African Journal of Aquatic Science is co-published by NISC (Pty) Ltd and Informa UK Limited (trading as Taylor & Francis Group)
Freshwater crayfish are not native to continental Africa, but interest in their use for aquaculture and fishery enhance-ment in this continent goes back fifty years (Mikkola 1996). Experience from around the world and specifi-cally in eastern and southern Africa, has shown they will usually escape the confines of any facility regardless of the biosecurity measures taken (Mikkola 1996; Nunes et al. 2017a). Once naturalised, freshwater crayfish are likely to cause ecological imbalances with dramatic and damaging consequences (Mikkola 1996; Smart et al. 2002). Globally, the negative ecological impacts of introduced crayfish are strikingly consistent, with all levels of freshwater food webs affected through reduction of basal resources, such as aquatic macrophytes, invertebrates (including snails and insects) and amphibians and fish (Twardochleb et al. 2013). Crayfish introductions also impact a variety of ecosystem services bringing about significant socio-economic costs (Lodge et al. 2012).
Four species of crayfish are known to have been imported to Zambia for aquaculture: Louisiana red swamp crayfish Procamburus clarkii, marron Cherax cainii, common yabby Cherax destructor and redclaw crayfish C. quadricarinatus (Audenaerde 1994). Anecdotal reports of C. quadricarinatus living in the wild first appeared early this century. By 2008, it was clear the species was naturalised and was spreading in the Kafue River
and Lake Kariba, causing concern amongst artisanal fishermen and in the Department of Fisheries (Phiri 2009; Nakayama et al. 2010).
Not much is known on the ecological impact of natural-ised C. quadricarinatus populations, but de Moor (2002) pointed out that, as detritus-feeders, the species’ ecolog-ical niche is also exploited by freshwater crabs, raising the prospect of competition between the two. In addition, in South Africa, C. quadricarinatus has been found to carry non-native temnocephalan flatworms, which might be transferred to native decapods, such as crabs (du Preez et al. 2013; Tavakol et al. 2016). Concerned that the spread of C. quadricarinatus in Zambia would have significant ecological and socio-economic consequences, the Kafue River Trust began a project to investigate the circumstances around their introduction into the wild in the Zambezi River basin (Figure 1); to monitor their spread and impact and to collect information on their ecological effects. Two short field surveys on the Kafue River, as well as a public appeal for information on the species’ occurrence were conducted. The findings are summarised in this paper.
Materials and methods
Field surveys to monitor the invasion of the Kafue River, from Lake Itezhi-tezhi, through the Kafue National Park to
The introduction, spread and ecology of redclaw crayfish Cherax quadricarinatus in the Zambezi catchment
RJ Douthwaite1* , EW Jones2, AB Tyser1 and SM Vrdoljak3
1 Kafue River Trust, Holly Oast, Canterbury, United Kingdom2 3 Cwm Arthur, Myddleton Park, Denbigh, United Kingdom3 Wildtracks Lodge, Chiawa, Lusaka Province, Zambia*Corresponding author, email: [email protected]
Two of the four crayfish species brought to Zambia for aquaculture since 1979 are now naturalised. Procamburus clarkii occurs in the Maramba River at Livingstone, close to a former fish farm, whereas Cherax quadricarinatus, deliberately introduced to a number of sites in the Zambezi and Kafue River catchments since 2001, is now widespread and highly invasive. High rates of dispersal, up to 111 km y−1 downstream, might be the result of passive transport on floating vegetation. Significantly more synodontid Synodontis sp. catfish were caught in Fladen traps in the Kafue River in crayfish-free areas compared with crayfish-infested areas, but the possibility that synodontids became trap averse in the presence of crayfish was not ruled out. No difference was found in the numbers of Single-spined River Crab Potamonautes unispinus caught in crayfish-free and infested areas. Alien temnocephalans, commonly found on crayfish, are now also present on crabs P. unispinus on the Kafue Flats. The artisanal gill net fishery has been harmed by the introduction of C. quadricarinatus and no significant commercial fishery has developed. However, without more information on the adverse impacts, and stronger fisheries regulation, there is a high risk C. quadricarinatus and P. clarkii will be introduced to uninfested catchments with irreversible consequences for artisanal fishermen and the environment.
Keywords: invasive species, Kafue River, Potamonautes unispinus, Procamburus clarkii, Synodontis
the Mushingashi Conservancy, were done from 31 May to 7 June 2015 and 10 to 16 May 2017, as flood levels were receding. Collapsible, cylindrical Fladen traps (dimensions: 60 × 30 cm, entrance diameter: 90 mm, mesh size 20 mm) baited with c. 50 g of proprietary meatloaf for dogs, wrapped in mosquito netting to prevent disintegra-tion, were used to assess the presence of crayfish and the relative abundance of any feeding competitors. Traps were set in the late afternoon and emptied early the following morning. The number set varied depending on the ease of access to the riverbank at each site. Crayfish and crabs caught were identified, sexed, weighed and checked for the presence of symbionts, such as flatworms. Crayfish carapace length and crab carapace width were also measured. Females were checked for the presence of eggs or young. Fish were identified, measured (TL mm) and weighed. Given that the taxonomy of synodontids in the Zambezi River basin is unresolved (P Skelton, South African Institute for Aquatic Biodiversity, pers. comm. 2015), no attempt to distinguish species was made.
Trapping was carried out in five areas on the Kafue River: in the Mushingashi Conservancy (catches from 14°27'11" S, 26°38'38" E and 14°28'34" S, 26°37'05" E combined); in Kafue National Park, at Mayukuyuku Bush Camp (14°54'54" S, 26°03'50" E), Kaingu Safari Lodge (15°17'56" S, 25°58'41" E) and Kantunta Safari Lodge (15°22'05" S, 25°59'06" E) and on Lake Itezhi-tezhi, at New Kalala Camp (15°46'23" S, 26°00'40" E).
