African Journal of Aquatic Science 2014, 39(4): xx–xx Copyright © NISC (Pty) Ltd Printed in South Africa — All rights reserved AFRICAN JOURNAL OF AQUATIC SCIENCE ISSN 1608-5914 EISSN 1727-9364 http://dx.doi.org/10.2989/16085914.2014.980774

Short Note

Predation on invasive redclaw crayfish Cherax quadricarinatus by native fishes in the Kafue River,

AB Tyser1* and RJ Douthwaite2

1 School of Biosciences, University of East Anglia, Norwich, UK 2 Kafue River Trust, Canterbury, Kent, UK * Corresponding author, e-mail: [email protected]

The stomach contents of eight species of predatory or omnivorous fish caught in gillnets in the Kafue River in May and June 2010 were examined to determine the relative importance, expressed as ‘prominence value’ (PV), of crayfish Cherax quadricarinatus in their diet. Four species, Clarias gariepinus, Schilbe intermedius, Serranochromis robustus and Serranochromis angusticeps, had fed on C. quadricarinatus. The PV of C. quadricarinatus was highest in C. gariepinus, in which the quantity and size of crayfish eaten was significantly correlated with standard length (SL) of fish >200 mm SL. Predated C. quadricarinatus were significantly smaller (mean carapace length [CL] 30 mm; SE 1.2) than those caught in gillnets (mean CL 76 mm; SE 0.9). No C. quadricarinatus remains were found in the stomachs of Oreochromis andersonii, macrostigma, Serranochromis macrocephalus or Mormyrus lacerda.

Keywords: Clarias gariepinus, Kafue floodplain, Namwala, Serranochromis robustus

The redclaw crayfish Cherax quadricarinatus (von Martens, pike Esox lucius (Linnaeus, 1758) (Elvira et al. 1996), and 1868) is a large, robust (up to 600 g) freshwater crayfish Micropterus salmoides (Lacepede, 1802) native to northern Australia and Papua New Guinea. (Hickley et al. 1994). Widely translocated around the world for aquaculture, it The aim of the present study was to investigate the has established feral populations in South Africa, Jamaica, occurrence and abundance of C. quadricarinatus in fish Puerto Rico and Mexico (Ahyong and Yeo 2007). Introduced diets in the Kafue River, Zambia. into Zambia in 1992 (Mikkola 1996), some are believed to The study was conducted near the fishing village of have escaped from a fish farm near the town of Kafue (F Namwala (15°44′ S, 26°27′ E) on the Kafue River some Flynn 2010, Kafue Fisheries Ltd, pers. comm.) and by 2009 300 km upstream of its confluence with the River. the crayfish had become established in the Kafue River Namwala lies beside the Kafue Flats, a floodplain where (Phiri 2009). seasonal flooding occurs for about six months of the year. True freshwater crayfish are not indigenous to continental The floodplains support a productive fishery and wetland Africa (Adegboye 1983). The ecosystem interactions and ecosystem, where the life cycle, breeding biology and effects of invasive C. quadricarinatus on the native fauna migratory movements of fish are closely related to floods are largely unknown. As detritus-feeders, their ecolog- (Williams 1971). ical niche is partly exploited by freshwater crabs, and thus Fieldwork was carried out during May–June 2010 as potential exists for competition between the two (de Moor flood levels receded. Fish and C. quadricarinatus were 2002). For example, the introduction of Procambarus clarkii sampled near three fish landing sites, Kalweza, Kalundu and (Girard, 1852) into Lake Naivasha may have led to declines Mundawanga, in a lagoon off the main channel of the river in local crab populations (Foster and Harper 2007). Cherax (Figure 1). quadricarinatus infected with a non-indigenous temnoceph- Samples were obtained using legal-sized gillnets (3 m alan flatworm parasite have also been reported from deep, 100 m long, 76 mm stretched mesh) set at 18:00 and KwaZulu-Natal, South Africa, raising the further possibility collected at 07:00 the following day. Catches were made at that this parasite might transfer to native decapods such as regular weekly intervals over four consecutive days during crabs (du Preez and Smit 2013). the eight-week study period. Fish samples were supple- Where native, crayfish are an important prey component mented by angling. Fish were identified in the field using of predatory freshwater fish (Fedoruk 1966; Snow 1971; keys in Bell-Cross (1976) and placed directly on ice to slow Clady 1974 cited in Stein 1977), and where they have been digestion in the field. In the laboratory, fish were measured introduced they have on occasion become an important to the nearest 1 mm standard length (SL), dissected, and component of the diets of predatory fish such as northern the gut contents were removed and placed in 99% alcohol.

