Caribbean Flamingo, Phoenicopterus ruber ruber September 2003

Fact Summary Taxonomy and Nomenclature Distribution and Habitat Physical Characteristics Behavior and Ecology Diet and Feeding Reproduction and Development Diseases and Pathology Managed Care Population and Conservation Status Web Resources Bibliography

• Higher level taxonomy is still under debate, due to mosaic of character similarities to other Orders of birds, although everyone agrees that the flamingos belong in their own Family.
• Order level taxonomic theories
  1. Ciconiiformes, Ardeidae or Ciconiidae (herons, storks); evidence based on shape of pelvis and ribs, structure of a chick's down, DNA-DNA hybridization, and mitochondrial DNA studies.
  2. Anseriformes (particularly geese); evidence based on presence of webbed feet, similarities in bill structure, vocalizations, and similar ectoparasites that have coevolved with the flamingo. In addition, the chicks are covered with down when they hatch, and they are precocious, leaving the nest within a few hours.
  3. Charadriiformes, Recurvirostridae (avocets, stilts); evidence based on comparison with fossil record, skeletal and muscular morphology, and behavior.
  4. Podicipediformes (grebes). Recent DNA studies have found a strong relationship between flamingos and grebes (Van Tuinen et al., 2001).
  5. Phoenicopteriformes Due to the unique combination of characters, many believe that flamingos belong in their own Order.
• Species level taxonomy: del Hoya et al. (1992) suggest that the 5 species are similar enough to be divided into only two groups, based on bill morphology.
  • Primitive bill: Greater flamingo (Phoenicopterus ruber subspp.) and chilean flamingo (P. chilensis)
  • More specialized: Lesser (Phoeniconaias minor), Andean (Phoenicoparrus andinus), and Puna (Phoenicoparrus jamesi).
• Scientific Name: Phoenicopterus = "crimson" (phoinix), "winged" (pterus), Greek; ruber = "red"

• Fossil Record
  • One of the oldest bird families: fossils of primitive forms date back 50 million years.
    • Juncitarsus: possible earliest ancestor in fossil record, Wyoming and Germany; shows characteristics of both shorebirds and flamingos; does not have modern flamingo-type beak.
  • Past distribution was more extensive than today.
    • Extinct species showing fully modern type of bill found in North America, Europe, and Australia.

• Four disjunct populations:
  • Galapagos Islands - 50 saline lagoons on Isabela, Santa Cruz, Floreana, Bainbridge, and Rabida Islands. Most breeding occurs on southern Isabela Island.
  • Southern Caribbean - Guajira Peninsula of Colombia, N coast of Venezuela, Bonaire, and nearby islands. A small number can be found farther east along the N coast of South America to French Guiana.
  • Yucatan Peninsula - N coast, from Campeche to Cabo Catoche, with rare sightings at Sian Ka'an Biosphere Reserve, and on Cozumel Island. Celestun Lagoon and Ria Lagartos Lagoon appear to be the most important localities, containing up to 75% of the population at a given time.
  • Northern Caribbean - Bahamas, Hispaniola, Cuba, Turks and Caicos, and southern Florida (probably escaped captives).
• Only four main breeding sites:
  • Great Inagua, Bahamas
  • Archipelago de Camaguey, Cuba
  • Rio Lagartos, Yucatan, Mexico
  • Bonaire, Netherlands Antilles
• Smaller  numbers breed in other areas within their overall range
• Distribution map based on Ogilvie &Ogilvie (1986)

• Saline lagoons, muddy flats, shallow lakes -coastal or inland. Prefers saline to fresh water.
• Can tolerate twice the salinity of sea water and alkalinity up to pH 10.5.
• Disturbances in the habitat, such as severe weather, affect resources which may cause flamingos to move around during the year, as they adapt to shifting food availability and good breeding sites.

