Paleoecological response of ostracods to early Late Pleistocene lake-level changes in Lake Malawi, East Africa

Palaeogeography, Palaeoclimatology, Palaeoecology 303 (2011) 71–80

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Palaeogeography, Palaeoclimatology, Palaeoecology j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / p a l a e o

Paleoecological response of ostracods to early Late Pleistocene lake-level changes in Lake Malawi, East Africa Lisa E. Park a,⁎, Andrew S. Cohen b a b

Department of Geology and Environmental Science, University of Akron, Akron, OH 44325-4101, USA Department of Geosciences, University of Arizona, Tucson, AZ 85721, USA

a r t i c l e

i n f o

Article history: Received 15 January 2009 Received in revised form 24 February 2010 Accepted 27 February 2010 Available online 10 March 2010 Keywords: Lake Malawi Ostracoda Lake levels Climate change

a b s t r a c t Ostracod species from at least seven genera were recovered from drill cores recently collected at Lake Malawi, a large (29,500 km2) and deep (706 m) African rift valley lake located in the southern African tropics (9–14° S). These genera include Limnocythere, Candonopsis, Ilyocypris, Sclerocypris, Gomphocythere, possible Allocypria? and an unknown Cypridosine. Taphonomic variables such as the percentage of valve breakage, adult individuals, carbonate and oxidized coatings as well as associated mineralogy, can be used to delineate lake-level low and highstands. This record of lake-level fluctuations is correlated with paleoecological changes in ostracod communities throughout the core record of the past ∼ 145 ka. Two major assemblages found within the Lake Malawi cores include a Limnocythere-dominated shallow, saline/alkaline assemblage that occurred between 133 and 130 ka and between 118 and 90 ka and a deeper water Cypridopsine assemblage that lived in waters 10s to 100s of meters in depth and dominated the ostracod assemblage during intervals of lake-level transitions (136–133 ka, 129–128 ka and 86–63 ka), between the occurrence of the littoral assemblage and the appearance of indicators of bottom water anoxia. Changes in occurrences and abundances indicate variations in paleoecological affinities related to lake chemistry and oxygenation of bottom waters. The characteristics of the different lineages influence how that lineage is likely to respond to environmental variability such as lake-level fluctuations. Clades that include large numbers of endemic species in Lake Malawi tend to be specialists and thus more susceptible to environmental perturbations. On the other hand, cosmopolitan species within the lake all appear to be generalists, suggesting that they have high tolerances to environmental variability and therefore, these genera tend to be monospecific within the lake and are less likely to have radiated within the basin. The distribution of these ostracods can be used to evaluate hypotheses about the environmental history at the landscape-scale and their potential influence on species' distribution and diversification histories. © 2010 Elsevier B.V. All rights reserved.

1. Introduction

1.1. Malawi and lake-level changes

Orbitally-induced climatic change has been responsible for a number of high-amplitude lake-level fluctuations documented from paleorecords throughout Africa (Gasse and Street, 1978; Gasse et al., 1989; Beuning et al., 1997; Gasse, 2000; Johnson et al., 2001). These changes have been faithfully recorded in the sediment record of large and small lakes alike—but the longer records, such as that recovered from the ancient Lake Malawi have the most extensive and highly resolved record, archiving not only the physico-chemical changes in the lake basin but the paleoecological response to these events (Fig. 1) (Cohen et al., 2007; Scholz et al., 2007).

Lake Malawi is a large (29,500 km2), deep (706 m) meromictic lake that is characterized by two barriers to vertical mixing—a thermocline at 40–100 m depth and a chemocline at approximately 230 m depth (Patterson et al., 2000). Today, Lake Malawi is hydrologically open and drained by the Shire River, although 82% of total water loss is through evaporation (Beadle, 1981). It is currently a dilute (240–250 μS/cm conductivity) water body with negligible nutrient concentrations in surface waters, which promotes very high water clarity (Patterson and Kachinjika, 1995). The modern lake's watershed experiences a mesic climate, with highly seasonal rainfall (800–2400 mm/yr) and lowland vegetation that is dominated by wet Zambezian woodlands that are replaced by evergreen and subsequent montane forests with increasing elevation (Cohen et al., 2007). Prior investigations show that Lake Malawi has undergone many lake-level fluctuations throughout its history. The Malawi region is estimated to have experienced extreme aridity episodically between 135 and 70 ka, with diminished climatic and ecologic variability after

⁎ Corresponding author. E-mail addresses: [email protected] (L.E. Park), [email protected] (A.S. Cohen). 0031-0182/$ – see front matter © 2010 Elsevier B.V. All rights reserved. doi:10.1016/j.palaeo.2010.02.038

