The hidden risk of keystone invaders in Canada: a case study using nonindigenous crayfish
Publication: Canadian Journal of Fisheries and Aquatic Sciences
13 September 2022
Abstract
Invasive species have long been recognized as a serious threat to freshwater ecosystems. This is especially true for invasive species in keystone positions in food webs that can cause major disruption and can lead to unexpected outcomes. Crayfish occupy a central trophic position and nonindigenous crayfish have been shown to substantially disrupt ecosystems they invade. Here, we assess eight nonindigenous crayfish to 21 freshwater ecoregions in Canada using a screening-level risk assessment. We found that ecoregions in Canada that were warmer and contained high native freshwater diversity were most at risk from crayfish invasions, particularly: the Laurentian Great Lakes, St. Lawrence, English–Winnipeg lakes, and Coastal British Columbia ecoregions. Four crayfish species consistently had higher-risk scores: rusty (Faxonius rusticus), virile (Faxonius virilis), signal (Pacifastacus leniusculus), and red swamp (Procambarus clarkii). Of these high-risk crayfish, only the red swamp crayfish is not yet established in Canada but is present in US waters of the transboundary Great Lakes ecoregion. Our study is the first to evaluate the relative risks that nonindigenous crayfish pose to freshwater ecosystems in Canada.
Résumé
Il est établi depuis longtemps que les espèces envahissantes constituent une menace sérieuse pour les écosystèmes d’eau douce, en particulier les espèces envahissantes occupant des positions de clé de voûte dans les réseaux trophiques, qui peuvent causer d’importantes perturbations et entraîner des conséquences imprévues. Les écrevisses occupent une position trophique centrale, et il est démontré que les écrevisses non indigènes perturbent considérablement les écosystèmes qu’elles envahissent. Nous évaluons huit écrevisses non indigènes dans 21 écorégions d’eau douce au Canada en utilisant une évaluation du risque au niveau du dépistage. Nous constatons que les écorégions du Canada qui sont plus chaudes et qui présentent une grande diversité d’espèces d’eau douce indigènes sont celles pour lesquelles l’envahissement par des écrevisses pose le plus grand risque, en particulier les écorégions des Grands Lacs laurentiens, du Saint-Laurent, de la rivière English – du lac Winnipeg et des côtes de la Colombie-Britannique. Quatre espèces d’écrevisses sont uniformément associées à des risques plus élevés, à savoir, l’écrevisse à taches rouges (Faxonius rusticus), l’écrevisse à pinces bleues (Faxonius virilis), l’écrevisse de Californie (Pacifastacus leniusculus) et l’écrevisse rouge des marais (Procambarus clarkii). De ces écrevisses à haut risque, seule l’écrevisse rouge des marais n’est pas encore établie au Canada, mais elle est présente dans les eaux américaines de l’écorégion transfrontalière des Grands Lacs. Notre étude constitue la première évaluation des risques relatifs que présentent les écrevisses non indigènes pour les écosystèmes d’eau douce au Canada. [Traduit par la Rédaction]
Introduction
Invasive species are a leading threat to biodiversity across all ecosystems (Lodge 1993; Mainka and Howard 2010; Sorte et al. 2010; Crystal-Ornelas and Lockwood 2020). Much of the world’s freshwater ecosystems have already been compromised by habitat alteration and pollution; therefore, the addition of nonindigenous species (NIS) to these systems is particularly concerning (Dextrase and Mandrak 2006). Vectors of freshwater NIS include intentional or accidental release or spread through activities such as shipping (e.g., ballast water), recreational boating (hull fouling), the aquarium pet trade, angling (e.g., bait buckets), and cultivation for food (Strayer 2010; Zieritz et al. 2017; Banha et al. 2019; Chan et al. 2019). Freshwater NIS spans all trophic levels from bacteria (Barkham et al. 2019) and viruses (Bain et al. 2010) to plankton (Cordell et al. 2008), aquatic plants (Hussner et al. 2017), invertebrates (Griffiths et al. 1991; Sousa et al. 2014), amphibians (Measey et al. 2012), and fish (Dextrase and Mandrak 2006; Gherardi 2010) and have been shown to have negative impacts on native populations, communities, and ecosystems regardless of trophic level (Gallardo et al. 2016). Impacts on native species can be felt both directly through interactions (both consumptive and competitive) or indirectly through release from interactions or ecosystem changes (e.g., habitat alteration by ecosystem engineers; Strayer 2010; Gallardo et al. 2016; Emery‐Butcher et al. 2020).
Crayfish are large and long-lived crustaceans that play an important role in freshwater food webs (Momot et al. 1978). These freshwater invertebrates can inhabit both lentic and lotic environments across a wide spectrum of habitats: some species are stream dwellers, some prefer slow-moving water (e.g., slow-moving rivers, ponds, lakes), and some are specialists that live in caves (Crandall and Buhay 2008). Burrowing behavior can also influence habitat choice by crayfish, as those that burrow extensively are less reliant on aquatic resources and can survive periods of drought (Florey and Moore 2019). Crayfish are generalist consumers, eating decaying plant and animal material, small aquatic invertebrates, mollusks, aquatic plants, and fish and amphibian eggs (Crandall and Buhay 2008). Since crayfish often feed at multiple trophic levels, they provide an important pathway for energy transfer in a food web, with many considered keystone species (Reynolds 2013). Predators of crayfish include fish, turtles, small mammals (e.g., mink and river otters), and large birds (e.g., herons) (Nyström et al. 2006; Yarra and Magoulick 2020). In addition to their ecological importance, crayfish are valued as food in many parts of the world (Lodge et al. 2000), are used as bait for fish (DiStefano et al. 2009), kept as pets (Faulkes 2015a), and have been used as bioindicators for water quality (Reynolds et al. 2013). Invasive crayfish have played a role in many of the declines in native crayfish populations, especially due to disease transmission (Lodge et al. 2000; Chucholl and Schrimpf 2016) but also have been shown to destroy habitats by grazing and uprooting plants (Gherardi and Acquistapace 2007; van der Wal et al. 2013), disrupting food webs by depleting prey species (Francesco Ficetola et al. 2011; Ficetola et al. 2012; Mathers et al. 2016, 2020), displacing competitors (Dunn et al. 2009), and by altering ecosystem functioning (Doherty-Bone et al. 2018; Mathers et al. 2020). Overall invasive crayfish species have a global record of wreaking havoc, particularly on macrophytes, benthic invertebrates, gastropods, amphibians, and fish (Twardochleb et al. 2013), but their risk to Canadian ecosystems has not been evaluated previously.