• Tall, slender, wading birds with webbed feet.
• Neck and legs longer, relative to body size, than any other bird.
• Overall plumage color is a deep pink to red/orange ; color may be darkest on rump, head, and neck.
• Black primary and secondary feathers.
• Beak with black tip, pink to red/orange middle, and pale yellow base near the eye; upper bill often lighter in color.
• Legs pink with slightly darker knees

Beak Thick bill with sharply down turned angle; Lower bill much thicker than upper. Odd shape is characteristic of the Family. Gap of an open beak is the same along entire length (=more efficient filtration); gap of straight bill would be much larger at tip. Inner surface of beak has rows of keratinous plates (lamellae), covered with tiny hairs (cilia) through which food is strained out of water. Similar in function to a baleen whale. Tongue fits into deep groove in lower bill and acts as a piston to pump water in and out. Proximal surface of tongue with 2 longitudinal rows of spiny protuberances that point towards the throat.

Flamingo head and beak, from Zweers et al. 1995.

• See Life Stages for a description of the changes in plumage with age.
• Molting cyle is variable:
• Can occur gradually, so that there is no period of flightlessness.
• Can occur simultaneously, as seen in waterfowl, resulting in a three-week flightless period. Most often observed in captive populations.
• Occurs from twice per year to every one or two years.
• Common molting periods: (a) Just before breeding displays begin, contour feathers are replaced with full breeding plumage color, (b) Just after breeding, almost all feathers replaced, (c) Just before egg laying and during incubation, head and neck feathers may be replaced.

• Bright pink of feathers, legs, and beak comes from carotenoids that are metabolized into several different byproducts (pigments) and deposited, through the blood, to different parts of the body.
• Major pigments found in P. ruber ruber:
• Canthaxanthin (red), main pigment in feathers of all flamingo species; also found in roseate spoonbill, and scarlet ibis.
• Astaxanthin (red), main contributor to skin color of legs, minor contribution to feather color.
• The carotenoids cannot be synthesized by the flamingo, but must be ingested.
• Because there is no blood supply to the feathers once they have finished growing, it is not known how the color is retained by the animal.

• Females up to 20% smaller than males; no overlap in body size

• All flamingos have black flight feathers, and wing coverts that are darker pink that the body.
• Caribbean: the brightest overall color, knees darker pink; beak deep pink, lower bill darker.
• Greater: similar in size to Caribbean, but body, neck and head very pale pink;  knees with less contrasting color; bill with less black, the rest a light pink. Distribution- Africa, Mediterranean, Middle East, Southern Russia, India.
• Lesser: smallest; pale pink, but not as pale as Greater; slight spotting of darker pink on back;  entire bill dark red, almost black, all the way to the eye; legs dark gray/pink w/o contrasting knee color. Distribution-  mostly southeastern Africa with outlying populations in western Africa, the middle east, and India.
• Chilean: very similar to the Greater, but slightly smaller; during breeding, breast and neck may become slightly more pink; legs yellow-gray with contrasting dark pink knees and feet; bill tip black, base is very pale pink. Distribution- southwestern South America in Peru, Bolivia, Chile and Argentina from lowlands to high altitude lakes.
• Andean: similar to Chilean, but head and neck a truer pink than other flamingos (more pink than orange/pink), which extends to spotting on the breast; legs bright yellow with no contrasting knees; bill with black tip and yellow base. Distribution- small area of the Andean Altiplano at 3500 - 4500 m (12,000-15,000 ft); overlaps with Chilean and James'.
• Puna: also called "James' Flamingo"; very similar to Chilean and Andean, but smaller than both; when breeding, has band of dark pink spots on the breast; legs dark pink without contrasting knees; bill tip black, basal 2/3 is a dark yellow which is lined with red along the proximal edge and around the eye. Distribution- high elevation (usually greater than 4000 m) salt flats in Peru, Bolivia, Chile and Argentina; range overlaps the other two South American species' ranges, but much more restricted.

