depends (8). Fortunately however, its population remains very large and is actually believed to be increasing overall (9).
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American flamingo

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American flamingo in Colombia
American flamingo in Colombia

The American flamingo (Phoenicopterus ruber) is a large species of flamingo closely related to the greater flamingo and Chilean flamingo native to the neotropics. 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 also present in the Galápagos Islands. It is the only flamingo that naturally inhabits North America.

Distribution

Skull MHNT

The American flamingo breeds in South America (in the Galápagos Islands of Ecuador, coastal Colombia and Venezuela, and northern Brazil), in the West Indies (Trinidad and Tobago, Cuba, Jamaica, Hispaniola (the Dominican Republic and Haiti), The Bahamas, the Virgin Islands, and the Turks and Caicos Islands), and tropical and subtropical areas of continental North America (along the northern coast of the Yucatán Peninsula in Mexico, and Cameron Parish, Louisiana, southern Florida and the immediate coastline of the rest of southern and southeastern United States). It is a vagrant to Puerto Rico, Anguilla, Barbados, and Honduras.[1] The population in the Galápagos Islands differs genetically from that in the Caribbean; the Galápagos flamingos are significantly smaller, exhibit sexual dimorphism in body shape, and lay smaller eggs.[3] They are sometimes separated as Phoenicopterus ruber glyphorhynchus.[4]

Its preferred habitats are similar to those of its relatives: saline lagoons, mudflats, and shallow, brackish coastal or inland lakes. An example habitat is the Petenes mangroves ecoregion of the Yucatán.[5]

In Florida

Flamingos in Florida

The American flamingo is also found in South Florida and the Florida Keys, both of which are likely one of the northernmost remaining strongholds of its distribution.[6] The existence of flamingo eggs in museum collections labeled as collected from Florida indicates that they likely nested there as well. Since the arrival of Europeans, the population started to decline, up until the 1900s, where it was considered completely extirpated. During the 1950s, birds from the captive population at Hialeah Park frequently escaped, thus leading to the conclusion that all modern flamingos in Florida were escapees, although at least one bird banded as a chick in the Yucatán Peninsula has been sighted in Everglades National Park.[7]

A study published in 2018, involving an abandoned young flamingo named Conchy found in Key West, indicates that the occasional flamingos observed in parts of Florida are in fact natives, with some even permanently staying in Florida Bay year-round. The study also indicated that these flamingos may be increasing in population and reclaiming their lost range, slowly but steadily returning home. Large flocks of flamingos are still known to visit Florida from time to time, most notably in 2014, when a very large flock of over 147 flamingos temporarily stayed at Stormwater Treatment Area 2, on Lake Okeechobee, with a few returning the following year.[8] From a distance, untrained eyes can also confuse it with the roseate spoonbill.[9][10][11][12][13][14]

Description

Close-up of head at São Paulo Zoo, Brazil
Individual at SeaWorld San Diego cleaning its feathers

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 their young. They may reach sexual maturity between 3 and 6 years of age, though usually they do not reproduce until they are 6 years old. 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.

A flock at Whipsnade Zoo
A group of immature birds at Lago de Oviedo, Dominican Republic

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

Mating and bonding behaviors

Mating and bonding behaviors of P. ruber individuals have been extensively studied in captivity. The American flamingo is usually monogamous when selecting a nest site, and incubating and raising young; however, extra-pair copulations are frequent.

The flock flight at Cayo Coco, Cuba

While males usually initiate courtship, females control the process. If interest is mutual, a female walks by the male, and if the male is receptive, he walks with her. Both parties make synchronized movements until one member aborts this process. For low-intensity courtships, males and females walk in unison with their heads raised. In high-intensity courtships, males and females walk at a quick pace with their heads dropped in a false feeding posture. This high-intensity courtship stops 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 stops walking and presents 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. A spectrum of pairing relationships is seen. 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 undertakes 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 two males and one female, the subordinate male is tolerated by both individuals and often becomes 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.[15]

The egg is attended constantly and equally by alternating parents. Chicks at the nest are attended constantly by alternating parents, up to 7–11 days of age. Most attentive periods during incubation and brooding last 21–60 hours, both in the case where the ‘off-duty’ parents remain in the same lagoon to feed, or (when breeding occurs in lagoons deficient in food), they fly to other lagoons to feed. Nest reliefs during incubation take place predominantly in late afternoon, or early morning.

