Effects of elevated water velocity on the invasive rusty crayfish (Orconectes rusticus Girard, 1852) in a laboratory mesocosm

Effects of elevated water velocity on the invasive rusty crayfish (Orconectes rusticus Girard,... Abstract Invasions of the rusty crayfish Orconectes rusticus (Girard, 1852) in lakes have led to the local extirpation of resident crayfishes and altered littoral communities. The spread of O. rusticus into streams poses an equally serious threat to the biodiversity of resident crayfishes and fishes. We found that O. rusticus in northern Wisconsin streams were significantly smaller than O. rusticus from lakes (P < 0.001) and not significantly different than Faxonius propinquus (Girard, 1852) (P < 0.001) from lakes or streams. We tested time to reach a limited food resource, performance, in 4 water velocities, 5, 30, 50, and 66 cm sec–1, in a laboratory flume. Performance of O. rusticus and F. propinquus did not differ within water velocities, but was reduced in water velocities of 50 and 66 cm sec–1. Performance also did not differ between large and small O. rusticus within water velocity treatments but was also reduced at 50 and 66 cm sec–1. Performance of O. rusticus and F. propinquus from lakes, however, was significantly lower than that of O. rusticus from streams (P < 0.05). In all experiments, performance of crayfish in the 66 cm sec–1 treatment was below 50%, suggesting that this is a critical water velocity for O. rusticus and F. propinquus. Our results also suggest that stream segments with high velocities may reduce upstream dispersal rates of O. rusticus from lakes thus potentially reducing the spread to upstream lake ecosystems. INTRODUCTION Spread of nonindigenous freshwater species poses a serious threat to resident species and changing aquatic ecosystems worldwide (Gurevitch & Padilla, 2004; Strayer, 2010). Studies of the dispersal of nonindigenous species with a free-swimming life stage have identified many factors limiting dispersal after establishment (Johnson & Carlton, 1996; Hrabik & Magnuson, 1999; Kocovsky et al., 2011). In contrast, dispersal of benthic species lacking a free-swimming life stage has received relatively little attention even though these species can have similar effects on invaded ecosystems (Covich et al., 1999; Schreiber et al., 2003; Bohonak & Jenkins, 2003; Hoffman et al., 2006; Sepulveda & Marczak, 2012). Crayfishes are often considered apex consumers or ecosystem engineers in streams and lakes and are capable of controlling the ecosystem structure and function of these systems (Olsen et al., 1991; Charlebois & Lamberti, 1996; Lodge et al., 1998; Covich et al., 1999; Hill & Lodge, 1999; Lodge et al., 2000; Nystrom et al., 2001). The primary source of crayfish introduction may be due to the bait and aquarium sales (DiStefano et al., 2009; Mrugała et al., 2014). In lake districts in the northern Midwestern USA, crayfish introductions likely occur in lakes with subsequent dispersal into streams (Byron & Wilson, 2001; Puth & Allen, 2005; Foster & Keller, 2011). The spread of nonindigenous crayfishes, such as the rusty crayfish, Orconectes rusticus (Girard, 1852), in lakes is affected by a combination of abiotic and biotic factors. The dispersal of crayfish after establishment in lakes is restricted to the littoral zone with limited dispersal through the cold, low-oxygen waters of the hypolimnion (Wilson et al., 2004; Jansen et al., 2009). Increased refuge availability, e.g., cobble, large woody debris, or macrophytes, leads to increased invasion rates which can be as high as 0.68 km yr–1 (Wilson et al., 2004). Spread through the littoral zone is reduced in areas where refugia provided by cobble, large woody debris, or macrophytes is limited, potentially due to the risk of fish predation (Kershner & Lodge, 1995). Resident species may persist in marginal habitats not preferred by O. rusticus after an invasion (Garvey et al., 2003). The biotic factors affecting invasion success of O. rusticus in lakes have been attributed primarily to the larger average size relative to residents (DiDonato & Lodge, 1993; Hill & Lodge, 1995; 