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early Late Pleistocene megadroughts (McGlue et al., 2007; Scholz et al., 2007). Unlike the smaller lake-level falls that have been suggested for the LGM, the early Late Pleistocene lowstands to a relatively shallow lake would have eliminated most rocky shoreline habitat in the lake, converting the majority of the lake's shoreline to muddy or sandy bottoms and sub-dividing the basin (Cohen et al., 2007; Scholz et al., 2007). This would have had enormous implications for community dynamics during this time period as sub-basins were isolated and lake physiography and chemistry were completely altered. In addition, the megadrought low-stand demonstrated for Lake Malawi has provided a robust constraint on genetic divergence of cichlid fish and other lake faunas. 1.2. Effect of lake-level changes on faunas Ancient lakes like Malawi and its sister Great Lake, Tanganyika have long been recognized as providing great opportunities for the study of community structure, particularly as it relates to the origin and maintenance of species diversity (Coulter, 1991; Martens, 1997; Cohen, 2000; Alin and Cohen, 2003). The extraordinary diversity within the ancient lakes of the world often has been attributed to both basin longevity and lake-level fluctuations. In most cases, basin longevity alone cannot explain the complex and sometimes conflicting evolutionary histories of the major clades within these lakes; and most studies have concluded that the lake-level changes experienced within these basins help explain the patterns of speciation and adaptive radiations for which they are so famous (Brooks, 1950; Fryer and Iles, 1972; Beadle, 1981; Wannik and White, 2000). The role that lake-level fluctuations have had in creating and maintaining the high degree of endemism in Malawi and other ancient lakes, as well as in possibly driving extinction events has also been linked to the ecological changes seen through each basin's history as communities respond to these environmental fluctuations. The cichlid fish and thiarid gastropods have documented complex ecological responses to lake-level changes that are linked to their diversity patterns (Sturmbauer and Meyer, 1992; Danley and Kocher, 2001; Sturmbauer et al., 2001; Genner and Turner, 2005; Genner et al., 2007). These studies suggest that ecological dynamics, particularly as they relate to extrinsic driving forces such as lake-level fluctuations play an important role in the overall diversity of these clades. These dynamics can be inferred from paleoecological records. Lake-level changes have had significant impact on basin morphometry, water salinity, mixing regimes, and habitat heterogeneity which in turn likely impacts species distributions and community structure. 1.3. Ostracods in the African rift lakes

Fig. 1. Location map of Lake Malawi with Sites 1 and 2 indicated. Bathymetric contours are 100 m.

70 ka (Cohen et al., 2007; Scholz et al., 2007). During these arid intervals Malawi became a shallow, alkaline/saline lake, with lake levels at least as low as − 580 m relative to modern, and the lake's surrounding watershed became a semi-desert. Although the Last Glacial Maximum (LGM) aridity is clearly demonstrable throughout tropical Africa, these findings suggest that its impact on lake and terrestrial ecosystems would have been smaller than the preceding

Among the crustaceans found within Lake Malawi and other ancient lakes, bivalved ostracods are one of the most important and diverse groups—having extensive radiations not just in East African Rift (EAR) lakes but in almost all of the ancient lakes in the world. The calcium carbonate shells of these microcrustaceans allow them to be preserved in core samples and therefore permits a more extensive understanding of their long-term ecological responses within these lake basins. Until the late 1990s, there had been only four major studies of modern ostracods from Lake Malawi (Daday, 1910; Sars, 1910; Fryer, 1957; Martens, 1990). Between 1994 and 1998, Martens (2002) conducted a modern census of all ostracods in Lake Malawi from several cruises parallel to trawls for demersal fish. This research was part of a larger INCO-DC project on the trophic ecology of the demersal fish community of Lake Malawi (contract number: ERBIC18CT970195) in which the ostracod census was part of Task 3 which examined the diversity, structure, seasonality and production of invertebrate communities within the lake. The primary objectives