There are at least 640 species belonging to four families of crayfish worldwide, and 382 species in two families (Cambaridae and Astacidae) in North America, which has high levels of endemism (Crandall and Buhay 2008). In Canada, there are nine native crayfish species, in these two families, which are regionally endemic. The signal crayfish (Pacifastacus leniusculus) the only species in Canada from the Astacidae family, is native to the Columbia River Basin which reaches up into the Okanagan and Kootenay regions of British Columbia. The Great Lakes region in Ontario has the highest native crayfish diversity with eight species: Appalachian brook crayfish (Cambarus bartonii), big water crayfish (Cambarus robusticus), digger crayfish (Creaserinus fodiens), calico crayfish (Faxionus immunis), northern clearwater crayfish (Faxonius propinquus), virile crayfish (Faxonius virilis), devil crayfish (Lacunicambarus diogenes), and painted mudbug crayfish (Lacunicambarus polychromatus). The virile crayfish is native to Central Canada but has expanded westward (Phillips et al. 2009b). Three provinces (Newfoundland and Labrador, Prince Edward Island, and Nova Scotia) as well as the three territories (Yukon, Northwest Territories, and Nunavut) have no native crayfishes nor any functionally similar taxa (Phillips et al. 2009b). The northern and eastern range limits of native crayfish are likely a function of temperature, calcium, pH tolerances, and evolutionary history (Phillips et al. 2009b).
There are a number of vectors of crayfish introduction. Many crayfish species are farmed for human consumption, and some of the first introductions of crayfish were intentional to develop harvestable stocks. Crayfish escaping stocking ponds (or natural waters where they were stocked) has resulted in substantial crayfish invasions in North America, Europe, and Africa (Holdich et al. 2009). The live bait industry is another important vector in crayfish invasions, particularly in the USA where the use of crayfish as bait is popular and regulations have historically been weak (Lodge et al. 2000; DiStefano et al. 2009). In Canada, however, consumption of crayfish and use of crayfish as bait is uncommon. The aquarium pet trade has recently been implicated in the spread of the marbled crayfish (Procambarus fallax virginalis) across Europe (Mrugała et al. 2015; Faulkes 2015b) and could be an important vector in Canada. Another less understood vector is the release of biological specimens from the biological supply industry (e.g., used for biology education in elementary schools; Larson and Olden 2008), which has been documented in Canada on at least one occasion (Phillips et al. 2009b). Finally, secondary spread from established populations in the USA via directly connected waterways (e.g., Great Lakes, Mississippi catchment) may become an important vector, especially as the climate warms.
Recovery of freshwater ecosystems requires addressing current species invasions and preventing new ones (Tickner et al. 2020). Managers are increasingly turning to tools like risk assessments to identify which species should be prioritized for limited resource allocations and to avoid lengthy and costly eradication efforts (Mandrak and Cudmore 2015; Marshall Meyers et al. 2020). Trait-based assessments are one approach to identify higher-risk species (Chan et al. 2021), including crayfish (Zeng et al. 2015). Another complimentary approach follows the invasion cycle and several screening-level risk assessment tools have been developed (reviewed in Kumschick and Richardson 2013) with most being either decision trees (Reichard and Hamilton 1997; Kolar and Lodge 2002; Caley and Kuhnert 2006) or scoring systems (Pheloung et al. 1999; Daehler et al. 2004; Copp et al. 2009; Drolet et al. 2016). Here, we adapt the Canadian Marine Invasive Screening Tool (CMIST; Drolet et al. 2016, 2017) for freshwater crayfish across Canada. While this tool was first applied to marine invertebrates (Drolet et al. 2016; Moore et al. 2018; Therriault et al. 2018), it is not taxa- or ecosystem-specific and has since been applied to marine plankton (Goldsmit et al. 2020, 2021) and freshwater fish (DFO 2017). The main reason we selected this tool is that it clearly parses risk in terms of both likelihood and impact of the invasion, is less overparameterized compared with other tools, and explicitly quantifies uncertainty using confidence intervals (Kumschick and Richardson 2013; Drolet et al. 2016, 2017; Srėbalienė et al. 2019).
Although globally recognized as invaders, in Canada nonindigenous crayfish have received relatively little attention. Here, we assess a suite of nonindigenous crayfish to Canada using a score-based screening level risk assessment tool, the CMIST. To our knowledge, this is the first attempt to evaluate the relative risks that crayfish pose to freshwater ecosystems in Canada. The goals of this paper are to develop and rank eight NIS crayfish that could impact Canadian watersheds. We identify both which crayfish species pose the most risk to Canadian ecoregions and which ecoregions are most at risk from crayfish invasions. We hypothesized that the warmest ecoregions of Canada would be at the greatest risk of invasion, as many of the invaders are from source regions with a warmer climate. We also expected that the marbled crayfish, a parthenogenic crayfish widely available in the aquarium trade and spreading rapidly across Europe (Chucholl 2016), would pose the greatest risk to Canadian freshwater ecosystems.
