BioInvasions Records (2019) Volume 8, Issue 4: 882–897

CORRECTED PROOF

Research Article Spread of the non-native redclaw quadricarinatus (von Martens, 1868) into natural waters of the region of Western , with observations on potential adverse ecological effects

Adrian Pinder1, Adam Harman2,*, Chris Bird3, Kirsty Quinlan1, Fintan Angel2, Mark Cowan1, Loretta Lewis1 and Emma Thillainath2 1Department of Biodiversity, Conservation and Attractions, 17 Dick Perry Avenue, Kensington, 6151, 2Wetland Research and Management, 16 Claude St, Burswood, 6100, Western Australia 3Department of Primary Industries and Regional Development, Aquatic Pest Biosecurity, 39 Northside Drive, Hillarys, 6025, Western Australia Author e-mails: [email protected] (AP), [email protected] (AH), [email protected] (CB), [email protected] (KQ), [email protected] (FA), [email protected] (MC), [email protected] (LL), [email protected] (ET) *Corresponding author

Citation: Pinder A, Harman A, Bird C, Quinlan K, Angel F, Cowan M, Lewis L, Abstract Thillainath E (2019) Spread of the non- native redclaw crayfish Cherax The redclaw crayfish, (von Martens, 1868), inhabits quadricarinatus (von Martens, 1868) into freshwater creeks and water bodies, and is native to the tropics of and natural waters of the Pilbara region of the in Australia, as well as south-eastern . It Western Australia, with observations on has been translocated to other parts of Australia and around the world, often potential adverse ecological effects. BioInvasions Records 8(4): 882–897, becoming established in the wild and potentially having negative impacts in invaded https://doi.org/10.3391/bir.2019.8.4.17 ecosystems. In north-western Australia, which lacks native crayfish, this species is known from the system in the Kimberley Region and from a water supply Received: 22 November 2018 reservoir, Harding Dam, in the Pilbara region. Following a report of their presence Accepted: 19 June 2019 in another area of the Pilbara region, Karijini National Park, a rapid assessment of Published: 11 September 2019 crayfish occurrence was undertaken in and around Karijini and Millstream-Chichester Handling editor: Ana Luisa Nunes National Parks. Redclaw crayfish were found at the known site within Karijini Thematic editor: David Wong National Park and at a river pool west of the park. They were also detected in George Copyright: © Pinder et al. River within Millstream-Chichester National Park. A separate baseline aquatic fauna This is an open access article distributed under terms survey, undertaken later as part of a mining environmental impact assessment, also of the Creative Commons Attribution License recorded populations of the species in a tributary of the , located (Attribution 4.0 International - CC BY 4.0). between these parks. The survey suggests that redclaw presence is associated with OPEN ACCESS. significant reorganisation of faunal and floral assemblages of river pools. With the new records presented here, the redclaw crayfish is now known from four catchments in the Pilbara Region, spread across three of the region’s five drainage basins. Management options for this alien species are limited in this remote area, but would require further surveys to better understand their current distribution and dispersion capability, setting up public education campaigns and targeted control measures to minimise their spread to new catchments and their impact on high conservation value aquatic ecosystems.

Key words: freshwater, non-native species, rivers, arid-zone, ecological impacts, translocation

Introduction A variety of freshwater crayfish have been moved around the world by humans, largely for aquaculture and the aquarium trade, and many have

Pinder et al. (2019), BioInvasions Records 8(4): 882–897, https://doi.org/10.3391/bir.2019.8.4.17 882 Spread of redclaw crayfish into Pilbara natural waters