In order to achieve wider coverage, a public appeal for information on the presence or absence of crayfish in the Zambezi catchment was launched through the Trust’s website (www.kafuerivertrust.org), social and printed media and directly with sport fishermen and tourist lodge owners with property next to the Kafue and Zambezi Rivers. Most respondents were private citizens not associ-ated with any research facility. Few published details of the introduction and initial occurrence in the wild of C. quadricarinatus were found and a search for grey litera-ture and key informants was also performed. Our enquiries led to the discovery of a second species of crayfish in the wild, the Louisiana red swamp crayfish Procamburus clarkii and a comprehensive review of crayfish introduc-tions into Zambia was therefore done.
Results
History of crayfish introductions and spread in the river basinThe first crayfish brought to the Zambezi catchment were Louisiana red swamp crayfish Procamburus clarkii, native to northern Mexico and the southern United States, which were brought from Lake Naivasha in Kenya to Grubb’s farm at Livingstone in 1979 (Audenaerde 1994). Some were then moved to ponds near Kitwe in 1979–1981, but cultivation failed when they escaped to the Kafue River (Audenaerde 1994). None has since been reported in the area. A
AFRICA
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BotswanaZimbabweNamibia
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Cherax quadricarinatus
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150 300 km
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Figure 1: Location of the study area with Cherax quadricarinatus and Procamburus clarkii introduction sites
African Journal of Aquatic Science 2018, 43(4): 353–366 355
separate introduction of P. clarkii was made to Siavonga on Lake Kariba in 1979, but cultivation there also failed (Mikkola 1996) and there have been no additional reports of this species in the lake.
Grubb (2007) claimed that none of his stock escaped, but in 2017 a population of Procamburus clarkii was reported to be present in the Maramba River, adjacent to Grubb’s former farm in Livingstone (Figures 1 and 2) (R Walker pers. comm. 2017; A Welz pers. comm. 2017). According to a local fisherman, they had been in the river since 1995, but never caught in large numbers (R Walker pers. comm. 2018). Following a failure to cultivate Cherax cainii at Livingstone, Cherax destructor and C. quadricarinatus were imported from South Africa in 1992 (Audenaerde 1994; Mikkola 1996) (Table 1). Cultivation of C. destructor failed (Mikkola 1996), but C. quadricarinatus, a native of northern Australia and Papua New Guinea, thrived. Some of these were taken to other sites, at unspecified times (Table 1) (Grubb 2007), but with the exception of those taken to Miengwe Farm in the upper Kafue catchment (Table 2), there is no evidence any reached the wild.
In 2001, a second batch of C. quadricarinatus was imported to Zambia, from a farm that was closing down near the Sand River Dam in Swaziland. They were taken to a fish farm at the eastern end of the Kafue Flats (A Piers pers. comm. 2010; Nunes et al. 2017a) and almost immedi-ately some escaped to the Kafue River (Table 1) (F Flynn pers. comm. 2017; Welz 2017). Stock was also transferred to aquaculture cages at Siavonga in Lake Kariba, whence they escaped to the lake in 2002 (Table 1) (A Piers pers. comm. 2010; Financial Gazette 2014).
The spread of C. quadricarinatus and rate of dispersalThere are no published records of the initial introduction or early occurrence of C. quadricarinatus in the wild, but by 2007/2008 it was sufficiently abundant in Lake Itezhi-tezhi and Lake Kariba to be used for the bioassay of heavy metals in lake sediments and aquatic biota (Nakayama et al. 2010). Similarly, on the Kafue Flats, it was sufficiently numerous to be causing a nuisance to artisanal fishermen and concern in the Department of Fisheries (Phiri 2009). Our enquiries indicate C. quadricarinatus was introduced to these and other sites from 2001 onwards (Table 2, Figure 1).
C. quadricarinatus was first noticed in the wild in 2001–2002, at Nyimba, in Lochinvar National Park in the central Kafue Flats (S Phiri, Department of Fisheries, Zambia, pers. comm. 2015); near Kafue Fisheries in the eastern Kafue Flats (F Flynn pers. comm. 2017; A Welz 2017) and at Siavonga on Lake Kariba (Financial Gazette 2014). By 2009, infestations were also well established near Mazabuka and Namwala on the Kafue Flats (Figure 1) (Tyser 2010) and in Lake Itezhi-tezhi (Nakayama et al. 2010), suggesting introductions had also been made there some years earlier.
From 2012, new infestations have been reported in the upper Kafue River catchment at Nsobe Dam near Kitwe (F Willems pers. comm. 2015); middle Kafue River in the Mushingashi Conservancy (G Bell-Cross pers. comm. 2015); the Garganta basin in Lake Cahora Bassa (W Mhlanga, Bindura University, Zimbabwe, pers. comm. 2015), Claw and Mazvikadei Dams in Zimbabwe, in the
middle Zambezi catchment (C Skinner pers. comm. 2015 and 2016) and in the upper Zambezi River near Lealui (P Ngalande, Department of Fisheries, Zambia, pers. comm. 2015) (Figure 1).
Reports indicate that C. quadricarinatus has rapidly spread from several of these sites (Table 3, Figures 3–5). On the Kafue River (Figure 3), the infestation in the Mushingashi Conservancy, first noticed in 2013/2014 (G Bell-Cross pers. comm. 2015), has extended downstream into Kafue National Park. In July 2016, large numbers were found at Lunga Island, 32 km downstream of the conservancy, with a few individuals also found at Hippo Lodge, 44 km downstream of the introduction point (G Mole pers. comm. 2016). However, no crayfish were caught in the same month at Kafwala Camp, 132 km downstream of the conservancy (B Danckwerts pers. comm. 2016) or,
Figure 2: Procamburus clarkii from the Maramba River (courtesy R Walker)
Douthwaite, Jones, Tyser and Vrdoljak356
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in May 2017, during our fieldwork, at either Mayukuyuku Bush Camp or Kaingu Safari Lodge farther downstream. Upstream of the Mushingashi Conservancy, so far, no specimens have been reported from the western Lukanga Swamps (C Phiri, BirdWatch Zambia, pers. comm. 2018) or near Mpongwe in Copperbelt Province (B and G Karg pers. comm. 2016; T Pelios pers. comm. 2016).