Materials and methods
Species selection
For our analysis, we selected eight nonindigenous crayfish species based on invasion history in Canada and North America. The species already present or established in at least one ecoregion are the spiny-cheek crayfish (Faxonius limosus), Allegheny crayfish (Faxonius obscurus), rusty crayfish (Faxonius rusticus), virile crayfish, white river crayfish (Procambarus acutus acutus), red swamp crayfish (Procambarus clarkii) (only established in the US portion of Laurentian Great Lakes ecoregion), and the signal crayfish (Pacifastascus leniusculus) (Table 1). We also assessed vectors of crayfish introduced to identify potential invaders, which resulted in the addition of the marbled crayfish (Procambarus f. virginalis). Not all eight species were assessed in each ecoregion, as some species such as the virile and signal crayfish are native to some ecoregions.
Table 1.
Assessment ecoregion selection
Canada’s freshwater landscape is vast and diverse: the highest number of lakes of any country (Messager et al. 2016), 2 million mapped rivers, and 130 867 km2 of internationally important wetlands (Tognelli et al. 2017). We used the Freshwater Ecoregions of the World (FEOW), a biogeographic classification system that used cluster analyses of fish distributions to identify distinct assemblages within freshwater communities (Abell et al. 2008). This process delineated 21 ecoregions in Canada (Table S1) (Abell et al. 2008). Since some ecoregions span international borders, if a crayfish species was not yet present in Canadian waters, it was assessed as NIS regardless of its status in the US portion.
CMIST process and modifications
We applied and adapted where necessary the CMIST (Drolet et al. 2016, 2017) to the suite of crayfish species (eight species; Table 1) within Canadian ecoregions (21 ecoregions; Table S1). CMIST is a screening-level risk assessment tool that uses 17 expert-assessed questions to assign risk scores and uncertainty. These 17 questions capture the likelihood of invasion (questions 1–8) and potential impact (questions 9–17) of a given species to a defined area. We followed the scoring guidance provided for each question (Drolet et al. 2016), and occasionally created subroutines to establish a score with multiple parts. These routines and the data sources used are described in full in Supplementary Materials B, but a brief description of the questions and considerations is outlined in Table 2. Both a score (1, 2, or 3) and an estimate of certainty (1, 2, or 3) were assigned for each question. A score of 1 (the lowest score) for a given question indicates species and region combinations where the probability or impact of invasion is low, whereas a score of 3 would indicate either high probability or impact of invasion. In general, if there was peer-reviewed literature on the species or ecoregion to support the score, certainty was high (3); if we had to infer a score based on how congeneric species scored, then certainty was low (1). To mitigate bias against new invasions for which there may not be available data yet, we inferred a midlevel baseline of impact for each species (i.e., score of 2) based on the history of crayfish invasions. This baseline was then modified by the weight of the evidence of impact, reflected in the error bars (certainty estimate).
Table 2.
To calculate the likelihood score (adjusted mean score of questions 1–8), the impact score (adjusted mean score of questions 9–17), and the overall risk score (likelihood × impact score) for each species (eight species) in each ecoregion (21 ecoregions), we used the CMISTScore function in the CMISTR package (Daigle 2021) using R (version 4.0.0; R Core Team 2020). The scores were adjusted and given confidence intervals based on the certainty estimates; confidence intervals were drawn from probability distributions developed by (Drolet et al. 2016). Finally, we identified High Relative Risk (HRR) species, as described by (Goldsmit et al. 2021). These species scored on average at least 2 within the possible range of 1–3 for both the likelihood and impact, falling in the upper right quadrant of a biplot of these two scores. The approach taken here provides a relative assessment within the taxa and ecoregions assessed.
Results
CMIST overall risk scores
By ecoregion
For eight species across 21 ecoregions in Canada, adjusted risk scores ranged from 1.73 (CI: 1.53, 2.14) to 6.70 (CI: 5.81,7.33) (Fig. 1). The ecoregions with the highest average risk from all crayfish were typically ecoregions with warmer temperatures: the Laurentian Great Lakes (ecoregion 116), Alaska and Canadian Pacific Coastal (ecoregion 103), St. Lawrence (ecoregion 117), followed by English–Winnipeg lakes (ecoregion 109). The ecoregions with the lowest average risk of crayfish invasion were the coldest parts of Canada: the Canadian Arctic Archipelago (ecoregion 112), Alaskan Coastal (ecoregion 101), and Upper Yukon (ecoregion 102). For these lowest risk ecoregions, the crayfish scores tended to group together (i.e., all species got similar scores within an ecoregion). However, across most of Canada, overall risk was not uniform with some ecoregions at substantially higher risk (Fig. 1). Uncertainty also varied between species and ecoregions. The ecoregion with the lowest average uncertainty (i.e., smallest confidence intervals) was the Canadian Arctic Archipelago (ecoregion 112). The largest uncertainty (largest confidence intervals) was in British Columbia (ecoregion 103) and the Laurentian Great Lakes (ecoregion 116).
Fig. 1.