subsequently established wild populations (Hobbs et al. 1989; Bortolini et al. 2007; Azofeifa-Solano et al. 2017; Chucholl and Wendler 2017; Nunes et al. 2017a). Non-native crayfish have a range of effects on aquatic ecosystems, including changes to aquatic habitats such as sediment composition, bank stability and macrophyte abundance (Chambers et al. 1990; Nystrom 1999; Gherardi et al. 2011; Twardochleb et al. 2013; Albertson and Daniels 2016). These impacts, plus biological interactions such as predation and competition, and the co-introduction of parasites (Volonterio 2009; Du Preez and Smit 2013; Strand et al. 2019), have cascading effects on other invertebrate and vertebrate fauna, including local crayfish fisheries (Lodge et al. 1998; Twardochleb et al. 2013). The redclaw crayfish, Cherax quadricarinatus (von Martens, 1868), is native to northerly and westerly flowing rivers of tropical Queensland, northerly and easterly flowing rivers of the Northern Territory and the southerly flowing rivers of Papua New Guinea (Austin et al. 2010). Translocated to various parts of the globe for aquaculture and the aquarium trade, the species has established wild populations in several locations, with scant information on its ecological impact being available (Ahyong and Yeo 2007; Snovsky and Galil 2011; Du Preez and Smit 2013; Azofeifa-Solano et al. 2017). In Australia, there are non-native populations along the East coast (Coughran and Leckie 2007; Leland et al. 2012), in the inland Eyre Basin (Lake Eyre Basin Ministerial Forum 2017), in the Flora-Katherine- Daly River system in the Northern Territory (Doupe 2007), and in the East Kimberley region (Lake Kununurra, Ord River) of far northern Western Australia (Doupé et al. 2004). In Western Australia’s Pilbara region (inset Figure 1), which lacks native crayfish, a population of redclaw crayfish has been established in a reservoir on the since at least 2013 (unpublished record from trapping undertaken by the Western Australia Department of Primary Industries and Regional Development following observation of carapaces on shore). In March 2016, another population was detected for the first time in Hamersley Gorge (in a small tributary of the Fortescue River) in Karijini National Park, about 170 km south-east of Harding Dam (Figure 1). This population, discovered during a routine aquatic fauna survey by two of the authors (FA, ET), represents a large range extension of the species in this remote arid region, and the first record for the region in a natural aquatic system. Beatty et al. (2019) suggest that reservoirs such as Harding Dam may act as sources or primary stepping stones for the subsequent spread of freshwater crayfish into natural waterways. Following this discovery, a rapid assessment of the spatial distribution of redclaw in the region’s national parks was undertaken. Additional information on the species’ distribution was obtained from a baseline aquatic fauna survey of river pools along Weelumurra Creek, a tributary of the Lower Fortescue River. This paper presents the results of these two surveys.

Pinder et al. (2019), BioInvasions Records 8(4): 882–897, https://doi.org/10.3391/bir.2019.8.4.17 883 Spread of redclaw crayfish into Pilbara natural waters

Figure 1. Location of numbered sampling sites for the 2016 rapid assessment survey (with and without redclaw). The locations of Harding Dam (where the species was first introduced in the region) and of Ophthalmia Dam (where a population has been recently detected, see Discusson) are also shown. Inset map shows the location of the Pilbara region in north-western Australia.

Materials and methods Study area The Pilbara is a hot and arid region in north-western Australia (Figure 1), with annual average rainfall of 250 to 350 mm and annual rainfall deficits between 2.3 and 3.2 m (McFarlane 2015). The region is traversed by numerous rivers with large catchments that flow only intermittently following large rainfall events and which have many isolated pools, many of them permanent and maintained by groundwater (Pinder et al. 2010). The area’s largest conservation reserves are Karijini and Millstream- Chichester National Parks (Figure 1), located in the Hamersley and Chichester Ranges, respectively. Apart from intermittently flowing rivers, Karijini has springs and numerous deep gorges with permanent pools in its northern extent. Millstream-Chichester also has numerous springs and permanent river pools, most notably along the Fortescue River as it passes through the south-west corner of the park. Pilbara environments are described in detail by McKenzie et al. (2010).