The infestation in Lake Itezhi-tezhi, already well established in 2008, was reported to have spread a few kilometres upstream in the Kafue River to reach Kantunta Lodge by July 2016 (V Humphrey pers. comm. 2016) (Figure 3). However our field survey in May 2017 found C. quadricarinatus to be very abundant in the area and with a wide size range, which suggests a longer presence in the area.
In the middle Zambezi River (Figure 4), the infestation in Lake Kariba first reported in 2002 had, by 2011, spread from Siavonga for at least 21 km along the Zimbabwean shoreline to Zebra Island (Marufu et al. 2014) and to Elephant Point, 36 km from Siavonga (Stutchbury cited in Marufu et al. 2014). In 2015, C. quadricarinatus was reported present at Sinazongwe, 180 km from Siavonga (J Kenney pers. comm. 2015) and in May 2018, at Nameso and Makunka fishing camps on the Zambian shore opposite Mlibizi Resort in Zimbabwe, near the head of the lake and some 240 km from Siavonga (O Siamweela per M Imakando pers. comm. 2018). Accordingly, colonisation of Lake Kariba has taken about 16 years.
The first C. quadricarinatus reported in the middle Zambezi River downstream of Lake Kariba was caught by an angler immediately below the dam wall, in September 2013 (Victoria Falls 24.com. 2013). Subsequent reports suggest colonisa-tion of the river between Kariba and the headwaters of Lake Cahora Bassa was rapid. In April 2014, a local fisherman reported catching his first in the river near Wildtracks Lodge, 90 km downstream (pers. obs. 2014). Additional reports then came from Baines Camp, 115 km downstream, in July 2015 (B-M McCarthy pers. comm. 2015); Chongwe River, 125 km downstream, in July 2015 (B-M McCarthy pers. comm. 2015), Chiawa Camp, 135 km downstream, in August 2015 (D Cumings pers. comm. 2015) and Anabezi Camp, 175 km downstream, in October 2015 (C Davy pers. comm. 2015). Finally, in December 2015, a local fisherman reported catching his first crayfish at Kanyemba in Zimbabwe, close to the head of Lake Cahora Bassa (B Schadie pers. comm. 2016), some 260 km from the Kariba Dam wall.
The year of introduction is unknown, but C. quadricarinatus is known to have been present in the easternmost Garganta basin of Lake Cahora Bassa since 2013 (W Mhlanga, Bindura University, Zimbabwe, pers. comm. 2013). However, no C. quadricarinatus have been reported yet by anglers fishing downstream in the lower Zambezi River (C Skinner pers. comm. 2017; Figure 4).
In the upper Zambezi catchment, the 2012 introduc-tion near Lealui had spread c. 45 km up the Luanginga River to Kalabo by November 2017 (I Pollard, African Parks, pers. comm. 2017) and in the Zambezi River for c. 85 km upstream to within 25 km of Lukulu and for c. 160 km downstream, almost to Senanga (A Chilala, Ministry of Agriculture and Livestock, Zambia, pers. comm. 2017) (Figure 5). However, in August and September 2016, anglers caught large male and female
African Journal of Aquatic Science 2018, 43(4): 353–366 357
Date Reported Location Source Reference2001 Nyimba, Lochinvar National Park, central
Table 2: Initial naturalisation sites and suspected sources
Source and Date of Introduction First Report
Distance (km)
Period (months)
Rate1 (km y−1)
Zambezi River DownstreamPlunge pool below Kariba Dam (Sept. 2013) Kanyemba, Zimbabwe (Dec. 2015) 260 28 111Lealui (2012) Katima Mulilo, Namibia (Aug. 2016) 360 50 86Lealui (2012) 10 km upstream from Senanga (Nov. 2017) 160 64 30
Kafue River DownstreamMushingashi (Sept. 2014) Hippo Lodge, Kafue National Park (July 2016) 44 22 24
Lake KaribaSiavonga (2002) Nameso and Makunka fishing camps (May 2018) 240 190 15
Zambezi River UpstreamLealui (2012) 25 km downstream of Lukulu (Nov. 2017) 85 64 16
Luanginga River UpstreamLealui (2012) Kalabo (Nov. 2017) 45 64 8
Note1: if the month of introduction is unknown, it is assumed to have been at the end of June
Table 3: Rates of dispersal of C. quadricarinatus in the Zambezi River catchment
C. quadricarinatus 360 km downstream of Lealui at Namwi Island near Katima Mulilo, Namibia (S Coertzen per D Tweddle, South African Institute for Aquatic Biodiversity, pers. comm. 2016; Blaauw family per B van der Waal, University of Venda, South Africa. pers. comm. 2017), suggesting more rapid dispersal downstream in the Zambezi River or a separate introduction event.
Rates of dispersal have been estimated from these records (Table 3). These vary from more that 100 km y−1 downstream in the middle Zambezi River to less than
10 km y−1 upstream in the Luanginga River, a tributary of the upper Zambezi River, with generally higher rates observed downstream than upstream.
Fieldwork: presence, abundance and population dynamics of C. quadricarinatus in the Kafue RiverTrapping in 2015 conf i rmed the presence of C. quadricarinatus in Lake Itezhi-tezhi (New Kalala) and discovered a previously unknown population in the Mushingashi Conservancy. Trapping in 2017 confirmed
Douthwaite, Jones, Tyser and Vrdoljak358
Lukanga Swamp
LegendCherax quadricarinatus
IntroducedPresentNot detected
Kitwe D R C O N G O
Z I M B A B W E
Mpongwe Nsobe Dam
Kafue National Park
Kafue
Mushingashi Conservancy
Z A M B I A
Lunga IslandLunga Island
Kafwala CampHippo LodgeHippo Lodge
Mayukukuyu CampMayukukuyu Camp
Kaingu Lodge
Kantunta LodgeKafue Flats
Lake Itezhi-tezhi
Namwala Nyimba
ChungaMazabuka
Lusaka
Chilanga
Kafue
Kafue Fisheries Zambezi
100 km
L Kariba
15°0'0" S
30°0'0" E
Figure 3: Occurrence of C. quadricarinatus in the Kafue River basin
Table 4: Trapping effort and catches in 2015 and 2017
crayfish had reached Kantunta, about 25 km upstream of Lake Itezhi-tezhi and their continuing absence from Kaingu (10 km farther upstream) and Mayukuyuku in the Kafue National Park (Figure 3, Table 4).
