Lake Nakuru Flamingoes

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Salty MattersJohn Warren - Friday, May 23, 2016 Lake Nakuru flamingoes– Life’s response to feast and famine in schizohaline lacustrine hydrologies The Flamingo Connection Nakuru, leaving enough pink carcases to spur an international newspaper to describe the lake as a “flamingo death An aviator once described Lake Nakuru as “a crucible of camp.” Two years prior, 43,800 of the birds had perished pink and crimson fire,” with a million flamingos painting at Tanzania’s Lake Manyara, the first major die-off docu- an astonishing band of colour that burst into pieces as the mented at that alkaline, soda-rich lake. Previous mass die- birds took flight (Figure 1). offs occurred at Lake Nakuru and two other Kenyan lakes Flamingo population levels in Lake Nakuru and any mass in 1993, 1995, and 1997, as well as at two lakes in Tanzania “die-offs” are popularly considered as indicators of the en- in 2002. At the same time, birds were gathering in places vironmental health of Nakuru and other lakes in the Af- they have never been documented before. Since 2006 there rican rift valley with significant flamingo populations. In have been additional population crashes at Nakuru and El- 2006, more than 30,000 of the birds were found dead at mentia (Table 1).

Figure 1. Flamingo ock feeding on the edge of Lake Nakuru (full-size image can be downloaded from http://www.yannarthusber- trand2.org)

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Date of crash Lake Reference where these birds dominate the macrofauna in 1971 Elmenteita Melack and Kilham 1974 some modern saline lakes, are described by Scott 1973 Nakuru Vareschi et al. 1981 et al. (2009, 2012). Ancient avian counterparts can 1973 (Mar- Sep) Bogoria Melack 1976 leave a characteristic set of trackways and trace 1973, 1974 Elmenteita Melack 1988 fossils (including nest mounds) that can be used 1974 Nakuru Vareschi 1982 1974, 1976 Elmenteita Tuite 1981 to refine mid-late Tertiary lacustrine depositional 1974 (Jan-Mar) Nakuru Tuite 2000 models (Melchor et al., 2012). Flamingo-like an- 2001 (Jun) Nakuru Ballot et al. 2004 cestors, which would give rise to modern ducks, 2001 (Oct) Bogoria Harper et al. 2003 even left traces in the shallow saline mudflats of 2002 (Sep) Elmenteita Ballot et al. 2004 Eocene soda lake sediments that define the saline 2004 Elmenteita Schargel and Odour 2008 portions of the trona/nahcolite-bearing sediments 2004 (Jul to Oct) Bogoria Schargel and Odour 2008 of the Green River formation in Utah (Figure 2). 2006 Bogoria Krienitz & Kotut 2010 2008 (Dec) - 2009 Nakuru Kaggwa etal. 2012 Two species of flamingo gather in huge numbers (Apr) & 2009 (Sep- in Lake Nakuru and a few other East African rift Oct) & 2013 lakes, namely, the greater and the lesser flamingo 2011 Elmenteita Krienitz at al., 2013 (Phoenicoptus ruber roseus and P. minor respec- 2012 Nakuru Krienitz et al. 2013 tively), with the lesser flamingo having character- Table 1. Biotal crashes in alkaline saline lakes of the African rift (from Schagerl et al., 2015) istic and spectacular pink-red colouration in their feathers. These bright pink waders feed and breed in mesohaline rift lake waters where cyanobacte- Flamingos numbers in Lake Nakuru are perhaps one of rial blooms can be so dense that a Secchi disc disappears the most visually impressive responses to episodic but very within a few centimetres of the lake’s water surface (War- high levels of organic productivity, driven by a well-adapt- ren, 1986, 2011). Lake Natron (Koeppen climate Aw), ed species feeding in a layered saline water body subject where trona is the dominant evaporite, is a major breeding to periodic salinity stress (Warren, 2011). The fluctuating ground for flamingos in East Africa and is the only regular richness of the lake’s flamingo population was dubbed the breeding site for the lesser flamingo in Africa (Simmons “flamingo connection” in a benchmark paper by Kirkland 1995). Lesser flamingos build nesting platforms on the and Evans (1981) that considered mesohaline evaporitic carbonates as hydrocarbon source rocks. Flamingo biology Flamingos (Aves, Phoenicopte- ridae) are an ancient lineage of long-legged, microphagous, colo- nial wading birds. Although popularly misperceived as tropical species, flamingo distribution is more closely tied to the great deserts of the world and to 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) A. B. and first noted in the geologi- cal literature in that benchmark Figure 2. Bird trackways in mud ats of soda lakes - present and past. A. Flamingo tracks in the mud ats of modern Lake Nakuru (fohuman footprint for scale). B. Kirkland and Evans paper. Sed- Flamingo-like trackways in the carbonate mud ats of the Eocene Green River Group imentary textures and structures (Soldiers Hill locality - wedding ring for scale) associated with flamingo lifestyles, Page 2 www.saltworkconsultants.com

b Sandai Wasages R. Lake Bogoria (Figure 3). Rift Valley Lakes Lake Nakuru Alluvial & colluvial deposits Loboi Landslips (megabreccias) Sands, silts, muds (deltaic) Lake Natron has the highest con- of the African Rift Njiro Sandai Organic muds & evaporites delta Volcanic rocks centration of breeding flamingos a Comorant Hydrothermal hot springs Point Quat. volcano Namarunu of any lake in East Africa. Both 2°N Rift lake Rift fault Emuruan- the greater and the lesser flamin- goglak

