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The Diet of an Invasive Crayfish, Cherax Quadricarinatus (Von Martens, 1868), in Lake Kariba, Inferred Using Stomach Content and Stable Isotope Analyses

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The Diet of an Invasive Crayfish, Cherax Quadricarinatus (Von Martens, 1868), in Lake Kariba, Inferred Using Stomach Content and Stable Isotope Analyses BioInvasions Records (2018) Volume 7, Issue 2: 121–132 Open Access DOI: https://doi.org/10.3391/bir.2018.7.2.03 © 2018 The Author(s). Journal compilation © 2018 REABIC Research Article The diet of an invasive crayfish, Cherax quadricarinatus (Von Martens, 1868), in Lake Kariba, inferred using stomach content and stable isotope analyses Lightone T. Marufu1,*, Tatenda Dalu2,3, Phiri Crispen4, Maxwell Barson1, Rutendo Simango4, Beaven Utete4 and Tamuka Nhiwatiwa1,5 1Department of Biological Sciences, University of Zimbabwe, Harare, Zimbabwe 2Department of Ecology and Resource Management, University of Venda, Thohoyandou, South Africa 3South African Institute for Aquatic Biodiversity, Grahamstown, South Africa 4Department of Wildlife Ecology and Conservation, Chinhoyi University of Technology, Chinhoyi, Zimbabwe 5University Lake Kariba Research Station, Kariba, Zimbabwe *Corresponding author E-mail: [email protected], [email protected] Received: 26 July 2017 / Accepted: 15 December 2017 / Published online: 27 January 2018 Handling editor: Ana Luisa Nunes Abstract The diet of an invasive crayfish, Cherax quadricarinatus (Von Martens 1868), in Lake Kariba, was investigated using stomach content analysis (SCA) and stable isotope analysis (SIA). The frequency of occurrence of macrophytes and detritus ranged between 63.6–97.1% and 20–45.5%, respectively, and the index of relative importance ranked these as the two most important food items across all size classes. Significant differences in the ranking of fish, macroinvertebrates and crayfish were found between size classes 29–37.9, 38–46.9 and 47–55.9 mm. Stomach content analysis showed 16% of crayfish stomachs were empty. Feeding intensity differed significantly between size classes and ranged from 3.46 to 5.21. Stable isotope analysis was done by comparing δ13C, δ15N and C/N ratios in crayfish muscle and potential dietary items in the lake. Macrophytes were the most dominant food item (57%), followed by macroinvertebrates (20%), then detritus, and finally fish and crayfish. Stable isotope analysis revealed that all crayfish size classes analysed were in the same trophic level. Nevertheless, while SCA showed high dietary overlap among all crayfish size classes (>65%), SIA showed that small crayfish (< 28.9mm) had limited overlap with large crayfish (> 56mm), with the former showing a higher proportion of macroinvertebrates in their diet. In Lake Kariba, C. quadricarinatus predominantly feeds on macrophytes, macro- invertebrates and detritus, which may bring about nutrient cycle alterations in the lake. Littoral habitat changes caused by the feeding characteristics of C. quadricarinatus might also lead to competition with, and eventual displacement of, some native littoral fishes in this lake. Key words: detritus, dietary shift, omnivorous, stomach content analysis Introduction al. 2006). Interaction between native and introduced species can also lead to structural and functional The deliberate and unintentional introduction of many changes in ecosystems due to changes in trophic aquatic invasive species has often led to adverse effects structure (Wong et al. 2003; Edgerton et al. 2007; on ecosystems (Lodge et al. 2006). Unintentional Sousa et al. 2012). Some invasive species, however, introductions of alien species into natural water have been reported to have positive effects in envi- systems often occur when they escape from water- ronments where they increased biodiversity and based production systems (Howard 2004; Padilla supported food webs (Griffith et al. 1994; Davis and Williams 2004). Invasive aquatic species can 2011). In other cases, indigenous species have also threaten biodiversity through predation, competition offered resistance to known invasive species and possible introduction of new diseases (Barki et (Kimbro et al. 2013; Dorn and Hafsadi 2016). 