Hydrobiologia (2008) 596:31–46 DOI 10.1007/s10750-007-9055-8

PRIMARY RESEARCH PAPER

Hydrochemical fluctuations and community composition in an ephemeral saline lake (Sua Pan, Makgadikgadi )

Graham Paul McCulloch Æ Kenneth Irvine Æ Frank D. Eckardt Æ Rob Bryant

Received: 21 January 2007 / Revised: 3 June 2007 / Accepted: 16 June 2007 / Published online: 4 August 2007 Ó Springer Science+Business Media B.V. 2007

Abstract Fluctuating hydrochemistry, as a result of the lake dried out and salinities increased. pH extreme hydrological regimes, imposes major phys- estimates generally ranged between 8.6 and 10, with iological constraints on the biota of ephemeral saline maximum values recorded during initial flooding. lakes. While the inverse relationship between salinity comprised mainly Branchinella spinosa, and zooplankton species richness is well-known Moina belli, Lovenula africana and Limnocythere across salinity gradients, few studies have docu- tudoranceai, all of which occurred across a wide mented closely the response of zooplankton to range of salinities, while halotolerant freshwater seasonal changes in salinity. Weekly sampling during species (Metadiaptomus transvaalensis, Leptestheria two flood seasons at Sua Pan, an intermittent saline striatochonca and the ostracods Plesiocypridopsis lake in central Botswana demonstrated the impor- aldabrae, Cypridopsis newtoni and a newly identified tance of spatial and temporal salinity gradients for Potamocypris species) disappeared above conductiv- crustacean community composition, associated with a ities of 1,500 lScm1. A unique crustacean compo- decline in species richness, from 11 to three species. sition in southern Africa was attributed to Sua Pans’ Conductivity ranged between 320 and 125,800 lS rare chemical composition among southern African cm1 during seasonal flooding; changing from dom- saline lakes; flood waters on Sua Pan contained a 2+ 2+ + + inance by HCO3 and CO3 ,Ca and Mg , at the higher proportion of Na and HCO3 , and less K , 2+ 2þ beginning of the floods, to NaCl dominated waters as Mg and SO4 than over 80% of records from pans elsewhere in southern African. The freshwater species of crustaceans in Sua Pan were similar to those found in other southern Africa lakes, and these Handling editor: J. M. Melack similarities decreased in lakes with higher pH and G. P. McCulloch (&) K. Irvine proportions of Na, and less SO4 and Mg in their Department of Zoology, University of Dublin, Trinity chemical composition. The predominant saline toler- College, Dublin 2, Ireland ant species on Sua Pan, however, showed a greater e-mail: [email protected] similarity to those in saline lakes in southern and East F. D. Eckardt Africa with higher proportions of HCO3 and, partic- 2+ Department of Environmental Sciences, University of ularly, Mg in their chemical composition. Cape Town, Cape Town, Keywords Saline lake Ionic composition R. Bryant Department of Geography, University of Sheffield, Zooplankton Makgadikgadi Species richness Sheffield, UK Salinity 123 32 Hydrobiologia (2008) 596:31–46

Introduction crustacean species richness and a simultaneous change in species composition in Lake Chad were Unpredictable and seasonal flood regimes (rainfall attributed to changes in temperature, oxygen and occurrence and intensity) among shallow and ephem- predation, while salinity was not suggested as a major eral saline lakes contribute high variability to their influencing factor (Saint Jean, 1983). physical and chemical character (Langbein, 1961; Although widely distributed in southern Africa, Hammer, 1986; Comin & Williams, 1994; Meintjes few detailed studies have been done on the hydro- et al., 1994; Williams, 1998). Salinity can vary chemistry and zooplankton communities of the enormously among and during individual flood and region’s shallow and ephemeral saline lakes (Allan- drying periods; through varying degrees of cyclical son et al., 1990; Seaman et al., 1991; Day, 1993). dissolution of surface evaporates during flooding and Ephemeral saline lakes in Namibia and South Africa evaporative concentration during drying phases (Har- range in salinities from 3 to 276 g l1 and are die et al., 1978; Williams, 1998). Evaporative con- generally dominated by Na+ and Cl ions, with 2 centration and sequential mineral precipitation on the HCO3 +CO3 prevalent in lower salinity waters surface and sub-surface layers alter the ionic propor- (Hutchinson et al., 1932; Seaman et al., 1991; Day, tions of vanishing flood waters (Stumm & Morgan, 1993). The aquatic fauna of these lakes are thought 1970; Eugster & Hardie, 1978). Such changes affect depauperate, with no well-defined fauna confined to lake ecology profoundly (Hammer, 1986; Williams, saline pans; appearing rather to comprise mostly 1998). tolerant freshwater forms (Seaman et al., 1991). Day Differences in zooplankton communities have (1990) found that crustacean species richness among been observed among lakes with different ionic small ephemeral pans in Namibia was largely influ- composition (e.g. Hecky & Kilham, 1973; Williams enced by isolation and did not correlate with salinity. et al., 1990; Bos et al., 1996; Derry et al., 2003) and However, in nearly all cases, where the hydrochem- the inverse relationship between zooplankton species istry and associated zooplankton of these saline lakes richness and salinity in saline lakes is well estab- and ephemeral pans have been sampled, data related lished (e.g. LaBarbara & Kilham, 1974; Green, 1986, to single samples and seasonal analysis is scarce 1993; Hammer, 1986, 1993; Williams et al., 1990). (Hutchinson et al., 1932; Allanson et al., 1990; Day, Other, or a combination of other abiotic and biotic 1990, 1993; Seaman et al., 1991). factors, such as predation and competition are also This study reports the hydrological, chemical and likely important for species richness and community biological characteristics of Sua Pan; part of the composition (Williams et al., 1990; Williams, 1998; Makgadikgadi salt pan complex, Botswana, one of Herbst, 2001). However, little is known about the the largest ephemeral lake systems in Africa. Until sequential response of zooplankton communities to our study, the chemical composition of Makgadikg- changing salinity and chemical composition in indi- adi was poorly understood and not included in vidual lakes. Melack (1988) studied changes in the reviews of saline water chemistry in southern Africa biota of Lake Elmenteita during a period of lake (Mepham, 1987; Allanson et al., 1990; Seaman et al., drying and salinity increase and suggested that 1991; Day, 1993). pH values from Sua Pan and small increased salinity directly affected a key macrofaunal pans adjacent to it, taken by the Rhodesian Schools element (Paradiaptomus africanus) and an important Exploration Society in 1957, were 9 and 10 (Eccles, primary producer (Anabaenopsis arnoldii), while D. H., Undated). Brendonck & Riddoch (1997) other biota were affected through altered biological recorded pH of 8.9–9.5 and conductivities of 5.2– interactions. Vareschi & Vareschi (1984), over sev- 21.3 mS cm1 in the north basin of Sua Pan and eral years, not only associated disappearances of some small adjacent pans. Details on the aquatic biota Lovenula africana in Lake Nakuru with increases of of Makgadikgadi is also scant (Seaman et al., 1991). conductivities above 25,000 lS, but also identified Identification of invertebrate taxa collected by the that the availability of Spirulina platensis at the base Rhodesian Schools Exploration Society suggested the of the food chain was important for the zooplankters crustacean species composition in the Makgadikgadi and rotifer population dynamics. During a 2-year was unusual for southern Africa. Subsequent collec- period of drought, a considerable reduction in tions of ostracods (Martens, 1988), copepods (Rayner 123 Hydrobiologia (2008) 596:31–46 33