Silali Lomudioc 4.4 go are found there, with the lesser Paka Ndolaita Korosi Maji ya flamingo outnumbering the great- Lake Bogoria Moto er by a hundred to one. Lesser fla- Lake Bogoria 0° Loburu mingos bred at Lake Natron in 9 Nyanza Rift 4.4 delta Lake Nakuru L. Elmenteita out of 14 years from 1954 to 1967. 4.3 Mawe Eburru L. Naivasha Baboon Cli Moto Olkaria Longonot But while the trona-rich nearby Suswa Lake Natron is an essential breeding site, it is not a focal feeding site 100 km Lake Magadi 3 3.9 Kipsirian R. Emsos 2°S 1 km 1.1 fan-delta for flamingos. Major feeding sites Parkimchai R. Lake Natron 1 in the Africa rift valley are Lakes A. Ol Doniyo B. C. 4 km 36°E 38°E Lengai Water depths in metres Makarlia Nderit Emsos Nakuru and Bogoria (formerly Figure 3. African rift valley A) Location of lakes and Quaternary volcanoes in the African rift valley centred Lake Hannington) in Kenya and on Lake Nakuru and Lake Bogoria. B) Lake Nakuru bathymetry (Dec 1979) and subsequent strandzone entrain waters that are mesohaline changes. Solid isopleths are actual shorelines at di erent 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 with an abundance of halotolerant soundings taken in December, 1971. Two sewage plants are located at a and b (after Vareschi, 1978) C) cyanobacteria, dominated by Ar- Surface geology of Lake Bogoria (after McCall, 2010). throspira (Schagerl et al., 2015). Lake Nakuru is a mesohaline soda trona pavement in the more central parts of the lake. These lake with a pH ≈ 10.5 and a typi- spectacular birds not only feed in saline waters, they can cal annual salinity range of 15-45‰, nearby lake Bogoria choose to build nest mounds on evaporite pavements! is somewhat larger, also an alkaline soda lake, with somewhat higher salinities. The Lake Nakuru depression mea- Worldwide, only six sites are used for breeding by the lesser sures some 6.5 km by 10 km, with a water covered area of flamingos: Lake Natron (Tanzania), Etosha Pan (Namib- some 5-45 km,2 experiencing an annual pan evaporation ia), Makgadikgadi-Pan (Botswana), Kamfers Dam (South rate of 1500 mm beneath a Cfb Köppen climate (Figure Africa), as well as two pans in the “Little Rann of Kachchh” 3b; Vareschi,1982; Krienitz and Kotut, 2010). It contains a (India). Recent estimates of lesser flamingos at the main eutrophic bottom water mass in the lake centre, with ther- distribution areas are as follows: 1.5–2.5 million in eastern mally stratified water column that can be up to 4.5 metres Africa; 390,000 in northwestern India; 55,000-65,000 in deep. The Lake Bogoria’ water mass is up to 4 km wide, southwestern Africa; and 15,000–25,000 in western Af- some 17 km long with thermally stratified eutrophic wa- rica. The highest population densities occur in Kenya (1.5 ters up to 10 m deep. It lies beneath a Cfb climate with a million) and Tanzania (600,000) (Childress et al. 2008). pan evaporation of 2600 mm. It is fed by a combination of Lesser flamingos are well adapted to the harsh con- 4 ditions associated with liv- 3.5 Mean annual rainfall = 750 mm Nakuru water depth ing and breeding in hyper- (peaks in Nov-Dec and Apr.-May 1930-1999 saline alkaline conditions. 3 Mean annual evaporation = 1800 mm Worldwide, they follow an 2.5 Lake elevation 1759 m.s.l itinerant lifestyle, ranging Mean water depth 2.5m, maximum 4.5m across their distribution ar- 2 eas in search of saline wa- 1.5 ter bodies with appropriate (m) Lake level 1 cyanobacterial blooms. In the east African rift the no data flocks can travel up to 200 0 no data km a day between feeding 1930 1931 1932 1933 1993 1994 1995 1996 1997 1998 1999 and breeding sites, which 1950 1951 1952 1953 1954 1955 1956 1957 1958 1959 1960 1961 1962 1963 1964 1965 1966 1967 1968 1969 1970 1971 1972 1973 1974 1975 1976 1977 1978 1979 YEAR

are generally at geograph- 1980-1992 1934-1949 ically separate locations Figure 4. Lake levels in Lake Nakuru from 1930 to 1999. Data are not su ciently 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).