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of the larger project were to provide trophic models to quantify energy flows through the demersal fish community of the lake and to determine fishing pressure in order to evaluate the accuracy of fishing statistics in the lake. The ostracod census conducted by Martens (2002) provides the most up-to-date recording of all non-insect invertebrates found within the lake. In his study, nearly one hundred benthic samples were taken for ostracods that included dredging, PONAR grab and hand net samples using SCUBA. Martens used the five dredge samples with the highest diversity for his analysis. Prior to this study few studies existed (Daday, 1910; Sars, 1910; Fryer, 1957; Martens, 1990)—and only 20 ostracod species (including 3 endemic species) had been documented from the lake. After the 2002 study, these numbers tripled. Ostracods are the most diverse group of crustaceans in the lake known with 63 currently described species, N62% of which are endemic to the lake (Martens, 2002). Unlike Lake Tanganyika which has flocks of cytherids and candonids, there have been no genera or species from these clades reported from Malawi. The main radiations are within the Cypridopsinae, Limnocythere sp.l., Gomphocythere and cypridid clades. Chrissia species that are found within the modern lake are not endemic and are found in associated water bodies—primarily inflowing rivers. Little is known about the origin and maintenance of ostracod diversity in Malawi. Controlling factors might be linked to dispersal ability, salinity and depth tolerances, feeding and/or reproductive strategies and extrinsic factors such as lake-level fluctuations, changes in water chemistry and depth as well as the development of subbasins. Therefore it is important to explore the relative roles of each, particularly as they are related to paleoecological changes throughout the lake's history. In particular, determining how species might react to a particular environmental factor or the increased variance of that factor is important because different species may have different responses to resource availability. There are obvious trade-offs associated with a species' ability to respond to varying environmental conditions and to compete for resources in the absence of that variability. There are species that have low resource requirements in the absence of variability. These species are typically the most negatively impacted by variation in resource levels (Chase and Leibold, 2003). Species that are unaffected by environmental variability or that benefit from variable resource availability have the ability to store consumption obtained during periods of high resource availability. Each ostracod species in Malawi most likely has its own response to environmental conditions and can drive the species ecological and evolutionary dynamics. To examine these responses we have studied the patterns of ostracod community change and its possible correlation to the paleolimnological history of Lake Malawi using the long drill core records now available from that lake. 2. Methods 2.1. Paleoecological response to lake-level change In 2003, the Lake Malawi Drilling Project collected seven cores from deep water sites in the lake. Site 1 (4 cores), in the central part of the lake, is located at 11° 17.66′S, 34° 26.15′E in 592 m water depth. Site 2 (3 cores) is in the northern part of the lake basin (10° 01.1′S 34° 11.2′E) in 359 m water depth. Core collection, basin dynamics, geochronology and sedimentation are described in Scholz et al. (2007). One of these cores, MAL 05-1C from the deep water drill site, has been sampled and its ostracod paleoecology briefly reviewed in a previous paper (Cohen et al., 2007). This paper adds new and more complete data to the analysis— particularly with respect to the ostracod occurrence, abundance and taphonomic data. Samples for ostracods (n = 471) were taken at 16 cm intervals (∼300 yr sample step resolution) and wet sieved with deionized (DI) water using a 125Ø mesh stainless steel sieves. One

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aliquot was weighed wet, oven-dried and re-weighed to determine water content, and this calculated water content was applied to the second (wet sieved and undried) aliquot to determine its dry weight. Sieved residues were counted for total number of ostracods per sample (expressed as #/g dry weight), % genera based on 100 valve counts, and taphonomic condition (% adult—as a proxy for size sorting, whole carapace, broken, carbonate coated, and reduction/oxidation stained). Fossil identifications were confirmed using a Phillips XL30 ESEM and compared to the modern material from Malawi and other EAR basins. 2.2. Statistical analyses The core sample data included a variety of data types that made it preferable to analyze via principal component analysis (PCA). Patterns were delimited and correlations were tested between taphonomic variables and species' distributions. First axis loadings are discussed below. Time series autocorrelation was conducted to identify periodicities and other spectral characteristics in a time series and to identify smoothing and cyclicity. Detrended correspondence analyses were performed on abundance data of the major faunal elements including the Limnocythere, Candonopsis and Cypridopsines as a way to reduce the large multivariate ecological data set and determine the strength of the environmental gradient. A Gaussian response model to generic abundances along the temporal gradient was developed using a least-squares algorithm. This allows for determining changes in abundances throughout the core, and identifying the peak abundances along the temporal gradient. 3. Results There are two major ostracod assemblages found within the Lake Malawi cores—a shallow, saline/alkaline lake assemblage and a deeper water assemblage. The saline/alkaline lake assemblage consists of monospecific Limnocythere sp. (with subordinate Candonopsis, Ilyocypris, and Sclerocypris in some samples) that typifies shallow littoral conditions in highly alkaline (pH 9–9.5, alk N 30 meq/l) and saline (K20 N 4000 µS/cm) African lakes. These Limnocythere assemblages are characterized by high adult/juvenile ratios, low levels of decalcification, common carbonate coatings and frequent valve abrasion, all typical of reworking and accumulation in the littoral zone of large African lakes. These taphonomic trends are seen in Fig. 2 which also shows that this type of assemblage dominates episodically between 133 and 130 ka and between 118 and 90 ka in Core 1C. It is notable that African cosmopolitan genera that are generally restricted to freshwater conditions are absent from all core samples examined (for example Stenocypris spp. which are present in modern dilute Lake Malawi). The second major ecologically-based assemblage is a deeper water fauna that is dominated by weakly calcified, juvenile valves of the endemic Cypridopsine flock (Fig. 2). These individuals are frequently abundant and show little or no signs of coatings or abrasion and most likely lived in waters 10s to a few 100s of meters depth. This type of assemblage occurs in transitional zones of the core (136–133 ka, 129– 128 ka and 86–63 ka) between the occurrence of the littoral assemblage and the appearance of indicators of bottom water anoxia (Figs. 2 and 4). Deltaic stillstands from the 62–64 ka interval at the −200 m level, coupled with the deep water ostracod assemblage from the same time interval demonstrate that Lake Malawi must have been ventilated to considerably greater depths (∼350–400 m) than at present, slightly greater than the maximum mixing depths observed in southern Lake Tanganyika today. The Limnocythere and Cypridopsines are negatively correlated as illustrated in the autocorrelation in Fig. 5. In general, if the autocorrelation sequence consists of somewhat smooth data, the correlation will remain relatively high for small lag times, but as lag time exceeds the interval of interdependency, the autocorrelation will drop. In general, the two genera do not occur together, but rather occur