Rapid assessment survey Following the discovery of redclaw crayfish in Hamersley Gorge in Karijini National Park in March 2016, a survey that aimed to determine the

Pinder et al. (2019), BioInvasions Records 8(4): 882–897, https://doi.org/10.3391/bir.2019.8.4.17 884 Spread of redclaw crayfish into Pilbara natural waters

occurrence of redclaw in and around this park and Millstream-Chichester National Park (Figure 1) was undertaken in July 2016. This was a rapid assessment to determine how widely redclaw had been translocated in and around these parks and did not set out to collect population data. Twenty two sites were surveyed (Figure 1, Supplementary material Table S1), with a focus on pools regularly visited by the public for recreation, which are more prone to be the recipient of crayfish translocations. Sites in the Karijini area included nine pools in Karijini National Park and two pools immediately to the west of the park, near the towns of Tom Price and Paraburdoo. Of these, eight sites were on northerly flowing upper tributaries of the Fortescue River and three (Coppin Pool, King Lake and Bellary Creek) were on tributaries of the Ashburton River. In the Millstream area, nine sites were surveyed in Millstream-Chichester National Park and two sites to the west of the park. Of these, five were on the Fortescue River or a small warm spring-fed pool that flows into the Fortescue, and six were on upper tributaries of the George River (adjacent to the Harding River). A combination of baited box traps, cameras and visual observations were used across sites to establish redclaw presence. Methods were not uniformly used at each site, so here we focus on where redclaws were detected, rather than where they were not. Collapsible black mesh box traps (670 mm × 470 mm × 200 mm), baited with a handful of dog biscuits, were set at each site. Traps were modified to minimise by-catch of turtles by restricting entry points to holes of about 8 cm diameter. Traps were placed up to about 20 m apart, across either the entire pool (for small pools) or a selected portion of the pool, favouring habitats where the species was likely present (i.e. in or adjacent to macrophytes, rocky areas or complex banks). Usually 5 to 10 traps were used, depending on the size of the sampled area. Traps were left in place for at least two hours and, where time and accessibility allowed, they were left overnight (Table S1). At a few sites, traps were left in for less than two hours: these were small sites, where visibility was very good and where visual surveys did not detect redclaw specimens. Absence of redclaw in traps is deemed a non-detection, rather than an absence, given the rapid assessment of this survey and the uneven trapping effort applied (both time and duration of trap set). At nine sites, two “GoPro Hero4 silver” cameras were deployed (Table S1). These were attached to steel plates and placed on the pool bed, where they were left running for 1.5 to 2.5 hours. They were set to take a 7 megapixel photograph every 30 seconds using the “medium” angle setting (72.2 vertical × 94.4 horizontal degree field of view). A mesh bag with dog biscuits as bait was wired to the base plate of each camera. Visual surveys of most pools were also conducted by one or two snorkelers after the traps (and cameras, if used) were set, for periods of up to 20 minutes (or shorter than 20 minutes if crayfish was detected sooner). As water clarity was poor at sites 10, 16, 17(A–C) and 20, the edge of those pools was walked to search for redclaw crayfish in the shallows (Table S1).

Pinder et al. (2019), BioInvasions Records 8(4): 882–897, https://doi.org/10.3391/bir.2019.8.4.17 885 Spread of redclaw crayfish into Pilbara natural waters

Figure 2. Locations of sampling sites for the Weelumurra Creek aquatic fauna survey. Red dots show where redclaw crayfish was detected and black dots where crayfish was not detected. See Figure 1 for location of this area.

Weelumurra Creek Aquatic Fauna Survey A baseline survey of aquatic fauna was conducted along Weelumurra Creek, a large ephemeral creek that discharges into the Fortescue River downstream of Fortescue Marsh, in June and September 2017 (Figures 1 and 2). The aim of this survey was to determine biodiversity values of Weelumurra Creek pools, as part of a broader pre-disturbance environmental impact assessment. However, as redclaw crayfish specimens were observed during the survey, and as they were known to be a non-native species, some population variables were collected. A total of eleven sampling sites (all permanent pools), comprising nine pools along one river and two pools on a tributary, were surveyed for in-stream habitat and aquatic biota (Table S1, Figure 2). At each site, submerged aquatic macrophyte diversity was recorded and percentage of species cover was visually estimated. Zooplankton (copepods, ostracods, cladocerans, rotifers and protozoans) were collected from the open water column at six of the 11 sites sampled in June and September, by gently sweeping over a distance of approximately 15 m with a 53 μm plankton