By species
In general, across all ecoregions, rusty crayfish had the highest mean risk score (Fig. 2). The highest scores observed for each species independent of ecoregion were as follows: 6.70 for rusty crayfish (ecoregion 109), 6.26 for signal crayfish (ecoregion 103), 5.96 for red swamp crayfish (ecoregion 116), 5.76 for virile crayfish (ecoregion 107), 4.77 for spiny-cheek crayfish (ecoregion 117), 4.33 for white river crayfish (ecoregion 103), 4.30 for Allegheny crayfish (ecoregion 116), and 3.81 for marbled crayfish (ecoregion 116). Furthermore, rusty crayfish was the highest risk crayfish for nine of the 21 ecoregions (101, 102, 109, 116, 117, 142, 108, 110, 114), while signal, virile, and red swamp were the highest risk for four ecoregions (101, 102, 103, 105; 107, 104, 120, 118; and 115, 113, 111, 106, respectively; Fig. 2). Furthermore, virile crayfish, native to much of eastern Canada, posed its largest risk to western Canada (particularly ecoregions 103, 107, 120), while red swamp crayfish posed its highest risk to Ontario, Quebec, and Manitoba (ecoregions 109, 116, 117). Confidence intervals were the smallest (i.e., scores most certain) for red swamp crayfish. The four crayfish that were generally lower risk across Canada included the marbled, Allegheny, spiny-cheek, and white river crayfish.
Fig. 2.
Likelihood, impact, and relative risk
By ecoregion
Likelihood scores ranged from 1.37 (CI: 1.25, 1.63) to 2.54 (CI: 2.35, 2.75) (Fig. 3). Averaging across all species, the Alaska and Canadian Pacific Coastal ecoregion (103) had the highest likelihood of invasion, followed by the Laurentian Great Lakes (116), Columbia Glaciate (120), and St. Lawrence (117). The ecoregion with the lowest mean likelihood of crayfish invasion was the Canadian Arctic Archipelago (112). Impact scores ranged from 1.26 (CI: 1.22, 1.44) to 2.85 (CI: 2.67, 3.00). Central Canada had a concentration of ecoregions with high average-projected impacts across multiple species, in particular, English–Winnipeg lakes (109), Laurentian Great Lakes (116), and St. Lawrence (117). Ecoregions in Southern (110), Western (111), and Eastern (113) Hudson Bay also had relatively high mean-projected impacts, although low likelihood of invasion. The lowest-projected impact was in the Canadian Arctic Archipelago ecoregion (112).
Fig. 3.
HRR species were species that scored over 2.0 for both impact and likelihood (dashed box Fig. 3). Many ecoregions had at least the confidence intervals of one species in this quadrant. We found eight ecoregions had unambiguous HRR species: Alaska and Canada Pacific Coastal (103), Upper Mackenzie (104), Upper Saskatchewan (107), Middle Saskatchewan (108), Winnipeg Lakes (109), Laurentian Great Lakes (116), St. Lawrence (117), and Upper Missouri (142). Four ecoregions in northern Canada had no HRR species: the Alaskan Coastal (101), Upper Yukon (102), Central Arctic Coastal (106), and Canadian Arctic Archipelago (112). Out of all the northern ecoregions, only the Upper Mackenzie (104) had an HRR species: the virile crayfish. Several ecoregions had multiple HRR species, notably Alaska and Canada Pacific Coastal (103) in British Columbia and parts of Ontario and Quebec: the Laurentian Great Lakes ecoregion (116) and the St. Lawrence (117) all had at least three HRR crayfish species.
By species
The rusty crayfish had the highest likelihood of invasion across all ecoregions (Fig. 3), and likelihood was highest for the English–Winnipeg lakes (109), Upper Saskatchewan (107), and Middle Saskatchewan (108) ecoregions, which span Saskatchewan and Alberta. The virile crayfish had high likelihood of invasion in both Upper Saskatchewan (107) and Middle Saskatchewan (108), in addition to British Columbia, both Alaska and Canadian Pacific Coastal (103) and Columbian Glaciate (120). The species with the lowest likelihood of invasion across all ecoregions was the marbled crayfish.
The species with the highest average impact across all ecoregions was the rusty crayfish, followed closely by the signal, virile, and red swamp crayfishes. Three of these species had their highest projected impacts in the Laurentian Great Lakes ecoregion (116). The Allegheny crayfish had the lowest projected impact but also the highest uncertainty.
The rusty crayfish was an HRR species in the highest number of ecoregions (at least partially in 13 ecoregions), followed by the virile, signal, and red swamp crayfishes. The marbled and Allegheny crayfishes were the only species that did not fall squarely into the HRR category in any ecoregion. Of the lower-scoring species, the spiny-cheek crayfish had high relative risk in the St. Lawrence ecoregion (117), and the white river crayfish had high relative risk in the Laurentian Great Lakes ecoregion (116).
Discussion
High-risk invaders and regional vulnerability
Four species consistently scored higher than the others: rusty, signal, virile, and red swamp crayfish of which only the red swamp crayfish is not yet established in Canada, although it is present in US tributaries of the Great Lakes transboundary ecoregion. Our results align with ecological risk screenings that identify these four crayfish as having high overall risk in the continental USA (US Fish and Wildlife Service 2015a, 2015b, 2015c, 2015d). The rusty crayfish (F. rusticus), was the highest-risk crayfish assessed (overall score of 6.70 for the English–Winnipeg lakes ecoregion). For comparison, the ten highest-risk freshwater fish (out of 128 assessed species) to British Columbia (common carp, largemouth bass, smallmouth bass, walleye, northern pike, brown bullhead, roach, pumpkinseed, and three Asian carps) had overall CMIST scores that fell between 6.0 and 7.8 (DFO 2017). Our results also align with Phillips et al. (2009b) that identified the rusty crayfish as having high invasion potential in Canada. Procambarus clarkii was the highest-risk species not yet present in Canadian waters. Our assessment agrees with the results of a Great Lakes Aquatic Nonindigenous Species Risk Assessment (GLANSRA) that identified the red swamp crayfish as one of two highest-scoring invertebrates on their surveillance watch list (Davidson et al. 2021), and the results of a recent habitat suitability model that identified that nearshore areas of the Great Lakes do provide suitable habitat for this species (Egly et al. 2019).
