Lake Nakuru's flamingo connection - cycles of feast and famine in schizohaline waters

Lesser flamingoes on the edge of Lake Nakuru

An aviator once described Lake Nakuru as “a crucible of pink and crimson fire,” with a million flamingos painting an astonishing band of colour that burst into pieces as the birds took flight (Figures). Flamingo population levels in Lake Nakuru and any mass “die-offs” are popularly considered as indicators of the environmental health of Nakuru and other lakes in the African rift valley with significant flamingo populations.

In 2006, more than 30,000 of the birds were found dead at Nakuru, leaving enough pink carcases to spur an international newspaper to describe the lake as a “flamingo death camp.” Two years prior, 43,800 of the birds had perished at Tanzania’s Lake Manyara, the first major die-off documented at that alkaline, soda-rich lake. Previous mass die-offs occurred at Lake Nakuru and two other Kenyan lakes in 1993, 1995, and 1997, as well as at two lakes in Tanzania in 2002. At the same time, birds were gathering in places they have never been documented before. Since 2006 there have been additional population crashes at Nakuru and Elmentia (Table).

Flamingos numbers in Lake Nakuru are perhaps one of the most visually impressive responses to episodic but very high levels of organic productivity, driven by a well-adapted species feeding in a layered saline water body subject to periodic salinity stress (Warren, 2011). The fluctuating richness of the lake’s flamingo population was dubbed the “flamingo connection” in a benchmark paper by Kirkland and Evans (1981) that considered mesohaline evaporitic carbonates as hydrocarbon source rocks.

Flamingo flock feeding on the edge of Lake Nakuru (full-size image can be downloaded from http://www.yannarthusbertrand2.org)
Table 1. Biotal crashes in alkaline saline lakes of the African rift (from Schagerl et a., 2015)

Flamingo biology

Flamingos (Aves, Phoenicopteridae) are an ancient lineage of long-legged, microphagous, colonial wading birds. Although popularly misperceived as tropical species, flamingo distribution is more closely tied to the great deserts of the world and hypersaline lake sites, than it is to equatorial regions (Bildstein, 1993). Flamingos are filter feeders that thrive on halotolerant cyanobacterial blooms in mesohaline shallows of saline lakes around the world. This creates the context between flamingos, mesohaline planktonic blooms, and saline lakes, well documented in Lake Nakuru by Vareschi (1982) and first noted in the geological literature in that benchmark paper authored by Kirkland and Evans (1981). Sedimentary textures and structures associated with flamingo lifestyles, where these birds dominate the macrofauna in some modern saline lakes, are described by Scott et al. (2009, 2012).

Ancient avian counterparts can leave a particular set of trackways and trace fossils (including nest mounds) that can be used to refine mid-late Tertiary lacustrine depositional models (Melchor et al., 2012). Flamingo-like ancestors, which would give rise to modern ducks, even left traces in the shallow saline mudflats of Eocene soda lake sediments that define the saline portions of the trona/nahcolite-bearing sediments of the Green River formation in Utah (Figure). Two species of flamingo gather in huge numbers in Lake Nakuru and a few other East African rift lakes, namely, the greater and the lesser flamingo (Phoenicoptus ruber roseus and P. minor respectively), with the lesser flamingo having characteristic and spectacular pink-red colouration in their feathers. These bright pink waders feed and breed in mesohaline rift lake waters where cyanobacterial blooms can be so dense that a Secchi disc disappears within a few centimetres of the lake’s water surface (Warren, 1986, 2011). Lake Natron (Koeppen climate Aw), where trona is the dominant evaporite, is a major breeding ground for flamingos in East Africa and is the only regular breeding site for the lesser flamingo in Africa (Simmons 1995). Lesser flamingos build nesting platforms on the trona pavement in the more central parts of the lake. These spectacular birds not only feed in saline waters, but they can also choose to build nest mounds on evaporite pavements.