1999; Lodge et al., 2000). Larger average crayfish size increases reproductive output of females relative to residents and young O. rusticus have faster growth rates with higher survivorship (Hill et al., 1993). When competing for food and shelter, similar sized O. rusticus and native Faxonius propinquus (Girard, 1852) (formerly listed as Orconectes propinquus but recently placed in FaxoniusOrtmann, 1905 by Crandall & De Grave, 2017) are competitively equal, but O. rusticus is dominant if the carapace length is as little as 3 mm larger than F. propinquus (Hill & Lodge, 1999). Risk of predation is also decreased as crayfish size increases (Garvey et al., 1994; Hill & Lodge, 1999). Size may be the determining factor explaining the success of O. rusticus and other crayfishes in lake invasions. Invasion of streams by crayfish may differ from lakes, with a greater importance of abiotic factors compared to biotic factors. Abiotic forces, particularly flow and substrate composition, strongly influence invasion success of introduced fishes and crayfishes, as in Pacifastacus leniusculus (Dana, 1852) in European and North American streams (Moyle & Light, 1996a; 1996b; Light, 2003; Bubb et al., 2004; Marchetti et al., 2004; Leprieur et al., 2006; Propst et al., 2008; Clark et al., 2013). High flow often reduces upstream dispersal abilities of crayfishes and likely limits invader abundance (Light, 2003; Bubb et al., 2006; Cruz & Rebelo, 2007). High flow events can alter substrates and reduce the impacts of nonindigenous crayfish on prey by reducing invader abundances and may limit invasion success (Poff & Ward, 1989; Moyle & Light, 1996a, b; Gamradt & Kats, 1996; Light, 2003; Kerby et al., 2005; Marchetti & Moyle, 2010). In Europe, crayfish barriers allowed upstream migration of pelagic fishes, but reduced dispersal of benthic fishes and crayfishes (Frings et al., 2013). The upstream movement of benthic fishes and crayfishes was not affected by slope or roughness of the barrier but by a critical stream-flow velocity (0.65 cm sec–1) (Frings et al., 2013). There was a negative correlation in stream studies between stream flow velocity and the abundance of F. propinquus (Kutka et al., 1996). The effect of culverts on crayfish did not necessarily create barriers, but elevated flow velocities altered crayfish behavior and slowed and perhaps prevented upstream movement in some cases (Puth & Allen, 2005; Foster & Keller, 2011). Thus, elevated velocities combined with substrate characteristics may be key factors affecting invasion rates and successes. While conducting surveys in lakes and streams in northern Wisconsin and the Upper Peninsula of Michigan, we observed that O. rusticus were less common in higher flow streams and were often absent upstream of culverts or areas of elevated water velocity (WLP, pers. obs.). We also observed that O. rusticus in streams appeared smaller than O. rusticus in lakes particularly where substratum was sparse and water velocities were high. We hypothesized that elevated velocities may be affecting both the upstream dispersal and the size frequency distribution of O. rusticus. Based on these observations, we experimentally tested the hypothesis that size-matched O. rusticus and F. propinquus differed in their ability to perform in elevated water velocities. We then tested whether the size of O. rusticus affected performance in flow. We finally examined if O. rusticus and F. propinquus from lakes differed from O. rusticus from streams differed in their ability to deal with increased water velocities. MATERIALS AND METHODS Comparison of size frequency distributions in lakes and streams To test for differences in the size of crayfish individuals between lake and stream populations, we measured crayfish carapace lengths of O. rusticus from 12 lakes and 13 streams and F. propinquus from 6 lakes and 5 streams during the summers of 2003 to 2005 (Table 1). The length of carapaces was measured to the nearest 0.1 mm with Mitutoyo digital calipers (Mitutoyo, Aurora, IL, USA) and sex and reproductive form were recorded. Male crayfish alternate between a non-reproductive form (Form