Research Article
Print
Research Article
Ecological and potential socioeconomic impacts of two globally-invasive crayfish
expand article infoTakudzwa C. Madzivanzira§, Olaf L. F. Weyl|§, Josie South§|
‡ Rhodes University, Makhanda, South Africa
§ DSI/NRF Research Chair in Inland Fisheries and Freshwater Ecology, South African Institute for Aquatic Biodiversity (SAIAB), Makhanda, South Africa
| Centre for Invasion Biology, SAIAB, Makhanda, South Africa
¶ University of Leeds, Leeds, United Kingdom
† Deceased author
Open Access

Abstract

Quantifying the impacts of invasive species, relative to native analogues, is crucial for management and policy development. Two freshwater crayfish species of global concern, Cherax quadricarinatus and Procambarus clarkii, have established populations across Africa. Negative impacts on native biodiversity and socioeconomic impacts have been documented in other continents; however, there is a paucity of information on impacts from Africa and for C. quadricarinatus. To fill this literature gap, this study used laboratory experiments to determine potential ecological and socioeconomic impacts conferred by the crayfish species relative to a functionally similar native analogue, the river crab Potamonautes perlatus, on two static, but different resources. Consumption rates were derived for the three focal species consuming the macrophyte Potamogeton nodosus and dead Oreochromis mossambicus under different temperatures regimes (19 °C and 28 °C), representing summer and winter seasons in Southern Africa, with maximum feeding rate used to infer impact. Potamogeton represents ecologically-important nutrient cycling macrophytes, as well as crucial habitat for juvenile fish, whereas dead O. mossambicus was used as proxy for fish catches in artisanal gillnet fisheries often scavenged by crayfish. Consumption of both resources by all the decapods increased with temperature. However, the two invasive crayfish showed different impact trends where P. clarkii had a significantly higher consumption of macrophytes than the other two decapods regardless of temperature and the same trends seen, but for C. quadricarinatus scavenging on fish. Crayfish introductions clearly have potential for highly destructive ecological and socioeconomic impacts to invaded systems as compared to the native crabs. The disparity between resource use emphasises the necessity to use appropriate geographical and species-specific contexts to avoid erroneous conclusions from generalised risk assessments. Derived feeding rates can be used for rapid impact assessments and comparisons in other invasion cores.

Keywords

Cherax quadricarinatus, fishery, freshwater crabs, macrophyte, Potamonautes perlatus, Procambarus clarkii, scavenging

Introduction

Invasive alien species (IAS) are widely recognised as drivers of change; thus, impetus is on predicting, quantifying and mitigating impacts across sectors whether they be positive or negative, to provide evidence for legislators (Ricciardi et al. 2013; Blackburn et al. 2014; Tickner et al. 2020; Vimercati et al. 2020). Inland waters are disproportionately at risk of invasion due to high levels of anthropogenic disturbance and lack of inclusion in major global policy and initiatives, such as the sustainable development goals, despite contributing to numerous facets, such as alleviating poverty and hunger (Lynch et al. 2020).

Ecological impacts of IAS are comparatively well described compared to other sectors, such as social or economic impacts. Yet, there remain large geographic and taxonomic gaps which must be assessed in order to compel policy-makers to prioritise IAS management (Diagne et al. 2020). African nations and rural populations globally, rely directly upon fish products for both food and nutrition security, as well as many social, cultural and economic benefits gained from the biodiverse water resources (Chan et al. 2019; Olden et al. 2020). Without suitable predictive assessments available, environmental management recommendations are often made on the basis of family level proxies or data from other geographic regions (Hawkins et al. 2015). Lack of sufficient knowledge regarding impact prediction therein puts economic, ecological and social sectors related to inland fisheries at risk of being overlooked in future policy developments, which may further exacerbate invasion impacts.

Freshwater crayfish are amongst the most notorious and destructive IAS globally (Lodge et al. 2012; Twardochleb et al. 2013; Haubrock et al. 2021). Five species of invasive crayfish have established populations in Africa (Madzivanzira et al. 2020); this is of particular concern as crayfish are phylogenetically unique in continental Africa and are, therefore, highly novel invaders (Lodge et al. 2012; Madzivanzira et al. 2020). The two most widespread and successful species: Australian redclaw crayfish Cherax quadricarinatus (von Martens 1868) and Louisiana red swamp crayfish Procambarus clarkii (Girard 1852), are spreading at a fast rate and are invasive in several ecologically- and economically-important wetlands (Madzivanzira et al. 2020, 2021c). Despite crayfish being a model ecological species and generally being shown to have broad pervasive negative impacts on both ecology and economics (Lodge et al. 2012), there are major data deficits with regards to impacts in African systems (Madzivanzira et al. 2020) and C. quadricarinatus impacts globally (Haubrock et al. 2021).

Crayfish impacts include the reduction of basal resources i.e. aquatic macrophytes, predation on invertebrates and reduction of amphibian and fish abundance (Twardochleb et al. 2013; Madzivanzira et al. 2021a). Procambarus clarkii, in particular, has been implicated as a major driver of macrophyte reduction which can cause cascading effects on fish, bird and invertebrate abundance via direct and indirect competition for resources (both habitat and energy requirements) (Grey and Jackson 2012). Macrophyte and leaf litter breakdown is a critical step in transferring energy and nutrients from basal resources to higher trophic levels (Choi and Kim 2020). Shredding behaviour by invasive crayfish is likely to accelerate macrophyte and leaf litter breakdown (Jackson et al. 2016). Large freshwater shredders are under-represented in African systems, with freshwater crabs of the Potamonautes genus (Jackson et al. 2016) presented as the closest native trophic analogue. Potamonautid crabs are predicted to be negatively impacted as a result of crayfish invasion as functionally similar species are more likely to be competitively excluded or outcompeted (de Moor 2002; Jackson et al. 2016; Dick et al. 2017). Replacement of the native crabs by invasive crayfish will considerably alter key ecosystem services, such as fishery production and water quality (Jackson et al. 2016; Madzivanzira et al. 2021a).