Pinder et al. (2019), BioInvasions Records 8(4): 882–897, https://doi.org/10.3391/bir.2019.8.4.17 886 Spread of redclaw crayfish into Pilbara natural waters

net. Four of these six sites (WC1, WC3, WC5, WC8) were located along the main channel of Weelumurra Creek, two of which had redclaw present, and two of which did not. The two other sites were located on the reference tributary and did not contain crayfish (Figure 2). Macroinvertebrates were collected from all 11 pools in June and September by using a 250 μm mesh D-frame pond net to kick sample dominant habitats at each site (i.e. root mats, detritus, submerged macrophytes, trailing riparian vegetation, woody debris, mineral substrate, etc.) for 10 minutes (Storey et al. 1991). Invertebrate samples were preserved in 70% ethanol prior to transport to the laboratory. Collected specimens were then identified to the lowest possible taxonomic resolution ( or species), counted and abundance was calculated. This provided a measure of relative abundance of macroinvertebrate species, and of total species richness (S) by site (for each month) for statistical analyses. Fish and redclaw crayfish were sampled at each site by a combination of electrofishing and baited traps. Electrofishing was conducted using a Smith-Root LR-24 battery powered back-pack electrofisher. All meso-habitats within a 50 m area (where available) were shocked with the intention of capturing as many aquatic fauna species/individuals as possible. In addition, a single collapsible black mesh box trap (670 mm × 470 mm × 200 mm) was set overnight (12 h) at each pool in the September survey. Each trap was baited with a mixture of laying pellets and dog biscuits. All fish and redclaw crayfish specimens captured were identified in the field, counted, their size recorded (standard length for fish and cephalothorax length for crayfish), and crayfish were also sexed. All redclaws were euthanised in an ice slurry, as per the licence requirements.

Redclaw identification The redclaw crayfish is a distinctive species and specimens captured (Figure 3) matched the description provided in Horwitz (1995). The identity of a specimen collected from George River, Millstream-Chichester National Park, was confirmed by sequencing CO1 and 16S genes, using species specific primers for CO1 and universal primers for 16S (Table 1). The sequences matched those for Cherax quadricarinatus on GenBank.

Statistical analysis A univariate analysis of variance (ANOVA; IBM SPSS Statistics (v22.0)) was used to test for differences in macroinvertebrate species richness (S) between pools with and without redclaw, using individual sites (pools) as replicates. Non-metric multi-dimensional scaling (MDS) ordination (PRIMER v7; Clarke and Gorley (2006)) was used to visualise relationships in macroinvertebrate assemblages among sites using Bray-Curtis

dissimilarities calculated from log10 abundance data. A one-way analysis of

Pinder et al. (2019), BioInvasions Records 8(4): 882–897, https://doi.org/10.3391/bir.2019.8.4.17 887 Spread of redclaw crayfish into Pilbara natural waters

Figure 3. Specimens of redclaw crayfish collected during the 2016 rapid assessment survey (A) and the 2017 Weelumurra Creek baseline aquatic fauna survey (B, C).

Table 1. Primers used to amplify DNA from crayfish tissues. Gene Primer name Sequence (5’–3’) Reference COcq CGGCATAGTCTCACACATCG Baker et al. 2008 CO1 CO1a-H AGTATAAGCGTCTGGGTAGTC Palumbi et al. 1991 1471 CCTGTTTANCAAAAACAT Crandall and Fitzpatrick 1996 16S 1472 AGATAGAAACCAACCTGG Crandall and Fitzpatrick 1996

similarity (ANOSIM) was undertaken to determine if there was a significant difference in macroinvertebrate assemblage composition between pools with and without redclaw. ANOVAs were performed to compare abundances of different fish species between sites with and without crayfish. The virtual absence of aquatic macrophytes and zooplankton from pools with redclaw meant that the distribution of this data was not amenable to statistical analyses.