• Highly variable site to site, and throughout a given year.
• Studies in Yucatan, Mexico show the following patterns.
• Major activities: feeding, preening, and resting. Other activities are associated with locomotion, aggression, alertness, and comfort.
• During the breeding season, energy is diverted to courtship, nesting, and incubation.
• Most feeding occurs just prior to courtship, suggesting that stored reserves are used during synchronous breeding activities.

• Highly social, forming large colonies with tens or hundreds of thousands of individuals.
• Large numbers provide security.
• Little competition for food -algae and invertebrates tend to be concetrated and abundant.

• Tend to not defend their nest or area around themselves very aggressively

• Four types of agonistic displays were described by Rooth (1965)
  • Bill-fighting: both individuals aggressive; face each other and try to bite the head/beak area of opponent
  • Chasing: one chases another; retreating bird stretches neck out straight; chaser pecks at tail end of other.
  • Threatening: face each other with outstretched necks and open mouths, sometimes with growling vocalizations.
  • Mate protection: If a mated pair  comes in contact with another, the male will become aggressive, defending the female.

• Done in groups to synchronize breeding in a colony.
• Wing salute- wings are spread for a few seconds, showing a flash of color; the neck is stretched out and the tail is flipped up. Usually followed by head twist to the back.
• Wing-leg stretch- simultaneous stretch of one wing and leg on the same side.
• Twist-preening- rapidly alternating between stretching neck forward and twisting head around to the back, bill touching shoulders
• Head flagging- head held high, neck stretched, head slowly and rhythmically turns left and right
• Head shaking- bend neck, head waggles side to side.
• Marching- tight group marches together in one direction, then suddenly flips around and walks the other direction.
• Bowing: neck stretched forward, and angled down toward the water; wings are open about a third

• Most important function: to keep flock together.
• Very similar to geese.
• Honking sound while flying and on the ground.
• A "low gabbling noise" from groups during feeding.
• Grunting, growling noises given during breeding or aggressive displays.
• Recent captive studies by Boylan (2000) show the following:
• There are many more vocalizations than previously thought.
• There are four main components to the calls: repetitive, tonal, "buzzy", and a combination repetitive/tonal.

• Walk and run easily when threatened. Take-off requires a short run, facing wind with wings flapping.
• Fly with necks and legs outstretched, similar to cranes and storks.
• Continuous, rapid flapping, reaching speeds of 50-60 km/h (31-37 mi/hr).
• Fly in loose "v" or diagonal line, similar to geese and cranes.

• Tend to be fairly nomadic throughout the year as they follow shifting resources.
• Move to different patches within sites; move between sites up to hundreds of km apart.
• Generally, non-migratory birds.
• Those that do, migrate between summer breeding sites and winter non-breeding areas.
• In Bonaire, migration does not occur all at once, but in successive waves.
• Galapagos population sedentary.
• See Distribution for a list of the four major breeding sites.