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rainfall (≈760mm/year) and numerous (>200) hydrother- into highly efficient plankton-extraction apparati that mal springs about the lake edge (Figure 3c). exploit the dense cyanobacterial populations periodically found in mesohaline lakes worldwide (Figure 5; Gould, Lake Bogoria hydrochemistry, it seems, is more stable 1987; Bildstein, 1993). The beak is unlike that possessed compared to other endorheic lakes in Kenya, because of its by any other bird group on earth; the affinity is more to greater depth (10 m), steep shores and larger water volume the baleen of whales used to filter planktonic krill from preventing it from drying up. In contrast, Lake Nakuru re- the lit upper waters of world's oceans. A flamingo beak sembles more a flat pan; it is much shallower (1 m) and is houses a high volume water-filtering system made up of a more subject to changes in size related to changes in water piston-like tongue and hair-like structures called lamellae levels, at times Lake Nakuru can dry up completely. Water made up of rows of fringed platelets that line the inside depths in both lakes vary from year to year, in large part of the mandible. In the lesser flamingo, the lamellae fibres depending on the vagaries of annual runoff/ inflow. The have the appropriated spacing for capturing coiled fila- higher level of hydrothermal inflow in Bogoria’s hydrolo- ments of Arthrospira. Lamellar spacings are wider in the gy, along with its somewhat steeper hydrographic profile, beaks of the greater flamingo than those in the beaks of the means the lake area salinity and water depth vary less from lesser flamingo so these larger-sized birds are more gener- year to year compared to Nakuru (Figure 4). alist feeders of lake zooplankton. Thus, in any mesohaline Lakes Nakuru and Bogoria, which at peak breeding times lake where the two bird species feed and co-exist, they do can support lesser flamingo populations in excess of 1.5 not compete for the same food source. By swinging their million birds, have surface areas that are less than half those upside-down heads from side to side just below the water of lakes Natron and Magadi, which in turn have small areas surface and using the piston-like tongue to swish water compared to most ancient lacustrine evaporites. Yet Nak- through their lamella-lined beaks, flamingos can syphon uru and Bogoria are two of the most organically produc- the lake plankton into their gullets at phenomenal rates. tive ecosystems in the world (Warren, 2011). What makes Lesser flamingos can pump and filter as many as 4 beakfuls both lakes so productive are dense populations of halotol- of plankton-rich water a second. This means some individ- erant cyanobacteria, especially Arthrospira sp, which flour- uals filter upwards of 20,000 litres of water per day. ish and periodically reach peak growth in their waters yet How the birds manage to cycle so much brackish to me- at other times organic productivity can crash. The morpho- sohaline waters, while maintaining their osmotic integrity, logical and hydrochemical contrasts likely accounts for the remains a mystery. When the rift lakes are typified by dense more frequent Arthrospira crashes and biotal community cyanobacterial blooms, each adult bird ingests around 72 g changes in Nakuru when compared to Bogoria and other dry weight of Arthrospira per day (Vareschi 1978). This lakes in the region (Table 1). means the Nakuru lesser flamingo flock is able to ingest Flamingoes as filter feeders 50–94% of the daily primary production in the lake (about 60-80 tons). Rates of planktonic renewal in these rift Flamingos pass water through their bill filters in two ways lakes is obviously extremely high and the required rates (as documented by Penelope M. Jenkin in her classic ar- of biomass production by Arthrospira can be spectacular. ticle of 1957): either by swinging their heads back and Vonshak (1997) reported doubling times of 11–20 hours 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 power- ful tongue that fills a large chan- nel 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 Figure 5. Head of the Greater Flamingo shown with the bill closed and tongue extended during the ltering stage of lter feeding numerous denticles that scrape (left), and with the bill open and tongue retracted during the intake stage (right). Note the large recurved spines on the attened upper surface of the tongue used to retain food (middle), as well as the lamellae along the articulating edge of the uncut upper the collected food from the filters. 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 ltering stage by the piston-like action of the large, Flamingo beaks have evolved fatty tongue. (After Jenkin, 1957.)

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of Arthrospira in a culture growing under mesohaline con- gets the slight pink tinge in its feather colour, mostly sec- ditions at 35°C. ond-hand from the lake zooplankton, which also feed on Arthrospira. Flamingo food As well as possessing very high levels of phycoerythrin in Flamingos (flamingoes) are mostly nocturnal feeders and its cytoplasm, Arthrospira is also unusual among the cya- will feed for up to 12-13 hours in a 24 hour period. The nobacteria in its unusually high protein content (some preferred planktonic food of the lesser flamingo is the cy- ten times that of soya). This, and the high growth rate of anobacterium Arthrospira platensis (formerly known as this species, explains why Nakuru and Bogoria acme pop- Spirulina platensis), which for much of an average year is ulations can support such spectacular population levels of the widespread phytoplankton component in Lake Nakuru flamingos. A lack of cellulose in the Arthrospira cell wall and Lake Bogoria waters (Figure 6). Unfortunately, dense means it is a source of plant protein readily absorbed by the populations of Arthrospira function best at a preferred gut, making it a potentially harvestable human food source range of temperature and salinity, meaning acme popu- in saline water bodies in regions of desertification. In Lake lations tend to collapse irregularly and unpredictably in Chad, and in some saline lakes in Mexico, Arthrospira ac- both Lake Nakuru and Bogoria, leading to highly-stressed cumulates as a lake edge scum that has been harvested for malnourished flocks of flamingos subject to mass dieback millennia by the local people (including the ancient Az- (Figure 6; Vareschi 1978; Kreinitz and Kotut, 2010). tecs) and used to make nutritious biscuits. Arthrospira has high levels of the red pigment phycoeryth- When Arthrospira stocks are low in the rift lakes, the less- rin and so when ingested in large volumes it accumulates er flamingo will consume benthic diatoms. However, net in flamingo feathers to giveHalobiota the birds their world famous primary productivityFlamingo of numbersbenthic diatoms in East African colouration, hence the “flamingoArthrospira connection.” Once di-Picocystissoda lakes is one to>500,000 two orders of magnitude less than that Other algae gested, the carotenoid pigment Anabaenopsisdissolves in fats, which are of Arthrospira, and>100,000 the carrying capacity of the habitat Other cyanobacteria >100,000 then deposited in the growing feathers. The same effect is with diatoms is lower by the same order (Tuite 2000). This seen when shrimp change colour during cooking due to lower productivity is seen in the peak 25,000 bird popula- carotenoid160 alteration. The amount of pigment laid down tion, which are768 diatom feeders, in Laguna de Pozuelos in 600 in the feathers depends on the quantity of pigment in the Argentina (area ≈100-130 km2, more than 3 times that flamingo’s diet. Lesser flamingos, with beak design max- of Nakuru, yet the peak flamingo numbers are two order imised120 to feed on Arthrospira have a more intense pink ) of magnitude lower). In Lake Nakuru, Arthrospira and -1 )