Human livelihoods are also affected directly by crayfish invasions. Artisanal fishermen have reported anecdotally how crayfish affect their catches through partial consumption of fish caught on static gillnets (Weyl et al. 2017; Madzivanzira et al. 2020). This has been reported for P. clarkii from Lake Naivasha, Kenya and the Nile River, Egypt and for C. quadricarinatus in the Kafue River, Lake Kariba and Barotse floodplain, Zambia, as well as in tilapia fisheries in Mozambique (Madzivanzira et al. 2020). Partially consumed fish left in the nets are not marketable as potential buyers consider the fish to be spoilt (TCM and JS, pers. obs). Owing to the significant contribution from fisheries to livelihoods as a source of protein, income or supplementary income, as well as the wider associated value chains (Aquatic Ecosystem Services and WWF 2020), the losses associated with crayfish damage pose potential for severe and escalating costs if mitigation efforts are not undertaken. The IUCN adopted protocol for assessing ecological impact [Environmental Impact Classification for Invasive Species (EICAT)] relies upon previously documented ecological impacts (Hawkins et al. 2015). Management actions are, thus, based upon their invasion history and impacts documented elsewhere (Ricciardi et al. 2013); however, this precludes the speculative assessment of novel or potential invaders (Laverty et al. 2017). Documenting field impact can often take a prohibitively long time and many resources. Various consumption rate experiments may be carried out in the laboratory to test the broad hypothesis that invasive species incur negative effects due to more efficient resource consumption relative to a native analogue (Dickey et al. 2020). In these instances, the use of a contextually and functionally relevant analogous species is integral for generating appropriate inferences.

Therefore, we quantify resource consumption by C. quadricarinatus and P. clarkii in comparison to a native analogue, Potamonautes perlatus feeding on two static resources: 1) Long-leaved pondweed Potamogeton nodosus (Poir) and 2) dead Mozambique tilapia Oreochromis mossambicus (Peters 1852). Both resources are economically and ecologically important to fishery productivity and value. Macrophytes constitute the diet of most fishery species in African freshwater systems (e.g. Red breast tilapia Coptodon rendalli) (Weyl and Hecht 1998) and provide spawning ground and shelter for fish (Choi and Kim 2020). Consumption rates were investigated at temperatures which are representative of field conditions (19 °C and 28 °C) as temperature is a major driver of resource assimilation patterns (Uiterwaal and DeLong 2020). Based on previous studies (see Madzivanzira et al. 2021a), we hypothesise that: 1) P. perlatus feeding decreases with increasing temperature, 2) C. quadricarinatus has an equal or higher feeding rate than P. perlatus, regardless of temperature, 3) P. clarkii increases feeding with temperature, but has a lower impact than the other focal species. The study further attempts to estimate the loss in catch in the invaded regions of the Zambezi Basin.

Materials and methods

Collections of animals

Live C. quadricarinatus specimens were collected from sugarcane irrigation ponds in Nkomazi, Komatipoort in the Inkomati Basin, Mpumalanga Province (-25.5°S, 31.9°E). The recommended standard gear for trapping the C. quadricarinatus (Madzivanzira et al. 2021b) was used. The same gear was also successfully used to catch P. perlatus samples from dams in the Eastern Cape (-33.3°S, 26.5°E; -33.3°S, 26.5°E).

Live P. clarkii crayfish samples were collected from Mimosa Dam (-27.8°S, 26.6°E) in Odendalsrus, Free State Province, South Africa. In addition to the trapping method described above, rectangular traps (63.5 × 38 cm) baited with fish heads (Barkhuizen et al., accepted) were used to capture P. clarkii.

All animals caught were placed in 60 litre cooler boxes with fresh water from the source, with battery-powered air pumps and transported to a biosecure laboratory at the South African Institute for Aquatic Biodiversity (SAIAB) in Makhanda where they were acclimatised to the laboratory for at least a month prior to experimentation. Water temperature was maintained at 22 ± 1 °C and the laboratory was held under a 12:12 light:dark regime with white light and total darkness. Crayfish and crabs are omnivores (Geiger et al. 2005; Gherardi 2007; Souty-Grosset and Fetzner 2016) and, hence, all animals were maintained on cabbage leaves and cultured Eisenia sp. worms.

Prior to the experiments, all animals were acclimatised to the desired temperature at a rate of 1 °C/day and allowed to acclimatise to the two temperatures for a week before experiments were conducted. No animals were re-used per temperature treatment for both resources.

Macrophyte consumption

Potamogeton nodosus was collected from a pond in Makhanda, South Africa. Potamogeton nodosus is a heterophyllous monocotyledonous aquatic plant with both floating and submerged leaves (Ryan 1985) present in most freshwater systems in Africa (Kaplan and Symoens 2005). In the lab, plant matter was rinsed thoroughly under tap water to remove any attached macroinvertebrates. To attain a reliable biomass measurement of the macrophytes, a wet – dry conversion equation was determined by drying known mass of P. nodosus (5, 10, 15, 20, 25. 30, 35, 40, 45 and 50 g; n = 3) in an oven at 60 °C for 24 hrs (Madsen and Bloomfield 1993; Bickel and Perrett 2015). The subsequent equation was derived, where dry mass = -0.0043 + 0.1134·wet weight (Suppl. material 1a) (Bickel and Perrett 2015).

Prior to experimentation, the pondweed was patted dry with a paper towel and weighed, then an average of 45.65 ± 0.27 g (equivalent to 5.13 ± 0.03 g dry mass) was put into each experimental tank with an animal. These animals were randomly selected from the holding tanks and patted dry before morphometric measurements were taken for each individual (Table 1). The animals were acclimatised to the experimental tanks for one hour and deprived of food for 24 hrs before the pondweed was added. The experiments were run under a 12:12 light:dark regime for 24 hrs. After the experiment, the remaining macrophytes were patted dry, weighed and dried in an oven to determine the dry weight. Control experiments were run at each temperature treatment with P. nodosus, but no consumers.

Table 1.

Morphometric averages (mean ± SE) of Cherax quadricarinatus, Procambarus clarkii and Potamonautes perlatus used in the macrophyte consumption and fish scavenging experiments.