African Journal of Aquatic Science is co-published by NISC (Pty) Ltd and Taylor & Francis 2 Tyser and Douthwaite

(a) (b)

Lusaka

AFRICA

Zambia Kafue River Itchzi-tchzi Kafue Namwala 15°40' S See enlarged area (b) Mazabuka

See enlarged area (a) ZAMBIA

C 1.2 km

AGOON L

AMWALA N

Namwala

A B

26°20' E 26°25' E

Figure 1: Map of the Kafue River at Namwala showing locations of landing/sampling sites: A  Kalweza, B  Kalundu, and C  Mundawanga

Gut contents were examined, using magnification where Table 1: Regression formulae for calculating Cherax necessary, and identified to the lowest possible taxonomic quadricarinatus total length (TL) from various body parts (all level. Ingested invertebrates were visually identified to measurements in mm). Sample size = 52 categories ranging from broad taxonomic groups to family, according to reasonable limits of identification (Hickley et al. Body part measurement Formula r2 1994). Identification of aquatic invertebrates was achieved Carapace length (CL) TL  2.19 CL + 1.06 0.97 using keys in McCafferty (1998) and Gerber and Gabriel Uropod width (UW) TL  2.08 UW 7.30 0.97 (2002). Terrestrial invertebrates were identified by referring Uropod length (UL) TL  6.69 UL + 0.81 0.97 to Griffiths (2002). Carapace width (CW) TL  5.36 CW + 0.48 0.97 The number of individuals in each food category was Telson width (TW) TL  9.16 TW + 1.30 0.96 recorded for all stomachs, and the relative importance Log chelae length*log (CHL) TL  0.80 CHL + 0.81 0.96 of each dietary component was expressed using a Telson length (TEL) TL  12.40 TEL + 3.35 0.93 prominence value (PV), calculated as: Chelae width (CHW) TL  6.51 CHW + 50.18 0.85

PV  % N u—% S where % S represents the occurrence of the food item in of 21 intact C. quadricarinatus found in fish stomachs. In all stomachs containing food % N, abundance, is the total the case of chelae length and total weight, regressions number of the item as a percentage of all food items found were constructed with log-transformed data to normalise (Hickley et al. 1994; Lorenzoni et al. 2002). and reduce the heteroscedasticity of the data (Field 2009). Where possible, ingested C. quadricarinatus were For crayfish caught in gillnets, the carapace length (CL, weighed whole and measured to the nearest 1 mm for total distance between rostrum tip and posterio-median carapace length (TL, tip of rostrum to distal tip of telson), carapace edge) was recorded to the nearest 1 mm. length, carapace width, chelae length, uropod length and Nine predatory or omnivorous fish species were sampled telson length. To predict the total length of predated C. (n  968; Table 2). Four of these, primarily piscivo- quadricarinatus when only the telson, chelae, carapace rous species, Clarias gariepinus (Burchell, 1822), Shilbe or uropod were found, regression models were developed intermedius (Rüppell, 1832), Serranochromis robustus and based on the morphometric measurements of various body Serranochromis angusticeps (Boulenger, 1907), had fed on parts of 52 specimens (Table 1), including the dimensions C. quadricarinatus (Table 3). African Journal of Aquatic Science 2014, 39(4): xx–xx 3