The mean catch trap−1 night−1 (catch per unit effort: CPUE) in infested areas was 6.7 (n = 27, s2 = 59.1, minimum–maximum: 0–24 individuals). The high variance was indicative of a contagious distribution (Figure 6) with 65% of the total catch caught in traps which contained 17 or more individuals.
The mean CPUE at Mushingashi increased significantly between 2015 and 2017, from 1.67 to 11.2 respectively (Mann–Whitney U-test: U = 8.5, Z = 2.278, p < 0.05) (Table 4).
C. quadricarinatus had a mean carapace length of 68 mm (n = 172, s2 = 190, minimum–maximum: 36–99 mm) and a mean mass of 78 g (n = 153, s2 = 2 012, minimum–maximum 12–200 g) (Table 5, Figure 7). Two individuals exceeded the scale maximum of 200 g and were estimated to have had a mass of 225 g. Similar numbers of males and
African Journal of Aquatic Science 2018, 43(4): 353–366 359
females were found in each area, except in Mushingashi in 2017, when significantly more females than males were recorded (binomial test, p < 0.01) (Table 5, Figure 7).
Crayfish mass was positively correlated with carapace length (n = 151, r2 = 0.9773) (Figure 8). Using data from 2017, the linear regression of log mass (M) on log carapace length (CL) was log M = 2.9377 × log CL − 3.5575.
Crayfish were generally larger in 2017 than in 2015 (Mann–Whitney U-test, carapace length, U = 842, Z = 2.98, p = 0.003) and in 2017 their size varied between sites and sexes (Figure 7). In 2017, they were larger and heavier at Kantunta than at Mushingashi (Mann–Whitney U-test, carapace length: U = 1 710.5, Z = −3.524, p < 0.001; mass: U = 1 773, Z = −3.284, p = 0.001) (Table 5, Figure 7). In addition, males were larger and heavier than females at both sites (Mann–Whitney U-test, Mushingashi: carapace length U = 732, Z = −3.015. p = 0.0025; mass U = 711, Z = −3.165, p = 0.0015; Kantunta: carapace length U = 181, Z = 2.857, p = 0.004; mass U = 166, Z = 3.132, p = 0.0017). No ovigerous females were caught in either 2015 or 2017.
Ecological observations: commensals, competitors and predatorsTwenty seven (24%) of the 112 C. quadricarinatus caught at Mushingashi in 2017 were infested with eggs, identi-fied as temnocephalan (L McLeay, South Australian Development and Research Institute, pers. comm. 2015). Only three (6%) of the 51 animals examined at Kantunta were found to be infested. No temnocephalans were found on crabs during our field surveys, but many of the crabs at Namwala on the Kafue Flats are now reported to be infested with their eggs (A Bruce-Miller pers. comm. 2018) (Figure 9).
Fladen traps set in the Kafue River in 2015 and 2017 caught C. quadricarinatus and other competitors for the bait, including crabs, synodontids Synodontis sp. and occasionally other fish, including Enteromius sp., Schilbe intermedius, Clarias sp., Labeobarbus marequensis and different species of cichlids (Table 4). Crabs were identified as the Single-spined River Crab Potamonautes unispinus (N Cumberlidge, Northern Michigan University, USA, pers. comm. 2015), known to occur in Zimbabwe and South
LegendCherax quadricarinatus
IntroducedPresentNot detected
Z I M B A B W E
Kafue
Z A M B I A
Lusaka
Kafue
30°0'0" E
100 km
16°30'0" S
M O Z A M B I Q U E
Chiawa Camp
Anabezi Camp Kanyemba
Chongwe
Wildtracks LodgeBaines River Camp
Lake Cahora Bassa
Garganta Basin
Lower ZambeziKariba Dam wall
Zebra IslandSiavonga
Elephant PointLake Karib
a
Sinazongwe
Sanyati
Mazvikadei Dam
ZambeziNameso/Makuko
Claw Dam
Harare
Figure 4: Occurrence of C. quadricarinatus in the middle and lower Zambezi River basin
Douthwaite, Jones, Tyser and Vrdoljak360
Year Site Sample Samplesize (n)
Mean (minimum–maximum) CL (mm)
Mean (minimum–maximum) mass (g)
2015 New Kalala All 9 61 (43–80) –Male 5 62 (54–80) –
Figure 6: Catches of C. quadricarinatus, synodontids and P. unispinus crabs in crayfish-free and crayfish-infested areas of the Kafue River
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Africa (Daniels et al. 2001; Cumberlidge 2008), but not previously recorded in Zambia.
Synodontids predominated numerically in traps in crayfish-free areas (Table 4). The mean CPUE in crayfish-free areas was 4.8 (n = 29, s2 = 23.3, minimum–maximum: 0–30 individuals). The high variance was indicative of a contagious distribution (Figure 6) with 67% of the total catch caught in traps containing 14 or more individ-uals. Significantly fewer synodontids were caught and no aggregations detected, in crayfish-infested areas (Mann–Whitney U-test, U = 251.5, Z = 2.288, p = 0.022) (Figure 6, Table 4). The mean CPUE was 0.6 per trap (n = 27, s2 = 1.2, minimum–maximum 0–4 individuals). At Mushingashi, where a significant increase in crayfish numbers occurred between 2015 and 2017 (see above), the mean CPUE for synodontids changed from 1.1 to 0.5 over the same period, a non-significant difference (Mann–Whitney U-test, U = 22, Z = 0.813, p > 0.05). The synodontid catches at Mushingashi are comparable with mean CPUEs of 4.6 and 6.6 at crayfish-free sites in 2015 and 2017 respectively. Synodontids had a mean total length (TL) of 14.0 cm (n = 100, s2 = 15.7, minimum–maximum: 5–22 cm) and three individuals of 14.0 cm TL averaged 32 g mass.