• Diet
  • Filter feeders; small crustaceans (such as amphipods), mollusks, insects (such as midges and brine flies), polychaete worms, fish (rarely), widgeongrass seeds, muskgrass tubercles, and algae.
  • One Caribbean flamingo needs ~32,000 brine-fly chrysalids or 50,000 larvae per day.
  • Sometimes swallow mud to obtain nutrients and microorganisms, such as bacteria, and protozoa.
  • Swallowing rough granuals of sand or stone makes the gizzard more effective in grinding up shelled organisms like snails.
  • Young are fed "crop milk", which is produced by glands lining the upper digestive tract, rather than in the crop. The milk contains a high level of fat and nutrition.
• Feeding mechanism:
  • Head held upside down in shallow water (beak parallel to waterline), sweeping side to side.
  • Tongue pumps water in and out of beak like a piston (5-6 times/second). Backward curving spines on tongue help guide food to the throat. For larger food particles, the beak is used as the pumping mechanism.
  • Food particles are strained out of the water through the lamellae.
  • Top bill not fixed to the skull, but moves up and down during the filtering process. Mammals and other birds have a fixed upper jaw.
  • Also feed by picking up larger prey in their beak and swallowing (uncommon).
• Six feeding behaviors were described by Rooth (1965)
• Skimming: moving beak back and forth in the top layer of water; mostly used for plankton
• Grubbing: up-ending, like a dabbling duck; used to feed along the bottom of meter-deep water. Long legs and neck permits feeding in areas that are deeper than those used by other waders.
• Walking and seizing with beak, as with use of forceps
• Stamping -"marking time": standing in one place, lifting feet up and down; in muddy bottoms; flushes out prey
• Stamping in a circle: around the bill, which is at the center; a small mound is formed, surrounded by shallow moat; in shallow water.
• Running: along the bank, stabbing at prey with forceps-like motion; similar to feeding activity of  small herons.
• Walking, the beak tip leaving a trail: very shallow water; used for scooping mud and filtering out microorganisms.
• Water: 
  • Often do not have access to fresh water
  • Will drink rainwater when available
  • Have a salt excreting organ above the eye similar to that seen in other sea dwelling vertebrates (gulls, turtles, etc.).

• Opportunistic, erratic breeders. Breeding season varies within and among populations. Rainfall most important cue.
• First breeding at approximately 3 to 6 years
• Only fully colored adults participate in breeding.
• Most populations require a large colony for successful breeding (at least 50, but ideally hundreds or thousands). Exception: Galapagos populations will breed in groups of 5 to 10 pairs.
• Form long term pair bonds that last through several breeding seasons
• Courtship displays are used to synchronize breeding in colonies. Copulation does not occur until the pair leaves the group. See Behavior and Ecology.

• Make nests of mud by scooping with lower jaw and piling bits of mud on top of one another, smoothing with their feet. Form small, cone-shaped mounds with scooped out top.
• Approximately 30 cm (12 in.) high
• Usually a small moat is excavated around the base.
• Sometimes twigs or roots used. On rocky islands without mud, may be pile of stones.
• Both sexes build nests.
• Old nests often reused.
• Nests in a colony are built close together.

• Eggs white. Pinkish on rare occasions
• Egg is laid on the bowl-shaped top of the mud nest
• Clutch size: one egg; rarely two.
• Incubation: 27-31 days; done by both parents
• Broods: one per year

• Covered with white/gray down
• Leave nest after 5-8 days.
• Form "crèches," groups of chicks, after leaving the nest. Small number of adults care for the crèches, which can contain hundreds or thousands of chicks.

• Bills are straight for first two weeks, and then begin to develop the characteristic shape and the filtering apparatus.
• Eyes are dark brown.
• Fed "crop milk" for the first couple of months (see Diet and Feeding). Drip milk from adult beak into young's mouth. Both parents feed young this way.
• Mortality estimated at 30% during the first year.
• Feed independently at 28-42 days, but parents continue to feed until birds fledge
• Fledge: 9-13 weeks.
• In about 4 weeks, downy plumage turns dark gray.
• In 6 to 10 months, down gives way to regular feathers; plumage turns whitish gray, primaries black; beak is a light pink with black tip; legs a grey brown and begin to turn pink.

• Plumage begins to turn pale pink; darker pink on the wings.
• As adulthood is approached, pale pink turns deeper and brighter
• Base of the neck turns first, giving the appearance of a collar.

• Overall color a deep red/orange when sexual maturity is reached, at 3-5 years.
• Eyes are light yellow.
• Upper wings are last to show full color.
• Legs and feet turn deeper pink-red color; beak is yellow at base, red/orange in the middle, and black at the tip.

• Have lived more than  60 years in captivity
• Life span in the wild is unknown

• Tropical storms and hurricanes can be lethal to coastal dwelling flamingos, and may alter the habitat by flooding, reducing salinity, and reducing food resources.
• Predators: raccoons, margay, gray fox, jaguar, crocodiles, humans, and probably birds of prey.