Bird trackways in mudflats of soda lakes - present and past. A. Flamingo tracks in the mudflats of modern Lake Nakuru (human footprint for scale). B. Flamingo-like trackways in the carbonate mudflats of the Eocene Green River Group (Soldiers Hill locality - wedding ring for scale)
Flamingoes with chicks at Lake Natron

Worldwide, only six sites are used for breeding by the lesser flamingos: Lake Natron (Tanzania), Etosha Pan (Namibia), Makgadikgadi-Pan (Botswana), Kamfers Dam (South Africa), as well as two pans in the “Little Rann of Kachchh” (India). Recent estimates of lesser flamingos at the main distribution areas are as follows: 1.5–2.5 million in eastern Africa; 390,000 in northwestern India; 55,000-65,000 in southwestern Africa; and 15,000–25,000 in western Africa. The highest population densities occur in Kenya (1.5 million) and Tanzania (600,000) (Childress et al. 2008). Lesser flamingos are well adapted to the harsh conditions associated with living and breeding in hypersaline alkaline conditions. Worldwide, lesser flamingoes follow an itinerant lifestyle, ranging across their distribution areas in search of saline water bodies with appropriate cyanobacterial blooms. In the East African Rift, the flocks can travel up to 200 km a day between feeding and breeding sites, which are generally at geographically separate locations (Figure).

Lake Natron has the highest concentration of breeding flamingos of any lake in East Africa. Both the greater and the lesser flamingo are found there, with the lesser flamingo outnumbering the greater by a hundred to one. Lesser flamingos bred at Lake Natron in 9 out of 14 years from 1954 to 1967. But while the trona-rich nearby Lake Natron is an essential breeding site, it is not a focal feeding site for flamingos. Major feeding sites in the Africa rift valley are Lakes Nakuru and Bogoria (formerly Lake Hannington) in Kenya and entrain waters that are mesohaline with an abundance of halotolerant cyanobacteria, dominated by Arthrospira sp. - aka Spirulina sp. (Schagerl et al., 2015). 

African rift valley A) Location of lakes and Quaternary volcanoes in the African rift valley centred on Lake Nakuru and Lake Bogoria. B) Lake Nakuru bathymetry (Dec 1979) and subsequent strandzone changes. Solid isopleths are actual shorelines at different lake levels over a 20 year period; from outer to inner are December 1979, January 1969, January 1967 and January 1961. Dashed isopleths are based on soundings taken in December, 1971. Two sewage plants are located at a and b (after Vareschi, 1978) C) Surface geology of Lake Bogoria (after McCall, 2010).

Lake Nakuru is a mesohaline soda lake with a pH ≈ 10.5 and a typical annual salinity range of 15-45‰, nearby lake Bogoria is somewhat larger, also an alkaline soda lake, with somewhat higher salinities. The Lake Nakuru depression measures some 6.5 km by 10 km, with a water covered area of some 5-45 km,2 experiencing an annual pan evaporation rate of 1500 mm beneath a Cfb Köppen climate (Figure 3b; Vareschi,1982; Krienitz and Kotut, 2010). It contains a eutrophic bottom water mass in the lake centre, with thermally stratified water column that can be up to 4.5 metres deep. The Lake Bogoria’ water mass is up to 4 km wide, some 17 km long with thermally stratified eutrophic waters up to 10 m deep. It lies beneath a Cfb climate with a pan evaporation of 2600 mm. It is fed by a combination of rainfall (≈760mm/year) and numerous (>200) hydrothermal springs about the lake edge (Figure 3c).

Lake Bogoria hydrochemistry, it seems, is more stable compared to other endorheic lakes in Kenya, because of its greater depth (10 m), steep shores and larger water volume preventing it from drying up. In contrast, Lake Nakuru resembles more a flat pan; it is much shallower (1 m) and is more subject to changes in size related to changes in water levels, at times Lake Nakuru can dry up completely. Water depths in both lakes vary from year to year, in large part depending on the vagaries of annual runoff/ inflow.