& Heeg, 1994) and anostracans (Brtek, 1967; Bren- lowest part of the Makgadikgadi complex, covers donck & Riddoch, 1997) have confirmed the presence approximately 3,400 km2, with an extensive catch- of some of the species identified in Eccles’ report. ment of about 27,000 km2, comprising Kalahari Similarities to crustacean communities in East Afri- sediment based calcisols, luvisols, vertisols and can lakes have been attributed to Makgadikgadis’ gleysols underlain by Carboniferous-Jurassic sand- relative proximity to East Africa and a similar stone and basalts (Thomas & Shaw, 1991). Most of chemical composition to East African saline lakes, the soils in the area, particularly those close to the with high HCO3 and CO3 concentrations (Seaman pan, have calcrete layers at shallow or moderate et al., 1991). This article provides the first detailed depths. The pan can be divided into three hydrolog- account of the Makgadikgadis’ crustacean commu- ically separate basins, the north, middle and south nity and its association with variable salinity and basins, separated by two sand spits that protrude from water chemistry. The work involved a detailed and the eastern shore (Fig. 1). During the wet season, five systematic survey over 2 years, and the results were rivers (Nata, Semowane, Mosetse, Lepashe and compared with other saline lakes of southern and east Mosope) flow intermittently onto their respective Africa. This provides an overview of the primary basins. The north basin sump, at 890 m above sea chemical characteristics contributing to the species level, is the deepest part of the pan and floods more composition of these lakes. frequently and for longer periods than other parts of the complex (Cooke, 1979). The pan surface com- prises brine-saturated sand and clay layers with

Materials and methods surface efflorescence of trona (Na2CO3Na2HCO3– 2H2O) and halite (NaCl) and large amounts of Site description carbonates and sulphates are thought to exist on and in the top layers of the pan surface (Thomas & Shaw, The Makgadikgadi salt-pan complex is a relict of an 1991). ancient lake that once covered most of contemporary northern Botswana (Cooke, 1979; Thomas & Shaw, Sampling and analysis 1991). Remnants of the lake exist in the form of two large endorheic salt pans, Ntwetwe Pan and Sua Pan, During two wet seasons (1999–2000 and 2000–2001), subject to intermittent flooding (Fig. 1). Mean annual daily rainfall and evaporation data were collected rainfall is estimated at between 400 and 500 mm, from the edge of Sua Pan using, respectively, a falling during the wet season, from November to standard rain gauge and Class A evaporation pan. The April, but large inter-annual fluctuations are charac- date of initial flooding and length of flood period teristic of the climate (Schulze, 1972). Sua Pan, the (duration of flood) were recorded for each basin.

Fig. 1 Map of the northern Botswana region, showing the Makgadikgadi salt pan complex, which comprises predominantly Ntwetwe and Sua Pan. Sua Pans’ inflowing rivers and catchment areas are encircled and concentric circles indicate the pattern of flood duration on the pan