Species Experiment CL (mm) Mass (g)
Cherax quadricarinatus Macrophyte 60.01 ± 1.31 68.83 ± 2.82
Procambarus clarkii Macrophyte 56.24 ± 1.14 59.63 ± 1.22
Potamonautes perlatus Macrophyte 53.28 ± 1.16 87.72 ± 4.92
Cherax quadricarinatus Fish 63.20 ± 1.10 67.34 ± 2.52
Procambarus clarkii Fish 58.62 ± 1.53 59.54 ± 1.58
Potamonautes perlatus Fish 53.27 ± 1.02 96.29 ± 4.95

Fish consumption

Dead O. mossambicus (160.65 ± 1.26 mm, mean total length ± SE, 74.54 ± 1.59 g mean mass ± SE) were purchased from Aquaculture Innovations in Makhanda. Experimental fish were kept frozen and defrosted prior to experimentation. Oreochromis mossambicus is native to eastward flowing rivers of central and southern Africa (Skelton 2001). The fish species, together with other Oreochromis species, are commonly referred to as “breams” in the Zambezi Basin and comprise more than 50% of their catch (Tran et al. 2019). Pre-experimental treatment of animals was identical to the macrophyte experiment.

Fish were patted dry and the total length and mass for each fish was recorded. A 50 g sinker was then inserted in their guts through the mouth so that the fish sank to the bottom. The fish were then introduced to the tanks with a consumer in each tank. Controls were also run, where the dead fish were not subjected to any consumer in the experimental tank. Fishermen in the Zambezi system deploy their gillnets around 1600 hrs and retrieve them around 0600 hrs (pers. obs.). Feeding rates of the three focal species vary with light regime (Madzivanzira et al. 2021a); therefore, to mimic natural conditions these experiments were run in dark from 1600 hrs and terminated at 0700 hrs (i.e. 15 h). At the end of the experiment, crayfish were removed and placed in respective holding tanks. The remains of the fish were removed from the water and placed in a tray with blotting paper for excess water to drip out. The sinkers were removed from the fish. The fish were patted dry and the mass was recorded as well as the parts that were eaten. The parts of fish damaged by the decapods were expressed as the proportion (%) of fish with damage ‘i’ where ‘i’ is the area (mouth, eyes, abdomen, fin, gut) damaged by the predator. As it was possible that one fish had several parts damaged, a single fish could have multiple damage categories.

Data analysis

There were morphometric differences between the three species (see Suppl. material 1b), but as consumption was determined per gram of consumer this does not affect the inferences. As we used dry mass as a benchmark to gauge the accuracy of macrophyte wet mass measurements, dry mass values were used for all macrophyte associated analyses.

In order to compare consumption rates between species and allow data to be relevant to field data, with respect to trends in biomass and individual size varying with time since invasion (Madzivanzira et al. 2021c), we calculated mass of resource consumed per gram of decapod per hour (mass-1 g-1 h-1) (1):

Mass −1 · g−1 · h−1 = (Ne / Mass) / T (1)

where Ne is the dry/wet weight of resource; Mass is the mass of individual; and T is the total experimental duration.

A t-test was used determine the extent of natural loss in mass of resource before and after the experiment in the absence of a consumer for the control treatments. As resources were presented separately and dry mass of plant matter used compared to wet mass of fish, two separate generalised linear models (GLM) were used to assess resource consumption. Both GLMs used temperature and species as factors with full interaction terms. Differences between factor levels were assessed using linear contrasts and Tukey HSD.

Differences in parts of fish damaged by the consumers was analysed with 3 × 7 contingency tables and differences tested with a Chi-square test.

For both resources, the max consumption per g of predator were chosen as the most informative measure, as the respective parameters from functional response analysis are somewhat less meaningful, and this allowed for quantification of the maximum feeding rate per g of predator. The mean mass of each crayfish (Kafue River: 63.22 ± 2.05 g: Lake Kariba: 55.85 ± 1.43 g; Barotse floodplain: 37.18 ± 2.17 g) (Madzivanzira et al. 2021c) and the maximum scavenging rate per gram of C. quadricarinatus in 15 h (the number of hours gillnets are deployed) was used to estimate the potential economic losses in catch in the invaded regions of the Zambezi Basin for Kafue River, Lake Kariba and Barotse floodplain. The following equations were used to calculate the economic losses due to crayfish:

loss per day (15 hrs) = crayfish consumption (15 hrs) × crayfish mean mass (2)

monetary loss per day = loss per day × US$ 1.30 (price of fish per kg) (3)

monetary loss per year = monetary loss per day × 365 (4)

The calculations were done for the low and high temperature treatments which corresponds to the low and high water flow seasons in the invaded regions, respectively.

Results

There was no significant change in resource mass (P > 0.05) from before to after each control experiment, at either of the temperatures; therefore, all change in resource mass is attributed to consumption.

Macrophytes consumption experiment

Temperature and species interacted significantly on the consumption rate of P. nodosus (Table 2), whereby consumption of all the three species was significantly higher at 28 °C than at 19 °C (P < 0.001) (Table 3). Voracity of P. clarkii on P. nodosus was significantly higher (P < 0.05) than that for C. quadricarinatus and P. perlatus at both temperatures (Fig. 1), but there was no significant difference between C. quadricarinatus and P. perlatus (P > 0.05).

Table 2.

Model terms for all factors from GLM with a quasi-Poisson error distribution used to determine differences in macrophytes consumption and fish scavenging with regards to factors “temperature” and “species”, using a Type 3 ANOVA and χ2 to report the effects.

Model term Resource Chi-square df P-value
Temperature P. nodosus 64.64 1 < 0.001
Species P. nodosus 37.57 2 < 0.001
Temperature × Species P. nodosus 79.37 1 < 0.001
Temperature O. mossambicus 85.11 1 < 0.001
Species O. mossambicus 114.42 2 < 0.001
Temperature × Species O. mossambicus 143.18 1 < 0.001
Table 3.

Mean (±SE) consumption of macrophyte Potamogeton nodosus (in 24 hrs) and scavenging of fish Oreochromis mossambicus by Cherax quadricarinatus, Procambarus clarkii and Potamonautes perlatus at 19 °C and 28 °C.