The higher level of hydrothermal inflow in Bogoria’s hydrology, along with its somewhat steeper hydrographic profile, means the lake area salinity and water depth vary less from year to year compared to Nakuru (Figure). Lakes Nakuru and Bogoria, which at peak breeding times can support lesser flamingo populations in excess of 1.5 million birds, have surface areas that are less than half those of lakes Natron and Magadi, which in turn have small areas compared to most ancient lacustrine evaporites. Yet, Nakuru and Bogoria are two of the most organically productive ecosystems in the world (Warren, 2011). What makes both lakes so productive are dense populations of halotolerant cyanobacteria, especially Arthrospira sp, which flourish and periodically reach peak growth in their waters, yet at other times organic productivity can crash. The morphological and hydrochemical contrasts likely accounts for the more frequent Arthrospira crashes and biotal community changes in Nakuru when compared to Bogoria and other lakes in the region (Table).

Lake levels in Lake Nakuru from 1930 to 1999. Data are not sufficiently detailed to record times of complete lake drying or drought and there are also substantial times when no data were collected/published (1934-1949 and 1978-1992).
Head of the Greater Flamingo shown with the bill closed and tongue extended during the filtering stage of filter feeding (left), and with the bill open and tongue retracted during the intake stage (right). Note the large recurved spines on the flattened upper surface of the tongue used to retain food (middle), as well as the lamellae along the articulating edge of the uncut upper mandible (complementary structures are also present on the lower mandible, which has been cut away in this illustration to expose the mouth cavity). Water is forced from the mouth cavity during the filtering stage by the piston-like action of the large, fatty tongue. (After Jenkin, 1957.)
Greater flamingoes feeding in Lake Nakuru
Athrospira platensis (Spirulina) is a filamentous cyanobacteria characterized by cylindrical, multicellular trichomes in an open left-hand helix and is a major food source for the lesser flamingo.

Flamingoes are filter feeders

Flamingoes (both Greater and Lesser) pass water through their bill filters in two ways (as documented by Penelope M. Jenkin in her classic article of 1957): either by swinging their heads back and forth just below the water surface, so permitting the water to flow passively through the filters of their beak, or by more efficient and more usual system of an active beak pumping. The latter is maintained by a large and powerful tongue that fills a large channel in the lower beak. As it moves rapidly back and forth, up to four times a second, it drawing water and plankton through the beak filters on the backwards pull and expelling it on the forward drive. The tongue's surface also sports numerous denticles that scrape the collected food from the filters.

Flamingo beaks have evolved into highly efficient plankton-extraction apparati that exploit the dense cyanobacterial populations periodically found in mesohaline lakes worldwide (Figure; Gould, 1987; Bildstein, 1993). The beak is unlike that possessed by any other bird group on earth; the affinity is more to the baleen of whales used to filter planktonic krill from the lit upper waters of the world's oceans. A flamingo beak houses a high volume water-filtering system made up of a piston-like tongue and hair-like structures called lamellae made up of rows of fringed platelets that line the inside of the mandible. In the lesser flamingo, the lamellae fibres have the appropriated spacing for capturing coiled filaments of Arthrospira.

Lamellar spacings are wider in the beaks of the greater flamingo than those in the beaks of the lesser flamingo, so these larger-sized birds are more generalist feeders of lake zooplankton. Thus, in any mesohaline lake where the two bird species feed and co-exist, they do not compete for the same food source. By swinging their upside-down heads from side to side just below the water surface and using the piston-like tongue to swish water through their lamella-lined beaks, flamingos can syphon the lake plankton into their gullets at phenomenal rates. Lesser flamingos can pump and filter as many as four beakfuls of plankton-rich water a second. This means some individuals filter upwards of 20,000 litres of water per day.