123 34 Hydrobiologia (2008) 596:31–46

Conductivity and pH measurements of water variation in pH among the three basins during the samples, taken from random sites in each of the 1999–2000 and 2000–2001 wet seasons. Skewed data north, middle and south basins, were carried out bi- were normalised by square root transformation. weekly from December 1999 to June 2000, and Linear regression was used to test the relationship weekly from November 2000 to July 2001, using a between conductivity and corresponding estimates Mettler Toledo1 MC 266 meter corrected to 25°C. for total dissolved solids (TDS). Pearson Product– From December 1999 to April 2000, monthly sam- Moment correlations were used to test the association ples for total dissolved salinity (TDS) and ionic between species richness and salinity for the entire composition calculation were taken from each basin salinity gradient on Sua Pan, the individual basins, and three of the inflowing rivers (the Nata, Semow- and over the saline categories sub-saline (03gl1), ane and Mosetse rivers). Water samples were hyposaline (3–20 g l1), mesosaline (20–50 g l1) collected in 500 ml plastic bottles, previously washed and hypersaline (>50 g l1)(sensu Hammer, 1986), with a 5% acid solution and rinsed with distilled using Data Desk1 Version 6. The BrayCurtis water, and stored at <4°C until analyses. Chemical dissimilarity coefficient index was used to compare analysis was carried out at the National Centre for US the crustacean community assemblage of Sua Pan Geological Survey (12201 Sunrise Valley Drive, with that of similar lakes and small wetlands in Reston, VA 20192) using the methods of Fishmen & southern and East Africa. Relationships among Friedman (1989). Results were plotted on a Ternary crustacean community similarity between Sua Pan plot diagram to illustrate the changes in Sua Pans’ and the other sample saline lakes (expressed as Bray chemical composition during a flood period and to Curtis index), and their various abiotic characteristics compare its chemistry with other saline lakes in were examined using linear regressions. southern and east Africa (Day, 1993). Invertebrates were sampled weekly; using a stan- dard 240-lm sweep net (25 cm wide) to sample the Results entire water column and benthic surface or, when deep, the top 25 cm of the water column. In addition, Flood regime and water chemistry a perspex tube (diameter 5.5 cm) was dropped vertically through the water column to the lake Annual rainfall for the 1999–2000 and 2000–2001 bottom to collect an integrated sample of the entire wet seasons were, respectively, 851 mm and water column (Edmonson & Winberg, 1971). Each 348 mm. Maximum air temperatures of 38–41°C sample technique was used at five sites, chosen and evaporation rates of up to 20 mm d1 led to rapid randomly, in each of the three basins; the north, water loss. Each basin was subject to different flood middle and south basin. Samples were then sieved regimes (Fig. 2). By the end of January 2000, the through a 70-lm mesh and each sample was north basin was completely flooded, with maximum preserved in >80 % industrial alcohol. Invertebrates depths exceeding 2 m. It remained flooded for the were identified under a dissecting microscope, remainder of the study period and only dried out according to Day et al. (1999, 2001), Brendonck & completely in February 2002. Both the middle and Riddoch (1997), Martens (1984, 1988) and Martens south basins flooded for approximately 8 months et al. (1996). Verification of ostracods was provided between November 1999 and September 2000, with a by Dr. Koen Martens (Royal Belgian Institute of brief flood period in November–December. Flooding Natural Sciences, Brussels). was considerably less during the 2000–2001 wet season, lasting less than 2 months in each basin. Statistical analysis Conductivity and pH showed both a significant spatial difference among the basins (RM-ANOVA,

Significant changes in salinity (conductivity) among F1,54 = 265, P 0.0001 for conductivity; the three basins were tested using Repeated Measures F1,53 = 593, P 0.0001 for pH) and a temporal ANOVA (RM-ANOVA) on Data Desk1 Version 6. change during both wet seasons within each basin A similar RM-ANOVA test was carried out, with H+ (Fig. 2). The north basin was least saline, increasing concentration as the dependent variable, to test the from 320 to 24,400 lScm1 during a two-year 123 Hydrobiologia (2008) 596:31–46 35

Fig. 2 pH and conductivity measurements from the north (diamonds), middle (Solid squares) and south basins (triangles) during the 1999–2000 and 2000–2001 wet seasons. Bold lines represent flood periods in the north, middle and south basin

continuous flood period, from December 1999 to June evident in both the rivers and basins (Table 1 and 2 2001. Middle basin conductivity increased from 730 to Fig. 3). Anion dominance was HCO3 >Cl >SO4 91,600 lScm1 in 1999–2000 and from 2,800 to (88% of the time) in the rivers, with Cl dominant in 1 65,600 lScm in 2000–2001. The most saline con- the first Nata River flood discharge. Cl > HCO3 > 2 ditions were recorded in the south basin where SO4 occurred 58% of the time in the basins, but conductivity increased from 22,400 to 111,000 lS HCO3 was the dominant anion at the beginning of cm1 in 1999–2000 and from 46,800 to 125,800 lS the flood periods in the north and middle basins. 1 2 cm in 2000–2001. A strong positive correlation SO4 concentrations varied little and rarely exceeded (r = 0.998, n = 12, P 0.001; variables square-root 5% of anionic composition. The pattern of cation transformed) was found between conductivity and dominance was Ca2+ >K+ >Na+ >Mg2+ (63% of corresponding TDS estimates (Table 1). In the north the time) in the rivers, with Na+ dominating for most basin, pH was highest at the beginning of the flood of the time in the Nata River discharge. In contrast, (10.1), but generally increased from 8.6 in December cation dominance in the basins was Na+ >K+ > 1999 to 9.8 in June 2001. Highest pH values in both the Ca2+ >Mg2+ for 92% of the time. Na+ increased middle and south basins were also recorded at the with salinity, while the divalent cations Ca2+ and beginning of the flood periods and ranged between 9 Mg2+ decreased, disappearing completely in the south and 10. basin when the highest salinities were recorded. Si+ Spatial and temporal changes in the relative ions made up a substantial proportion of the cations proportions of the major cations and anions were in both river and basin waters. 123 36 Hydrobiologia (2008) 596:31–46

Table 1 Ionic composition of three inflowing rivers and the three basins of Sua Pan during the 1999–2000 wet season, with TDS in gl1 and individual ion concentrations in mg l1