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Fig. 2. Distribution of taphonomic variables throughout Core 1C from Lake Malawi. Ostracod abundance has been log transformed and normalized per gram. The dominant genera of Limnocythere and Cypridopsines are indicated. The percent broken valves, whole carapaces, adults as well as carbonate, reduced and oxidized staining are all indicated. PC1 diatom curve is of the combined diatom plus screen wash data sets (Stone et al., 2011–this issue). Lightly shaded areas represent shallower lake levels and dark shaded areas are deeper water.

in counter dominance to each other in accordance with various high and low lake stands as independently indicated by the taphonomic characters associated with these assemblages (Fig. 2). Comparing the changes seen within the core with the taxa found in modern Malawi, it is apparent that there is both a shallow and deep water assemblage within the lake. The modern Limnocythere flock in

Malawi is unusual for African lakes; but highly speciose Limnocythere lineages exist in other lakes around the world, mostly in highly alkaline and slightly saline systems. The comparably speciose deeper water Cypridopsine lineage also occurs in other African lakes like Tanganyika. The co-occurrence of both assemblages in several parts of the core may indicate transitional times of environmental instability.

Fig. 3. Principle component analysis of taphonomic variables associated with Core 1C. Correlations are plotted in inset.

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Fig. 4. Distribution of taxa throughout Core 1C. Ostracod abundance has been log transformed and normalized per gram. Percent Cypridopsines, Limnocythere, Candonopsis as well as other species. PC1 diatom curve is of the combined diatom plus screen wash data sets (Stone et al., this issue). Lightly shaded areas represent shallower lake levels and dark shaded areas are deeper water.

3.1. Ostracod taphonomy and mineralogy Taphonomic variables such as % broken valves, whole carapaces, adults, carbonate coating, iron and oxidation staining were plotted against depth and the PC1 of the diatom curve (which is the proxy for lake-level changes; Stone et al., 2011–this issue). The % broken valves variable does not appear to be directly correlated with lake-level fluctuations, but the percent of whole carapaces and adults does appear to increase during the times when Limnocythere and Candonopsis species dominated the assemblage between 133 and 130 and between 118 and 90 ka (Fig. 2). The percent of reduced Fe staining increased upcore between 86 and 63 ka, during an interval when lake levels were starting to rise towards modern levels. This corresponds with the dominance of the Cypridopsine species, most of which are

endemic and not defined to species level (Martens, 2002, 2003). The number of juveniles also increases along with the dominance of Cypridopsines (Fig. 2), probably as a result of the death of immature cohorts during episodic anoxia at or near the oxicline in the deeper water settings where these assemblages formed. These variables are all correlated with the PC1 of the diatom assemblage, which is used as the major proxy for lake-level fluctuations. Principal component analyses of these variables indicate that % whole carapaces, adults and oxidized coatings are strongly correlated (Fig. 3). Slightly over 34.6% of the variance is explained by this axis, which we interpret, based on the loadings, as being fundamentally related to lake level and (indirectly) available moisture (high positive loadings correlate with low lake levels and aridity).

Fig. 5. Time series autocorrelation between the Limnocythere and Cypridopsine lineages throughout the core showing a negative correlation of the two clades through time.