• Little if any information is available regarding diseases in the wild.
• The following have been reported in captive populations
• Stress can make flamingos more vulnerable to sodium depletion, aspergillosus, and pneumonia.
• Bacterial diseases/infections: infection of bursae and joints from cuts caused by standing on hard surfaces; salmonellosis; septicemia; synovitis; tuberculosis
• Fungal infections: in the lungs and air sacs; infection of the plumage causes feathers to deteriorate along the edges, giving them a frayed look and making them difficult to dry
• Rickets-like disease causing bending and thinning of the bones
• Cardiovascular disease: atherosclerosis
• Kidney disease: nephritis

• Most common species found in captivity: Caribbean, Chilean, and Greater.
• Captive Breeding
  • Often will not engage in breeding displays if not part of a large enough colony. Captives in small groups have been tricked into displaying by using mirrors.
  • The color of plumage is an important breeding cue; faded flamingos in captivity often do not breed. Without the proper diet, flamingos lose their color and/or become ill.  San Diego Zoological Society uses feed that contains a chemical found in crustaceans and algae in order to avoid this.
  • Captives usually have a more consistently defined breeding season than in the wild; chicks usually hatch May - July.
• 1932: First Caribbean flamingos obtained by San Diego Zoo
• 1957: First Caribbean flamingo hatched at San Diego Zoo
• April 2003: San Diego Zoo opened its newly renovated Flamingo Lagoon, containing only P. ruber ruber.
• SD Zoological Society collections:
  • San Diego Zoo: Caribbean flamingos (Phoenicopterus ruber ruber).
  • Wild Animal Park: mixed flock of greater and lesser flamingos (Phoenicopterus ruber roseus and Phoeniconaias minor) in the Heart of Africa exhibit; Chilean flamingos (Phoenicopterus chilensis) in Nairobi Village

• Galapagos Islands: 435
• 2001 estimate.
• References: Brueker & Vargas, 1998; Delany & Scott, 2002
• Bahamas: 60,000
• ~2000 (?) estimate
• References: Delany & Scott, 2002
• Cuba: 100,000 to  200,000
• 2000 and 1996 estimates, respectively
• References: FSG, 2000; Delany & Scott, 2002
• Venezuela, and Bonaire: 34,000
• 1996 estimate
• References: Delany & Scott, 2002; Espinoza et al., 2000
• Yucatan Peninsula:  30,000
• ~2000 (?) estimate
• References: Delany & Scott, 2002
• ISIS captive population

• Believed extinct in 1924, the James' flamingo was rediscovered in 1957, its range overlapping that of the  Chilean flamingo.
• IUCN: Andean and James' flamingos are listed as species of concern
• CITES: Caribbean, Greater, Chilean, Andean, and James' flamingos, Appendix II.
• Because food and breeding sites shift spatially (due to seasonality of food resources or changing environmental conditions), larger protected areas are better than small ones because they are more likely to contain enough resources throughout the year to accommodate these shifts.

• Because the color of feathers fades quickly after plucking, the feather trade of the early 20th century did not exploit flamingos the way it did many other bird species.
• Before the relationship between diet and feather color  was well understood, zoos often over-collected in order to replace groups that had lost color or had died from poor nutrition.
• Habitat loss due to road construction and development of housing and shipping docks.
• Lead poisoning: due to the ingestion of lead shot, about 100 flamingos were reported to have died in the Yucatan in 1989. Lead bullets are now prohibited.
•  Large numbers of tourists, bird watchers and photographers can disturb colonies enough to cause substantial losses of eggs and young.

• Caribbean flamingo conservation in Mexico
• IUCN Flamingo Specialist Group
• Satellite tracking of the lesser flamingo, East Africa, Wildfowl and Wetlands Trust.

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