+ + 2+ 2+ 2 Date TDS Na K Ca Mg Si Cl HCO3 &CO3 SO4

Rivers Nata Nov’99 1.71 560 (91.7) 30 (4.9) 11 (1.8) 3.9 (0.6) 5.5 (0.9) 670 (60.9) 350 (31.8) 75 (6.8) Jan’00 0.12 6.4 (15.9) 8.1 (20.2) 14 (34.9) 3.1 (7.7) 8.4 (20.9) 6.8 (8) 75 (87.9) 2.1 (2.5) Feb’00 0.24 35 (44.5) 7.6 (9.7) 22 (28) 4.3 (5.5) 9.5 (12.1) 35 (21.5) 120 (73.6) 6.2 (3.8) Semowane Nov’99 0.09 2.2 (7.7) 5.3 (18.5) 13 (45.3) 2.6 (9.1) 5.5 (19.2) 4.8 (7.7) 55 (88) 2.3 (3.7) Jan’00 0.1 3 (9.9) 6.1 (20.3) 14 (46.6) 2.7 (9) 4.11 (13.7) 4.8 (6.4) 65 (87.4) 2.1 (2.8) Mosetse Nov’99 0.09 4.1 (14.5) 5.6 (19.8) 10.5 (37) 2.6 (9.2) 5.4 (19) 4.9 (8) 50 (83) 2.6 (4.3) Jan’00 0.086 8.3 (29) 5.7 (20) 8.4 (29.5) 1.6 (5.6) 4.4 (15.5) 9.3 (16) 45 (77.4) 2.4 (4.1) Feb’00 0.012 4.6 (13) 5.6 (15.7) 16 (44.8) 3.3 (9.2) 6.1 (17) 5.8 (6.9) 75 (89.6) 2.5 (3) Basins North Dec’99 0.26 65 (70.2) 9.8 (10.6) 4.4 (4.8) 0.5 (0.5) 12.8 (13.8) 55 (33) 105 (63.3) 5.8 (3.5) Jan’00 1.1 335 (86) 25 (6.4) 5.2 (1.3) 0.37 (0.1) 24 (6.2) 360 (52) 300 (43.4) 29 (4.2) Feb’00 0.7 205 (81) 19 (7.5) 10.3 (4.1) 1.1 (0.4) 17 (6.7) 210 (46) 220 (48) 24 (5.3) Mar’00 1.12 365 (86.2) 27 (6.4) 6.5 (1.5) 0.79 (0.2) 24 (5.7) 425 (60.6) 240 (34.2) 35 (5) Middle Dec’99 0.58 175 (85.5) 8.4 (4.1) 8.8 (4.3) 0.8 (0.4) 11.6 (5.7) 180 (47.6) 185 (49) 11 (2.9) Jan’00 0.23 55 (75.4) 6.4 (8.8) 2.3 (3.2) 0.14 (0.2) 9 (12.4) 18 (11.6) 135 (87) 2.2 (1.4) Feb’00 6.75 2550 (93) 150 (5.5) 4.8 (0.2) 0.05 (0.01) 38 (1.4) 3600 (89.7) 155 (3.9) 250 (6.2) Mar’00 11.8 4300 (93.7) 230 (5) 4.25 (0.1) 0.05 (0.1) 55 (1.2) 6250 (86.6) 475 (6.6) 475 (6.6) Apr’00 12.9 4800 (91.2) 400 (7.6) 3.4 (0.1) 0.05 (0.1) 58 (1.1) 7000 (91.2) 160 (2.1) 500 (6.5) South Dec’99 17.8 6500 (92) 350 (5) 2.25 (<0.1) 0.4 (<0.1) 215 (3) 8500 (79.4) 1800 (16.8) 380 (3.6) Mar’00 31.5 11500 (93.5) 650 (5.3) 3.7 (<1) 0.009 (<1) 140 (1.1) 16400 (85.1) 1770 (9.2) 1050 (5.4) Apr’00 31.2 11500 (94) 600 (4.9) 4.9 (0) 0.035 (0) 125 (1) 16000 (84.4) 1700 (9) 1200 (6.3) Values in parenthesis are percentage equivalents of cations or anions

Fig. 3 Ternary diagram illustrating the patterns of ionic squares) basins. Apices indicate 100% equivalent of ions in dominance among the major cations and anions in the Nata gl1. Areas showing the chemical composition of waters from (plus), Mosetse (cross) and Semowane (triangle) rivers, and saline lakes in East Africa and South Africa (encircled in the north (solid circles), middle (circles) and south (solid broken line), are adapted from Day (1993) 123 Hydrobiologia (2008) 596:31–46 37

Table 2 Taxonomic species list of crustaceans and other small invertebrates found on Sua Pan between November 1999 and June 2001 Class Order Species Basin Reference

Crustacean Anostraca Branchinella spinosa N, M, S (Milne-Edwards, 1840) Branchinella ornata N, M, S (Daday, 1910) Spinicaudata Leptestheria striatoconcha N (Barnard, 1924) Anomopoda Moina belli N, M, S (Gurney, 1904) barbata N (Weltner, 1897) Copepoda Calanoida Lovenula africana N, M (Daday, 1908) Cyclopoida Metadiaptomus transvaalensis N (Methuen, 1910) Ostracoda Podocopida Limnocythere tudoranceai N, M, S (Martens, 1990) Sclerocypris exserta makarikarensis N, M (Martens, 1988) Potamocypris new sp ? N (Martens, pers comm.) Plesiocypridopsis aldabrae N (Meisch, 1988) Others Coryxid hemiptera of Sigara and Notonecta genus Dytiscus species of beetle Beetle larvae, Cybister Dragonfly larvae, Libellulidae Nematode worms N, M and S represent the presence of species in the north, middle and south basins, respectively

Crustacean community composition and species- Table 3 Pearson product-moment correlations between salinity relations salinity and species richness in Sua Pan Salinity range (lScm1) nr Significance Twelve species of crustaceans were recorded in Sua Pan (Table 2). Metadiaptomus transvaalensis, Sua Pan (320125,800) 74 0.45 P 0.001 Plesiocypridopsis aldabrae and a new species of North Basin (32024,400) 40 0.294 P 0.05 Potamocypris were, however, rare, occurring in low Middle basin (73091,600) 21 0.207 P 0.2 numbers at the beginning of the 1999–2000 wet South basin (22,400–125,800) 12 0.216 P 0.5 1 season on the north basin only. Macro-invertebrates Sub-saline (0–3 g l )* 21 0.556 P 0.005 1 also occurred mainly in the north basin and Hyposaline (3–20 g l )* 28 0.159 P 0.2 included some predatory beetles and species of Mesosaline (20–50 g l1)* 38 0.502 P 0.001 insect larvae. Hypersaline (>50 g l1)* 19 0.691 P 0.001 There was a striking reduction in crustacean * represents salinity ranges converted from conductivity species richness, from 11 to 4, among the basins as estimates to g l1 estimates according to Williams & salinity increased along a north–south gradient. Sherwood (1994), where the relationship between salinity and conductivity is described with a high degree of confidence Overall species richness was correlated, strongly 1.0878 2 1 by: s = 0.466 K (r = 0.988), s is the salinity in g l and negatively with salinity during the 2-year flood (between ca. 3 and 70 g l1) and K is conductivity at 25°Cin period (Table 3). This was most noticeable in the mS cm1 north basin, where the number of species was reduced from 11 to 3 during the flood period and the except hyposaline (Table 3). The relationship found correlation was significant, while the relationships between species richness and pH was not significant in the middle and south basins were not significant (r = 0.23; P > 0.025; n = 74). (Table 3). The species-salinity relationship examined Some species tolerated large variations in salinity within narrower salinity categories revealed highly and pH (Fig. 4). Metadiaptomus transvaalensis and significant negative correlations in all categories the ostracods, Plesiocypridopsis aldabrae, and a 123 38 Hydrobiologia (2008) 596:31–46