II: gonopods inflexible and white) in early summer to a reproductive from (Form I: gonopods threadlike and often orange) from late summer to spring. We used a mixed two-way analysis of variance with fixed effects of species (O. rusticus or F. propinquus), sex (male and female), and habitat type (lake or stream), and site (the stream or lake) as a random effect. All statistical analyses of carapace lengths were conducted using the R (R Core Team, 2017) and the car (Fox & Weisberg, 2011) and nlme (Pinheiro et al., 2017) packages. Pairwise comparisons of least squares means were performed with a Bonferroni correction using the LSMEANS package (Lenth, 2016). Table 1. Locations where Faxonius propinquus and Orconectes rustics were collected. Species  Location  Lat. (N)  Long. (W)  Number of individuals collected  Faxonius propinquus  Allequash Lake, WI  46o02ʹ  89o37ʹ  47    Little John Lake, WI  46°00ʹ  89°38ʹ  39    Long Lake, WI  45°50ʹ  88°40ʹ  51    Plum Lake, WI  45o59ʹ  89o31ʹ  10    South Turtle, WI  46°12ʹ  89°53ʹ  49    Trout Lake, WI  46°01ʹ  89°40ʹ  99    Allequash Creek, WI  46°01ʹ  89°39ʹ  57    Cisco Branch Ontonagon River, MI  46o17ʹ  89o04ʹ  42    Manitowish River, WI  46o07ʹ  89o39ʹ  47    Mill Creek, MI  42°09ʹ  86o15ʹ  36    Plum Creek, WI  45°58ʹ  89°32ʹ  70  Orconectes rusticus  Big Lake, WI  46°09ʹ  89°45ʹ  21    Birch Lake, WI  46o13ʹ  89o50ʹ  22    Bond Falls Flowage, MI  46o23ʹ  89o06ʹ  18    Little John Lake, WI  46°00ʹ  89°38ʹ  19    Papoose Lake, WI  46°10ʹ  89°48ʹ  20    Plum Lake, WI  45o59ʹ  89o31ʹ  50    Presque Isle Lake, WI  46°13ʹ  89°46ʹ  33    Star Lake, WI  46o01ʹ  89o28ʹ  22    South Turtle Lake, WI  46°12ʹ  89°53ʹ  32    Trout Lake, WI  46°01ʹ  89°40ʹ  265    Van Vliet Lake, WI  46o11ʹ  89o45ʹ  31    White Sand Lake, WI  46o05ʹ  89o35ʹ  20    Allequash Creek, WI  46°01ʹ  89°39ʹ  31    Bank Lick Creek, KY  39o02ʹ  84o29ʹ  19    Big Blue River, IN  39o20ʹ  85o59ʹ  19    Brandywine Creek, MI  41o57ʹ  86o23ʹ  16    Cherry Fork Creek, OH  38o55ʹ  83o39ʹ  51    Cisco Branch Ontonagon River, MI  46°21ʹ  89°04ʹ  54    Garrison Creek, KY  39o06ʹ  84o48ʹ  50    Manitowish River, WI  46o07ʹ  89o39ʹ  35    Plum Creek, WI  45o59ʹ  89o33ʹ  31    Middle Branch Ontonagon River, MI  46o14ʹ  89o09ʹ  21    Prairie River, WI  45o13ʹ  89o38ʹ  25    Roselawn Creek, MI  46o24ʹ  89o10ʹ  36    Wisconsin River, WI  44o54ʹ  89o29ʹ  42  Species  Location  Lat. (N)  Long. (W)  Number of individuals collected  Faxonius propinquus  Allequash Lake, WI  46o02ʹ  89o37ʹ  47    Little John Lake, WI  46°00ʹ  89°38ʹ  39    Long Lake, WI  45°50ʹ  88°40ʹ  51    Plum Lake, WI  45o59ʹ  89o31ʹ  10    South Turtle, WI  46°12ʹ  89°53ʹ  49    Trout Lake, WI  46°01ʹ  89°40ʹ  99    Allequash Creek, WI  46°01ʹ  89°39ʹ  57    Cisco Branch Ontonagon River, MI  46o17ʹ  89o04ʹ  42    Manitowish River, WI  46o07ʹ  89o39ʹ  47    Mill Creek, MI  42°09ʹ  86o15ʹ  36    Plum Creek, WI  45°58ʹ  89°32ʹ  70  Orconectes rusticus  Big Lake, WI  46°09ʹ  89°45ʹ  21    Birch Lake, WI  46o13ʹ  89o50ʹ  22    Bond Falls Flowage, MI  46o23ʹ  89o06ʹ  18    Little John Lake, WI  46°00ʹ  89°38ʹ  19    Papoose Lake, WI  46°10ʹ  89°48ʹ  20    Plum Lake, WI  45o59ʹ  89o31ʹ  50    Presque Isle Lake, WI  46°13ʹ  89°46ʹ  33    Star Lake, WI  46o01ʹ  89o28ʹ  22    South Turtle Lake, WI  46°12ʹ  89°53ʹ  32    Trout Lake, WI  46°01ʹ  89°40ʹ  265    Van Vliet Lake, WI  46o11ʹ  89o45ʹ  31    White Sand Lake, WI  46o05ʹ  89o35ʹ  20    Allequash Creek, WI  46°01ʹ  89°39ʹ  31    Bank Lick Creek, KY  39o02ʹ  84o29ʹ  19    Big Blue River, IN  39o20ʹ  85o59ʹ  19    Brandywine Creek, MI  41o57ʹ  86o23ʹ  16    Cherry Fork Creek, OH  38o55ʹ  83o39ʹ  51    Cisco Branch Ontonagon River, MI  46°21ʹ  89°04ʹ  54    Garrison Creek, KY  39o06ʹ  84o48ʹ  50    Manitowish River, WI  46o07ʹ  89o39ʹ  35    Plum Creek, WI  45o59ʹ  89o33ʹ  31    Middle Branch Ontonagon River, MI  46o14ʹ  89o09ʹ  21    Prairie River, WI  45o13ʹ  89o38ʹ  25    Roselawn Creek, MI  46o24ʹ  89o10ʹ  36    Wisconsin River, WI  44o54ʹ  89o29ʹ  42  View Large Effects of water velocity on performance in flow To test for effects of elevated water velocities on crayfish we used a