Perhaps not surprisingly, there was considerable variation in ecoregional risk from possible crayfish invasions but, in general, we found that the freshwater ecoregions most vulnerable to crayfish invasion were in central, southern, and western Canada. These ecoregions have higher population density, which was an important factor for assessment questions concerning vectors or propagule pressure. The most vulnerable ecoregions were also adjacent to the USA, where some of the nonindigenous crayfish to Canada have established populations (both native and invaded ranges), leading to a higher potential for natural or human-mediated secondary spread. Also, the most southern ecoregions all have warmer temperatures and were therefore more suitable for the suite of crayfish species assessed here as the risk posed by crayfish invasions in the cold (and less populated) northern ecoregions of Canada was substantially lower.
Another source of variation between ecoregions was native biodiversity. The impact section of CMIST assessed if there was substantial impact to native biodiversity, species at risk, or commercial fisheries. Ecoregions that had higher native biodiversity, like the Great Lakes, St. Lawrence, southern Manitoba, and British Columbia (Chu et al. 2015), were therefore more vulnerable to a larger impact on biodiversity than Arctic ecoregions with lower aquatic biodiversity.
Laurentian great lakes
The Laurentian Great Lakes were a high-risk ecoregion for crayfish invasions, as several species scored high for both likelihood and impact. The Great Lakes basin is a well-studied hotspot for invasive species, with over 180 freshwater species invasions documented (Pagnucco et al. 2015). This ecoregion also has the highest diversity of freshwater species in Canada, the highest proportion of those that are endangered, and the highest number of key biodiversity areas of global importance (Abell et al. 2008; Tognelli et al. 2017; COSEWIC 2018). This includes the highest diversity of native crayfishes (eight) in Canada including the vulnerable Creaserinus fodiens (Guiaşu 2021), the painted mudbug (Lacunicambarus polychromatus) recently discovered in the ecoregion (Jones et al. 2019), and F. propinquus, the primary prey of the endangered queensnake (Reid and Nocera 2015). Two invasive crayfish have established populations in the Canadian portion of the Great Lakes basin: rusty and Allegheny crayfishes, and a third is established in the US portion: the red swamp crayfish (Peters et al. 2014).
The rusty crayfish is native to the Ohio River drainage in the north central USA but has been introduced to at least 18 states and two provinces, likely through live bait-related introductions (Lodge et al. 2000), and although the invasive status and native range of this species is contentious in many regions (Guiaşu and Labib 2021), it has certainly expanded its range since the 1960s (Olden et al. 2006; Phillips et al. 2009b; Smith et al. 2019). Rusty crayfish are established in all of the Great Lakes and many smaller lakes within the ecoregion (Peters et al. 2014; O’Shaughnessey et al. 2021; iNaturalist contributors, iNaturalist 2022).
The Allegheny crayfish is established in Lake Huron and Lake Ontario and other smaller lakes in the area (Peters et al. 2014, iNaturalist 2021). White river crayfish is established (and considered native to) the portion of the ecoregion in the USA and has been found in the Canadian portion on the north side of Lake Erie (Peters et al. 2014; iNaturalist contributors, iNaturalist 2022). It is unclear if this range expansion is human-mediated or not.
Procambarus clarkii, the red swamp crayfish, is native to the southern USA and northeastern Mexico and has been globally distributed first through commercial aquaculture (Oficialdegui et al. 2019) and more recently via the biological supply and aquarium trades (Larson and Olden 2008; Banha et al. 2019). These vectors have led to established populations across Europe, Africa, Asia, and the Americas. The red swamp crayfish is considered a warm water species (Zhang et al. 2020), but has been shown to survive for months at low temperatures (Veselý et al. 2015; Haubrock et al. 2019), and has established populations in colder climates than its native range (e.g., Poland; Maciaszek et al. 2019). Red swamp crayfish is present in the ecoregion in US waters but has yet to be found in the Canadian portion of the Great Lakes (Peters et al. 2014; Smith 2018; O'Shaughnessey et al. 2021), although nearshore warm areas of the Canadian Great Lakes do provide suitable habitat (Egly et al. 2019).
In the Great Lakes ecoregion, invasive crayfish have recently increased in abundance and are having documented impacts on native ecology (Peters et al. 2014). While recent reports show that P. clarkii is bigger and more aggressive than F. rusticus (O'Shaughnesseyet al. 2021); overall, the dynamics between the two species and the impact that multiple NIS crayfish will have on native ecosystems is yet to be determined. The rusty and red swamp crayfish are among the best-studied crayfish globally, with widely documented impacts in invaded ecosystems (Bobeldyk and Lamberti 2010; Jackson et al. 2014; Carvalho et al. 2016; Kreps et al. 2016; Wellnitz et al. 2019).