Species Temperature (°C) Macrophyte Wet mass consumed (g) Macrophyte Dry mass consumed (g) Fish scavenged (g)
Cherax quadricarinatus 19 4.88 ± 0.62 0.55 ± 0.07 10.50 ± 0.66
Procambarus clarkii 19 7.29 ± 0.41 0.82 ± 0.05 6.92 ± 0.62
Potamonautes perlatus 19 3.59 ± 0.59 0.40 ± 0.07 7.59 ± 0.88
Cherax quadricarinatus 28 9.08 ± 0.62 1.02 ± 0.07 16.77 ± 0.66
Procambarus clarkii 28 11.48 ± 0.41 1.29 ± 0.05 12.89 ± 0.75
Potamonautes perlatus 28 7.79 ± 0.59 0.87 ± 0.07 13.89 ± 0.88
Figure 1.

Mean consumption of macrophyte (Potamogeton nodosus) per hour per gram of Cherax quadricarinatus, Procambarus clarkii and Potamonautes perlatus at 19 °C and 28 °C. Points indicate raw data values, boxplots indicate ± Standard Error and solid line across the box represents the mean.

Fish scavenging experiment

There was a significant interaction between species and temperature on consumption of O. mossambicus (Table 2), whereby increased temperature significantly increased consumption of all three species (P < 0.001). Voracity of C. quadricarinatus was significantly higher (all P < 0.05) than that for P. clarkii and P. perlatus at either temperature (Fig. 2), but there was no difference between P. clarkii and P. perlatus voracity (P > 0.05).

Figure 2.

Mean consumption of fish (Oreochromis mossambicus) per hour per gram of Cherax quadricarinatus, Procambarus clarkii and Potamonautes perlatus at 19 °C and 28 °C. Points indicate raw data values, boxplots indicate ± Standard Error and solid line across the box represents the mean.

All three decapods caused aesthetic damage to the fish through consumption (See Suppl. material 2). Each scavenger caused significantly different damage to different areas of O. mossambicus2 = 152.68, df = 12, P < 0.001). The two crayfish species mostly damaged the tail, abdomen and the fins (proportion > 80%), whilst P. perlatus only targeted the head (proportion = 100%) (Table 4).

Table 4.

Proportion of fish with different categories of damage i.

Species Temperature (°C) Tail Abdomen Fin Guts Mouth Head Eyes
Cherax quadricarinatus 19 20 19 19 0 0 0 1
Procambarus clarkii 19 20 20 20 1 0 0 0
Potamonautes perlatus 19 1 4 0 0 20 20 20
Cherax quadricarinatus 28 20 17 17 3 4 0 1
Procambarus clarkii 28 20 20 20 1 0 0 0
Potamonautes perlatus 28 0 4 0 1 20 20 20

Potential economic losses

The potential loss in catch due to crayfish scavenging in the invasion cores per fishing night per individual crayfish ranges between: $0.01 – $0.02; $0.01 – $0.02; and $0.01 – $0.01 (Suppl. material 1). This translates to an average annual loss of $6.15; $5.42; and $3.62 per crayfish for Kafue River, Lake Kariba and Barotse floodplain, respectively (Suppl. material 1).

Discussion

High consumption of native resources, relative to that of a native analogue, is regarded as indicative of high impact IAS according to the Resource Consumption Hypothesis (Ricciardi et al. 2013; Paterson et al. 2015; Dick et al. 2017; Laverty et al. 2017). Understanding these impacts on specific ecosystem services is necessary, not only for the regulation and management of these IAS, but also to guard against detriment to human well-being, especially important in areas where food security and water resources are already precarious (Egoh et al. 2020). Here, we compare temperature- and resource-specific feeding rates by invasive crayfish and a native freshwater crab to infer ecological and potential economic impacts on fisheries. We found that consumption of static resources increases with temperature regardless of species or resource and rejected Hypothesis 1. Hypotheses 2 and 3 were also partially rejected due to species specific differences in consumption. Cherax quadricarinatus had a higher impact on dead fish regardless of temperature than the other two species (2) and the same trend was seen in the macrophyte experiment, but in this case, P. clarkii was the most damaging regardless of temperature, thus emphasising the importance of context specific impact assessments to avoid the ambiguity which arises when generalising impacts across families in the absence of species specific evidence per EICAT recommendations (Hawkins et al. 2015). The results also provide maximum feeding rates for the three decapods under two temperature treatments which can be used along with fisheries data in the future to derive potential for economic loss as well as parameterising models.

The temperature treatments in this study directly reflect the conditions in invaded African systems; however, these data can be used globally to gauge temperature-dependent impacts in other areas. Global annual mean temperatures are projected to increase by 1.5 °C between 2030 and 2052 (IPCC 2018). Thus impact of crayfish species will likely increase with the projected climatic changes, as demonstrated in this study. However, the mechanisms and outcomes of ecological impact differ depending on the crayfish species, resource type as well as native analogue dynamics as illustrated by the change in impact patterns between the present study and Madzivanzira et al. (2021a).

All species consumed P. nodosus and increased consumption with increasing temperature in line with the metabolic theory of ecology (Brown et al. 2004; Uiterwaal and DeLong 2020). Impact of C. quadricarinatus on macrophytes did not differ from that of P. perlatus, but P. clarkii showed potential for adverse ecological impacts as intense herbivory can have cascading effects across different trophic levels (Marshall 2019). The destruction of macrophytes can also modify nutrient cycling, as a result of removing the stabilising effect of macrophytes upon littoral sediments (Gherardi et al. 2011). Procambarus clarkii is well known for high consumption of macrophytes on a global scale (Lodge et al. 2012; Twardochleb et al. 2013; Madzivanzira et al. 2020) and exhibits a preference for plant matter over animal protein (Gherardi and Barbaresi 2007). In Lake Naivasha, the introduction of P. clarkii coincided with notable declines in the water lily Nymphaea nouchalii var. caerulea suggesting consumptive impacts on this macrophyte (Lowery and Mendes 1977). This high preference for macrophytes by P. clarkii explains the difference between the comparatively low impact on juvenile fish prey in Madzivanzira et al. (2021a) and the high impact in the macrophyte experiment of the present study. The high consumption of macrophytes by P. clarkii could be related to feeding and processing morphology as P. clarkii has thin chelae and a low closing force (South et al. 2020) and a gastric mill which may specialise them for processing plant matter over other resources (Chisaka and Kozawa 2003; McGaw and Curtis 2013). Cherax quadricarinatus is an emerging invader with few recorded impacts (Haubrock et al. 2021). However, introductions into the Pilbara Region of Australia resulted in the complete loss of macrophyte cover and subsequent community reorganisation (Pinder et al. 2019) and, in Lake Kariba, Zimbabwe, macrophytes dominated the diet of C. quadricarinatus across size ranges (Marufu et al. 2018).