colour in their feathers than greater flamingos. The latter -1 other400 lake plankton are also consumed by one species of species sits higher in the Lake Nakuru food chain and so 80

Biomass (mg.l 400

40 Biomass (mg.l

0 0 100 100 75 80 60 50 40 25 Arthrospira

Arthrospira % 20 0 0 60 60

40 50

20 40 Salinity ‰ Salinity ‰ 0 30 Jul. 2008 Jul. Jan. 2002 Jan. 2010 Jul. 2008 Jul. Nov. 2001 Nov. Oct. 2003 Feb. 2005 Feb. 2006 Feb. 2009 Feb. Sep. 2002 Sep. 2004 Sep. Mar. 2002 Mar. 2003 Mar. 2004 Mar. June 2001 Aug. 2006 Aug. Jan. 2002 Jan. 2010 Nov. 2001 Nov. Oct. 2003 Feb. 2005 Feb. 2006 Feb. 2009 Feb. Sep. 2002 Sep. 2004 Sep. Mar. 2002 Mar. 2003 Mar. 2004 Mar. June 2001 Aug. 2006 Aug. Lake Nakuru Lake Bogoria Figure 6. Changes in total phytoplankton biomass, biomass contribution of the dominant phytoplankton species, number of amingos, 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 lake while vertical scales dier in magnitude for some of the measured parameters (after Krienitz and Kotut, 2010).

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introduced tilapid fish and one species of copepod and a the total water mass. As a result, the flamingo numbers crustacean. Rotifers, waterboatmen, and midge larvae also feeding in the lake declined from 1 million to several thou- flourish in the mesohaline waters of Lake Nakuru. The sand, driving a significant die-back as the salinity-stressed mouth-breeding tilapid Sarotherodon alcalicum grahami flamingo population moved to other lakes, like Bogoria, was introduced to the lake in the 1950s to control the mos- where Arthrospira were flourishing (Vareschi, 1978). quito problem and fish-feeding birds (such as pelicans) The lower salinity limit for an Arthrospira bloom is ≈ 5‰, have flourished ever since (Vareschi, 1978). During times but it does better when salinity is more than 20‰. The of non-optimum water conditions, when either freshening species dominance of Arthrospira and its higher biomass or somewhat elevated hypersalinity lessens the number of in somewhat more saline lake waters in the African Rift Arthrospira, the tilapids can displace the flamingos as the lakes is clearly seen in the near unispecific year-round bio- primary consumers of planktonic algae. mass of nearby Lake Bogoria (salinity 40-50‰). Its sur- In 1972 Lake Nakuru waters held a surface biomass of face salinity is higher year round than Lake Nakuru (sa- 270 g/m3 and an average biomass of 194g/m3 but, as in linity ≈ 30‰) and the somewhat fresher waters of Lake most hypersaline ecosystems, Nakuru’s organic production Elmenteita (salinity ≈ 20‰; Figure 3a). Because of this, rate varies drastically from year to year as water condi- Lake Bogoria is a more reliable food source for feeding tions fluctuate (Figure 7; Vareschi, 1978). Arthrospira was flamingos compared to either Nakuru or Elmenteita. Birds in a long-lasting bloom in 1971-1973, and accounted for tend to migrate there to feed when conditions for Arthro- 80-100% of the copious phytoplankton biomass in those spira growth are not ideal in other nearby alkaline lakes years. In 1974, however, Arthrospira almost disappeared (too fresh or too saline). This was the case in 1999 when from the lake and was replaced by much smaller-diame- high rainfall and dilution of lake waters caused the Ar- ter planktonic species, such as coccoid cya- Temperature °C nobacteria that dealt A. C. 20 21 21 21 21 23 21 23 25 21 23 25 21 23 21 Conductivity 0 better with elevated 250 Algal biomass 35 salinities. This trans- Spirulina percent 0.5 200 30

fer in primary pro- , dry wt.) 1.0 3 ducer make-up in the m 150 25 1.5 lake waters also made 100% Depth (m ) 2.0 the lesser flamingos 100 20 2.5 less efficient feeders. 50% Conductivity (mS, 20°C ) 50 15 When the relative- 10 0 10% 10 ly large filaments of Algal biomass (g/ 0 0900- 1 1 1972 1973 1974 1975 1976 1978 100-130 0 2200-020 0 0600-090 0 1300-150 0 0200-060 0 1500-180 0 Av. Air 1800-220 0 Arthrospira dominate Year Temp °C 16.1 14.3 15.5 19.2 22.1 24.3 22.0 17.4 the lake plankton, the 20 200 120 5 flamingo’s beak filters O Conductivity 2 Flamingo numbers between 64 and 86% Depth 100 4 of the plankton held 15 150 ) in each mouthful of 80 4 lake water (Vares- 3 10 chi, 1978). When the 100 60