The Single-spined River Crab P. unispinus was found in every sample area in both years (Table 4). The mean CPUE in crayfish-free areas was 0.48 (n = 29, s2 = 1.76, minimum–maximum: 0–5 individuals) compared with a mean CPUE in crayfish-infested areas of 1.44 (n = 27, s2 = 10.87, minimum–maximum: 0–15 individuals) (Table 4). The difference was not significant (Mann–Whitney U-test, U = 302, Z = −1.459, p > 0.05). P. unispinus was reported to prefer rocky habitats (A Bruce-Miller pers. comm. 2018) and most of ours were caught immediately below the rapids at Kantunta and on the rocky shore of Lake Itezhi-tezhi at New Kalala (Table 4). No ovigerous or brooding females were found.
P. unispinus had a mean carapace width (CW) of 53 mm (n = 53, s2 = 79, minimum–maximum: 34–71 mm) and mean mass of 40 g (n = 34, s2 = 393, minimum–maximum: 11–73 g). Males had a significantly narrower carapace than females but had a similar mass (Mann–Whitney U-test, carapace width: U = 155.5, Z = 3.457, p = 0.0005; mass: U = 87, Z = −1.949, p = 0.051).
Local residents at Kantunta reported seeing clawless otter Aonyx capensis, reed cormorant Phalacrocorax africanus, marabou stork Leptoptilos crumeniferus, hadada ibis Bostrychia hagedash, fish eagle Haliaeetus vocifer, catfish Clarias sp., silver barbel Schilbe intermedius and largemouth bream Serranochromis sp., eating crayfish nearby (A Kaluwe, S. Mawushiluwe pers. comm. 2017). In addition, a pied kingfisher Ceryle rudis has been seen eating small crayfish on the middle Zambezi River (R Pope pers. comm. 2016) and crayfish have been found inside bass Micropterus salmoides caught at the Claw and Mazvikadei Dams in Zimbabwe (C Skinner pers. comm. 2017).
Discussion
Populations and ecologyC. quadricarinatus was first detected in the wild in Zambia in 2001/2002, at much the same time as in Swaziland and South Africa, when a farm near the Sand River Dam in Swaziland closed and stock was brought to Zambia (A Piers pers. comm. 2010; Nunes et al. 2017b).
Although the precise dates of introduction are unknown, the subsequent spread of C. quadricarinatus has been faster in the Zambezi River catchment than in Swaziland and South Africa (Table 3). Dispersal upstream in the upper Zambezi River basin has occurred at the rate of 8–16 km y−1, compared with 5 km y−1 on the Komati River (Nunes et al. 2017a), whereas colonisation of the
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1.55 1.6 1.65 1.7 1.75 1.8 1.85 1.9 1.95
LOG
MA
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y = 2.9377x − 3.5575R² = 0.9773, n = 151
Figure 8: Linear regression for log mass (g) on log carapace length (mm) for all C. quadricarinatus caught in 2017
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Zambezi River downstream has occurred at the rate of 24–111 km y−1 compared with 8 km y−1 on the Komati River.
C. quadricarinatus is sometimes found amongst the roots of floating vegetation (Marufu et al. 2014; D Wheeler pers. comm. 2014) and passive transport on mats of vegetation might have contributed to the rapid dispersal of crayfish downstream in the Zambezi River. Drifting vegeta-tion is often seen downstream of Lake Kariba having been dislodged from backwaters by large fluctuations in water level, caused by changes in discharge from the hydropower stations at Kariba.
Dispersal downstream might well be hindered by hydropower dams. The apparent absence of C. quadricarinatus for 11 years below the Kariba Dam following their introduction to the reservoir suggests crayfish do not survive passage through hydropower turbines or over high dam spillways. Similarly, movement upstream could be hindered by rapids and dams. Consequently, dispersal upstream from Lake Itezhi-tezhi appears to have been prevented or delayed by 10 km of rapids between Kantunta Lodge and Kaingu Safari Lodge, farther upstream on the Kafue River. The Driekoppies Dam on the Lomati River in Swaziland might also be acting as a barrier to upstream dispersal (Nunes et al. 2017b).
The degree to which irrigation pumps prevent dispersal is less clear. C. quadricarinatus has apparently survived passage through large irrigation pumps to colonise irriga-tion ponds on the Zambeef Chiawa Estate, near the conflu-ence of the Kafue and Zambezi Rivers. The ponds are also populated by tigerfish Hydrocynus vittatus, sharp-tooth catfish Clarias gariepinus and bream Pharyngochromis acuticeps and we are unaware of any stocking of these species taking place. The means of colonisation of several irrigation dams in the Komatipoort area of South Africa is similarly uncertain (Nunes et al. 2017a).
Catches of C. quadricarinatus in the Kafue River were larger (CPUE: mean 6.7; maximum 24) than those in either the Komati River (CPUE: mean 3.3; maximum 9.4)
(Nunes et al. 2017b) or Lake Kariba (CPUE: mean 1.1; maximum: 4) (Marufu et al. 2014). However trap design and baits varied between studies invalidating any direct compar-ison. Consequently, Nunes et al. (2017b) used traps with a finer mesh size (10 mm) than ours (20 mm) and as a result their catches included smaller crayfish (cephalothorax length: 20–98 mm) than we trapped (cephalothorax length: 36–99 mm).
None of the C. quadricarinatus caught during May and June in this study was ovigerous or brooding. On the Kafue Flats females with eggs or young have been found from late October to April (A Bruce-Miller pers. comm. 2018), whereas in South Africa they have been found in October and December (Nunes et al. 2017b).