Results Rapid assessment survey The presence of redclaw crayfish at Hamersley Gorge (site 1) in Karijini National Park, first recorded in 2016, was confirmed by capturing crayfish specimens in traps and on camera at that site (Table S1, Figure 1). No redclaws were detected in any other Karijini National Park sites. A small number of redclaws were caught at Bellary Creek (site 10), to the west of Karijini National Park (Table S1, Figure 1). Visual surveys at this site were limited due to low water clarity and to cameras not being used due to the presence of tourists. In Millstream-Chichester National Park, redclaw crayfish were detected only in three closely located and irregularly connected pools on the upper reaches of George River (sites 17A–C; Table S1, Figure 1). At these sites, redclaws were captured in traps in all pools and observed by one of the two

Pinder et al. (2019), BioInvasions Records 8(4): 882–897, https://doi.org/10.3391/bir.2019.8.4.17 888 Spread of redclaw crayfish into Pilbara natural waters

Figure 4. Composition of aquatic invertebrate taxa recorded from pools at Weelumurra Creek and its tributary in June and September 2017. Sites not sampled for zooplankton are denoted by “NS” and absence of zooplankton fauna is denoted as A. Redclaw presence at each site is denoted by a grey star, with number of redclaws (n) captured provided in the grid above, along with percent cover of submerged aquatic macrophytes and gastropod species richness.

cameras in site 17A. Water clarity was low, and visual surveys of shallow water did not reveal redclaw presence.

Weelumurra Creek Aquatic Fauna Survey Redclaws were detected at six of the nine sites surveyed on the main channel, but at none on the tributary (Figures 2 and 3). A total of 1254 redclaws were caught, with 300 specimens recorded in June, and 954 in September (Table S1, Figure 4). Where they were detected, catch size varied between pools and surveys, ranging from 21 individuals at WC7 in June to 285 at WC2 in September (Table S1, Figure 4). Redclaws varied in size, with cephalothorax length ranging from 10 to 70 mm (mean 44 ± 14 mm). Individuals less than 20 mm, which are considered juveniles (i.e. 0+ age class, Leland et al. 2015), represented 19% of all measured redclaws (Figure 5). There was substantial recruitment between surveys in June and September (Figure 5), as evidenced by the presence of ovigerous females (Figure 3C), or females carrying newly hatched redclaws at five of the six pools, also suggesting that populations in Weelumurra Creek are self-sustaining. Pools with redclaws present completely lacked submerged macrophytes (macrophyte cover = 0% for all of them), whereas pools without redclaw had between 5 to 48% cover of submerged macrophytes (median 20%) (Figure 4). Macrophyte diversity in these pools varied between one species

Pinder et al. (2019), BioInvasions Records 8(4): 882–897, https://doi.org/10.3391/bir.2019.8.4.17 889 Spread of redclaw crayfish into Pilbara natural waters

(A) June 2017 (B) September 2017 300 300

250 250

200 200

150 150

100 Abundance Abundance 100

50 50

0 0 WC1WC2WC3WC4WC5WC6WC7WC8 WC1 WC2 WC3 WC4 WC5 WC6 WC7 WC7a WC8 Figure 5. Abundance of redclaw crayfish from each size/age-class (i.e. juvenile – black column, sub-adult/adult – grey column) recorded from Weelumurra Creek sites in a) June and b) September surveys. Note WC7a sampled during September only.

Figure 6. nMDS ordination of macroinvertebrate assemblages of Weelumurra Creek pools, based on log10 abundances of 190 taxa. Samples are labelled either P (redclaw present) or A (redclaw absent).

(at WC8) to three species (at WC1 and WCT1), with the flora consisting of Najas tenuiflora, Vallisneria spp. and Chara spp. Zooplankton fauna sampled comprised a total of 35 taxa across the two sampling occasions, with taxa richness ranging from zero to 16 taxa per pool on a sampling occasion. In the four pools without redclaw crayfish, zooplankton diversity ranged from four to 16 taxa, whereas the two pools with redclaw supported zero and one zooplankton species (the latter being a protist, Arcella discoides; Figure 4). The macroinvertebrate fauna found comprised 190 taxa across the 11 pools and two sampling occasions. Species richness ranged from 28 at site WC4 (June) to 64 at site WCT2 (September). Mean richness was significantly higher in river pools without redclaw (52.7 ± 2.2 taxa) compared to those with redclaw (40.3 ± 2.3 taxa) (one-way ANOVA df = 1, MS = 792.893, F = 13.894, p = 0.001). Multivariate analysis (ANOSIM) detected a significant difference in the composition of macroinvertebrate communities between pools with and without redclaw (R statistic = 0.904, p = 0.002), with the two groups of pools clearly separated in ordination space (Figure 6). Analysis of the taxa contributing to this separation showed lower