St. Lawrence
The St. Lawrence ecoregion also is at considerable risk from crayfish invasions. This ecoregion is centered around the St. Lawrence River and surrounding wetlands and small lakes. This ecoregion has the second highest freshwater diversity in Canada, after the Great Lakes ecoregion (Abell et al. 2008), including native crayfish of which there are five species. This is the drainage route for the Great Lakes, a major shipping route, and has been heavily modified by humans (Hudon and Carignan 2008; Hudon et al. 2018). Like the adjacent Great Lakes ecoregion, the St. Lawrence ecoregion is most at risk from rusty and red swamp crayfish. Rusty crayfish are established in the western part of this ecoregion, near Ottawa, and in the portion of the ecoregion in the USA (Vermont) but red swamp crayfish are not yet present. Spiny-cheek crayfish, a moderate-risk invader, is also established in the ecoregion, primarily in the south, in Vermont. Although Allegheny crayfish are established in the southwest of this ecoregion, they received a lower score particularly on impact.
English–Winnipeg
The English–Winnipeg ecoregion includes the Lake of the Woods in Ontario and most of Manitoba and a small part of Saskatchewan. Large lakes such as Lake Winnipeg and Lake Winnipegosis dominate the freshwater landscape, in addition to many small shallow lakes typical of the Canadian shield. This ecoregion has relatively high freshwater biodiversity and several SARA-listed freshwater species including fish, amphibians, molluscs, and reptiles (Stewart and Watkinson 2004; Abell et al. 2008), many of which could be threatened by crayfish invasions. This ecoregion also has two native crayfish: virile and calico crayfish, and is most vulnerable to rusty crayfish invasion. Rusty crayfish is established in the Lake of the Woods and could spread to Lake Winnipeg, where it are currently not present. Rusty crayfish have been listed on the prohibited species list in Manitoba (Province of Manitoba 2021). The red swamp crayfish also is a high-risk invader, but scores over a point lower than the rusty crayfish. The red swamp crayfish is found in the Eastern Wild Rice region of Minnesota in this ecoregion but has yet to arrive in the Canadian portion of the ecoregion.
Coastal British Columbia
Coastal British Columbia is home to temperate river systems and small lakes with high freshwater biodiversity (Chu et al. 2003, 2015). There are no native crayfishes in coastal British Columbia, but the signal crayfish (native to the Okanagan) is present as an invasive species (Larson et al. 2012). A single individual red swamp crayfish was reported in the lower mainland of British Columbia (GBIF 2021), but it is unclear if this represents and new incursion or not. The red swamp crayfish scored slightly lower than the other crayfish in this ecoregion, since it prefers lentic habitats and much of the freshwater in coastal British Columbia is faster-flowing rivers but in habitats that are suitable for the red swamp crayfish, it is still a considerable and impactful invader. In the portion of this ecoregion in the USA, in Washington State, there are several more nonindigenous crayfish: Sanborn (Faxonius sanbornii), signal, virile, and white river crayfish (Larson and Olden 2011). This ecoregion is most at risk from signal crayfish, which are already established in much of the lower mainland, followed by the virile crayfish and the rusty crayfish which are not yet established in the ecoregion but pose a significant risk.
Signal crayfish (P. leniusculus) are native to the Columbia River basin, from British Columbia to Northern California, although there is considerable cryptic genetic diversity within both the species and genus (Larson et al. 2012, 2016). Signal crayfish have been intentionally stocked as fish forage globally (Hogger 1986; Kawai et al. 2004; Bohman et al. 2006; Velema et al. 2012) and have spread from these areas. Invasive signal crayfish have caused population reductions in an endangered native congener, Pacifastacus fortis (Light et al. 1995), the collapse of a rare three-spine stickleback (Taylor et al. 2006; Velema et al. 2012), among other wide-ranging impacts (see Supplementary Materials B).
The virile crayfish (F. virilis) is the most widespread crayfish in Canada, the native range extending from Quebec westward to Saskatchewan and south to some parts of Oklahoma and Texas (Phillips et al. 2009b). In Canada, the virile crayfish have been expanding westward into Alberta (McAlpine et al. 1999; Phillips et al. 2009a, 2009b; Williams et al. 2011) and eastward into New Brunswick (McAlpine et al. 2007) and its disjointed distribution suggests human-mediated spread, likely via bait buckets, although in the last two decades, it has been introduced via the aquarium trade to several countries in Europe (Ahern et al. 2008; Filipova et al. 2010; James et al. 2016; Roessink et al. 2017; Lemmers et al. 2021) and so this pathway cannot be ruled out for Canada. There is much less information on F. virilis impacts, particularly in situ, than the rusty, signal, or red swamp crayfish (Twardochleb et al. 2013), which contributed to larger uncertainty in the impact scores in our assessment (see Supplementary Materials B).
Marbled crayfish
In contrast with our initial hypothesis marbled crayfish (Procambarus f. virginalis) but known colloquially as Marmokrebs, scored lower risk to Canadian freshwater ecosystems. This species emerged in the German aquarium trade in 1995 as a parthenogenic, single-origin descendant of the Floridian species Procambarus fallax, the slough crayfish (Scholtz et al. 2002). The first individuals were found in the wild in lower Saxony, Germany, in the early 2000s and since there have been at least 25 independent confirmed introductions across Europe (Chucholl 2014) and into Africa and Asia (Jones et al. 2009; Kawai et al. 2009; Faulkes et al. 2012). These introductions have likely come from hobbyist aquarists dumping excess individuals in ponds or streams, although escape from open-air markets and bait buckets are also vectors of concern (DiStefano et al. 2009). Some of these releases have now resulted in stable wild populations in Europe and Madagascar (Jones et al. 2009; Chucholl and Pfeiffer 2010; Chucholl et al. 2012; Deidun et al. 2018; Andriantsoa et al. 2019). The risk of marbled crayfish has been evaluated in several different ecoregions. The first use of the Freshwater Invertebrate Invasiveness Scoring Kit (FI-ISK) applied to Italy classified marbled crayfish as medium risk (Tricarico et al. 2010), possibly because at the time only one individual had been found in the wild in Italy (Patoka et al. 2014). Since then, that tool has been used several times to estimate risk for marbled crayfish in several regions in Europe and each time Marmokrebs has been identified as high risk (Chucholl 2013; Patoka et al. 2014; Kotovska et al. 2016; Chucholl and Wendler 2017; Uderbayev et al. 2017; Weiperth 2019). Because of the invasion history and parthenogenic traits of this species, there is considerable concern that marbled crayfish could escape the pet trade in North America where it is extremely popular into natural habitats (Faulkes 2010, 2018). In North America, bioclimatic species distribution models predict the southeastern and south central USA, Mexico, and Cuba (i.e., warmer areas) would be the most likely to support populations of marbled crayfish (Feria and Faulkes 2011). Marbled crayfish is on a watch list for Great Lakes in Canada where it ranked “High” for environmental impact (GLANSRA; Davidson et al. 2021) but have yet to be spotted in the wild in North America. However, there is currently no monitoring regime in any region in Canada designed to detect marbled crayfish should they be introduced or escape into the wild.