A large proportion of C. quadricarinatus from the Kafue River was infested with non-native temnocephalan flatworms, as was the case in South Africa (du Preez et al. 2013). Du Preez et al. (2013) raised the possibility that these might transfer to native decapods, e.g. crabs; our enquiries indicate this has now happened on the Kafue Flats (A Bruce-Miller pers. comm. 2018) (Figure 9).
On the Kafue River, C. quadricarinatus, P. unispinus and synodontids are locally abundant, benthic scavengers. Little more is known of the dietary preferences of P. unispinus, but synodontids and C. quadricarinatus are omnivorous. Synodontids feed on macroinvertebrates and small fish, as well detritus and macrophytes (Bell-Cross et al. 1988; Taylor et al. 2017), whereas C. quadricarinatus in Lake Kariba and in South Africa feeds mainly on macrophytes, macroinvertebrates, detritus and occasionally, on fish (Marufu et al. 2018; T Zengeya, South African National Biodiversity Institute, pers. comm. 2018).
Little is known of the habitat preferences of the three taxa. However C. quadricarinatus and P. unispinus differ in their habitat preferences. C. quadricarinatus appears to avoid rapids and has not been reported from seasonal streams, whereas P. unispinus breeds in seasonal streams (Gratwicke 2004) and might prefer swifter flowing rocky stretches of the river (current study; A Bruce-Miller pers. comm. 2018). No particular habitat preferences of synodontids have been identified, but large shoals can be seen in clear rivers with sandy substrate and some species might breed on floodplains during the wet season (Bell-Cross et al. 1988).
This study found no evidence to support de Moor’s concern (de Moor 2002) that crabs and C. quadricarinatus might compete for resources. On the other hand, synodon-tids and C. quadricarinatus appear to share the same spatial and dietary niches and the inverse relationship between catches of the two taxa is indicative of competi-tion. However it remains unclear whether this relationship reflects trap aversion by synodontids in the presence of crayfish or a decline in the synodontid population, owing to competition for food on a wider scale.
In addition to those recorded in this study, the predators of C. quadricarinatus now include sharptooth catfish Clarias gariepinus, nembwe Serranochromis robustus and thinfaced bream Serranochromis angusticeps on the Kafue Flats (Tyser and Douthwaite 2014) and tigerfish Hydrocynus vittatus in Lake Kariba (Marufu et al. 2017). The invasion of Procamburus clarkii in Spain resulted in population increases amongst some predators, but a decline in other species at
Figure 9: Potamonautes unispinus carrying temnocephalan eggs (courtesy A Bruce-Miller)
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lower trophic levels (Tablado et al. 2010). However, apart from the possible decline of synodontids reported here, no population level effects of the invasion of C. quadricarinatus have been detected among native species in the Zambezi River catchment so far, but such effects are likely and closer monitoring and assessment should be undertaken.
Crayfish managementZambia has a political economy characterised by collusion between the government and private sector and neglect of the rural economy, including smallholder farming, fisheries, wildlife and forestry management (Reed and Scott 2001). Consequently, there is little capacity to monitor or manage environmental problems involving invasive species, such as crayfish. Crayfish were imported under licence from the Ministry of Commerce and Industry, but without reference to the Department of Fisheries (Mikkola 1996) despite a requirement under the Fisheries Act 1974 for any importation to be approved by the Director of Fisheries (Audenaarde 1994).
The SADC Protocol on Fisheries prohibits the introduc-tion of alien species into aquatic ecosystems without the approval of all riparian states (de Moor 2004) and no stocking of natural rivers or dams has been authorised in either Zambia or Zimbabwe (Mikkola 1996). It has been suggested that the appearance C. quadricarinatus popula-tions on the Kafue Flats and in Lake Kariba from 2001 onwards might be linked to flooding or poor biosecu-rity at fish farms at Kafue, Mazabuka and Siavonga (Financial Gazette 2014; F Flynn pers. comm. 2017). However, Piers (A Piers pers. comm. 2015), who brought C. quadricarinatus from Swaziland to Zambia in 2001, has stated their introduction to the Kafue Flats and Lake Kariba was deliberate and made in the belief they would only thrive in areas where the flood regime had been regulated for hydropower production. Moreover Nyimba, Namwala and Mushingashi on the Kafue River are far from any aquaculture facility and there can be little doubt crayfish were deliberately introduced at these sites. The intended beneficiaries are unknown, but other introductions, notably to Nsobe Dam in the upper Kafue catchment and Claw and Mazvikadei Dams in the middle Zambezi catchment have been made to improve sport fishing (F Willems pers. comm. 2015; C Skinner pers. comm. 2017). On the upper Zambezi River, C. quadricarinatus was introduced near Lealui by road contractors when they cleared their construction camp in 2012 (CFRI 2015; P Ngalande pers. comm. 2015).
A new Fisheries Act was passed in 2011. This Act strengthens the conservation of aquatic biodiversity and new aquaculture and fish stocking projects now require the approval of both the Director of the Department of Fisheries and the Zambia Environmental Management Agency. It remains an offence to import any live fish (including “shell fish”) or introduce them to waters where they do not naturally occur without the permission of the Director of the Department of Fisheries. However, despite recent prioritisation of fisheries and aquaculture in Zambia’s Seventh National Development Plan (Ministry of National Development and Planning 2017) and second National Agricultural Plan (Ministry of Agriculture and Ministry of
Livestock and Fisheries 2016) the sector still faces serious challenges to effective management and implementation. These include the lack of a standalone National Fisheries Policy (Kefi Shula and Mofya-Mukuka 2015, PSAf 2017); the lack of a dedicated enforcement division within the Department of Fisheries (PMRC 2015) and severely limited financial and human resources (PMRC 2016).
In the absence of a fisheries enforcement department, fishery regulations in Zambia are widely disregarded. The release of C. quadricarinatus in the upper Zambezi River caused considerable distress amongst artisanal fishermen and complaints to government were made in 2014, yet crayfish were still being kept by road construction workers in the Western Province as late as July 2015 (N Mubonda, WorldFish, pers. comm. 2015).