Pinder et al. (2019), BioInvasions Records 8(4): 882–897, https://doi.org/10.3391/bir.2019.8.4.17 890 Spread of redclaw crayfish into Pilbara natural waters

gastropod species richness in pools with redclaw, compared to pools without redclaw (Figure 4). Three gastropod species were recorded in pools without redclaw (Bullastra vinosa, Ferrissia petterdi and Gyraulus sp.), whereas pools with redclaw either lacked gastropods or only supported the smallest species, F. petterdi, and only in low abundances. Three native fish species were collected across the 11 pools: western rainbowfish (Melanotaenia australis), spangled perch (Leiopotherapon unicolor) and a possibly undescribed tandan catfish (Neosilurus sp.). The most abundant of the fish species, M. australis, reported no significant difference in mean abundance between pools with redclaw (mean 76.3 ± 10.9 individuals/m), compared to those without redclaw (mean 55.0 ± 17.5 individuals/m) (one-way ANOVA; df = 1, p = 0.311). Mean abundance of L. unicolor was also similar between pools with (mean 1.8 ± 1.5 individuals/m) and without redclaw (mean 1.4 ± 0.8 individuals/m) (one-way ANOVA; df = 1, p = 0.810), whereas Neosilurus sp. was rare in pools without redclaws (only one individual captured in total) compared to those with redclaws (mean of 6.4 ± 1.2 individuals/m) (one-way ANOVA, df = 1, p = 0.004).

Discussion Occurrence and translocation in the Pilbara region The surveys reported here extend the known distribution of redclaw crayfish in the Pilbara region from the Harding Dam into three additional catchments. One of these is the small (2.8 million km2) George River catchment adjacent to the Harding River. Of more concern, however, is their presence in the much larger Fortescue and Ashburton catchments (20 million and 86 million km2, respectively). Our records are from the lower Fortescue River, which is a separate catchment to the endorheic upper Fortescue River that terminates at Fortescue Marsh. However, a population has recently (early 2018) been recorded in Ophthalmia Dam (see Figure 1) in the upper Fortescue River (D. Thorburn, Indo-Pacific Environmental Pty Ltd, pers. comm. 2018). The timing of introductions across the region is unknown, but is likely to be very recent. A survey of aquatic invertebrates in Pilbara rivers undertaken between 2003 and 2006 did not detect redclaw presence (Pinder et al. 2010). Furthermore, Hamersley Gorge, where redclaws were first recorded outside of the Harding catchment in 2016, was included in the Pinder et al. (2010) survey and was sampled by one of the authors (AH) biannually between 2009 and early 2016, without detecting redclaw. Redclaws were also not detected in a previous study performed at three Fortescue River pools between Weelumurra Creek and Hamersley Gorge on Mount Florence Station in April 2017 (Pinder et al. 2017). This suggests that Weelumurra Creek and Hamersley Gorge populations represent independent introductions.

Pinder et al. (2019), BioInvasions Records 8(4): 882–897, https://doi.org/10.3391/bir.2019.8.4.17 891 Spread of redclaw crayfish into Pilbara natural waters

In addition to the confirmed records, photographs on social media of a redclaw purportedly caught by recreational fishers at Wittenoom Gorge on the northern edge of Karijini National Park, support anecdotal reports of their presence in that gorge. The new redclaw crayfish locations reported here are not hydrologically connected to the Harding River and, while temporary pools and episodic flooding may facilitate within catchment dispersal, it is unlikely that redclaw would travel the significant overland distances between suitable habitats in different catchments in the arid Pilbara. It is much more likely that specimens have been translocated intentionally (and illegally) from Harding Dam to other locations, mostly to popular pools, in order to provide a new recreational fishery component.