laboratory recirculating flume where the time for crayfish to successfully move from a refugium to a food source was timed and used as an estimate of performance in flow (Fig. 1). Crayfish used in the experiment were collected from lakes and streams in northern Illinois and northern Wisconsin in late summer 2005 (Table 1). Streams from which crayfish were collected had mid-channel water velocities of approximately 25 cm sec–1 with maximum water velocities in faster flowing areas of 40 cm sec–1 during the summer. Crayfish were maintained in 15 large species-specific flow-through aquaria (115 l) with excess shelters and a 12:12h photoperiod. The effect of housing stream crayfish in non-flowing aquaria does not affect them in subsequent experiments (Pecor et al., 2008). Water temperatures were maintained at 20 oC and water velocities were less than 5 cm sec–1. Crayfish were fed an ad libitum diet of calcium enriched guinea pig food (Teklad GP Diet 7006) (Teklad, Indianapolis, IN, USA). Crayfish were acclimated to captive conditions for at least five days prior to experimental trials. No crayfish were held in captivity for more than 45 days. Figure 1. View largeDownload slide Recirculating flow chamber showing overhead view (A) and side view (B). Figure 1. View largeDownload slide Recirculating flow chamber showing overhead view (A) and side view (B). The recirculating laboratory flume consisted of two independent, parallel channels that were 157 cm long by 36 cm wide with collimators (mesh size = 1 cm) at the upstream and downstream ends of the channel. Water depth was maintained at 41 cm. The water was recirculated through two 30 cm diameter PVC pipes using two ¾ HP 90 volt DC motors controlled with a variable speed controller and three-blade propeller in the outflow pipe of the chamber. Water velocities could be controlled from 0 to 80 cm sec–1. In the trials, we used four fixed velocities: 5 cm sec–1, 30 cm sec–1, 50 cm sec–1, and 66 cm sec–1 measured in the center of the flume channels 2 cm above the substratum using a March McBirney Flo-Mate 2000 flow meter (Hach, Loveland, CO, USA). We also measured the water velocity across the chamber and the water velocity in the center: 50% of the channel was within 10% of the tested water velocity and this was the region most crayfish moved. The 33 cm sec–1 water velocity represented a commonly observed near-bed water velocities in the streams we sampled and is close to the slip speed of O. rusticus and F. propinquus (Maude & Williams, 1983). We used the 50 cm sec–1 water velocity because this as an upper summer velocity in our study streams having low crayfish populations, and the 66 cm sec–1 water velocity because this was the velocity at which the substrate in the flume was not mobile and was later shown to limit upstream dispersal in weirs (Frings et al., 2013). Due to the inability to collect sufficient numbers of crayfish during the experiment, we used a subset of these velocities in some experiments. The substrate in the chamber was composed a 10 cm layer of gravel (1.5 cm average diameter) with a gradual slope on the sides to ensure even water velocity across the chamber. To standardize hunger levels, crayfish were starved for 24 h (Hill & Lodge, 1999) and then placed in the experimental channel with the opening facing downstream and covered with a plexiglas plate prior to the start of the trial. A limited food item (5 ± 0.5 g piece of chicken liver) was placed upstream and the crayfish were allowed to exit the shelter. The time it took a crayfish to move from the downstream shelter to the upstream food source within a 60 min period was recorded. Initial tests revealed that the ability to reach the food source did not increase with longer trial durations. Each crayfish was used only once and then euthanized. Water velocity effects on O. rusticus and F. propinquus from streams To test for species-specific differences in the time required to successfully reach an upstream food item, male (Form I) O. rusticus and F. propinquus were tested on gravel substrates. Crayfish carapace lengths (CL), measured from tip of the rostrum to the end