All three species showed propensity for scavenging behaviour on dead fish, corroborating the anecdotal accounts of crayfish destruction of fisher catch (Weyl et al. 2017; Madzivanzira et al. 2020). Cherax quadricarinatus consumption was more pronounced in the fish scavenging experiment, to the extent that consumption at the lowest temperature was still higher than that of P. perlatus at the highest temperature. The results are similar to Madzivanzira et al. (2021a) in that C. quadricarinatus had the highest impact on fish resources; however, P. perlatus did not suffer from a reduction in per capita consumption with increased temperature in the present study. This suggests that the results in Madzivanzira et al. (2021a) are likely due to a temperature driven mismatch in attack and escape speeds of P. perlatus and Clarias gariepinus, rather than the physiological performance of P. perlatus under high temperature. In contrast, P. clarkii had similar scavenging rates to P. perlatus, indicating a possible lack of impact on fish catch. However, aesthetic damage to catch often translates to economic loss regardless of extent. The two crayfish species damaged mostly the posterior parts of the fish, whilst the crabs damaged mostly the anterior parts. The fish head, preferentially damaged by the crabs, contains higher nutrient content compared to other body parts of the fish (Petricorena 2014). The higher closing force of crab chela compared to the two crayfish species may facilitate access to the anterior parts (head) of the fish which are tougher compared to the soft parts (abdomen and guts) which were more likely to be damaged by the crayfish species (South et al. 2020).

Both resource types investigated here have direct and indirect economic implications besides the ecological ramifications of generalist omnivores on aquatic communities. Healthy and high integrity macrophyte stands provide crucial fish nursery habitat and indirectly support fishery productivity and resilience (Choi and Kim 2020). The loss of macrophyte beds in Kenya due to P. clarkii invasion reduced food resources for a variety of African wetland birds (Taylor and Harper 1988; Harper et al. 2002) which indirectly negatively affects ornithological tourism (Gherardi et al. 2011). Inland fisheries provide livelihoods and ecosystem services for millions of people globally (Lynch et al. 2020). African artisanal fisheries suffer from pressures similar to most capture fisheries worldwide, for example, overexploitation, unemployment and rapid population growth (Tweddle et al. 2015). Fish products form part of a larger value chain commercially and when crayfish cause a percentage of the catch to be unmarketable as a result of scavenging, targets are not met and the impacts cascade to the public, making the situation a food security cause for concern. The impact is aggrandised by low overall fish catches as crayfish entangle themselves in the gillnets, thereby reducing the efficiency of these gillnets (Weyl et al. 2017) and, further, as fishers must then increase their fishing effort to compensate for the lost catch. These dynamics might not be isolated to African systems alone (see Madzivanzira et al. 2020) and should not be underestimated. In Europe, crayfish have been shown to cause serious damage to carp rigs by clawing and nipping at the line and scavenging on bait for catching fish (see https://carp-fishing-reels.com/blog/general-advice/combatting-crayfish/). The artisanal fishery is likely to be further threatened by low catches as the crayfish species were shown to be able to consume a high number of catfish fry (Madzivanzira et al. 2021a) which could affect recruitment, productivity/yield and hence human livelihoods.

This study also estimated the potential monetary losses fishermen are likely to experience due to catch spoilage by crayfish in the invaded regions of the Zambezi Basin. The study showed high potential economic impacts in older invasions (Kafue and Lake Kariba). The potential losses in catch and income shown in this study could be even greater in the field, because the mass consumed in the lab was used to up-calculate the overall mass lost due to crayfish spoilage. This overall mass may under-represent the spoiled catch as when crayfish consume a small amount/part of the fish in the field, the whole fish is regarded as spoiled. Over- and underestimation of the losses can result in several assumptions such as that crayfish feed only on fish caught in the gillnets (overestimation in this case), not considering that small amounts consumed ruin the entire fish for sale (underestimation) and not considering fishing bans (overestimation). While this study gives a snapshot of the potential losses due to crayfish invasions, field surveys and further investigations are more appropriate to calculate the realistic losses in catch and income.

Incorporating context-specific comparisons with an ecologically relevant native trophic analogue is essential to determine the relative difference in resource consumption (Dick et al. 2017). The results of the present study show that, on a 1:1 (g) basis, the impact of both invasive crayfish is comparable to P. perlatus which seems to more provide evidence for possible biotic resistance (see South et al. 2020). Nonetheless, freshwater crabs, while ubiquitous across the continent, are relatively low in abundance and suffer from large data deficits in basic ecology which can confound comparative inferences (Madzivanzira et al. 2020; South et al. unpublished data). The invasion by crayfish species can lead to more diverse impacts and threaten resources that were not previously threatened by the crabs alone. We stress the need to combine laboratory data, such as the present study and Madzivanzira et al. (2021a) with contextually relevant field abundance patterns to improve prediction of impact magnitude (Dick et al. 2017; Zeng et al. 2019; Dickey et al. 2020). It is, thus, likely that the actual field impact of crayfish invasions is exacerbated by extreme differences in relative abundance between trophic analogues (South et al. 2020; Madzivanzira et al. 2021c, South et al. unpublished data). The derivation of temperature-specific per gram maximum feeding estimate for global invaders can facilitate rapid assessments and comparisons from other invasion cores which ultimately will assist in hypothesis testing and impact prediction.