There are several possible explanations for lower CMIST scores for marbled crayfish in Canada, both from the likelihood calculations and impact calculations. First, for likelihood of establishment, marbled crayfish scored slightly lower in environmental tolerances than other warm-water species (e.g., red swamp crayfish) in four of the 21 ecoregions assessed. Established and overwintering populations of marbled crayfish have been found in European countries with colder winter temperatures including Germany (Chucholl et al. 2012) and Czech Republic (Patoka et al. 2016), where lake temperatures under ice are likely less than 4 °C (Martin et al. 2010). In laboratory experiments, marbled crayfish can survive but not reproduce below 15 °C (Seitz et al. 2005), and mortality rapidly increases below 5 °C (Veselý et al. 2015; Haubrock et al. 2019), especially for smaller individuals (Kaldre et al. 2015). The climate in Canada is considerably colder than the current distribution of marbled crayfish in Europe and the CMIST score reflected this. The red swamp crayfish, a species with a warm native range, scored higher in the environmental match category than marbled crayfish, since it has established populations is the northern USA which has a substantial frost period and that was used for its cold tolerance calculations. While temperature seems to have played a minor part in a lower likelihood score, another area of lower scoring was in vectors and propagule pressure. When compared with the other crayfish that are established in Canada, that may arrive in a new region from human-assisted spread, the only vector for arrival is the aquarium trade. While this may be a substantial vector (Cohen et al. 2007), the CMIST tool is designed to act comparatively, so the crayfish species that scored higher were in at least three pathways of entry, versus only one vector for the marbled crayfish.
Similarly, in the impact section of the scoring rubric, the marbled crayfish had relatively lower scores with higher uncertainty. Although there are many records of marbled crayfish introductions, there is little information to support the impact section of the CMIST tool, which scores impacts on populations, communities, ecosystems, and habitats. Since most marbled crayfish introductions are relatively new, there is not yet extensive evidence that marbled crayfish introductions have caused habitat destruction or displaced native species. While we inferred a baseline level of impact based on impacts from congeneric species (with increased uncertainty due to necessary assumptions, as described by Drolet et al. 2016), assessors may need additional guidance on how to better assess species with new or limited invasion histories. Finally, while parthenogenic replication is a trait that might make marbled crayfish a unique invader, this tool does not use particular traits to score species, perhaps because traits are inconsistent predictors of invasion success (Hayes and Barry 2008).
Improvements to the tool
CMIST is intended as a rapid assessment tool, some elements may be coarser than desired. For example, species distribution models set by crayfish physiological tolerances (e.g., Larson and Olden 2012) may more accurately reflect potential range of invasion. Unfortunately, there are few published studies on physiological tolerances of most crayfish and we therefore relied on climatic conditions experienced by established populations in North America or Europe to infer a coarse estimate of temperature tolerances. The coarseness of these estimates is reflected in the associated certainty scores and crayfish may have broader or narrower environmental tolerances than reported, especially at the invasion fronts. This tool is also currently only applied to current climate regimes; however, as the climate warms, more areas of Canada will become more suitable to crayfish invasion since many of the invaders have native ranges with warmer climates. We recommend repeating this exercise considering the likely future climate in Canada and interactions between native and invasive crayfish under warmer temperatures (Gherardi et al. 2013). Finally, the CMIST tool could be improved by expanding beyond three levels of scores, to further encourage scoring differentiation between lack of evidence due to lack of impact versus lack of evidence due to recent invasion.
Policy and management considerations
Crayfish have a long history of translocation by humans for food, bait, pets, and scientific supply (e.g., Lodge et al. 2000; Scholtz et al. 2002; Larson and Olden 2008) but are subject to a patchwork of policies and regulations around their import or movement. For example, the aquarium trade in Canada and the USA is largely unregulated, contains many high-profile invasive species, and may pose high propagule pressure to regions with high human population density (Cohen et al. 2007; Banha et al. 2019; Chan et al. 2019). Other vectors like the live bait industry are variably regulated (DiStefano et al. 2009), and several provinces do not mention crayfish specifically in angling regulations. Two of the ecoregions with the highest risk of crayfish invasion, the Laurentian Great Lakes and the Pacific Coastal ecoregions are in Ontario and British Columbia, respectively, and which have among the least restrictive regulations on crayfish use as bait across Canada. In Ontario, although there are regulations against buying and transporting crayfish overland, crayfish are permitted to be used as bait in the same waterbody where they are caught while in British Columbia, crayfish may be used as bait in streams but not lakes. In British Columbia, there are no regulations that prohibit the sale of crayfish for bait use and no guidelines for potentially invasive crayfish while most of the other Canadian provinces (excluding Nova Scotia, PEI, and Newfoundland and Labrador) specifically prohibit the possession, purchasing, or use of crayfish as bait. These gaps and inconsistencies in regulations across Canada could facilitate the introduction and spread of invasive crayfish. Finally, while almost all angling regulations mention invasive species, crayfish are rarely listed among angling watchlist species. For example, none of the four current crayfish invaders in Ontario are on the prohibited species list, only the common yabby (Cherax destructor), which is an Australian species in the aquarium trade is regulated but not yet seen in the wild in North America.