of the carapace, ranged 33–36 mm CL. Time required to reach the upstream food source was tested at four water velocities: 5 cm sec–1 (N = 24 O. rusticus, N = 26 F. propinquus), 30 cm sec–1 (N = 13 O. rusticus and N = 9 F. propinquus), 50 cm sec–1 (N = 23 O. rusticus and N = 22 F. propinquus), and 66 cm sec–1 (N = 10 O. rusticus and N = 5 F. propinquus). Comparison of time required to reach upstream food item in large and small O. rusticus To examine the elevated water velocity on size of male (Form I) O. rusticus, we determined the time required to reach an upstream food source for small (17–28 mm CL, N = 32) and large (34–43 mm CL, N = 32) O. rusticus. These size categories were one standard deviation larger and smaller than the mean sizes observed in streams. These tests were conducted in the experimental flume in four water velocities: 5 cm sec–1, 30 cm sec–1, 50 cm sec–1, and 66 cm sec–1. Comparison of the time required for O. rusticus and F. propinquus from lakes with O. rusticus from streams to reach the upstream food item To compare O. rusticus and F. propinquus from lakes with O. rusticus from streams in the time required to reach the upstream food item, we used water velocities of 5 cm sec–1, 30 cm sec–1, and 50 cm sec–1. We did not use the 66 cm sec–1 water velocity treatment due to the limited number of crayfish and poor performance at this velocity. Form II or non-reproductive male crayfish were used because we were not able to collect Form I males when the experiment was conducted. We used O. rusticus (N = 32) from Little John Lake and F. propinquus (N = 32) (26–38 mm CL) from Allequash Lake and O. rusticus from Allequash Creek (N = 24) in the three water velocities. No F. propinquus from streams were run in this experiment due to an inability to find enough individuals. Statistical analyses of movement rates in the flume We used the R survival package (Therneau, 2017) to perform a Kaplan-Meier survival analysis. Survival analysis allows for the use of censored data, observations where the event of interest (success in reaching the food source) did not occur by the end of an experimental trial. We allowed crayfish 60 min to reach the food source before the trial was ended. Omission of censored observations can cause bias when making comparisons or calculating medians and 95% confidence intervals from the time failure functions, but only for cases where > 50% of the individuals completed the trial. Confidence intervals are not symmetric due to the inclusion of censored values. Survival analysis provides a failure-time function of the proportion of crayfish that have reached the upstream food source. The analysis also allows an estimation of the restricted mean and standard error of the survival function while accounting for the censored data. We used the R survminer package (Kassambara & Kosinski, 2017) to perform a pairwise log-rank test with a Bonferroni correction on all pairwise combinations of treatments. A log-rank test is a nonparametric test used to compare pairwise right-skewed and censored data in the survival functions. RESULTS Mean crayfish size in streams versus lakes There was a significant interaction between species and lake or stream (F1,33 = 8.306, P = 0.0069). Orconectes rusticus from streams were significantly smaller than O. rusticus from lakes (P < 0.05) and not significantly different than F. propinquus from streams (P > 0.05) (Fig. 2). Figure 2. View largeDownload slide Box and whisker plot showing the median (horizontal line) and quartiles from lakes and streams where Orconectes rusticus and Faxonius propinquus were collected (Table 1). Orconectes rusticus and F. propinquus males in lakes and streams. Orconectes rusticus from lakes were significantly larger than O. rusticus from streams and also significantly larger than F. propinquus in lakes and streams (P < 0.05). Figure 2. View largeDownload slide Box and whisker plot showing the median (horizontal line) and quartiles from lakes and streams where Orconectes rusticus and Faxonius propinquus were collected (Table 1). Orconectes rusticus and F. propinquus males in lakes and streams. Orconectes