The introduction of C. quadricarinatus to the Zambezi River catchment has damaged the artisanal fishing industry, because the crayfish caught are of no commercial value, damage gillnets and might spoil a third of the finfish catch (J Kenney pers. comm. 2015). Piers (quoted in Ramsden 2014) predicted the commercial fishery on Lake Kariba could yield 5 000 metric tonnes of crayfish annually, perhaps as much as 10 000 tonnes. No significant fishery has developed. A nascent attempt to export live C. quadri-carinatus as “blue lobsters” from Lake Kariba and the Kafue Flats to China is currently under way (A Bruce-Miller pers. comm. 2018).
The risk of additional translocations of crayfish within Zambia remains high. Given the adverse impacts on artisanal fishing and hazard to native fauna, there is a necessity for greater public awareness of the law and additional resources for its enforcement, as well as an urgent requirement for research to clarify the ecolog-ical risks. It is particularly necessary to survey the extent of the P. clarkii infestation of the Maramba River at Livingstone and to assess the feasibility of eradication. Nunes et al. (2016) have highlighted the threat of invasion to the Okavango Delta, a World Heritage Site, because the delta is connected intermittently during high floods via the Selinda Spillway to the Chobe and Linyanti Rivers and the Zambezi. If invasion is to be prevented intervention by multilateral organisations, such as SADC or CABI, which have specialist knowledge of invasive species manage-ment in the region, is needed to investigate the feasibility of a creating a barrier to crayfish movement on the Selinda spillway.
Acknowledgements — Many individuals sent in records and provided other information on crayfish or gave us material support. We thank G Bell-Cross, A Bruce-Miller, E Bruce-Miller, A Chilala, S Coertzen, N Cumberlidge, D Cumings, B Danckwerts, C Davy, G Dickson (Kaingu Safari Lodge), C Fastiggi, T Featherby, F Flynn, J Harvey, V Humphrey, M Imakando, A Kaluwe, B Karg, G Karg, A Katchenjela, J Kenney, Konkola Copper Mines Plc, L Marufu, S Mawushiluwe, M Mbewe, B-M McCarthy, M McLeay, W Mhlanga, G Mole, K Moonga, N Mubonda, P Ngalande, A Nunes, T Pelios, C Phiri, S Phiri, A Piers, I Pollard, R Pope, B Schadie, G Shanungu, G Shone, P Skelton, C Skinner, P Turner (Mayukuyuku Bush Camp), D Tweddle, B van der Waal, R Walker, T Wataru, A Welz, D Wheeler, F Willems, C Wilson and T Zengeya. We also thank C Legg and J Pender for preparing the maps. EWJ thanks the Kafue River Trust and his parents Ifor and Ann Jones for financial support.
African Journal of Aquatic Science 2018, 43(4): 353–366 365
Audenaerde DFET van den. 1994. Introduction of aquatic species into Zambian waters, and their importance for aquaculture and fisheries. ALCOM Field Document No. 24. FAO, Harare, Zimbabwe. http://www.fao.org/docrep/005/AD005E/AD005E00.htm [Accessed 29 January 2018].
Bell-Cross G, Minshull JL. 1988. The Fishes of Zimbabwe. Harare: National Museums and Monuments of Zimbabwe.
CFRI. 2015. The presence of alien invasive species (crayfish) in the upper Zambezi River - Lealuei area of the Barotse flood plain and implications. Unpublished internal presentation, Department of Fisheries, Chilanga, Zambia.
Cumberlidge N. 2008. Potamonautes unispinus. The IUCN Red List of Threatened Species 2008: e.T64391A12768559. http://dx.doi.org/10.2305/IUCN.UK.2008.RLTS.T64391A12768559.en [Accessed 14 July 2017].
Daniels SR, Stewart BA, Ridgway TM, Florence W. 2001. Carapace dentition patterns, morphometrics and allozyme differentiation amongst two toothed freshwater crab species (Potamonautes warreni and P. unispinus) (Decapoda: Brachyura: Potamonautidae) from river systems in South Africa. Journal of Zoology 255: 389–404.
de Moor I. 2002. Potential impacts of alien freshwater crayfish in South Africa. African Journal of Aquatic Science 27: 125–139.
de Moor I. 2004. Protocols for moving germplasm among countries in Africa. In: Gupta MV, Bartley DM, Acosta BO (Eds), Use of genetically improved and alien species for aquaculture and conservation of aquatic biodiversity in Africa. Panang: WorldFish Center Conference Proceedings 68: 77–92.
du Preez L, Smit N. 2013. Double blow: Alien crayfish infected with invasive temnocephalan in South African waters. South African Journal of Science 109:1−4.
Financial Gazette. 2014, Zambia: Harare. Crayfish Invade Bumi Basin, 3 July 2014.
Gratwicke B. 2004. Migration of the freshwater crab Potamonautes unispinus in a seasonal stream, Zimbabwe. African Zoology 39: 25–29.
Grubb CJ. 2007. Redclaw crayfish in Zambia. Crayfish News 29(2). Austria: International Association of Astacology.
Kefi Shula A, Mofya-Mukuka R. 2015. The Fisheries Sector in Zambia: Status, Management, and Challenges. Technical Paper No. 4. Indaba Agricultural Policy Research Institute (IAPRI). Lusaka, Zambia.
Lodge DM, Deines A, Gherardi F, Yeo DCJ, Arcella T, et al. 2012. Global introductions of crayfishes: evaluating the impact of species invasions on ecosystem services. Annual Review of Ecology, Evolution and Systematics 43: 449–472.
Marufu LT, Phiri C, Nhiwatiwa T. 2014. Invasive Australian crayfish Cherax quadricarinatus in the Sanyati Basin of Lake Kariba: a preliminary survey. African Journal of Aquatic Science 39: 233–236.
Marufu L, Dalu T, Phiri C, Nhiwatiwa T. 2017. Diet composition changes in tigerfish of Lake Kariba following an invasion by redclaw crayfish. International Journal of Limnology 53: 47–56.