How the birds manage to cycle so much brackish to mesohaline waters, while maintaining their osmotic integrity, remains a mystery. When dense cyanobacterial blooms typify the rift lakes, each adult bird ingests around 72 g dry weight of Arthrospira per day (Vareschi 1978). This means the Nakuru lesser flamingo flock can swallow 50–94% of the daily primary production in the lake (about 60-80 tons). Rates of planktonic renewal in these rift lakes are incredibly high, and the required rates of biomass production by Arthrospira are spectacular. Vonshak (1997) reported doubling times of 11–20 hours of Arthrospira in a culture growing under mesohaline conditions at 35°C.

Flamingo food stock fluctuates

Flamingos (flamingoes) are mostly nocturnal feeders and will feed for up to 12-13 hours in a 24 hour period. The preferred planktonic food of the lesser flamingo is the cyanobacterium Arthrospira platensis (formerly known as Spirulina platensis), which for much of an average year is the widespread phytoplankton component in Lake Nakuru and Lake Bogoria waters (Figure ). Unfortunately, dense populations of Arthrospira sp. function best at a preferred range of temperature and salinity, meaning acme populations tend to collapse irregularly and unpredictably in both Lake Nakuru and Bogoria, leading to highly-stressed malnourished flocks of flamingos subject to mass dieback (Figure; Vareschi 1978; Kreinitz and Kotut, 2010).


Changes in total phytoplankton biomass, biomass contribution of the dominant phytoplankton species, number of flamingos, percentage contribution of Arthrospira to total phytoplankton biomass, and salinity in Lake Nakuru and Lake Bogoria in the African rift valley for the period 2001 to 2010. Note that the time scales are irregular but the same for the two lakes, while vertical scales differ in magnitude for some of the measured parameters (after Krienitz and Kotut, 2010).

Arthrospira has high levels of the red pigment phycoerythrin, and so when ingested in large volumes, it accumulates in flamingo feathers to give the birds their world-famous colouration, hence the “flamingo connection.” Once digested, the carotenoid pigment dissolves in fats, which are then deposited in the growing feathers. The same effect is seen when shrimp change colour during cooking due to carotenoid alteration. The amount of pigment laid down in the feathers depends on the quantity of pigment in the flamingo’s diet. Lesser flamingos, with beak design maximised to feed on Arthrospira, have a more intense pink colour in their feathers than greater flamingos. The latter species sits higher in the Lake Nakuru food chain and so gets the slight pink tinge in its feather colour, mostly second-hand from the lake zooplankton, which also feeds on Arthrospira.

As well as possessing very high levels of phycoerythrin in its cytoplasm, Arthrospira is also unusual among the cyanobacteria in its unusually high protein content (some ten times that of soya). This and the high growth rate of this species explains why Nakuru and Bogoria acme populations can support such spectacularly dense flamingo population levels. A lack of cellulose in the Arthrospira cell wall means it is a source of plant protein readily absorbed by the gut, making it a potentially harvestable human food source in saline water bodies in regions of desertification. In Lake Chad and some saline lakes in Mexico, Arthrospira accumulates as a lake edge scum that has been harvested for millennia by the local people (including the ancient Aztecs) and used to make nutritious biscuits.

When Arthrospira stocks are low in the rift lakes, the lesser flamingo will consume benthic diatoms. However, net primary productivity of benthic diatoms in East African soda lakes is one to two orders of magnitude less than that of Arthrospira, and the carrying capacity of the habitat with diatoms is lower by the same order (Tuite 2000). This lower productivity is seen in the peak 25,000 bird population, which are diatom feeders, in Laguna de Pozuelos in Argentina (area ≈100-130 km2, more than three times that of Nakuru, yet the peak flamingo numbers are two order of magnitude lower). In Lake Nakuru, Arthrospira and other lake plankton are also consumed by one species of introduced tilapid fish and one species of copepod and a crustacean. Rotifers, waterboatmen, and midge larvae also flourish in the mesohaline waters of Lake Nakuru. The mouth-breeding tilapid Sarotherodon alcalicum grahami was introduced to the lake in the 1950s to control the mosquito problem, and fish-feeding birds (such as pelicans) have flourished ever since (Vareschi, 1978). During times of non-optimum water conditions, when either freshening or somewhat elevated hypersalinity lessens the number of Arthrospira, the tilapids can displace the flamingos as the primary consumers of planktonic algae.