rusticus from lakes were significantly larger than O. rusticus from streams and also significantly larger than F. propinquus in lakes and streams (P < 0.05). Experimental water velocity effects on O. rusticus and F. propinquus from streams The time required for crayfishes to reach the upstream food item increased significantly (P < 0.05) as water flow increased above 30 cm sec–1 (Fig. 3). Crayfish tended to walk in the middle section of the flume the majority of the time and did not use the edges due in part to the gravel added to the edges. There was, however, no significant difference (P > 0.05) between crayfish species within water velocity treatments (Fig. 3). The number of censored individuals increased dramatically at higher water velocities with only 2 of 10 O. rusticus and 2 out of 5 F. propinquus reaching the food resource preventing the calculation of median times as less than 50% reached the food source. Figure 3. View largeDownload slide Comparison of time required for size matched Orconectes rusticus and Faxonius propinquus to reach a food source at 4 water velocities using Kaplan-Meier survival probability (A). Median time (± 95% CI) at which 50% of the individuals have reached the limited food source (B). At higher water velocities, less than 50% of the crayfish reached the food source so no median is reported. A pairwise Log-Rank test was used to test for significant differences between groups using a Bonferroni adjusted p value using the survminer package (Kassambara & Kosinski 2017). Figure 3. View largeDownload slide Comparison of time required for size matched Orconectes rusticus and Faxonius propinquus to reach a food source at 4 water velocities using Kaplan-Meier survival probability (A). Median time (± 95% CI) at which 50% of the individuals have reached the limited food source (B). At higher water velocities, less than 50% of the crayfish reached the food source so no median is reported. A pairwise Log-Rank test was used to test for significant differences between groups using a Bonferroni adjusted p value using the survminer package (Kassambara & Kosinski 2017). Experimental water velocity effects on large and small O. rusticus The time required for large and small O. rusticus to reach the limited food resource increased significantly from 5 to 50 and to 66 cm sec–1 (P < 0.05) (Fig. 4). There were, however, no significant differences between these size classes of O. rusticus within water velocity treatments (P < 0.05). At 66 cm sec–1, 70% of the small O. rusticus were successful, whereas only 45% of the large individuals were successful (Fig. 4). Figure 4. View largeDownload slide Comparison time required for large (34–43 mm CL) versus small (17–28 mm CL) Orconectes rusticus to reach a food source at four water velocities using Kaplan-Meier survival probability (A). Median time (+/- 95% CI) at which 50% of the individuals reached the limited food source (B). At higher water velocities, less than 50% of the crayfish reached the food source so no median is reported. A pairwise Log-Rank test was used to test for significant differences between groups using a Bonferroni adjusted p value using the survminer package (Kassambara & Kosinski, 2017). Figure 4. View largeDownload slide Comparison time required for large (34–43 mm CL) versus small (17–28 mm CL) Orconectes rusticus to reach a food source at four water velocities using Kaplan-Meier survival probability (A). Median time (+/- 95% CI) at which 50% of the individuals reached the limited food source (B). At higher water velocities, less than 50% of the crayfish reached the food source so no median is reported. A pairwise Log-Rank test was used to test for significant differences between groups using a Bonferroni adjusted p value using the survminer package (Kassambara & Kosinski, 2017). Experimental water velocity effects on O. rusticus and F. propinquus from lakes and streams Form II male O. rusticus from streams reached the food source significantly faster than O. rusticus and F. propinquus from lakes at 30 and 50 cm sec–1 (P < 0.05) (Fig. 5). Orconectes rusticus from lakes took significantly longer than