Fig. 6. Detrended correspondence analysis of the major clades of ostracods throughout Core 1C based on % of fauna recovered at each core interval.

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Fig. 7. Genus packing (Gaussian) response model along the temporal axis. The solid line represents all genera other than Candonopsis, Limnocythere and the Cypridopsines; the double dots and dashed line are the Candonopsis; the dashed line represents the Limnocythere and the small dashed line represents the Cypridopsines.

Plotting the log of ostracods/g against the % of Cypridopsines, Limnocythere, Candonopsis and other species reveals an asynchronous trend between the Limnocythere species flock and the Cypridopsines (Fig. 4). Modeling the gradient packing of major genera (with weighted averaging) fits generic abundance data along a temporal gradient and demonstrates for this data that these generic assemblages have changed through time and have experienced optimal conditions at different times through the basin's history (Fig. 5). Specifically, the Candonopsis sp. and other genera were optimized between 135 and 112 ka, followed by the Limnocythere between 112 and 90 ka, and then the Cypridopsines between 98 and 90 ka (Figs. 4, 6 and 7). Community assemblages and their dominant genera changed through time during various time intervals and those lineages tracked environmental changes through the basin's history. The DCA results support the different assemblages along the environmental gradient (Fig. 6). DCA1 has 74.5% of the variance and DCA2 has 14.5%. Detrending separates the genera into three distinct groupings—Limnocythere, Candonopsis, and Cypridopsine species. The environmental gradient is lake level along the temporal axis. Although it is evident that lake levels affect ostracod community composition and individual clades respond to changes in water depth, basin physiography, and water chemistry, it is not as clear how individual species or lineages may respond to environmental variability. Correlation analyses indicate that the endemic elements of the ostracod fauna—the Limnocytherid and Cypridopsines are the most sensitive to lake-level fluctuations and are negatively covarying (Figs. 4 and 5). The species of cosmopolitan genera are not as strongly influenced by environmental variability, suggesting that their distribution and diversity are reflected in the overall paleoecological associations and diversity patterns in the lake's history. 4. Discussion The fossil ostracod species recovered from the Lake Malawi drill core were exclusively benthic/epibenthic and required oxygenated waters in which to live—conditions that only exist in the lake today in water depths above 200–250 m (Martens, 2003). The ostracods recovered from Core 1C typically occur in sediments deposited prior to 63 ka.

These assemblages are assumed to have been in situ and not transported downslope via gravity flows or mixing because of their fragile nature as well as high number of juveniles. Based on experimental work done by Park et al. (2003) a high juvenile:adult ratio indicates little or no downslope transport within these faunas. Additional evidence relates to the anoxic zone that is typically undersaturated with respect to CaCO3. Based on these criteria as well as the understanding of the maximal depths of the oxygenated zone in nearby Lake Tanganyika, we interpret the occurrence of abundant ostracods at these core intervals to indicate water depths in Lake Malawi that were at least ∼280 m shallower than at present (Cohen et al., 2007). The ecological affinities of the two major assemblages of ostracods found in the cores support this interpretation and lead to further insight into the effect of lake-level fluctuation on origination and maintenance of species diversity. Within the modern faunas of Lake Malawi, depth appears to be more important in determining similarities between faunas than geographical location, even if the sampling locations are several hundred kilometers apart from one another (Martens, 2002). Differential depth zonations of the ostracod clade mimic the patterns seen in the earliest radiation of cichlid fish—between the rock and sand dwelling lineages (Danley and Kocher, 2001). The origin of the two major flocks—the shallow water Limnocytherids, which are adapted to more saline/alkaline conditions, and the deeper water Cypridopsines is unknown and may or may not have resulted from multiple invasions of each group into the lake basin. Subsequent diversification of these initial lineages was most likely promoted by repeated lake-level fluctuations and species selection. Several ostracod taphonomic variables such as the percent adult and whole carapaces, % whole carapaces, % carbonate coated valves and oxidized coated valves seem to be associated with lake-level fluctuations. Examples of these coatings can be seen in Plate IA, B, G and J. Reduced coatings can be seen in Plate ID. Some algal borings can be seen on the Candonopsis species in Plate IF but these were not that common as taphonomic features. The relative amounts of mica, siderite, vivianite, and pyrite within the sand fraction as well as the percent of reduced-stained ostracod valves provide clues to lake-level fluctuations that in some cases are related to changes in circulation and water body stratification (Fig. 2). Mica flakes accumulate in the distal portions of deltaic deposits in lakes, often with finer grained mud as a result of their hydrodynamic characteristics. Siderite, vivianite and pyrite are all redox sensitive minerals, that form commonly in anoxic water, although poorly oxygenated conditions can occur in both deep (below oxicline) and shallow water (e.g. deltaic marshes) settings. The latter, in particular is a common setting for pyrite formation, where sulfates are readily available for reduction. Pyrite and mica abundances were positively correlated in the PCA analysis (Fig. 2), perhaps as a result of cooccurrence in deltaic deposits or from reducing conditions as a result of lake-level fluctuations. 4.1. Comparing Lake Malawi to Tanganyika Documented ostracod diversity differs considerably between Lake Malawi and its closest counterpart, Lake Tanganyika. Whereas generic diversity is identical (n = 21 genera), the total number of species in Tanganyika is estimated to be well over 100 species versus Malawi at 63. Also, the morphological disparity of ostracods from Lake Tanganyika is much greater than in Lake Malawi. Furthermore, alpha (within-sample) diversity is also typically much higher in Lake Tanganyika ostracod faunas (Martens, 2002). A much higher proportion of the Tanganyikan