Marufu LT, Dalu T, Chrispen P, Barson M, Simango R, Utete, B, Nhiwatiwa T. 2018. The diet of an invasive crayfish, Cherax quadricarinatus (Von Martens, 1868), in Lake Kariba, inferred using stomach content and stable isotope analyses. Bioinvasions Records 7: 121–132.
Mikkola H. 1996. Alien Freshwater Crustacean and Indigenous Mollusc Species with Aquaculture Potential in Eastern and Southern Africa. Southern African Journal of Aquatic Sciences 22: 90–99.
Ministry of Agriculture and Ministry of Livestock and Fisheries. 2016. Second National Agricultural Policy. Lusaka, Zambia: Government of the Republic of Zambia.
Ministry of National Development and Planning. 2017. Seventh National Development Plan 2017–2021. Lusaka, Zambia: Government of the Republic of Zambia.
Nakayama SMM, Ikenaka YI, Muzandu K, Choongo K, Oroszlany B, Teraoka H, Mizuno N, Ishizuka M. 2010. Heavy metal accumulation in lake sediments, fish (Oreochromis niloticus and Serranochromis thumbergi), and crayfish (Cherax quadricarinatus) in Lake Itezhi-tezhi and Lake Kariba, Zambia. Archives of Environmental Contamination and Toxicology 59: 291–300.
Nunes AL, Douthwaite RJ, Tyser B, Measey J, Weyl, OLF, 2016. Invasive crayfish threaten Okavango Delta. Frontiers in Ecology and the Environment 14: 237–238.
Nunes AL, Zengeya TA, Measey GJ, Weyl OLF. 2017a. Freshwater crayfish invasions in South Africa: past, present and potential future. African Journal of Aquatic Science 42: 309–323.
Nunes AL, Zengeya TA, Hoffman AC, Measey GJ, Weyl OLF. 2017b. Distribution and establishment of the alien Australian redclaw crayfish, Cherax quadricarinatus, in South Africa and Swaziland. PeerJ, 5, e3135.
Phiri S. 2009. Mansangu Fisheries Research Station Annual Report 2009. Unpublished internal report, Department of Fisheries, Chilanga.
Piers A. quoted in Ramsden N. 2014. African Lake’s multimillion dollar crayfish fishery awaits entrepreneur. https://www.undercurrentnews.com/2014/09/08/african-lakes-multimillion-dollar-crayfish-fishery-awaits-entrepreneur/ [Accessed 1 February 2018].
PMRC. 2015. Effective management of fisheries in Zambia. Policy Monitoring and Research Centre. Lusaka, Zambia. http://www.pmrczambia.com/wp-content/uploads/2017/08/Effective-Management-of-Fisheries-Research-Report.pdf [Accessed 1 February 2018].
PMRC. 2016. Analysis of the Second National Agricultural Policy 2016–2020. Policy Monitoring and Research Centre. Lusaka, Zambia. http://www.pmrczambia.com/analysis-of-the-second-national-agricultural-policy-2016–2020/ [Accessed 1 February 2018].
PSAf. 2017. Deepening Community-Based Natural Resource Management in Zambia. Lusaka, Zambia: Panos Institute Southern Africa
Ramsden N. 2014. African lake’s multimillion dollar crayfish fishery awaits entrepreneur. https://www.undercurrentnews.com/2014/09/08/african-lakes-multimillion-dollar-crayfish-fishery-awaits-entrepreneur/ [Accessed 1 February 2018].
Reed D, Scott G. 2001. Zambia. In: Reed D, Economic Change, Governance and Natural Resource Wealth. The Political Economy of Change in Southern Africa. London: Eathscan. pp 66–95.
Smart AC, Harper DM, Malaisse F, Schmitz S, Coley S, Gouder de Beauregard A-C. 2002. Feeding of the exotic Lousiana red swamp crayfish, Procamburus clarkii (Crustacea, Decapoda), in an African tropical lake: Lake Naivasha, Kenya. Hydrobiologia 488: 129–142.
Tablado Z, Tella JL, Sanchez-Zapata JA, Hiraldo F. 2010. The paradox of the long-term positive effects of a North American crayfish on a European community of predators. Conservation Biology 24: 1230–1238.
Tavakol S, Luus-Powell WJ, Smit WJ, Baker C, Hoffman A, Halajian A. 2016. First introduction of two Australian temnocephalan species into Africa with an alien host: double trouble. Journal of Parasitolology 102: 653–658.
Taylor GC, Weyl OLF, Hill JM, Peel RA, Hay CJ. 2017. Comparing the fish assemblages and food-web structures of large floodplain rivers. Freshwater Biology 62: 1891–1907.
Twardochleb LA, Olden JD, Larson ER. 2013. A global meta-analysis of the ecological impacts of non-native crayfish. Freshwater Science 32: 1367–1382.
Tyser AB. 2010. Predation by native fishes of an invasive crayfish Cherax quadricarinatus in the Kafue River, Zambia, and its wider ecosystem implications. MSc thesis, School of Biological Sciences, University of East Anglia.
Tyser AB, Douthwaite RJ. 2014. Predation on invasive redclaw crayfish Cherax quadricarinatus by native fishes in the Kafue River, Zambia. African Journal of Aquatic Science 39: 473–477.
Victoria Falls 24.com. 2013. Australian redclaw crayfish reach the Zambezi River. 1 September 2013. https://victoriafalls24.com/blog/2013/09/01/australian-redclaw-crayfish-reach-the-zambezi-river/[Accessed 30 October 2018].
Welz A. 2017. How Aquaculture Is Threatening the Native Fish Species of Africa. Yale Environment 360, Yale School of Forestry and Environment Studies. https://e360.yale.edu/features/how-aquaculture-is-threatening-the-native-fish-species-of-africa [Accessed 30 October 2018].
Manuscript received 1 March 2018, revised: 20 August 2018, accepted: 23 August 2018Associate Editor: J Simaika
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