The rise of potentially toxin producing cyanobacteria in Lake Naivasha, Great African Rift Valley, Kenya

Highlights

• Strong signals of degradation of the second largest freshwater lake in the Kenyan Rif Valley indicated by phytoplankton successions 2001–2013.

• First detection of cyanotoxins in field samples of Lake Naivasha.

• Molecular phylogenetic placement and detection of cyanotoxin gene in uncultured clones of Microcystis and Planktothrix.

Abstract

Lake Naivasha, an important inland water ecosystem and a crucial freshwater resource in the Great African Rift Valley, has displayed clear signals of degradation in recent decades. We studied the phytoplankton composition and biomass levels in the period 2001–2013 and noted a progressive increase in the occurrence of potentially toxic cyanobacteria. Analyses for the presence of cyanotoxins such as microcystins (MC), cylindrospermopsin (CYN) and anatoxin-a (ATX-a) were carried out on samples collected in 2008–2013. Among the cyanotoxins tested, low concentrations of MC were detected in the lake. This is the first record of the occurrence of MC in Lake Naivasha. For the first time, molecular phylogenetic investigations of field clones of cyanobacteria from Lake Naivasha were carried out to establish the taxa of the dominant species. Amplification of the aminotrasferase (AMT) domain responsible for cyanotoxin production confirmed the presence of the mcyE gene belonging to the microcystin synthesis gene cluster in field samples containing Microcystis and Planktothrix species. These findings suggest that toxin producing cyanobacteria could become a threat to users of this over-exploited tropical lake in the near future.

Introduction

Lake Naivasha is – beside Lake Victoria – the second largest freshwater body in Kenya. It is the coolest and the freshest of the smaller lakes in the Gregory Rift Valley (Worthington and Worthington, 1933, Harper and Mavuti, 2004). Some four decades ago, Lake Naivasha was praised as a crystal clear gem in the floor of the Great African Rift Valley. Enthusiastic naturalists described the lake as a “bird-watcher's and fisherman's paradise near Nairobi” (Brown, 1971, loc. cit. p. 82; Willcock, 1974). However, in the last 70 years, the lake's water quality has deteriorated significantly. At the end of the 1930s, a higher sediment accumulation rate induced by increased human activities in the catchment of the lake was recorded (Stoof-Leichsenring et al., 2011). In this phase, a shift in the diatom assemblage from littoral and periphyton to planktonic taxa has taken place, indicating a changing light regime characterized by loss of water transparency (Stoof-Leichsenring et al., 2012). Furthermore, the lake ecosystem of Naivasha was considerably degraded by the introduction of alien species, and a multitude of impacts leading to eutrophication. All in all, during the last century, about 23 exotic species, fishes, invertebrates and macrophytes entered the lake (Gherardi et al., 2011). The invading species established a complicated network of interactions, which led to considerable fluctuations in the population density of the primary producers. Notable among the invasive species is the water hyacinth, which has the ability to outcompete other macrophytes, and dominant phytoplankton.

The presence of microphytes, such as colonial and filamentous cyanobacteria, in Lake Naivasha were recorded by early surveys of the Cambridge Expedition to East African lakes in 1930 (Rich, 1933). However, first mass developments of cyanobacteria were witnessed in 1980 (Kalff and Watson, 1986) and subsequently in 2005 and 2006 (Harper, 2006). Nowadays, mass developments of cyanobacteria are common components of the phytoplankton communities in Lake Naivasha and hence influence the lake's water quality.

Lake Naivasha is located in a tropical semi-arid zone and subjected to dramatic fluctuations in lake level. Water level changes covering or exposing several metres of shoreline within a period of a few months occur in response to drought or flood events (Becht et al., 2006). These fluctuations have been exacerbated by excessive abstraction of lake water to support the geothermal power industry, the horticulture industry and water supply to human settlements in the catchment area (Harper et al., 2011). Consequently the lake looses much more water than it receives from rainfall and other inflows. During periods of low water level, the swamp vegetation found along the shoreline is exposed and this results in a dramatic decline of macrophyte community dominated by papyrus Cyperus papyrus L. Presently, only 10% of the area previously inhabited by papyrus remains available as the natural filter of sediments and eroded materials from the catchment (Morrison and Harper, 2009). The inflowing rivers, especially the Malewa, transport large quantities of silt and nutrients from the deforested agricultural land into the unprotected lake. Surface runoff from urban settlements, untreated wastewater from horticultural farms, wildlife and domestic animal droppings also contribute to nutrient loading of the lake.

One major consequence of the sustained degradation of the lake's environment is the progressive eutrophication, which makes the lake more vulnerable to cyanobacterial blooms (Kitaka et al., 2002, Harper et al., 2011). The occurrence of dense blooms of colonial coccoid cyanobacteria is indicative of the potential production of cyanotoxins in this lake. Cyanotoxins create health hazards both for humans (through the consumption of drinking water and fish from the lake), to livestock and wild animals watering at the lake shore.

In this paper, we present data on; (i) abundance of cyanobacteria in comparison to the entire phytoplankton community in Lake Naivasha between 2001 and 2013, (ii) characterization of uncultured field clones of the dominant cyanobacteria, (iii) detection of toxin genes in field samples, and (iv) toxin content in field samples.