Impacts on Pilbara river pool ecosystems Although redclaw crayfish has been studied intensively for aquaculture purposes, there is little information about their position in the food web of natural ecosystems or about possible impacts of translocated populations on natural environments. Elsewhere, other introduced freshwater crayfish species have been reported to impact native species and fisheries, and to modify habitats (Chucholl 2012; Lodge et al. 2012; Twardochleb et al. 2013; Monde et al. 2017). For example, the introduction of the red swamp crayfish into Kenya’s Lake Naivasha resulted in reduced macrophyte cover (Harper et al. 2002) and mesocosm experiments showed that this species reduced invertebrate abundance, including snails and freshwater (Lodge et al. 2005). Our results, although circumstantial, also suggest that introduction of redclaw crayfish resulted in the complete loss of macrophyte cover and in significant changes in invertebrate communities. This is not surprising, as a recent study performed in the Sanyati Basin of Lake Kariba, Zimbabwe, found macrophytes, detritus and macroinvertebrates to be the most important dietary items of redclaw crayfish (Marufu et al. 2018). The depauperate zooplankton fauna recorded for Weelumurra Creek pools supporting redclaw crayfish is exceptional, particularly for groundwater/spring fed pools in the Pilbara. For context, a survey of 100 river pools, springs and wetlands across the Pilbara region documented a very diverse and abundant zooplankton fauna (protozoans, rotifers, copepods, cladocerans and ostracods), positively associated with clear river pools of longer hydroperiod, abundant macrophytes, and presence of flow, with an average of 27 species collected per sample (albeit samples were three times larger than those collected for this project) (Pinder et al. 2010). Regarding the Weelumurra Creek macroinvertebrate fauna, the absence of two species of gastropod, and reduced abundance of a third species in pools with redclaw, is also notable. Adult redclaws have known molluscivorous tendencies (Monde et al. 2017), while zooplankton are considered the optimal food for juveniles in aquaculture (Saoud et al. 2012; Jones 2015).

Pinder et al. (2019), BioInvasions Records 8(4): 882–897, https://doi.org/10.3391/bir.2019.8.4.17 892 Spread of redclaw crayfish into Pilbara natural waters

Nevertheless, the association of redclaw presence with lack of macrophytes may also be implicated in this reorganisation of invertebrate communities. Kay et al. (1999) found that macrophytes in river pools of the Pilbara had higher invertebrate richness than in other habitats. Pinder et al. (2010) recorded > 5% macrophyte cover at two-thirds of such pools in the Pilbara region and found strong correlations between richness of aquatic invertebrate assemblages and macrophyte biomass and/or cover. These observations are likely driven by effects of macrophytes on micro-flow environments, water chemistry, carbon cycling, water temperature and clarity, provision of egg laying surfaces, material for invertebrate case construction and food for herbivores (Gregg and Rose 1985; Cyr and Downing 1988; Schramm and Jirka 1989; Boulton and Lloyd 1992; Stansfield et al. 1997). As such, the absence of macrophytes in pools with redclaw present might have caused a reduced abundance/richness of macroinvertebrates in those habitats. Furthermore, a loss of macrophytes can also expose zooplankton to greater fish predation (Schriver et al. 1995; Phillips et al. 1996). The most abundant fish species found in pools, the western rainbowfish, was recorded in similar abundance at pools with and without crayfish, suggesting that fish density is not associated with reduced zooplankton abundance (or presence). The results of the Weelumurra Creek survey suggest that redclaw, either directly (through predation or competition) or indirectly (through habitat modification, especially loss of macrophytes), may have caused a significant reorganisation of the ecological community in invaded pools. From an ecosystem function perspective, there is also concern that redclaw may accelerate the breakdown of allochthonous detritus (Weyl et al. 2017), which plays an important role in nutrient regulation in aquatic ecosystems (Lodge and Hill 1994; Buck et al. 2003). Our results call for further assessment of potential ecological impacts of spread of the non-native redclaw crayfish into high conservation value ecosystems of the Pilbara region of Western Australia.