Crayfish invasions have high negative implications for ecology and socio-economic dynamics of the recipient area. Intersectional adverse impacts are likely to persist and escalate, especially considering the low level of conservation management resources available (Madzivanzira et al. 2020). The pressing issue of unhindered crayfish invasions, especially in Africa, needs to be prioritised as the food security of livelihoods in invaded regions will be affected. There is need to investigate whether results from this study translate to the actual declines in catches through fish catch assessments and value chain analysis, while considering field abundance patterns. However, this relies upon interdisciplinary collaboration to compile the relevant information for robust assessment.

Data availability statement

The raw data generated and used in the analysis, as well as the data that supports the use of the temperature treatments, are publicly available at: https://doi.org/10.6084/m9.figshare.15019593.v2.

Acknowledgements

This article is dedicated to Prof. Olaf LF Weyl, who passed away suddenly on 14 November 2020. We miss him, his advice and his friendship dearly.

This study forms part of a PhD research project supported by the National Research Foundation (NRF)—South African Research Chairs Initiative of the Department of Science and Innovation (DSI) (Inland Fisheries and Freshwater Ecology, Grant No. 110507) and the NRF Extension Support Doctoral Scholarship. We acknowledge use of infrastructure and equipment provided by the NRF-SAIAB Research Platform and the funding channelled through the NRF-SAIAB Institutional Support system. JS acknowledges funding from the DSI-NRF Centre of Excellence for Invasion Biology (CIB). We are grateful to the Department of Environmental Affairs (DEA) for issuing us with permits to sample, transport and keep a maximum 150 of each of the crayfish species (Permit Numbers: 50869181001115242, 50869181001120608 for C. quadricarinatus and 50869181001113030, 50869181002121045 for P. clarkii) and the Eastern Cape Department of Economic Development, Environmental Affairs and Tourism for issuing permits to sample crabs (Permit numbers: CRO 19/18CR and CRO 190 21/18CR). We are also grateful to Andre Hoffman from Mpumalanga Parks and Tourism Agency (MTPA) and Dr. Leon Barkhuizen from the Free State Department of Economic, Small Business Development, Tourism and Environmental Affairs (FS DESTEA) for assisting with the collection of redclaw and red swamp crayfish, respectively. This research was given ethics clearance by the Animal Ethics Subcommittee, Rhodes University (Ethics No. DIFS2718) and SAIAB Ethics Committee (#25/4/1/7/5_2018_06). Any opinion, finding and conclusion or recommendation expressed in this material is that of the authors. The NRF of South Africa does not accept any liability in this regard.