121 L.T. Marufu et al. The differing conclusions from past invasion Kreps et al. 2015). In terms of feeding ecology, SIA biology studies demonstrates that predicting the has shown that the invasive crayfish Orconectes impacts of invasive species is not easy without base- rusticus caused a change in the trophic structure of line investigations (Dalosto et al. 2015). Past studies some lakes by reducing the abundance of benthic have identified native species richness, vacant niches, macroinvertebrates and small fishes (Kreps et al. 2015). absence of natural predators/enemies and competitive Another study showed that the crayfish Procambarus abilities of resident species (Elton 1958; Herbolt and clarkii has a preference for particular macrophytes in Moyle 1986; Mack et al. 2000) as key biotic factors their diet, causing their reduction due to overgrazing that have caused some ecosystems to be vulnerable (Gherardi and Barbaresi 2007). However, the potential to invasion. Other studies have identified local climate, effects of C. quadricarinatus are not well understood nutrient levels and habitat modifications as key phy- in tropical Africa owing to limited studies of the sical factors (Moyle and Light 1996; Rejmanek 2000). species in the wild and the inexistence of freshwater While an investigation into all possible factors is not crayfish species native to the continent. Therefore, always possible, an understanding of the feeding the potential effects of C. quadricarinatus on native ecology of invasive species can be important in biota in Africa should be accorded research priority. assessing the risk they might pose for indigenous The current study was conducted to provide the biota and ecosystems (Chucholl 2012). first assessment of the diet of the invasive Cherax Stomach content analysis (SCA) is a useful tool in quadricarinatus in the Sanyati Basin of Lake Kariba, analysing the diet of animals at a given time (Whitmore Zimbabwe, using a combination of stomach content et al. 2000; Parkyn et al. 2001; Hollows et al. 2002). and stable isotope analyses. Investigating the diet Differences in digestion rates of food items and their and potential trophic changes caused by an invasive assimilation can, however, give misleading indications species like C. quadricarinatus may help provide of the importance of various dietary items (Hyslop evidence for, and give impetus to, conservation of 1980). As such, some studies now couple SCA with indigenous fauna (Mohanty et al. 2016). stable isotope analysis (Hollows et al. 2002), which is useful in analysing the long term diet of animals Material and methods by indicating which food items were assimilated after ingestion (Jussila et al. 2015) and can conse- Study area quently help our understanding of the possible threats The study was done on the northern shore of the posed by invasive species (Bodey et al. 2011). Thus Sanyati Basin of Lake Kariba, Zimbabwe (Figure 1). SCA can give an indication of the short term Lake Kariba is a man-made lake shared between consumption of diet items, while stable isotope Zimbabwe and Zambia that was built in 1956 for analysis (SIA) can give an indication of the assimi- hydroelectric power generation. It has five basins, lation of dietary items (Junger and Planas 1994). namely Mlibizi, Binga, Sengwa, Bumi and Sanyati The redclaw crayfish Cherax quadricarinatus (Von (Cronberg 1997). The Lake Kariba catchment area is Martens, 1868) is native to northern Australia and semi-arid with annual mean temperatures, rainfall and Papua New Guinea (Austin 1996). It is an invasive evaporation of 26 °C, 766 mm and 1700 mm, respec- crayfish species which has established feral popu- tively. The dominant macrophytes found in the Sanyati lations in several tropical and subtropical countries Basin include Eichhornia crassipes, Ceratophyllum (Jones 2011). Cherax quadricarinatus is able to grow demersum, Lagarosiphon ilicifolius, Ludwigia stolo- fast under a wide range of water quality conditions nifera, Najas pectinata, Panicum repens, Potamogeton and is known to have an omnivorous diet (Holdich octandrus, Potamogeton pectinatus, Pistia stratiotes, 2002; Snovsky and Galil 2011). The species was Salvinia molesta, and Vallisneria aethiopica (Phiri initially introduced into Zambia from South Africa 2010). Forty five species of fish have been recorded for aquaculture purposes (Thys van den Audenaerde in Lake Kariba (Marshall 2006) and all of them are, 1994), from where it escaped into Lake Kariba (Phiri at a given time of their life cycle, associated with the 2009). A study by Nakayama et al. (2010) showed littoral zone of the lake (Phiri and Mhlanga 2014). that in 2008 C. quadricarinatus was already present The main fish families found in the lake include in the Bumi Basin of Lake Kariba, and it has since Cichlidae, Cyprinadae, Claridae, Characidae, Momy- spread to other parts of the lake, such as the Sanyati ridae and Alestidae (Phiri and Mhlanga 2014). Basin in Zimbabwe (Marufu et al. 2014). Introductions of alien crayfish have been associated Crayfish sampling with decreases in vegetation, detritus, macroinverte- brates and displacement of benthic fish (Feminella Crayfish were sampled between July and October and Resh 1989; Guan and Wiles 1997; Sala et al. 2000; 2012 from nine sites along the northern shoreline of 122 The diet of Cherax quadricarinatus in Lake Kariba Figure 1. Location of the study sites in the Sanyati Basin of Lake Kariba, Zimbabwe (for details see Supplementary Table S1). the Sanyati Basin (Figure 1), using opera house trap Dietary items were identified and separated within the nets (rectangular frame: 70 × 30 cm, mesh: 3 mm). petri dish
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