2 Depth (m ) much smaller coc- 40 Oxygen (mg/l ) coids come to dom- 5 Conductivity (mS/cm ) 50

Flamingoes (x1 0 1 inate, the filters are 20 a much less efficient 0 0 0 0 feeding mechanism. 1993 1994 1995 1996 1997 1998 1999 2000 2001 The change in plank- B. ton species was also Figure 7. Lake Nakuru. A) Trends of algal biomass and conductivity of lake water during 1972-1978. tied to a severe reduc- The percent contribution of Arthrospira platensis to the total algal biomass is also shown. B) Moni- tion in algal biomass tored water depths, conductivities, oxygen levels and amingo numbers at Lake Nakuru for the (and protein availabil- period 1993 to mid 2001. Water depth and amingo data only available from 1994 to mid 2000. ity), which in 1974 Data is digitised and replotted to a common time scale from data in an online progress report by was down to 71 g/m3 Odadda et al. 2006 discussing conditions in the Lake Nakuru area (http://www.worldlakes.org last in surface waters and accessed Sept 24, 2012) C) Mean water temperature proles at dierent times of day from averaged 137 g/m3 in 1972-1973.(A and C after Vareschi, 1982).

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throspira levels to fall in both Nakuru and Elmenteita. It also the possibility of the growth of strains that produce was also true in late 2012 when Nakuru water levels were toxins (such as Anabaenopsis or Microcystis), possibly not at near-historic highs and the waters too fresh to support a in the feeding areas, which tend to remain too saline for healthy Arthrospira population. Microcyctis, but in the spring waters where the flamingos fly in order to bathe and cleanse their feathers after a night Flamingo biomass controls spent feeding (Kotut and Krienitz, 2011). A driving mechanism for the abrupt change in biomass It seems that breeding flamingos come to Lake Nakuru in Lake Nakuru in the period 1972 -1974 was not clearly to feed in large numbers when there is water in the lake defined. It was thought to be related to increased salinity with appropriate salinity and nutrient levels to facilitate an and lowering of lake levels, driving the growth of coccoid Arthrospira bloom. In some years when heavy rains occur, species other than Arthrospira sp. that are better adapted lake levels rise significantly and the lake waters, although to higher salinity, but offering less protein to the feeding perennial, stay in the lower salinity tolerance range for Ar- birds (Figure 7a; Vareschi, 1978). There is also the simple throspira platensis, keeping cyanobacterial numbers and fact that in a lake with no surface outflow, ever more sa- protein levels at the lower end of the spectrum, as in the line waters cover ever-smaller areas on the lake floor. There El Niño period between October 1997 to April 1998 and have been times in the last 70 years when most of Lake again in 2013. Once lake levels start to fall, salinities and Nakuru has dried up and pools of saline water only a few rates of salinity change return to higher levels, then water tens of centimetres deep remained. This was the case in conditions once again become appropriate for an Arthro- 1962 and most recently the case in 2008 (Figure 4). spira bloom. But the environmental stress on the flamingos After the lake level lows of the 1960s, during the mid to also comes with further-elevated salinities and desiccation late 1970s and in the 1980s the Nakuru hydrology re- moving lake hydrochemistry into salinities at the upper turned to more typical inherent oscillations in water level end of Arthrospira tolerance. and salinity (schizohalinity). The flamingo populations in One of the reasons Lake Nakuru is suitable for phenome- Nakuru returned to impressive numbers but followed the nal cyanobacterial and algal growth at times of Arthrospira vagaries of Arthrospira blooms. Since the early 1990s more bloom is the maintenance of suitable temperatures and oxy- reliable long-term datasets on physical lake condition and genation in the upper water mass, where the photosynthet- flamingo numbers have been compiled (Figures 5, 7b). In ic Arthrospira thrive. Nakuru develops a daily thermocline that time frame, in 1993, 1995 1998, 2008 and 2012, the in the top 1.5 metres of the water column that dissipates flamingo populations feeding in Lake Nakuru were once each day in the late afternoon via wind mixing. Overturn again at very low levels and the remaining bird populations recycles nutrients (derived from the decomposition of bird were stressed and subject to mass dieback. and other droppings, including those of resident hippopot- In 1998, unlike 1974, the stress on the flamingo popula- ami) back to the oxygenated lit surface waters to facilitate tion was related to lake freshening and rising water levels an ongoing bloom the next day (Figure 7c). driving the decrease in Arthrospira biomass, not increased Numbers of flamingos feeding in Lake Nakuru and Lake salinity and desiccation. In the preceding bountiful years, Bogoria are used in the popular press as indicators of the the Arthrospira-dominated biomass had bloomed at times environmental health of the lakes. Thousands of birds when salinities were favourable and died back at times of died in Lake Nakuru in 1995 and more than 30,000 birds elevated salinities and lake desiccation, as in 1974. By 2000 may have died in Lake Bogoria in the first half of 1999. formerly low salinities had once again increased making The most dramatic die-offs in the last two decades were surface waters suitable for another widespread Arthrospira at Lake Nakuru in August 2006, when some 30,000 died, bloom and the associated return of high numbers of feed- and Lake Bogoria in July 2008, when 30,000 birds died. ing flamingos, which continued until 2007 (Figure 7c). In Some environmentalists have argued in the popular press 2013 there was another freshening event, with associat- that mass die-offs and their perception of lowered num- ed rising water levels and the lakes flamingo population bers of flamingos in Lake Nakuru and Lake Bogoria across moved to Lake Bogonia to feed. the 1990s and 2000s were indicators of uncontrolled forest Freshening favours a cyanobacterial assemblage dominat- clearance, an uncontrolled increase in sewerage encourag- ed by picoplanktic chlorophytes (Picocyctis salinarum) ing eutrophication, and increase in heavy metals from in- and the nostocalean Anabaenopsis; the latter creates slimy creasing industrial pollutants in the lake, along with general masses that clog the flamingo’s feeding apparatus. The stress on the bird population from tourists and the drastic combination can drive much of the flamingo population to increase in local human population centred on the town of starvation or migration to other lakes with suitable salin- Nakuru (third largest in Kenya). Numbers of people in the ities (Krienitz and Kotut, 2010). With freshening, comes town, which is the main city in the rift valley, have grown by an average of 10% every decade for the past 30 years.