Fig. 4 Salinity ranges for the crustacean species at Sua Pan

2 Potamocypris sp, occurred only at the beginning of Increased proportions of HCO3 and SO4 were also the 1999–2000 flood, when the water was least saline. concurrent with similarities between Sua Pans’ Leptestheria striatochonca and Daphnia barbata community composition and that of East African disappeared above conductivities of approximately and southern African lakes, respectively. Similarities 1,500 and 12,000 lScm1, respectively. Similarly, in species composition between Sua Pan and those of Branchinella ornata disappeared quickly from both African lakes, particularly in East Africa, however, the middle and south basins at salinities above decreased with increased proportions of Na and with 20,000 lScm1. In contrast, B. spinosa, Moina belli, pH, while distance was an important constituent in and Limnocythere tudoranceai occurred in all three reducing saline tolerant species similarity between basins across a wide salinity range (320 lScm1 to Sua Pan and other lakes. >50,000 lScm1) and between pH 8.5 and 10. L. tudoranceai and M. belli disappeared from Sua Pan when conductivities exceeded 70,000 and Discussion 65,000 lScm1, respectively, while Branchinella spinosa disappeared above salinities of 112,000 lS Adaptation of crustaceans to a variable cm1. Lovenula africana was found in the middle environment basin, where it disappeared at salinities >38,000 lS cm1. It was, however, absent from the south basin Species in ephemeral lakes are adapted to large even though salinity there was within its tolerance variability of water chemistry, particularly salinity, range. A similar decrease in the number of macro- temperature and cyclical droughts of varying duration invertebrate species occurred among the basins. All (e.g. Williams, 1964; Hutchinson, 1967; Weir, 1969; were present in the north basin, but only Dytiscus, Horne & Viner, 1971; Hartland-Rowe, 1972; Kok, Cybister, and Odonata larvae were present in the 1987; Williams, 1987; Hammer & Appleton, 1991). middle basin; all were absent from the south basin. While crustacean species richness and composition Regression analysis between similarities of the can be correlated with salinity over its entire range community composition in Sua Pan and those of (LaBarbara & Kilham, 1974; Hammer, 1986; Wil- other African saline lakes using a Bray Curtis Index liams et al., 1990) categorising saline lakes according in relation to a number of physical and chemical to their flora and/or fauna in general is difficult constituents indicated a strong positive relationship because of site specific differences; including those of between species similarity and increased proportions temperature, oxygen and biological composition of Mg2+ in lake chemistry (Fig. 5; Table 4). Indeed, (Hammer, 1986; Williams et al., 1990; Meintjes Mg2+ was an important constituent contributing to et al., 1994). Our work suggests that across at least increased species similarity between Sua Pan and southern and eastern Africa, regional differences both east African and southern African lakes. per se may not be so important. 123 Hydrobiologia (2008) 596:31–46 39

Fig. 5 Relationships between the similarity of Sua Pan’s characteristics of these saline lakes; Lake depth, Distance from + 2 2+ crustacean community with other saline lakes in southern and Sua Pan, pH, and the % Na , % HCO3 ,%SO4 , and % Mg East Africa (expressed as Bray-Curtis index) and the abiotic in the chemical composition of their waters

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Table 4 Regression equations for some of the relationships shown in Fig. 5 Lake charact’s All lakes, all spp. All lakes saline S Africa lakes, E Africa lakes, S Africa lakes, spp. (i–v) all spp. all spp. saline spp.

Surface area y = 0.001x + 24.12 y = 0.001x + 12.178 R2 < 0.1 R2 < 0.1 R2 < 0.1 R2 = 0.1 R2 = 0.1 Distance from Sua R2 < 0.1 y = 0.01x + 18.9 R2 < 0.1 R2 < 0.1 R2 < 0.1 R2 = 0.59 pH y = 4.87x + 68.1 y = 3.21x + 43.4 y = 3.71x + 58.5 y = 6.81x +86 y = 01.7x + 27.4 R2 = 0.41 R2 = 0.16 R2 = 0.3 R2 = 0.45 R2 = 0.3 %Na y = 0.45x + 43.7 R2 < 0.1 y = 0.49x + 44.2 y = 0.46x +45 R2 < 0.1 R2 = 0.63 R2 = 0.44 R2 = 0.8 2 2 % HCO3 y = 0.13x + 23.17 y = 0.07x + 14.12 R < 0.1 y = 0.25x + 16.6 R < 0.1 R2 = 0.12 R2 = 0.29 R2 = 0.46 2 2 2 2 %SO4 R < 0.1 R < 0.1 y = 0.4x + 21.62 R < 0.1 R < 0.1 R2 = 0.32 %Mg y = 4.6x + 20.2 R2 < 0.1 y = 4.07x + 21.4 y = 5.48x + 18.64 y = 7.94x + 10.44 R2 = 0.83 R2 = 0.85 R2 = 0.85 R2 = 0.59