Table 2: Summary of fish samples collected for gut content analysis from the Kafue River in 2010

Mean SL ± standard SL range No. of stomachs Species n error of the mean (mm) (mm) containing food Schilbe intermedius 242 198 ± 2 113–342 58 Clarias gariepinus 230 348 ± 5 173–767 81 Serranochromis angusticeps 204 223 ± 2 107–370 114 Serranochromis macrocephalus 182 215 ± 2.5 106–367 91 Serranochromis robustus 87 256 ± 6 186–396 33 Oreochromis andersonii 32 239 ± 6 160–297 12 Synodontis macrostigma 16 130 ± 4 106–157 4 Mormyrus lacerda 9 309 ± 20 238–456 4

Table 3: Diets of Clarias gariepinus, Shilbe intermedius, Serranochromis angusticeps and Serranochromis robustus from the Kafue River in 2010. % S  percentage occurrence of a given food item in stomachs containing food, PV  prominence value. Items, other than crayfish, with a PV <0.01 omitted

C. gariepinus S. intermedius S. angusticeps S. robustus S. robustus* Food item % S PV % S PV % S PV % S PV % S PV Fish 70 0.34 95 0.66 88 0.38 59 0.64 62 0.39 Brycinus lateralis 17 0.02 25.5 0.08 24 0.18 53 0.32 14 0.04 Cichlidae spp. –– 10 0.02 41 0.18 –– –– Oreochromis niloticus –– – – – – – – 5 0.02 Schilbe intermedius –– – – 10 0.02 6 0.01 –– Serranochromis macrocephalus –– 10 0.02 –– – – – – Synodontis spp. –– – – – – – – 19 0.08 Coptodon rendalli 21 0.1 9 0.03 –– – – 14 0.17 Fish remains 13 0.01 24 0.05 16 0.03 31 0.15 14 0.09 Crustacea 56 0.08 6 0.01 – – 6.5 0.06 48 0.19 Cherax quadricarinatus 49 0.046 5 0.007 1 0.0009 3 0.004 38 0.08 Decapoda – Potamonautidae – – – – – – 6 0.01 9.5 0.01 Gastropoda 33 0.11 – – – – – – – – Planorbidae 15 0.04 –– –– –– –– Insecta 52 0.16 8 0.01 9 0.02 9 0.03 6 0.01 Diptera spp. –– – – – – 9 0.01 4 0.01 Insecta spp. 8 0.02 –– 4 0.01 –– –– Seeds and vascular plants 11 0.03 6 0.06 11 0.02 – – – – * Rod-caught S. robustus listed separately from those caught in gillnets