Plate I. Plate indicating typical examples of ostracods found throughout core MAL05-1C. A—Right valve of Cypridopsine cf sp A from MAL05-1C 24E 3 78.2–79.5; B—Left valve of Cypridopsine cf sp G from MAL05-1C 24E 3 78.2–79.5 cm; C—Right valve of Cypridopsine cf sp G from MAL05-1C-24E3 58.1–59.1 cm; D—Right valve of Cypridopsine sp. S from MAL05-1C-17H2-78–79 cm; E—Right valve of Cypridopsine sp. R from MAL05-1C-24E3 58.1–59.1 cm; F—Left valve of Candonopsis sp from MAL05-1C-24E-3 58.1–59.1 cm; G—Right valve of Limnocythere sp 4 from MAL05-1C-24E3 58.1–59.1 cm; H—Right valve of possible Allocypria sp. 1 from MAL05-1C-24E3 58.1–59.1 cm; I—Left valve of Sclerocypris sp juv from MAL05-1C-24E3 58.1–59.1 cm; J—Right valve of Gomphocythere sp. 1 MAL 1C 24E3 78.2–79.5 cm. Scales are all 100 µm and as indicated. Letters A, B, G and J are examples of carbonate coating.

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Table 1 Species list of modern and fossil ostracods found within Lake Malawi. Endemic species are indicated by *. Species found in modern Lake Malawi are indicated by +. Fossil species found in the core material are indicated by ♦. Note that many of these species are not described and identified only by informal letter and numerical designations that refer to Martens (2002) report. Species list Class Ostracoda Latrielle, 1806 Subclass Podocopa G.W. Müller, 1894 Order Podocopida Sars, 1866 Suborder Podocopina Sars, 1866 Superfamily Cypridoidea Baird, 1845 Family Candonidae Kaufmann, 1900 Subfamily Candoninae Kaufmann, 1900 ♦ + Candonopsis africana s.l. Subfamily Cyclocypridinae Kaufmann, 1900 + Cypria lenticularis Müller, 1898 + Physocypria castanea (Brady, 1904) Family Cyclocyprididae ♦ possible Allocypria sp.1 ♦ possible Allocypria sp.2 Family Cyprididae Baird, 1845 Subfamily Cypricercinae + Cypricerus inermis (Brady, 1904) + Neocypridella fossulata (Daday, 1910) + Strandesia laticauda Daday, 1910 Subfamily Cypridopsinae +* Cypridopsinae n.gen. cunningtoni Sars, 1910 ♦ + * Cypridopsinae n.gen. sp. A ♦ + * Cypridopsinae n.gen. sp. B +* Cypridopsinae n.gen. sp. C +* Cypridopsinae n.gen. sp. D +* Cypridopsinae n.gen. sp. E +* Cypridopsinae n.gen. sp. F ♦ + * Cypridopsinae n.gen. sp. G +* Cypridopsinae n.gen. sp. H +* Cypridopsinae n.gen. sp. I +* Cypridopsinae n.gen. sp. J +* Cypridopsinae n.gen. sp. K +* Cypridopsinae n.gen. sp. L +* Cypridopsinae n.gen. sp. M +* Cypridopsinae n.gen. sp. N +* Cypridopsinae n.gen. sp. O +* Cypridopsinae n.gen. sp. P +* Cypridopsinae n.gen. sp. Q ♦* Cypridopsinae n.gen. sp. R ♦* Cypridopsinae n.gen. sp. S + Cypridopsis vidua (Müller, 1776) + Plesiocypridopsis fulleborni (Daday, 1910) + Zonocypris costata (Vavra, 1897) Subfamily Cyprinotinae Bronstein, 1947 +* Cyprinotinae n.gen. sp.1 +* Cyprinotinae n.gen. sp.2 +* Cyprinotinae n.gen. sp.3 Subfamily Herpetocypridinae Kaufmann, 1900 Acocypris platybasis + Chrissia fasciculata (Daday, 1910) + Chrissia fullborni (Daday, 1910) + Chrissia marginata (Daday, 1910) + Chrissia perarmata (Brady, 1904) + Chrissia sinuate (Müller, 1898) + Chrissia stagnalis (Daday, 1910) +* Humphcypris sp.1 Martens, 1998 + Stenocypris major (Baird, 1859) Subfamily Megalocyprinae ♦ Sclerocypris sp. Family Ilyocyprididae Kaufmann, 1900 + Ilyocypris propinqua Sars, 1910 Family Notodromadidae Kaufmann, 1900 Subfamily Oncocypridinae, DeDeckker, 1979 + Oncocypris mulleri (Daday, 1910) Superfamily Cytheroidea Baird, 1850 Family Limnocytheridae Klie, 1938 Subfamily Limnocytherinae Klie, 1938 +* Limnocythere jocquei Martens, 1990 ♦ + * Limnocythere sp.1 ♦ + * Limnocythere sp.2 ♦ + * Limnocythere sp.3