Most species from the large Branchiopoda (mem- one, was likely a result of dissolution of mineral bers of the orders anostraca, notostraca and conc- efflorescence on the pan surface and the influx of hostraca) are confined to temporary waters, having saline groundwater (Thomas & Shaw, 1991). Differ- requirements that can only be satisfied by the ences in the ionic composition of this groundwater alternating wet and dry phases of these ecosystems entering the basins may also affect the spatial salinity (Broch, 1965; Bishop, 1967; Brown & Carpelan, gradient on Sua Pan. Rapid evaporative ‘pumping’ of 1971; Belk & Cole, 1975; Hildrew, 1985). Many of ground water in dry conditions facilitates the depo- these species may be highly susceptible to predation sition of large amounts of efflorescence (Eugster & (Williams et al., 1990) and, consequently, are typi- Hardie, 1978): which could be seen clearly from the cally absent or uncommon, in permanent waters. Salt air during the end of the wet seasons. Highest tolerant species of copepoda, anomopoda and ostra- salinities in the south pan, which were quickest to coda also occur in these ephemeral habitats, with increase, reflected lower hydrological inputs from stages of their life cycle also resistant to prolonged smaller rivers and the broad shallow nature of the periods of high salinity and desiccation (e.g. Hutch- basin, conducive to rapid evaporation. Owing to more inson et al., 1932; LaBarbara & Kilham, 1974; river discharge and longer flood periods than the Martens, 1988; Day, 1990; Seaman et al., 1991; middle and south basins, the north basin was Martens et al., 1996). As found in Sua Pan, in the consistently the least saline, and a distinct salinity early stages of flooding, crustacean species common gradient was evident across the pan from north, to freshwater habitats can also inhabit these systems, middle to south basin. but die out as salinities increase (e.g. Seaman & Kok, The ionic composition of the Mosetse and Sem- 1987; Frey, 1993). owane rivers are consistent with those of the majority of freshwaters in southern Africa (Day, 1993). High Flood regime and water chemistry Na+ and Cl ion concentrations in the Nata River (240–1,710 mg l1), however, suggest an effect of Large spatial and temporal variations in the water dams and permanent pools along the Nata River; chemistry on Sua Pan can be attributed to the variable adding saline standing water, subjected to evapora- flood durations that occurred over the 2 years. tive concentration, during initial discharge. Upstream Following initial flooding, high salinities in the development of weirs and dams has implications for middle and south basins, compared with the northern the ecology of the pan downstream. The chemical

123 Hydrobiologia (2008) 596:31–46 41 composition of Sua Pan, however, appears distinct osa was only recorded in adjacent pans. Salinity and compared with other inland saline lakes in southern pH levels at the time were similar to those taken and East Africa (Fig. 3). Anion and cation dominance during the early part of the 1999–2000 flood period in the lakes of Sua Pan differ from 80% of saline pans (5,200–21,300 lScm1, with pH 8.9–9.5). S. probo- in southern Africa, where Na+ >Mg2+ >Ca2+ >K+ scideus could be a vagrant species from small pans and Cl >SO4 > HCO3 predominates (Seaman et nearby, although its absence during our study could al., 1991; Day, 1993). In contrast, Sua Pan has less reflect longer-term change of hydrology or chemical + 2+ + K ,Mg and SO4 , more HCO3 , and K is more regime (Hamer & Rayner, 1996). Mesocyclops leu- abundant than Ca2+ and Mg2+. Increased evaporative ckarti and the ostracod Cypridopsis newtoni were concentration and the consequential loss of HCO3 , also absent during this study, although their rare Ca2+ and Mg2+ ions by precipitation of calcite status reported by Eccles suggests they were also

(CaCO3), halite (NaCl) and trona (Na3H(CO3)2:2- vagrant species. In addition, the occurrence of H2O) would account for the reduction in these ions Mesocyclops leuckarti in Africa has been questioned later in the flood periods in the middle and south by Van de Velde (1984). The absence of M. belli in basins (Stumm & Morgan, 1970). Sua Pans’ ionic Eccles’ report may have been the result of it being composition is more similar to that from Pretoria Salt misidentified as M. macrocopa by the expedition Pan (Ashton & Schoeman, 1983) and Etosha Pan team in 1957, considering its description is very (Berry, 1972), where bicarbonate ions are also similar to that of M. belli (Seaman et al., 1999). abundant. Some of the most predominant species on Sua Pan, High pH of between 8.5 and 10 is consistent B. spinosa and L. africana, are found nowhere else in with high values reported in similar saline lakes southern Africa (Rayner & Heeg, 1994; Brendonck & 2 around southern Africa rich in HCO3 +CO3 ions Riddoch, 1997; Day et al., 2001), while others, (Hutchinson et al., 1932;Berry,1972;Ashton& M. belli and L. tudoranceai have been found in a Schoeman, 1983). Salinities of above *60 mS cm1 few temporary waters in Namibia (Day, 1990; resulted in an asymptotic relationship and a subse- Martens et al., 1996; Day et al., 2001). Among the quent decrease, owing perhaps to rapid precipitation of ostracods, Sclerocypris exserta makarikarensis and 2 CaCO3 at high salinities, removing HCO3 +CO3 the new Potomocypris species may be endemic to the ions from solution and altering the pH equilibrium in Makgadikgadi, but because of the general shortage of favour of slightly more acidic conditions (Stumm & work on ostracods this must be a very tentative Morgan, 1970). The opposite may be the case at the statement. L. tudourancea has been found in only a beginning of the rainy seasons, accounting for sea- small number of ephemeral pans in Namibia. Overall, sonal maxima, when initial flooding dissolved surface Sua Pans’ crustacean community appears, as is the trona efflorescence (Na2CO3–Na2HCO3–2H2O) and chemistry, distinct among southern African saline 2 CaCO3, resulting in a large input of HCO3 &CO3 lakes. A species rich community on Sua Pan com- + and H into solution and a withdrawal of CO2 and pared with saline lakes in southern Africa, high- H2CO3 (Stumm & Morgan, 1970). lighted by Seaman et al. (1991), may also reflect the large variation in flood duration, salinity and chem- Crustacean community composition and species- ical composition that contribute to seasonal habitat salinity relations heterogeneity. Sua Pan’s crustacean community was similar to While the crustacean community composition in the those in a number of ephemeral pans, mainly in north basin of Makgadikgadi is similar to that southern Africa, and the highly saline, alkaline recorded by Eccles (undated) in the 1950s, some lakes of East Africa (Table 5). Species similar to notable differences were also evident. Most notable is those found in southern African lakes and ephem- the absence of the anostracan Streptocephalus probo- eral pans were predominantly freshwater species scideus, found by the expedition team of 1957 and that disappeared from Sua Pan early on in the flood again in the late 1990s by Brendonck & Riddoch periods. Among these freshwater species found in (1997); who found that B. ornata was the only other other lakes, Daphnia barbata was the most com- anostracan present in the north basin, while B. spin- mon. Plesiocypridopsis aldabrae is also found in 123 42 Hydrobiologia (2008) 596:31–46