Lake Nakuru. A) Trends of algal biomass and conductivity of lake water during 1972-1978. The percent contribution of Arthrospira platensis to the total algal biomass is also shown. B) Monitored water depths, conductivities, oxygen levels and flamingo numbers at Lake Nakuru for the period 1993 to mid-2001. Water depth and flamingo data only available from 1994 to mid-2000. Data is digitised and replotted to a common time scale from data in an online progress report by Odadda et al. 2006 discussing conditions in the Lake Nakuru area (http://www.worldlakes.org last accessed Sept 19, 2019) C) Mean water temperature profiles at different times of day from 1972-1973.(A and C after Vareschi, 1982).

In 1972 Lake Nakuru waters held a surface biomass of 270 g/m3 and an average biomass of 194g/m3 but, as in most hypersaline ecosystems, Nakuru’s organic production rate varies drastically from year to year as water conditions fluctuate (Figure A; Vareschi, 1978). Arthrospira was in a long-lasting bloom in 1971-1973 and accounted for 80-100% of the copious phytoplankton biomass in those years. In 1974, however, Arthrospira almost disappeared from the lake and was replaced by much smaller-diameter planktonic species, such as coccoid cyanobacteria that dealt better with elevated salinities. This transfer in primary producer make-up in the lake waters also made the lesser flamingos less efficient feeders. When the relatively large filaments of Arthrospira dominate the lake plankton, the flamingo’s beak filters between 64 and 86% of the plankton held in each mouthful of lake water (Vareschi, 1978). When the much smaller coccoids come to dominate, the filters are a much less efficient feeding mechanism. The change in plankton species was also tied to a severe reduction in algal biomass (and protein availability), which in 1974 was down to 71 g/m3 in surface waters and averaged 137 g/m3 in the total water mass. As a result, the flamingo numbers feeding in the lake declined from 1 million to several thousand, driving a significant die-back as the salinity-stressed flamingo population moved to other lakes, like Lake Bogoria, where Arthrospira were flourishing (Vareschi, 1978).

The lower salinity limit for an Arthrospira bloom is ≈ 5‰, but it does better when salinity is more than 20‰. The species dominance of Arthrospira and its higher biomass in somewhat more saline lake waters in the African Rift lakes is seen in the near unispecific year-round biomass of nearby Lake Bogoria (salinity 40-50‰). Its surface salinity is higher year-round than Lake Nakuru (salinity ≈ 30‰) and the somewhat fresher waters of Lake Elmenteita (salinity ≈ 20‰). Because of this, Lake Bogoria is a more reliable food source for feeding flamingos compared to either Nakuru or Elmenteita. Birds tend to migrate there to feed when conditions for Arthrospira growth are not ideal in other nearby alkaline lakes (too fresh or too saline). This was the case in 1999 when high rainfall and dilution of lake waters caused the Arthrospira levels to fall in both Nakuru and Elmenteita. It was also true in late 2012 when Nakuru water levels were at near-historic highs and the waters too fresh to support a healthy Arthrospira population.

Flamingo biomass controls

A driving mechanism for the abrupt change in biomass in Lake Nakuru in the period 1972 -1974 was not clearly defined. It was thought to be related to increased salinity and lowering of lake levels, driving the growth of coccoid species other than Arthrospira sp. that are better adapted to higher salinity, but offering less protein to the feeding birds (Figure A; Vareschi, 1978). There is also the simple fact that in a lake with no surface outflow, ever more saline waters cover ever-smaller areas on the lake floor. There have been times in the last 70 years when most of Lake Nakuru has dried up and pools of saline water only a few tens of centimetres deep remained. This was the case in 1962 and more recently the case in 2008 (Figure). After the lake level lows of the 1960s, during the mid to late 1970s and in the 1980s the Nakuru hydrology returned to more typical inherent oscillations in water level and salinity (schizohalinity). The flamingo populations in Nakuru returned to impressive numbers but followed the vagaries of Arthrospira blooms. Since the early 1990s, more reliable long-term datasets on physical lake condition and flamingo numbers have been compiled (Figures).