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But like much environmental doomsday argument, it is biota flourishes is at trona/halite saturation with a pH up more based on opinionated prediction than on scientific to 12. Stratified moat waters around the trona platform fact. When numbers of feeding flamingos in Lake Nak- edge are less chemically extreme and moat bottom sedi- uru are plotted across last few decades, it is evident that ments preserve elevated levels of organics (≈6-8%). Lake flamingo numbers oscillate widely, but it is also apparent Magadi also harbours a varied anaerobic bacterial commu- that the peak numbers in 2000s are equivalent to the peak nity in the moat waters, including cellulolytic, proteolyt- numbers in 1990s. A notion of longterm fall in numbers ic, saccharolytic, and homoacetogenic bacteria (Shiba and rather than wide natural fluctuations in numbers of feed- Horikoshi, 1988; Zhilina and Zavarzin, 1994; Zhilina et ing flamingos in the lake is not based on scientific reality. al., 1996). When the homoacetogen Natroniella acetigena was isolated from this environment, its pH growth opti- Likewise, when studies were done on the cause of the mass mum was found to be 9.8–10.0, and it continued to grow die-off in Lake Bogoria in 1999, it was found to have a in waters with pH up to 10.7 (Zhilina et al., 1996). natural, not an anthropogenic cause (Krienitz at al., 2003). The flamingos had ingested the remains of toxic cyanobac- Flamingo numbers track feast and famine teria that constitute part of the population of the microbial mats that had bloomed to form a floor to the fresh water Rise and fall of lake levels, drastic changes in salinity, a pe- thermal spring areas about the lake edge. There the mats riodically stressed biota, and a lack of predictability in wa- are dominated by thermally tolerant species; Phormidium ter character are endemic to life in saline ecosystems (cycles terebriformis, Oscillatoria willei, Arthrospira subsalsa and of “feast or famine”). Natural variations in hydrochemistry Synechococcus bigranulatus. The influence of cyanotoxins control the number of feeding flamingos in Nakuru and in the deaths of the birds is reflected in autopsies which Bogoria. In general, sufficient base-line scientific data in revealed: (a), the presence of hot spring cyanobacterial cells these schizohaline ecosystems is not yet available and so and cell fragments (especially Oscillatoria willei), and high accurate determinations of the relative import of increased concentrations of the cyanobacterial hepato- and neuro- human activity versus natural environmental stresses on toxins in flamingo stomach contents and faecal pellets; (b), longterm bird numbers are not possible. observations of neurological signs of bird poisoning - birds Regionally, salinities in the east African rift valley lakes died with classic indications of neurotoxin poisoning - the range from around 30-50‰ total salts (w/v) in the more ophistotonus behaviour (neck snapped back like a snake) northerly lakes in the rift (Figure 3a; Bogoria, Nakuru, of the flamingos in the dying phase, and the convulsed Elmenteita, and Sonachi) to trona and halite saturation position of the extremities and neck at the time of death. (>200‰) in lakes to the south (Lakes Magadi and Na- Cyanobacterial toxins in stomach contents, intestine and tron). Yet across this salinity range a combination of high faecal pellets were 0.196 g g-1 fresh weight (FW) for the ambient temperature, high light intensity and a continuous microcystins and 4.34 g g-1 FW for anatoxin-a. Intoxi- resupply of CO2, makes some of these soda lakes amongst cation with cyanobacterial toxins probably occurred via the highest in the world in terms of their seasonal plank- uptake of detached cyanobacterial cells when birds come tonic biomass (Grant et al., 1999) and also places them daily to the springs to drink and wash their feathers after among the world’s most productive ecosystems (Figure 8; an overnight feeding session in the saline waters of the lake Melack and Kilham, 1974). Organic production is period- proper. ic, and pulses of organic product periodically swamp the When heavy metal studies were undertaken in Nakuru ability of the decomposers and so accumulate as laminites lake sediments, the amount of heavy metals (Cd, Cr, Cu, in the perennial water-covered areas of some lake centres. Hg, Ni, Pb, Zn) were found to be in the typical range of Less-alkaline lakes in the rift valley are dominated by peri- metals in sediments in lakes worldwide. The exception is odic blooms of cyanobacteria, while the hypersaline lakes, Cd, which is elevated and can perhaps be ascribed to an- such as Magadi, can on occasion support blooms of cya- thropogenic activity (Svengren, 2002). All other metals are nobacteria, archaea and alkaliphilic phototrophic bacteria present at low levels, especially if one considers that Lake ( Jones et al., 1998). Halotolerant and halophilic biota liv- Nakuru lies within a labile catchment where the bedrock is ing in the variably saline and layered water columns con- an active volcanogenic-magmatic terrane. stitute small-scale “feast or famine” ecosystems, which at Nearby Lake Magadi is also characterised by seasonal times of “feast” are far more productive than either tropical freshening, high productivity levels and bright red waters. seagrass meadows or zones of marine upwelling (Figure 8). In this case, the colour comes from haloalkaliphilic archaea, The “flamingo connection” across the African Rift Lakes not cyanobacteria. Archaeal species belonging to the gen- supports a general observation that short periods of en- era Natronococcus, Natronobacterium, Natrialba, Halo- hanced organic productivity are followed by episodes of rubrum, Natronorubrum and Natronomonas, all occur in lessened productivity in various schizohaline saline lake soda brines of Lake Magadi. Lake centre brines where this and seaway waters worldwide. both past and present