Table 5 East and southern African lakes with similar crustacean communities to Sua Pan Region Lake Crustacean species at Sua Pan References

1 2 3 4 5 6 i ii iii iv v BrayC index

Southern Barbers Pan X 25.5 Hutchinson et al. (1932), Mepham (1987), Africa Day (1993) Etosha Pan X 24 Berry, (1972), Mepham (1987) Etosha Pan X 24 Berry (1972), Mepham (1987) Brak Pan 1 X 25.5 Hutchinson et al. (1932), Seaman et al. (1991) Reit Pan 1 X 45 Hutchinson et al. (1932), Seaman et al. (1991) Brak Pan 2 X 27 Hutchinson et al. (1932), Seaman et al. (1991) Flamingo Pan X 26.25 Hutchinson et al. (1932), Day et al. (2001) Avenue pan X X 25 Hutchinson et al. (1932), Seaman et al. (1991) Eliazar Pan X X 30 Hutchinson et al. (1932), Seaman et al. (1991) Leeuwkraal Pan X X 24 Hutchinson et al. (1932), Seaman et al. (1991) L. le Roux X 22.52 Hart, (1986), Hart (1987) Temporary pans in X X X 56.25 Day (1990, 1993) Namibia East Africa L. Nakuru X 18 Talling & Talling, 1965, Vareschi & Vareschi, (1984) L. Chilwa, fresh X 27 Kalk et al. (1979), Mepham (1987) L. Chilwa, saline X 21 Kalk et al. (1979), Mepham (1987) L. Pawlo X 19.5 Green (1986, 1993) L. Bishoftu X 21 Green (1986, 1993) L. Aranguadi X 18 Green (1986, 1993) L. Kilotes X 19.5 Green (1986, 1993), Wood & Talling, (1988) L. Abaya X 30 Green (1986, 1993), Wood & Talling, (1988) L. Elmenteita X 21 Hecky & Kilham (1973), Melack (1988) L. Shala X 40.5 Green (1993) Central L. Chad X 19.5 Carmouze et al. (1983) Africa Species numbering refers to; 1 = Daphnia barbata,2=Leptestheria striatoconcha,3=Metadiaptomus transvaalensis, 4=Sclerocypris exserta makarikarensis,5=Plesiocypridopsis aldabrae,6=Potamocypris new sp., i = Branchinella spinosa, ii = Branchinella ornata, iii = Moina belli,iv=Lovenula africana and v = Limnocythere tudoranceai

some lakes in the Eastern Cape, South Africa (Day species that were predominant on Sua Pan occurred et al., 2001). The saline tolerant Moina belli and elsewhere, mainly in the highly saline lakes of the Limnocythere tudoranceai were the only species East African rift valley (Table 5). However, not found in a few ephemeral pans in Namibia. more than one similar species has been found in Similarities with the saline tolerant crustacean each of these lakes. Most common was the calanoid