Across that time frame, in 1993, 1995 1998, 2008 and 2012, the flamingo populations feeding in Lake Nakuru were once again at very low levels, and the remaining bird populations were stressed and subject to mass dieback. In 1998, unlike 1974, the stress on the flamingo population was related to lake freshening and rising water levels driving the decrease in Arthrospira biomass, not increased salinity and desiccation. In the preceding bountiful years, the Arthrospira-dominated biomass had bloomed at times when salinities were favourable and died back at times of elevated salinities and lake desiccation, as in 1974. By 2000, formerly low salinities had once again increased making surface waters suitable for another widespread Arthrospira bloom and the associated return of high numbers of feeding flamingos, which continued until 2007 (Figure). In 2013, there was another freshening event, with associated rising water levels and the lake's flamingo population moved to Lake Bogonia to feed.

Freshening favours a cyanobacterial assemblage dominated by picoplanktic chlorophytes (Picocyctis salinarum) and the nostocalean Anabaenopsis; the latter creates slimy masses that clog the flamingo’s feeding apparatus. The combination can drive much of the flamingo population to starvation or migration to other lakes with suitable salinities (Krienitz and Kotut, 2010). With freshening, comes also the possibility of the growth of strains that produce toxins (such as Anabaenopsis or Microcystis), possibly not in the feeding areas, which tend to remain too saline for Microcyctis, but in the thermal-spring waters where the flamingos fly in order to bathe and cleanse their feathers after a night spent feeding (Kotut and Krienitz, 2011).

It seems that breeding flamingos come to Lake Nakuru to feed in large numbers when there is water in the lake with appropriate salinity and nutrient levels to facilitate an Arthrospira bloom. In some years when heavy rains occur, lake levels rise significantly and the lake waters, although perennial, stay in the lower salinity tolerance range for Arthrospira platensis, keeping cyanobacterial numbers and protein levels at the lower end of the spectrum, as in the El Niño period between October 1997 to April 1998 and again in 2013. Once lake levels start to fall, salinities and rates of salinity change return to higher levels, then water conditions once again become appropriate for an Arthrospira bloom. But the environmental stress on the flamingos also comes with further-elevated salinities and desiccation moving lake hydrochemistry into salinities at the upper end of Arthrospira tolerance.

One of the reasons Lake Nakuru is suitable for phenomenal cyanobacterial and algal growth at times of Arthrospira bloom is the maintenance of suitable temperatures and oxygenation in the upper water mass, where the photosynthetic Arthrospira thrive. Nakuru develops a daily thermocline in the top 1.5 metres of the water column that dissipates each day in the late afternoon via wind mixing. Overturn recycles nutrients (derived from the decomposition of bird and other droppings, including those of resident hippopotami) back to the oxygenated lit surface waters to facilitate an ongoing bloom the next day (Figure).

Numbers of flamingos feeding in Lake Nakuru and Lake Bogoria are used in the popular press as indicators of the environmental health of the lakes. Thousands of birds died in Lake Nakuru in 1995, and more than 30,000 birds probably died in Lake Bogoria in the first half of 1999. The most dramatic die-offs in the last few decades were at Lake Nakuru in August 2006, when some 30,000 died, and Lake Bogoria in July 2008, when 30,000 birds died. Some environmentalists have argued in the popular press that mass die-offs and their perception of lowered numbers of flamingos in Lake Nakuru and Lake Bogoria across the 1990s and 2000s were indicators of uncontrolled forest clearance, an unchecked increase in sewerage encouraging eutrophication, and an increase in heavy metals from increasing industrial pollutants in the lake, along with general stress on the bird population from tourists and the drastic increase in local human population centred on the town of Nakuru (third largest in Kenya). Numbers of people in the town, which is the main city in the rift valley, have grown by an average of 10% every decade for the past 30 years.