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Upwelling zone (Peru near 15°S) 3000

Dry Valley Lake (Antarctica) 3600 Biomass

Soap Lake (USA) 7000 Drakesbad Hot Spring (USA) 2919 Great Salt Lake (USA) 6147 Devils Lake (USA) 140 Borax Lake (USA) 525 Marine upwelling Abundanc e Biodiversity Waldsea Lake (Canada) 345 Little Manitou Lake (Canada) 2620 Humbolt Lake (Canada) 7968 Environmental stress (salinity, temperature, exposure) Shark Bay (Australia) 480 Spencer Gulf (Australia) 3100 Werowrap Lake (Australia) 7683 Red Rock Lake (Australia) 7531 Pink Lake (Australia) 184 Corongamite Lake (Australia) 4425

Lake Nakuru (Kenya) 12000 Kilotes Lake (Ethiopia) 4133 Aranguidi Lake (Ethiopia) 19000 Mariut Lake (Ethiopia) 9611 Solar Lake (Sinai) 12000

0 2000 4000 6000 8000 10000 12000 14000 16000 18000 20000 mg Carbon per sq. m. per day Figure 8. Organic productivity (maxima) in various saline ecosystems. Typical marine upwelling zone ≈ 250-500 mg C/m2day (the dashed line is world marine maxima based on oshore 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 and coastal waters 40-50 mg C/m2day. But, preservation is more important than production rate in terms of source potential. Compiled from sources listed in Warren (1986, 2016).

(Warren, 2011). It reflects the general principle that in- References creased environmental stress favours the survival of a few Bildstein, K. L., C. B. Golden, B. J. McCraith, and B. W. well-adapted and specialised halotolerant species. This bi- Bohmke, 1993, Feeding Behavior, Aggression, and the ota is well adapted to the feast and famine life-cycle that Conservation Biology of e: Integrating Studies of Captive exists in most saline depressions and means their numbers and Free-ranging Birds: American Zoologist, v. 33, p. 117- are subject to wide fluctuations tied to wide fluctuations in 125. a saline lakes hydrochemistry (schizohaline waters). This same general principle of schizohaline ecosystem adap- Childress, B., S. Nagy, and B. Hughes, 2008, International tion is clearly seen in the periodic decrease in invertebrate Single Species Action Plan for Conservation of the Lesser species (grazers and predators) numbers with increasing Flamingo (Phoenicopterus minor): CMS Technical Series salinity in the carbonate lakes of the Coorong of South- No. 18, AEWA Technical Series No. 34, Bonn, Germany, ern Australia, where the only metazoan to remain alive in 59 pp. waters with salinities more than 200‰ are the southern Gould, S. J., 1987, The Flamingo's Smile: Reflections in hemisphere brine shrimp (Paratemia zietziania). It is seen NAtural History: New York, W. W. Norton and Company. in population fluctuations of the motile alga Dunaliella sp. in the Dead Sea, and in the fluctuating purple bacterial Grant, S., W. D. Grant, B. E. Jones, C. Kato, and L. Li, communities of Lake Mahoney in Canada (Warren, 2011). 1999, Novel archaeal phylotypes from an East African al- All these examples underline a general principle of “life kaline saltern: Extremophiles, v. 3, p. 139-145. will expand into the available niche” a paradigm that in the Jenkin, P. M., 1957, The Filter-Feeding and Food of Fla- cases we have discussed is driven by fluctuating salinities mingos (Phoenicopteri): Philosophical Transactions of the inherent to saline-tolerant and saline-adapted ecosystems. Royal Society of London. Series B, Biological Sciences, v. 240, p. 401-493.