Regression of C. quadricarinatus TL against length of various body parts (Table 1) indicated that specimens ranging from 23 to 139 mm TL had been eaten by the 125 four fish species. Those C. quadricarinatus eaten by C. gariepinus ranged in size from 12 to 64 mm CL (mean 100 30 mm, SE 1.2, n  77). This was significantly smaller than of those caught in gillnets (33–111 mm CL, mean 76 mm, SE 0.9, n  407) (Mann–Whitney U-test, U  438.5; p < 75 0.001). Clarias gariepinus predated on C. quadricarinatus ranging from 5% to 34% of their own SL (C. quadricarinatus 50 23–139 mm, mean 64 mm TL, SE 2.5). Clarias gariepinus CRAYFISH TL (mm) TL CRAYFISH was the most important predator of C. quadricarinitus. There was a positive relationship between C. gariepinus SL 25 and the quantity of crayfish consumed (linear regression: 200 300 400 500 600 700 2 df  77, r  0.32, p < 0.05) and the reconstructed lengths C. GARIEPINUS SL (mm) of ingested crayfish indicated that larger C. gariepinus prey 2 on larger crayfish (y  0.12x + 22.03, r  0.140, p < 0.001) Figure 2: Relationship between crayfish total length (TL) and (Figure 2). Clarias gariepinus standard length (SL) Too few intact C. quadricarinatus were found in the stomachs of S. robustus (n  9, mean 94 mm CL, SE 8.6), S. intermedius (n  9, mean 50 mm CL, SE 6.5) and S. 4 Tyser and Douthwaite angusticeps (n  1) to allow analysis of the size of crayfish Prominence values for C. quadricarinatus in fish diets prey in relation to fish size. No C. quadricarinatus or other were relatively low in this study, even in C. gariepinus. crustaceans were found in the stomachs of Oreochromis However, PV may underestimate the importance of C. andersonii (Castelnau, 1861), Synodontis macrostigma quadricarinatus for a number of reasons. This is partly due (Boulenger, 1911), S. macrocephalus (Boulenger, 1899) to the fact that PV depends upon the relative abundance or Mormyrus lacerda (Castelnau, 1861). Oreochromis of the particular item – and not its relative size – and will andersonii fed chiefly on hydrobiid snails and vascular underestimate the importance of large items such as C. plants (PV 0.3 and 0.06, respectively). Serranochromis quadricarinatus compared with small items such as seeds macrocephalus was piscivorous, feeding mostly on Brycinus consumed in large quantities (Figure 2). Furthermore, lateralis (Peters, 1852) (PV 0.15) and S. intermedius (PV because PV is also dependent upon the presence or 0.04). Mormyrus lacerda fed most heavily on ceratopogonid absence of the item in the stomach at the time of sampling, larvae (PV 0.36), while plant detritus was the main it may under-represent large food items that are eaten component in the diet of S. macrostigma (PV 0.49). infrequently and digested relatively quickly. Previous Carey (1968) described the diet of 15 Kafue fish species. studies have shown that freshwater crayfish contain little However, no measures of abundance/occurrence were energy compared with fish prey, although they are eaten in quantified so it was not possible to extrapolate from this large numbers and digested quickly (Elvira 1996). Further earlier study any dietary shifts that may have arisen study is needed to determine whether C. quadricarinatus following the introduction of C. quadricarinitus. will become an important food item for native fish species. Clarias gariepinus is an opportunistic predator, employing a variety of feeding methods including surface Acknowledgements — I thank the following, without whom this feeding, foraging and pack hunting (Bruton 1979; Merron study and paper would have been impossible: Robert Douthwaite, 1993) and therefore it is not surprising that it also feeds The Kafue River Trust; Dr Alistair Grant, University of East Anglia; Daniel and Ailsa Green, Chenga Farm, Choma, who assisted on C. quadricarinitus. Clarias gariepinus has a wide gape with logistics; Dr Patrick Ngalande, Department of Fisheries, who and it may be this feature that allows even relatively helped me secure a research permit; and Department of Fisheries small fish to ingest crayfish specimens. Clarias spp. have staff, Namwala, who provided me with sampling facilities and a been known to consume prey 25–58% of their length desk. Financial support was provided by the University of East (Groenewald 1963) although, in general, prey rarely Anglia and the Sir Philip Reckitt Educational Trust. Dr Roger Bills exceeds 20% of predator length (Bruton 1979). In this and Margie Shaw, South African Institute for Aquatic Biodiversity study, most C. quadricarinatus eaten by C. gariepinus (SAIAB), kindly provided reprints from the Fisheries Research were under 20% of the predator length, although almost Bulletin of Zambia. 30% of those eaten were larger. There is little published data on the diet of S. robustus. References Carey (1968) did not include this species in his study, but Bell-Cross (1976) described crabs as favoured prey in the Adegboye D. 1983. On the non-existence of indigenous species diet of S. robustus in . Winemiller (1991) of crayfish on the continent of Africa. Freshwater Crayfish 5: 564–569. found ‘crustaceans’ were a minor constituent (<10% Ahyong ST, Yeo CJ. 2007. 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Manuscript received 7 June 2013, revised 11 September 2014, accepted 18 October 2014 Associate Editor: OLF Weyl