Management Management and eradication of introduced crayfish populations has proven to be challenging around the world (see review in Gherardi et al. 2011). It is illegal to use traps to catch crayfish and to translocate them in Western Australia, so a first and critical step should be launching a campaign of public education, at the same time as imposing law enforcement to minimise further translocations, particularly into aquatic ecosystems in the conservation estate or associated catchments. Options for control are limited and of uncertain effectiveness. Nunes et al. (2017a) suggest that while chemical poisoning seems to be the most effective technique for eradicating pest crayfish populations, the high concentrations required and non-specificity of chemical agents used (Peay

Pinder et al. (2019), BioInvasions Records 8(4): 882–897, https://doi.org/10.3391/bir.2019.8.4.17 893 Spread of redclaw crayfish into Pilbara natural waters

et al. 2006), make this technique undesirable in pools with high ecological value, which is the case throughout the Pilbara. We suggest that mechanical removal techniques (e.g. intensive trapping, electrofishing; see Nunes et al. 2017b) may be suitable in some situations, especially where populations are believed to be relatively confined and isolated, and where education and enforcement is likely to minimise reintroductions, but such actions need to be implemented soon after populations are detected to minimise population growth and further spread. While it is not feasible to eradicate redclaws across a large area like Western Australia’s Pilbara region, there could be significant value in targeted redclaw population control programs that will minimise disruption of ecosystem functioning at some high conservation value sites. Physical techniques, such as drying of pools, could also be effective due to the fact that redclaws do not exhibit burrowing habits (Wingfield 2002), suggesting they are less likely to withstand extreme environmental conditions such as prolonged drought (Kouba et al. 2016; Souty-Grosset et al. 2016) or deliberate dewatering. This technique, like chemical control, is likely to have negative impacts on other aquatic biota, although the aquatic fauna of the region is largely adapted to seasonal drying. Our results, and those of other studies of freshwater crayfish introductions, suggest that the biologically unique Pilbara riverine ecosystems is likely to be significantly and irrevocably modified by the introduction of redclaw crayfish. Efforts to minimise further redclaw translocations and, where feasible, control established populations, should be seriously considered in order to, at least, minimise the magnitude of their impact.

Acknowledgements

We acknowledge the Banjima, East Guruma and Yinhawangka peoples as traditional owners of the lands and waters sampled in the Karijini area and the Yindjibarndi and Ngarluma peoples as traditional owners of the lands and waters sampled in the Millstream National Park area. Department of Biodiversity, Conservation and Attractions (DBCA) staff of Karijini and Millstream NP for facilitated surveys in those reserves and the Ngurrawaana Rangers welcomed us to the Gregory Gorge sampling locations on Yindjibarndi lands. DBCA’s Pilbara Region and Biodiversity and Conservation Science co-funded the rapid assessment survey. Stephen Beatty from Murdoch University provided advice on modifying and using cage traps. Russell Shiel (University of Adelaide) identified the zooplankton. Chris Hofmeester and Bonita Clark (Wetland Research and Management) identified the macroinvertebrates against an established voucher collection. Rodney Duffy and Aaron Schoenberg from the Western Australian Department of Primary Industries and Regional Development provided advice on sampling methodology and potential control methods. Fortescue Metals Group (FMG) provided funding for the Weelumurra Creek Baseline Aquatic Fauna Survey. We thank Matt Dowling (FMG) who provided insight and expertise that greatly assisted the research. We would also like to thank two anonymous reviewers and the editor who greatly improved our manuscript.

Permits/Licences

Traps were used under Department of Primary Industries and Regional Development exemptions 2760/2796 from the Fish Resources Management Act 1994 (Section 792) (a). Invertebrate samples were collected under Department of Biodiversity, Conservation and Attraction licence to take fauna for scientific purposes 08-000316.

Pinder et al. (2019), BioInvasions Records 8(4): 882–897, https://doi.org/10.3391/bir.2019.8.4.17 894 Spread of redclaw crayfish into Pilbara natural waters

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Supplementary material The following supplementary material is available for this article: Table S1. Sites surveyed during the 2016 rapid assessment survey and for the 2017 aquatic fauna survey of Weelumurra Creek (WC sites), with information on survey methods used and numbers of redclaw crayfish captured. This material is available as part of online article from: http://www.reabic.net/journals/bir/2019/Supplements/BIR_2019_Pinder_etal_Table_S1.xlsx

Pinder et al. (2019), BioInvasions Records 8(4): 882–897, https://doi.org/10.3391/bir.2019.8.4.17 897