Table 1 (continued) Species list ♦ + * Limnocythere sp.4 +* Limnocythere sp.5 ♦ + * Limnocythere sp.6 +* Limnocythere sp.7 ♦ + * Limnocythere sp.8 +* Limnocythere sp.9 +* Limnocythere sp.10 ♦* Limnocythere sp.11 ♦* Limnocythere sp.12 ♦* Limnocythere sp.13 ♦* Limnocythere sp.14 ♦* Limnocythere sp.15 ♦* Limnocythere sp.16 Subfamily Timiriaseviinae Mandelstam, 1960 +* Gomphocythere emrysi Martens, 2003 +* Gomphocythere huwi Martens, 2003 +* Gomphocythere irvinei Martens, 2003 +* Gomphocythere lisae Martens, 2003 +* Gomphocythere piriformis Martens, 2003 ♦* Gomphocythere sp.1 Superfamily Darwinuloidea Brady and Norman, 1889 Family Darwinulidae Brady and Norman, 1889 +* Alicenula inverse Rossetti and Martens, 1998 +* Alicenula serricaudata Rossetti and Martens, 1998 + Darwinula stevensoni Brady and Robertson, 1870 +* Penthesilenula gr.incae Rossetti and Martens, 1998 SUPERFAMILY CYPRIDOIDEA * Indicates endemic species to Lake Malawi. + Indicates present in modern Lake Malawi. ♦ Indicates fossil species that occurs in cores.

species (18%) is found in associated water bodies in Tanganyika compared with Lake Malawi (9.5%), although the Malawi fauna remains much less studied than that of Tanganyika (Martens, 2002). The pattern of greater ostracod diversity in Tanganyika relative to Malawi is part of a broader pattern, as Tanganyika has about twice as many documented non-insect invertebrate species as Malawi. Since Tanganyika is older than Malawi, the age of the lake has been invoked as a reason for this discrepancy (Martens, 2002). Basin age is also hypothesized to correlate with endemicity, since Lake Tanganyika has a high rate of ostracod species endemism (70%). However, as noted above, the effect of basin age is confounded by the impacts of much more recent lake-level fluctuations that almost certainly differ between the two lakes. Of particular significance in this regard are the much more profound ecological impacts of Early Late Pleistocene megadrought events on Lake Malawi versus Tanganyika, which may or may not have caused much more extensive selective extinction in the former lake (Park et al., 2000). If true, this could possibly have contributed to the much higher levels of morphological disparity observed in the modern Tanganyika fauna relative to Lake Malawi. High generic diversity is common in lakes, with many genera represented by a single species. Having high species diversity within single lineages is far less common within lacustrine ecosystems. While Malawi and Tanganyika share the same total number genera, they share only five in common (23.8%) and remarkably only one species— Darwinula stevensoni. Examining the species present in modern Lake Malawi, most appear to be within two genera, the Cypridopsinae n. gen. and Limnocythere (Plate I and Table 1). The origins of these clades within the Malawi basin most likely came from the surrounding watersheds with subsequent endemic speciation. Examining the ecological tolerances/preferences of the ostracod lineages within Malawi suggests that key differences may help to explain overall diversification patterns that may not be related to lake longevity or habitat variability. Genera and species found in modern Lake Malawi tend to be more cosmopolitan—the lake exhibits far less endemism in ostracods than other ancient lakes and include taxa such as Cypridopsis vidua, Candonopsis africana, various species of Oncocypris, Physocypria, Ilyocypris, Stenocypris, Sclerocypris, Strandesia and