The lack of recognition of important crayfish invaders in management policies or watchlists is a reflection of the general lack of information on crayfish in Canada. There are few recent distribution maps (Phillips et al. 2009b) and little information on temperature tolerances, ecology, and invasion dynamics. Finally, there is little information on the impact of current crayfish invasions and the rate of spread within Canada. Given that the risk evaluated here from some crayfish ranks alongside the risk posed by Asian carps and northern pike, crayfish invaders deserve more attention.
Our assessment identified both higher-risk crayfish species and Canadian ecoregions at risk of invasion such that preventing the introduction and spread of these species should be a priority. Changes to policy or regulations are an important step to reducing the likelihood of a crayfish invasion, including education and outreach such as adding high-risk crayfish (particularly rusty, red swamp, virile, and signal) to NIS watch lists (Davidson et al. 2021), but are unlikely to be fully effective. Thus, surveillance or early detection monitoring programs are essential, especially for those ecoregions with higher propagule pressure from multiple vectors (such as Laurentian Great Lakes, St. Lawrence, English–Winnipeg lakes, and Coastal British Columbia) and those transboundary ecoregions where existing populations in US portions (perhaps driven by lack of policy) could naturally spread into Canadian waters via majorly connected waterways (e.g., Upper Missouri, Great Lakes). In addition to traditional trapping surveys, large-scale surveys using eDNA have been suggested (Chucholl et al. 2021) with molecular markers available to detect rusty, red swamp, signal, and marbled crayfish (Treguier et al. 2014; Dougherty et al. 2016; Larson et al. 2017; Riascos et al. 2018; Mauvisseau 2019). Surveillance or early detection monitoring could be especially important for ecoregions without native crayfish, as the food webs in these ecoregions may be more vulnerable to a functionally unique invader.
For crayfish that are already well established in an ecoregion or following the detection of a new invader, management efforts should focus on containment. Admittedly, this is a challenge in larger systems but in-stream barriers have been successful at reducing the spread of some crayfish species (Kerby et al. 2005; Krieg and Zenker 2020; Krieg et al. 2021). These populations can also be targets for control efforts (Hein et al. 2007; Hansen et al. 2013; Green and Grosholz 2021). Most management efforts involve trapping to reduce densities (Hansen et al. 2017; Manfrin et al. 2019), but other techniques such as fish predation (Elvira et al. 1996; Hein et al. 2007), biocidal control (Cook and Moore 2008), and temporary drainage of a habitat (Krieg et al. 2020) have been applied with limited success. Although eradication is often desirable when populations are small and spatially constrained, management generally shifts to localized control to limit impacts to valued species or habitats (Drury and Rothlisberger 2008). Ecoregions with high native freshwater biodiversity, such as the Great Lakes, St. Lawrence, southern Manitoba, and British Columbia, are among the most vulnerable to crayfish invasion and defensive protection of these high conservation areas should be a priority.
Conclusions
Of the eight species assessed here, we found four were high risk to several Canadian freshwater ecoregions: rusty, signal, virile, and red swamp crayfish. Our risk assessment found these species have a high likelihood of arriving and large impacts once introduced. Each of these species has well-documented impacts globally where they have been introduced outside their native range. Furthermore, the overall risk is comparable with high-risk freshwater invaders such as Asian carps. Of the 21 freshwater ecoregions assessed, we found eight were at high risk due to crayfish invasions. Finally, we found that beyond the Great Lakes ecoregion, there was relatively little information on crayfish in Canada, and we highlight this as an understudied area for further research.
Acknowledgements
We are grateful to Keith Somers and two anonymous reviewers for their in-depth revisions, which significantly improved this manuscript.
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Published In
Canadian Journal of Fisheries and Aquatic Sciences
Volume 79 • Number 9 • September 2022
Pages: 1479 - 1496
History
Received: 8 September 2021
Accepted: 4 April 2022
Accepted manuscript online: 8 April 2022
Version of record online: 13 September 2022
Copyright
© 2022 The Author(s). This work is licensed under a Creative Commons Attribution 4.0 International License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author(s) and source are credited.
Data Availability Statement
Data are archived on Figshare at https://doi.org/10.6084/m9.figshare.19543792.v1. Code to run analyses is archived at https://doi.org/10.5281/zenodo.6422579.
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Author Contributions
NB collected the data, analyzed the data, and wrote the first draft; NB and TT contributed to the ideas, analytic methods, and writing.
Competing Interests
The authors declare no competing interests.
Funding Information
This research was supported by funding from DFO Science’s Aquatic Invasive Species program (TT); NB was supported by an NSERC PDF.
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Norah E.M. Brown and Thomas W. Therriault. 2022. The hidden risk of keystone invaders in Canada: a case study using nonindigenous crayfish. Canadian Journal of Fisheries and Aquatic Sciences.
79(9): 1479-1496. https://doi.org/10.1139/cjfas-2021-0245
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