References

  • Barkhuizen LM, Madzivanzira TC, South J (accepted) Population ecology of a wild population of red swamp crayfish Procambarus clarkii (Girard, 1852) in the Free State Province, South Africa and implications for eradication efforts. BioInvasion Records
  • Bickel TO, Perrett C (2015) Precise determination of aquatic plant wet mass using a salad spinner. Canadian Journal of Fisheries and Aquatic Sciences 73: 1–4. https://doi.org/10.1139/cjfas-2015-0274
  • Blackburn TM, Essl F, Evans T, Hulme PE, Jeschke JM, Kühn I, Kumschick S, Marková Z, Mrugała A, Nentwig W, Pergl J, Pyšek P, Rabitsch W, Ricciardi A, Richardson DM, Sendek A, Vilá M, Wilson JRU, Winter M, Genovesi P, Bacher S (2014) A Unified classification of alien species based on the magnitude of their environmental impacts. PLOS Biology 12(5): e1001850. https://doi.org/10.1371/journal.pbio.1001850
  • Brown JH, Gillooly JF, Allen AP, Savage VM, West GB (2004) Toward a metabolic theory of ecology. Ecology 85: 1771–1789. https://doi.org/10.1890/03-9000
  • Chan CY, Tran N, Pethiyagoda S, Crissman CC, Sulser TB, Phillips MJ (2019) Prospects and challenges of fish for food security in Africa. Global Food Security 20: 17–25. https://doi.org/10.1016/j.gfs.2018.12.002
  • Chisaka H, Kozawa Y (2003) Fine structure and mineralization of the gastric mill in the crayfish Procambarus clarkii during intermolt stage. Journal of Crustacean Biology 23(2): 371–379. https://doi.org/10.1163/20021975-99990347
  • Choi J-Y, Kim S-K (2020) Effects of aquatic macrophytes on spatial distribution and feeding habits of exotic fish species Lepomis macrochirus and Micropterus salmoides in shallow reservoirs in South Korea. Sustainability 12(4): 1–14. https://doi.org/10.3390/su12041447
  • Diagne C, Leroy B, Gozlan RE, Vaissière A-C, Assailly C, Nuninger L, Roiz D, Jourdain F, Jarić I, Courchamp F (2020) InvaCost, a public database of the economic costs of biological invasions worldwide. Scientific Data 7: 277. https://doi.org/10.1038/s41597-020-00586-z
  • Dick JTA, Laverty C, Lennon JJ, Barrios-O’Neill D, Mensink PJ, Britton JR, Médoc V, Boets P, Alexander MA, Taylor NG, Dunn AM, Hatcher MJ, Rosewarne PJ, Crookes S, MacIsaac HJ, Xu M, Ricciardi A, Wasserman RJ, Ellender BR, Weyl OLF, Lucy FE, Banks PB, Dodd JA, MacNeil C, Penk MR, Aldridge DC, Caffrey JM (2017) Invader Relative Impact Potential: A new metric to understand and predict the ecological impacts of existing, emerging and future invasive alien species. Journal of Applied Ecology 54: 1259–1267. https://doi.org/10.1111/1365-2664.12849
  • Dickey JWE, Cuthbert RN, South J, Britton JR, Caffrey J, Chang X, Crane K, Coughlan NE, Fadaei E, Farnsworth KD, Ismar-Rebitz SMH, Joyce PWS, Julius M, Laverty C, Lucy FE, MacIsaac HJ, McCard M, McGlade CLO, Reid N, Ricciardi A, Wasserman RJ, Weyl OLF, Dick JTA (2020) On the RIP: using Relative Impact Potential to assess the ecological impacts of invasive alien species. NeoBiota 55: 27–60. https://doi.org/10.3897/neobiota.55.49547
  • Egoh BN, Ntshotsho P, Maoela MA, Blanchard R, Ayompe LM, Rahlao S (2020) Setting the scene for achievable post-2020 convention on biological diversity targets: A review of the impacts of invasive alien species on ecosystem services in Africa. Journal of Environmental Management 261: 110171. https://doi.org/10.1016/j.jenvman.2020.110171
  • Geiger W, Alcorlo P, Baltanás A, Montes C (2005) Impact of an introduced crustacean on the trophic webs of Mediterranean wetlands. Biological Invasions 7: 49–73. https://doi.org/10.1007/s10530-004-9635-8
  • Gherardi F (2007) Understanding the impact of invasive crayfish. In: Gherardi F (Ed.) Biological invaders in inland waters: profiles, distribution, and threats. Springer, Dordrecht, 507–542. https://doi.org/10.1007/978-1-4020-6029-8
  • Gherardi F, Barbaresi S (2007) Feeding preferences of the invasive crayfish, Procambarus clarkii. Bulletin Français de la Pêche et de la Pisciculture 385: 07–20. https://doi.org/10.1051/kmae:2007014
  • Gherardi F, Britton JR, Mavuti KM, Pacini N, Grey J, Tricarico E, Harper DM (2011) A review of allodiversity in Lake Naivasha, Kenya: Developing conservation actions to protect East African lakes from the negative impacts of alien species. Biological Conservation 144: 2585–2596. https://doi.org/10.1016/j.biocon.2011.07.020
  • Haubrock PJ, Oficialdegui FJ, Zeng Y, Patoka J, Yeo DCJ, Kouba A (2021) The redclaw crayfish: A prominent aquaculture species with invasive potential in tropical and subtropical biodiversity hotspots. Reviews in Aquaculture 13(3): 1488–1530. https://doi.org/10.1111/raq.12531
  • Harper DM, Harper MM, Virani MA, Smart A, Childress RB, Adatia R, Henderson I, Chege B (2002) Population fluctuations and their causes in the African Fish Eagle (Haliaeetus vocifer (Daudin) at Lake Naivasha, Kenya. Hydrobiologia 488: 171–180. https://doi.org/10.1023/A:1023390800872
  • Hawkins CL, Bacher S, Essl F, Hulme PE, Jeschke JM, Kühn I, Kumschick S, Nentwig W, Pergl J, Pyšek P, Rabitsch W, Richardson DM, Vilà M, Wilson JRU, Genovesi P, Blackburn TM (2015) Framework and guidelines for implementing the proposed IUCN Environmental Impact Classification for Alien Taxa (EICAT). Diversity and Distributions 21: 1360–1363. https://doi.org/10.1111/ddi.12379
  • IPCC (2018) Summary for Policymakers. In: Masson-Delmotte V, Zhai P, Pörtner H-O, Roberts D, Skea J, Shukla PR, Pirani A, Moufouma-Okia W, Péan C, Pidcock R, Connors S, Matthews JBR, Chen Y, Zhou X, Gomis MI, Lonnoy E, Maycock T, Tignor M, Waterfield T (Eds) Global Warming of 1.5 °C. An IPCC Special Report on the impacts of global warming of 1.5 °C above pre-industrial levels and related global greenhouse gas emission pathways, in the context of strengthening the global response to the threat of climate change, sustainable development, and efforts to eradicate poverty. World Meteorological Organization, Geneva.
  • Jackson MC, Gryy J, Miller K, Britton JR, Donohue I (2016) Dietary niche constriction when invaders meet natives: evidence from freshwater decapods. Journal of Animal Ecology 85: 1098–1107. https://doi.org/10.1111/1365-2656.12533
  • Kaplan Z, Symoens JJ (2005) Taxonomy, distribution and nomenclature of three confused broad-leaved Potamogeton species occurring in Africa and on surrounding islands. Botanical Journal of the Linnean Society 148: 329–357. https://doi.org/10.1111/j.1095-8339.2005.00410.x
  • Laverty C, Green KD, Dick JTA, Barrios-O’Neill D, Mensink PJ, Médoc V, Spataro T, Caffrey JM, Lucy FE, Boets P, Britton JR, Pegg J, Gallagher C (2017) Assessing the ecological impacts of invasive species based on their functional responses and abundances. Biological Invasions 19: 1653–1665. https://doi.org/10.1007/s10530-017-1378-4