But like much environmental doomsday argument, it is more based on opinionated prediction than on scientific fact. When numbers of feeding flamingos in Lake Nakuru are plotted across last few decades, it is evident that flamingo numbers oscillate widely, but it is also apparent that the peak numbers in the 2000s are equivalent to the peak numbers in the 1990s (Figure). A notion of longterm fall in numbers rather than wide natural fluctuations in numbers of feeding flamingos in the lake is not based on scientific reality

Dead lesser flamingo on the shore of Lake Bogoria, the body preserves the ophistotonus death throes.
Lake Bogoria thermal spring, with lesser flamingoes in the background.
Flamingo nest mounds atop pavement in Lake Natron
Abandoned nest moundss in Lake Natron, following  a hyena attack
Lesser flamingo chick with trone anklets due to chicks hatching while nest mounds were still surrounded by trona-saturated brine.(https://blog.nationalgeographic.org/2013/10/26/message-from-a-50-year-old-flamingo-2/) Acessed Sept 19, 2019

Likewise, when studies were done on the cause of the mass die-off in Lake Bogoria in 1999, it was found to have a natural, not an anthropogenic cause (Krienitz et al., 2003). The flamingos had ingested the remains of toxic cyanobacteria that constitute part of the population of the microbial mats that had bloomed to form a floor to the freshwater thermal spring areas about the lake edge. There the mats are dominated by thermally tolerant species; Phormidium terebriformis, Oscillatoria willei, Arthrospira subsalsa and Synechococcus bigranulatus. The influence of cyanotoxins in the deaths of the birds is reflected in autopsies which revealed: (a), the presence of hot spring cyanobacterial cells and cell fragments (especially Oscillatoria willei), and high concentrations of the cyanobacterial hepato- and neurotoxins in flamingo stomach contents and faecal pellets; (b), observations of neurological signs of bird poisoning - birds died with classic indications of neurotoxin poisoning - the ophistotonus behaviour (neck snapped back like a snake) of the flamingos in the dying phase, and the convulsed position of the extremities and neck at the time of death. Cyanobacterial toxins in stomach contents, intestine and faecal pellets were 0.196 g g-1 fresh weight (FW) for the microcystins and 4.34 g g-1 FW for anatoxin-a. Intoxication with cyanobacterial toxins probably occurred via uptake of detached cyanobacterial cells when birds come daily to the springs to drink and wash their feathers after an overnight feeding session in the saline waters of the lake proper.

When heavy metal studies were undertaken in Nakuru lake sediments, the amount of heavy metals (Cd, Cr, Cu, Hg, Ni, Pb, Zn) were found to be in the typical range of metals in sediments in lakes worldwide. The exception is Cd, which is elevated and can perhaps be ascribed to anthropogenic activity (Svengren, 2002). All other metals are present at low levels, especially if one considers that Lake Nakuru lies within a labile catchment where the bedrock is an active volcanogenic-magmatic terrane. Nearby Lake Magadi is also characterised by seasonal freshening, high productivity levels and bright red waters. In this case, the colour comes from haloalkaliphilic archaea, not cyanobacteria. Archaeal species belonging to the genera Natronococcus, Natronobacterium, Natrialba, Halorubrum, Natronorubrum and Natronomonas, all occur in soda brines of Lake Magadi.