Phoenicopterus ruber - MHNT
A chick and its mother

The time for receiving food from parents decreases from hatching to about 105 days, and the decrease is greatest after the chicks have left the nest at 7–11 days to band into crèches. The frequency and the duration of feeds by male and female partners do not differ significantly. After chicks have left the nest, feeds are predominantly nocturnal.[16]

Adaptations

The American flamingo has adapted to its shallow-water environment in several ways. It has evolved long legs and large webbed feet to wade and stir up the bottom of the water bed to bring up their food source to then be retrieved. 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 differently sized food from water.[17] Depending on the food source in their area, diets depend on the exact morphology of their beaks on what can and cannot be strained out of them. The American flamingo's diet consists of small crustaceans, molluscs, some worms, nematodes, insects and their larvae, small fish, widgeon grass, seeds and algae.[18][19] They are also known to consume mud from which they are able to get microorganisms and bacteria and obtain nutrients.[18][19] It submerges its head under water to retrieve its food, and may have its head under water for long times, 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 do not meet the needs of the flamingos or the temperature is not appropriate to their requirements, they move to a better feeding or more temperate area.

Osmoregulation

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 P. 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.

American flamingos are saltwater 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 . Also, 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 osmoregulate is through the use of a salt gland, which is found in their beaks.[20] This salt gland helps excrete 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,[21] 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.[22]

As food and saltwater are ingested, sodium and water absorption begins 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 birds' 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.[21]

Flamingos, like many other marine birds, have a high saline intake, yet even 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.[21] Renal reabsorption can be increased through the output of the antidiuretic hormone called arginine vasotocin (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.[23] 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.[24] 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.[25] 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.[23] 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.[26] 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.[26] 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.[27] 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.[27] 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 their 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.[28]

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.[29] The American flamingo's four-chambered heart is myogenic, meaning that all the muscle cells and fibers have the ability to contract rhythmically.[29] 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 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.[30] 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.[31]

Blood composition and osmoregulation

Avian erythrocytes (red blood cells) have been shown to contain approximately ten times the amount of taurine (an amino acid) as 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, effectively changing the osmotic pressure.[32] 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.[26] 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.[33] This effect of the panting is accelerated by a process called gular fluttering;[34] 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,[35] 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.[26] In particular, flamingos have a trachea that is longer than its body length[36] with 330 cartilaginous rings.[37] As a result, they have a calculated dead space twice as high as another bird of the same size.[38] To compensate for the elongation, they usually breathe in deep, slow patterns.[26]

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.[39]

Thermoregulation

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).[40] 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).[34] 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.[26]

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.[41] Like most birds, the largest amount of heat is lost through the legs and feet;[41] 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.[40] 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.[41]

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.[42] While the flights are not as long as other migratory birds, flamingos still fly for periods without eating.

References

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  2. ^ "Appendices | CITES". cites.org. Retrieved 2022-01-14.
  3. ^ Frias-Soler, Roberto; Tindle, Elizabeth; Lopez, Georgina Espinosa; Blomberg, Simon; Studer-Thiersch, Adelheid; Wink, Michael; Tindle, Robert (2014). "Genetic and Phenotypic Evidence Supports Evolutionary Divergence of the American Flamingo (Phoenicopterus ruber) Population in the Galápagos Islands" (PDF). Waterbirds. 37 (4): 349–468. doi:10.1675/063.037.0402. S2CID 83573624.
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American flamingo: Brief Summary

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American flamingo in Colombia American flamingo in Colombia

The American flamingo (Phoenicopterus ruber) is a large species of flamingo closely related to the greater flamingo and Chilean flamingo native to the neotropics. 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 also present in the Galápagos Islands. It is the only flamingo that naturally inhabits North America.

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Description

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Length: 136-172 cm ; 127-140 cm . Plumage: generally white with pink wash; wing coverts and axillaries bright red; flight feathers black. Immature greyish without red in wings. Bare parts: iris red; lores and eye-ring pink; bill pink with black tip, grey in immature; feet and legs bright coral pink, grey in immature. Habitat: brackish and saline coastal and inland waters.

Reference

Brown, L.H., E.K. Urban & K. Newman. (1982). The Birds of Africa, Volume I. Academic Press, London.

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