  • Lodge DM, Deines A, Gherardi F, Yeo DCJ, Arcella T, Baldridge AK, Barnes MA, Chadderton WL, Feder JL, Gantz CA, Howard GW, Jerde CL, Peters BW, Peters JA, Sargent LW, Turner CR, Wittmann ME, Zeng Y (2012) Global introductions of crayfishes: Evaluating the impact of species invasions on ecosystem services. Annual Review of Ecology, Evolution and Systematics 43: 449–472. https://doi.org/10.1146/annurev-ecolsys-111511-103919
  • Lynch AJ, Elliott V, Phang SC, Claussen JE, Harrison I, Murchie KJ, Steel EA, Stokes GL (2020) Inland fish and fisheries integral to achieving the Sustainable Development Goals. Nature Sustainability 3: 579–587. https://doi.org/10.1038/s41893-020-0517-6
  • Madzivanzira TC, South J, Wood LE, Nunes AL, Weyl OLF (2020) A review of freshwater crayfish introductions in continental Africa. Reviews in Fisheries Science & Aquaculture 29(2): 218–241. https://doi.org/10.1080/23308249.2020.1802405
  • Madzivanzira TC, South J, Weyl OLF (2021a) Invasive crayfish outperform Potamonautid crabs at higher temperatures. Freshwater Biology 66(5): 978–991. https://doi.org/10.1111/fwb.13691
  • Madzivanzira TC, South J, Nhiwatiwa T, Weyl OLF (2021b) Standardisation of Australian redclaw crayfish Cherax quadricarinatus sampling gear in southern Africa. Water SA 47(3): 380–384. https://doi.org/10.17159/wsa/2021.v47.i3.11866
  • Madzivanzira TC, South J, Ellender BR, Chalmers R, Chisule G, Coppinger CR, Khaebeb HF, Jacobs FJ, Chomba M, Musando B, Mwale C, Nhiwatiwa T, Rennie CL, Richardson N, Weyl OLF (2021c) Distribution and establishment of the alien Australian redclaw crayfish, Cherax quadricarinatus, in the Zambezi Basin. Aquatic Conservation: Marine and Freshwater Ecosystems 31(11): 3156–3168. https://doi.org/10.1002/aqc.3703
  • Marufu L, Dalu T, Phiri C, 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(2): 121–132. https://doi.org/10.3391/bir.2018.7.2.03
  • Olden JD, Vitule JRS, Cucherousset J, Kennard MJ (2020) There’s more to fish than just food: Exploring the diverse ways that fish contribute to human society. Fisheries 45(9): 453–464. https://doi.org/10.1002/fsh.10443
  • Paterson RA, Dick JT, Pritchard DW, Ennis M, Hatcher MJ, Dunn AM (2015) Predicting invasive species impacts: a community module functional response approach reveals context dependencies. Journal of Animal Ecology 84(2): 453–463. https://doi.org/10.1111/1365-2656.12292
  • Pinder A, Harman A, Bird C, Quinlan K, Angel F, Cowan M, Lewis L, Thillainath E (2019) Spread of the nonnative redclaw crayfish Cherax quadricarinatus (von Martens, 1868) into natural waters of the Pilbara Region of Western Australia, with observations on potential adverse ecological effects. BioInvasions Records 8(4): 882–897. https://doi.org/10.3391/bir.2019.8.4.17
  • Ricciardi A, Hoopes MF, Marchetti MP, Lockwood JL (2013) Progress toward understanding the ecological impacts of non-native species. Ecological Monographs 83: 263–282. https://doi.org/10.1890/13-0183.1
  • Ryan FJ (1985) Isolation and characterization of photosynthetically active cells from submersed and floating leaves of the aquatic macrophyte Potamogeton nodosus Poir. Plant Cell Physiology 26: 309–315.
  • Skelton P (2001) A Complete Guide to the Freshwater Fishes of Southern Africa, Struik Publishers. [ISBN: 1 86872 643 6]
  • South J, Madzivanzira TC, Tshali N, Measey J, Weyl OLF (2020) In a pinch: mechanisms behind potential biotic resistance toward two invasive crayfish by native African freshwater crabs. Frontiers in Ecology and Evolution 8: e72. https://doi.org/10.3389/fevo.2020.00072
  • Souty-Grosset C, Fetzner JW (2016) Taxonomy and identification. In: Longshaw M, Stebbing P (Eds) Biology and ecology of crayfish. CRC Press, Boca Raton, FL, 1–30. https://doi.org/10.1201/b20073-2
  • Tickner D, Opperman JJ, Abell R, Acreman M, Arthington AH, Bunn SE, Cooke SJ, Dalton J, Darwall W, Edwards G, Harrison I, Hughes K, Jones T, Leclère D, Lynch AJ, Leonard P, McClain ME, Muruven D, Olden JD, Ormerod SJ, Robinson J, Tharme RE, Thieme M, Tockner K, Wright M, Young L (2020) Bending the curve of global freshwater biodiversity loss: An emergency recovery plan, BioScience 70(4): 330–342. https://doi.org/10.1093/biosci/biaa002
  • Tran N, Chu L, Chan CY, Genschick S, Phillips MJ, Kefi AS (2019) Fish supply and demand for food security in Sub-Saharan Africa: An analysis of the Zambian fish sector. Marine Policy 99: 343–350. https://doi.org/10.1016/j.marpol.2018.11.009
  • Twardochleb LA, Olden JD, Larson ER (2013) A global meta-analysis of the ecological impacts of non-native crayfish. Freshwater Science 32(4): 1367–1382.
  • Tweddle D, Cowx IG, Weyl OLF (2015) Challenges in fisheries management in the Zambezi, one of the great rivers of Africa. Fisheries Management and Ecology 22: 99–111. https://doi.org/10.1111/fme.12107
  • Vimercati G, Kumschick S, Probert AF, Volery L, Bacher S (2020) The importance of assessing positive and beneficial impacts of alien species. In: Wilson JR, Bacher S, Daehler CC, Groom QJ, Kumschick S, Lockwood JL, Robinson TB, Zengeya TA, Richardson DM (Eds) . NeoBiota 62: 525–545. https://doi.org/10.3897/neobiota.62.52793
  • Weyl OLF, Nunes AL, Ellender BR, Weyl PSR, Chilala AC, Jacobs FG, Murray-Hudson M, Douthwaite RJ (2017) Why suggesting Australian redclaw crayfish Cherax quadricarinatus as biological control agents for snails is a bad idea, African Journal of Aquatic Science 42(4): 325–327. https://doi.org/10.2989/16085914.2017.1414685
  • Zeng Y, Shakir KK, Yeo DCJ (2019) Competition between a native freshwater crab and an invasive crayfish in tropical Southeast Asia. Biological Invasions 21: 2653–2663. https://doi.org/10.1007/s10530-019-02009-6

Supplementary materials

Supplementary material 1 

Macrophyte dry weight determination and morphometric averages (± SE) of used animals

Takudzwa C. Madzivanzira, Olaf L.F. Weyl, Josie South

Data type: regression analysis and morphometric measurements

Explanation note: The supplementary file shows the graph that was used for the wet – dry macrophyte weight conversion. The file also shows the mean mophometric measurements of the decapods and reports the statistics to determine their differences.

This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited.
Download file (192.75 kb)
Supplementary material 2 

Field and laboratory photos showing crayfish damage

Takudzwa C. Madzivanzira, Olaf L.F. Weyl, Josie South

Data type: images

Explanation note: Supplentary file 2 shows photos of field and lab-based evidence of crayfish impacts on the artisanal fishery as reported in Southern Africa.

This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited.
Download file (820.08 kb)