123 Hydrobiologia (2008) 596:31–46 43 copepod Lovenula africana. Branchinella spinosa conchostracans. Co-existence of large crustaceans has been found in very few lakes in Africa and only and planktivorous fish elsewhere in southern Africa recorded in one other lake in East Africa, Lake has been explained by high levels of turbidity, Elmenteita. providing a visual refuge for crustaceans (Hart, Species’ tolerance to salinity appeared greater on 1986; Jarvis, 1986). High turbidity may have Sua Pan compared with alkaline lakes in East Africa explained the Branchinella re-emergence during and Ethiopia (La Barbara & Kilham, 1974; Vareschi the 2000–2001 wet season, while salinity and pH & Vareschi, 1984; Melack, 1988; Green, 1993). No may have been too high for the re-emergence of M. belli have been recorded in East African soda L. striatochonca during 2001. Additional predation lakes with salinities >21 mS cm1 and L. africana by aquatic insects like Anisops may have exacer- have been observed to disappear from lake waters bated predatory exclusion (Brendonck & Riddoch, between 21 and 25 mS cm1. It is possible that this 1997). Large reductions in anostracan populations 2 reflects higher pH and/or HCO3 &CO3 levels, and also occurred in the middle and south basins. At higher proportions of lethal ions, such as fluoride, in high densities, Greater flamingo (Phoenicopterus the chemical composition of East African saline ruber roseus) have a considerable impact on lakes. It is, however, unclear why species like invertebrate abundance (Arengo & Baldassare, Daphnia and L. striatochonca were not found in the 1995; Comin & Hernandez, 1997; Glassom & middle basin, or why Lovenula was not found in the Branch, 1997). Glassom & Branch (1997) estimated south basin, even though their salinity range was that Greater flamingo in two Namibian coastal inside that of the middle and south basins, respec- lagoons reduced macro-invertebrate densities by up tively. We can speculate that this was related to to a third, and Zweers et al. (1995) found Greater higher temperatures of shallower water and less O2 in flamingo filter efficiency was highest on prey of those basins. Notwithstanding this, there was an between 2 and 4 mm length. This concurs with the overall strong relationship between salinity and size of anostracans in Sua Pan, and a high species richness (Table 3). proportion of anostracans were found in crops of Among the basins of Sua Pan, variations in Greater flamingo collected opportunistically during species richness over time were most noticeable in the study. Biological interactions may also have the north. The occasional appearance of Metadia- been important for the absence of M. belli from Sua ptomus transvaalensis, and the ostracods Plesiocy- Pan coincident with the larger D. barbata dominat- pridopsis aldabrae, and Potamocypris, for example, ing the zooplankton during March and September suggest they may have been opportunistic vagrant 2000. Successions among anomopoda species have species from surrounding pans, and with low been associated with food resources in other salinity tolerance. Salinity may not have been, southern Africa lakes with large Daphina dominat- however, the only factor in the observed species ing during periods when small edible algae are reductions among the basins. The unusual presence abundant, and declining subsequently during dom- of Tilapia and, in particular, ‘Barbel’ fish (Cyprin- inance of cyanophtes; when small bodied taxa such idae) in the north basin, during the exceptional as Moina and Ceriodaphnia become more prevalent floods, may have caused local extinctions of (e.g. Kalk, 1979; Jarvis, 1986). Seasonality of L. striatochonca and other large crustaceans through anomopoda species may also depend on turbidity size selective predation, as described, classically, by (Hart, 1986) and temperature, with D. barbata Brooks & Dodson (1965). Indeed, an unusual associated with the cool season (e.g. Kalk, 1979; disappearance of both Branchinella species in the Saint-Jean, 1983; Hart, 1986). While the possibility north basin, in mid February (B. spinosa) and early of salinity intolerance cannot be discounted, the May 2000 (B. ornata), with their subsequent reap- disappearance of D. barbata from the north basin pearance when the lake became much shallower, coincided with a reduction in small green algae, and the Barbel population reduced, supports the sampled during this study, and an increase in water likelihood of large Branchiopoda species exclusion temperature. by fish predation. Gut contents of fish caught during Among lakes of variable ionic composition, the study period included large crustaceans, mainly different zooplankton communities have been iden- 123 44 Hydrobiologia (2008) 596:31–46 tified (Bos et al., 1996). While the role of salt ion US Geological Survey, who kindly carried out the ionic composition relative to salt concentration in deter- analysis of our water samples. Also, a big thanks to Dr Koen Martens, who kindly helped with the ostracod identifications mining zooplankton communities is not fully under- and to Peter Stafford and Alison Boyce from the Zoology stood, differences in zooplankton communities have Department, Trinity College Dublin for their consistent and been linked to different ionic compositions (e.g. Bos much appreciated assistance in the laboratory. et al., 1996; Derry et al., 2003). Some studies have indicated distinct anion preferences among zooplank- ton groups, such as the ostracod genus Limnocythere References in carbonate, sulphate and chloride-dominated waters (Forester, 1986) and the relative abundance of some Allanson, B. R., R. C. Hart, J. H. O0Keeffe & R. D. Robarts, species of Artemia, Moina, Daphnia and calanoid 1990. Inland Waters of Southern Africa: An Ecological copepods is said to be determined by their preferred Perspective. Kluwer Academic Publishers, Dordrecht. Arengo, F. & G. A. Baldassarre, 1995. Effects of food density on cations calcium and magnesium (Bos et al., 1996). the behaviour and distribution of nonbreeding American Similarities between Sua Pans’ crustacean commu- flamingos in Yucatan, Mexico. The Condor 97: 325–334. nity composition and those of saline lakes in East Ashton, P. J. & F. R. Schoeman, 1983. Limnological studies on Africa may reflect similarities in chemical composi- the Pretoria Salt Pan, a hypersaline maar lake. Hydrobi- ologia 99: 61–73. tion and, particularly, an abundance of bicarbonate Barnard, K. H., 1924. 4. Contributions to a knowledge of the ions (Seaman et al., 1991). This study also identified fauna of South-West Africa. II: Crustacea, Entomostraca, 2+ 2þ Phyllopoda. Annals of the South African Museum. 20: that Mg and, to a lesser degree SO4 were also important ionic constituents contributing to species 213–230. Belk, D. & G. A. Cole, 1975. Adaptational biology of desert similarity between Sua Pan and other saline lakes in temporary-pond inhabitants. In Hadley, N. F. (ed.), Africa. Environmental Physiology of Desert Organisms. Hutch- inson & Ross, Inc., Pennsylvania, Dowden, 207–226. Berry, H. H., 1972. Flamingo breeding on the Etosha Pan, South West Africa, during 1971. Madoqua 5: 5–31. Conclusions Bishop, J. A., 1967. Some adaptations of Limnadia stanleyana King (Crustacea: Branchiopoda: Conchostraca) to a tem- Sua Pan’s chemical definition places it between the porary fresh water environment. Journal of chemically defined groups of southern African and Ecology 36: 599–609. Bos, D. G., B. F. Cumming, C. E. Watters & J. P. Smol, 1996. East African saline lakes. Similarities between Sua The relationship between zooplankton, conductivity and Pans’ crustacean community composition and those lakewater ionic composition in 111 lakes from the Interior of saline lakes in East Africa may reflect similarities Plateau of British Columbia, Canada. International Jour- in chemical composition and, particularly, an abun- nal of Salt Lake Research. 5: 1–15. 2+ Brendonck, L. & B. Riddoch, 1997. Anostracans (Branchiopoda) dance of bicarbonate and Mg ions. The crustacean of Botswana: morphology, distribution, diversity, and communities in Sua Pan are unlike those of most endemicity. Journal of Crustacean Biology 17(1): 111–134. other inland saline lakes in southern Africa. As a Broch, E. S., 1965. Mechanisms of adaptation of the fairy result of rapid increases in the salinity of its waters shrimp Chirocephalus bundyi Forbes to the temporary pond, Vol. 392. 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