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Jones, B. E., W. D. Grant, A. W. Duckworth, and G. G. Svengren, H., 2002, A study of the environmental con- Owenson, 1998, Microbial diversity of soda lakes: Extrem- ditions in Lake Nakuru, Kenya, using isotope dating and ophiles, v. 2, p. 191-200. heavy metal analysis of sediments: Masters thesis, Dept. Structural Chemistry, University of Stockholm, Swededn. Kirkland, D. W., and R. Evans, 1981, Source-rock potential of evaporitic environment: Bulletin American Associ- Tuite, C. H., 2000, The Distribution and Density of Lesser ation of Petroleum Geologists, v. 65, p. 181-190. Flamingos in East Africa in Relation to Food Availability and Productivity: Waterbirds: The International Journal of Kotut, K., and L. Krienitz, 2011, Does the potentially toxic Waterbird Biology, v. 23, Special Publication 1: Conserva- cyanobacterium Microcystis exist in the soda lakes of East tion Biology of Flamingos, p. 52-63. Africa?: Hydrobiologia, v. 664, p. 219-225. Vareschi, E., 1978, The ecology of Lake Nakuru (Kenya). I. Krienitz, L., A. Ballot, K. Kotut, C. Wiegand, S. Pütz, J. S. Abundance and feeding of the lesser flamingo: Oecologia, Metcalf, G. A. Codd, and S. Pflugmache, 2003, Contribu- v. 32, p. 11-35. tion of hot spring cyanobacteria to the mysterious deaths of Lesser Flamingos at Lake Bogoria, Kenya: FEMS Mi- Vareschi, E., 1982, The ecology of Lake Nakuru (Kenya). crobiology Ecology, v. 43, p. 141-148. III. Abiotic factors and primary production: Oecologia, v. 55, p. 81-101. Krienitz, L., and K. Kotut, 2010, Fluctuating algal food populations and the occurrence of Lesser Flamingos Vonshak, A., 1997, Spirulina: Growth, physiology and bio- (Phoeniconaias minor) in three Kenyan rift valley lakes: chemistry, in A. Vonshak, ed., Spirulina platensis (Arthro- Journal of Phycology, v. 46, p. 1088-1096. spina): Physiology, cell-biology and biotechnology: Lon- don, Taylor and Francis, p. 43-65. Melack, J. M., and P. Kilham, 1974, Photosynthetic rates of phytoplankton in East-African alkaline saline lakes: Lim- Warren, J. K., 1986, Shallow water evaporitic environments nology and Oceanography, v. 19, p. 743-755. and their source rock potential: Journal Sedimentary Pe- trology, v. 56, p. 442-454. Melchor, R. N., M. C. Cardonatto, and G. Visconti, 2012, Palaeonvironmental and palaeoecological significance of Warren, J. K., 2011, Evaporitic source rocks: mesohaline flamingo-like footprints in shallow-lacustrine rocks: An responses to cycles of “famine or feast” in layered brines, example from the Oligocene-Miocene Vinchina Forma- Doug Shearman Memorial Volume, (Wiley-Blackwell) tion, Argentina: Palaeogeography, Palaeoclimatology, Pa- IAS Special Publication Number 43, p. 315-392. laeoecology, v. 315-316, p. 181-198. Zhilina, T. N., and G. A. Zavarzin, 1994, Alkaliphilic an- Schagerl, M., A. Burian, M. Gruber-Dorninger, S. O. aerobic community at pH 10: Curr. Microbiol., v. 29, p. Oduor, and M. N. Kaggwa, 2015, Algal communities of 109-112. Kenyan soda lakes with a special focus on Arthrospira fu- Zhilina, T. N., G. A. Zavarzin, F. Rainey, V. V. Kevbrin, N. siformis: Fottea, v. 15, p. 245-257. A. Kostrikina, and A. M. Lysenko, 1996, Spirochaeta al- Scott, J. J., R. W. Renaut, L. A. Buatois, and R. B. Owen, kalica sp nov, Spirochaeta africana sp nov, and Spirochaeta 2009, Biogenic structures in exhumed surfaces around sa- asiatica sp nov, alkaliphilic anaerobes from the Continen- line lakes: An example from Lake Bogoria, Kenya Rift Val- tal soda lakes in Central Asia and the East African Rift: ley: Palaeogeography, Palaeoclimatology, Palaeoecology, v. International Journal of Systematic Bacteriology, v. 46, p. 272, p. 176-198. 305-312. Scott, J. J., R. W. Renaut, and R. B. Owen, 2012, Impacts of flamingos on saline lake margin and shallow lacustrine sediments in the Kenya Rift Valley: Sedimentary Geology, v. 277-278, p. 32-51. Shiba, H., and K. Horikoshi, 1988, Isolation and charac- terization of novel anaerobic, halophilic eubacteria from hypersaline environments of western America and Kenya: In: Proceedings of the FEMS symposium—The microbi- ology of extreme environments and its biotechnological potential, Portugal, p. 371-373. Simmons, R. E., 1995, Population declines, viable breeding areas and management options for flamingos in southern Africa: Conservation Biology, v. 10, p. 504-514.

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John Warren, Chief Technical Director SaltWork Consultants Pte Ltd (ACN 068 889 127) Kingston Park, Adelaide, South Australia 5049 [email protected] www.saltworkconsultants.com

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