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Zonocypris that are commonly found in lakes throughout the world. These genera are common in less permanent water bodies in Africa and none of them are found in Lake Tanganyika. The two major flocks within modern Malawi, the Cypridopsine and Limnocythere groups, are associated with different ecological conditions—specifically water depth and salinity/alkalinity tolerances that may have influenced their respective radiations. We cannot yet determine how rapidly the Malawian ostracod clades radiated, pending a thorough phylogenetic analysis of both fossil and modern faunal molecular genetic data. The rates of the cichlid fish and thiarid gastropod evolution within the Malawi basin appear to have varied throughout their histories as one would expect as did the ostracods. Likewise, the type of change most likely varied between anagenic to cladogenic processes, responding to disparities in extrinsic forcing mechanisms causing differential species sorting and selection. Ostracod clades comprising eurytopic species may have experienced low extinction rates and would likely have been widely distributed geographically, and would probably display high retention of plesiomorphies. The species radiations seen in the Limnocythere and Cypridopsine flocks could have resulted from the short term acquisition of autapomorphies that arose due to lake fluctuations in response to climatic change. Water level fluctuations have been shown to be important modulators of speciation processes in tropical lakes, particularly ancient ones such as Malawi and Tanganyika, because they temporarily form or break down barriers to gene flow among adjacent populations and/or incipient species (McCune and Lovejoy, 1998). There is building and substantial evidence that climatic phenomena synchronized the onset of genetic divergences of lineages in various species flocks such that recent evolutionary history seems to be linked to the same external modulators of adaptive radiation (Sturmbauer et al., 2001; Genner et al., 2007). The interplay between the intrinsic characters of different species and lineages and the extrinsic driving force of lake-level fluctuation needs to be further examined to better understand the role of niche optimization and ecological distribution of ostracods in this speciose ancient lake. 5. Conclusions Ostracod species from at least seven genera were recovered from drill cores recently collected at Lake Malawi, a large (29,500 km2) and deep (706 m) African rift valley lake located in the southern African tropics (9–14° S). These genera include Limnocythere, Candonopsis, Ilyocypris, Sclerocypris, Gomphocythere, possible Allocypria? and an unknown Cypridosine. Taphonomic variables such as the percentage of valve breakage, adult individuals, carbonate and oxidized coatings as well as associated mineralogy, can be used to delineate lake-level low and highstands. This record of lake-level fluctuations is correlated with paleoecological changes in ostracod communities throughout the core record of the past ∼ 145 ka. Two major assemblages found within the Lake Malawi cores include a Limnocythere-dominated shallow, saline/alkaline assemblage that occurred between 133 and 130 ka and between 118 and 90 ka and a deeper water Cypridopsine assemblage that lived in waters 10s to 100s of meters in depth and dominated the ostracod assemblage during intervals of lake-level transitions (136–133 ka, 129–128 ka and 86–63 ka), between the occurrence of the littoral assemblage and the appearance of indicators of bottom water anoxia. Changes in occurrences and abundances indicate variations in paleoecological affinities related to lake chemistry and oxygenation of bottom waters. The characteristics of the different lineages influence how that lineage is likely to respond to environmental variability such as lake-level fluctuations. Clades that include large numbers of endemic species in Lake Malawi tend to be specialists and thus more susceptible to environmental perturbations. On the other hand, cosmopolitan species within the lake all appear to be generalists, suggesting that they have high tolerances to environ-

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mental variability and therefore, these genera tend to be monospecific within the lake and are less likely to have radiated within the basin. The distribution of these ostracods can be used to evaluate hypotheses about the environmental history at the landscape-scale and their potential influence on species' distribution and diversification histories. Acknowledgements This project was funded by the U.S. National Science Foundation— Earth System History Program (EAR-0602350), the International Continental Scientific Drilling Program, and the Smithsonian Institution. Initial core processing and sampling were carried out at LacCore, the National Lake Core Repository at the University of Minnesota. The authors wish to particularly thank D. Gauggler, R. Markus and C. Johnson, T. Astrop and C. Boush. References Alin, S., Cohen, A.S., 2003. Lake-level history of Lake Tanganyika, East Africa, for the past 2500 years based on ostracode-inferred water-depth reconstruction. Palaeogeogr. 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