Lake centre brines where this halobiota flourishes is at trona/halite saturation with a pH up to 12. Stratified moat waters around the trona platform edge are less chemically extreme, and moat bottom sediments preserve elevated levels of organics (≈6-8%). Lake Magadi also harbours a diverse anaerobic bacterial community in the moat waters, including cellulolytic, proteolytic, saccharolytic, and homoacetogenic bacteria (Shiba and Horikoshi, 1988; Zhilina and Zavarzin, 1994; Zhilina et al., 1996). When the homoacetogen Natroniella acetigena was isolated from this environment, its pH growth optimum was found to be 9.8–10.0, and it continued to grow in waters with pH up to 10.7 (Zhilina et al., 1996).

Flamingo numbers in the rift track cycles of “feast and famine”

Rise and fall of lake levels, drastic changes in salinity, a periodically stressed biota, and a lack of predictability in water character are endemic to life in saline ecosystems (cycles of “feast or famine”; Warren 2011, 2016). Natural variations in hydrochemistry control the number of feeding flamingos in Nakuru and Bogoria. In general, sufficient base-line scientific data in these schizohaline ecosystems is not yet available and so accurate determinations of the relative import of increased human activity versus natural environmental stresses on long-term bird numbers are not possible.

Regionally, salinities in the East African rift valley lakes range from around 30-50‰ total salts (w/v) in the more northerly lakes in the rift (Figure; Bogoria, Nakuru, Elmenteita, and Sonachi) to trona and halite saturation (>200‰) in lakes to the south (Lakes Magadi and Natron). Yet across this salinity range a combination of high ambient temperature, high light intensity and a continuous resupply of CO2, makes some of these soda lakes amongst the highest in the world in terms of their seasonal planktonic biomass (Grant et al., 1999) and also places them among the world’s most productive ecosystems (Figure; Melack and Kilham, 1974). Organic production is periodic, and pulses of organic product periodically swamp the ability of the decomposers and so accumulate as laminites in the perennial water-covered areas of some lake centres.

Less-alkaline lakes in the rift valley are dominated by periodic blooms of cyanobacteria, while the hypersaline lakes, such as Magadi, can on occasion support blooms of cyanobacteria, archaea and alkaliphilic phototrophic bacteria (Jones et al., 1998). Halotolerant and halophilic biota living in the variably saline and layered water columns constitute small-scale “feast or famine” ecosystems, which at times of “feast” are far more productive than either tropical seagrass meadows or zones of marine upwelling (Figure).

Organic productivity (maxima) in various saline ecosystems. Typical marine upwelling zone ≈ 250-500 mg C/m2day (the solid vertical line is world marine maxima, based on upwelling in offshore Peru); tropical shoal water seagrass banks ≈ 500-1200 mg C/m2day; open marine waters are less than 100 mg C/m2day and average 20 mg C/m2day, with coastal waters 40-50 mg C/m2day. However, preservation is more important than production rate in terms of source potential. Compiled from sources listed in Warren (1986, 2016).

The “flamingo connection” across the African Rift Lakes supports a general observation that short periods of enhanced organic productivity are followed by episodes of lessened productivity in various schizohaline saline lake and seaway waters worldwide, both past and present (Warren, 2011). It reflects the general principle that increased environmental stress favours the survival of a few well-adapted and specialised halotolerant species. A biota that is well adapted to the feast and famine life-cycle exists in most saline depressions and means biomass numbers are subject to wide fluctuations tied to wide fluctuations in a saline lakes hydrochemistry (schizohaline waters). This same general principle of schizohaline ecosystem adaption is clearly seen in the periodic decrease in invertebrate species (grazers and predators) numbers with increasing salinity in the carbonate lakes of the Coorong of Southern Australia, where the only metazoan to remain alive in waters with salinities more than 200‰ are the southern hemisphere brine shrimp (Parartemia zietziania). It is seen in population fluctuations of the motile alga Dunaliella sp. in the Dead Sea, and the fluctuating purple bacterial communities of Lake Mahoney in Canada. All these examples underline a general principle of “life will expand into the available niche” a paradigm that in the hypersaline cases we have discussed is driven by fluctuating salinities inherent to saline-tolerant and saline-adapted ecosystems (Warren, 2011).

Lake Bogoria, Kenya