F. propinquus from lakes and O. rusticus from streams to reach the food source in the 5 cm sec–1 treatment (P < 0.05) (Fig. 5). Orconectes rusticus and F. propinquus from lakes did not differ significantly in their performance in flow at 30 and 50 cm sec–1 as in the prior experiment (P > 0.05) (Fig. 5). Orconectes rusticus and F. propinquus from lakes took significantly longer to reach the food source as water velocity was increased from 5 to 30 and 30 to 50 cm sec–1 (P < 0.05) (Fig. 5). The number of individuals from lakes reaching the limited food source at 66 cm sec–1 was less than 35% for both O. rusticus and F. propinquus, thus median times are unavailable but were significantly longer than O. rusticus from streams (P < 0.05) (Fig. 5). Figure 5. View largeDownload slide Comparison of the time required for size matched Orconectes rusticus and Faxonius propinquus from lakes and O. rusticus from streams to reach a food source at 4 water velocities using Kaplan-Meier survival probability (A). Median time (± 95% CI) at which 50% of the individuals reached the limited food source (B). At higher water velocities, less than 50% of the crayfish reached the food source so no median is reported. A pairwise Log-Rank test was used to test for significant differences between groups using a Bonferroni adjusted P value using the survminer package (Kassambara & Kosinski, 2017). Figure 5. View largeDownload slide Comparison of the time required for size matched Orconectes rusticus and Faxonius propinquus from lakes and O. rusticus from streams to reach a food source at 4 water velocities using Kaplan-Meier survival probability (A). Median time (± 95% CI) at which 50% of the individuals reached the limited food source (B). At higher water velocities, less than 50% of the crayfish reached the food source so no median is reported. A pairwise Log-Rank test was used to test for significant differences between groups using a Bonferroni adjusted P value using the survminer package (Kassambara & Kosinski, 2017). DISCUSSION Our results show that Orconectes rusticus in streams are smaller than those in lakes we sampled in northern Wisconsin. Our results also suggest that both O. rusticus and F. propinquus have limited abilities to tolerate water velocities in excess of 50 cm sec–1. In particular, lake individuals had a reduced ability to tolerate water velocities greater than 30 cm sec–1. In northern Wisconsin, O. rusticus introductions likely occur in lakes with the potential for subsequent dispersal through streams to other lakes. The existence of higher flow areas, especially in culverts or natural high flow areas, could have the potential to reduce, but not prevent the rate, of the spread of O. rusticus through streams. The larger size of O. rusticus in lakes is largely responsible for the success of O. rusticus, but in streams this size difference is absent. The effect of higher water velocities on crayfish combined with the smaller average size of O. rusticus has the potential to reduce the success of O. rusticus in streams. The idea that elevated water velocities could alter dispersal in streams is especially well known for fishes and has been used to limit dispersal of nonindigenous crayfishes in Europe (Frings et al., 2013). Fish dispersal is significantly reduced in areas of elevated water velocities and culvert pipes, particularly for benthic fishes (Wheeler et al., 2006; Noonan et al., 2011). European resource managers have attempted to utilize structures that increase water velocity over smooth surfaces to control the dispersal of invasive crayfishes to new habitats (Kerby et al., 2005; Frings et al., 2013). The effectiveness of these structures has been dependent on maintaining water velocity greater than 60 cm sec–1 and other factors, e.g., roughness of surfaces and slope, were found to be less important (Frings et al., 2013). Field studies have also shown that dispersal of crayfish species appears to be strongly influenced by elevated water velocities and in particular flood events (Light, 2003; Bubb et al., 2004). It is noteworthy that these studies have shown that water velocities in excess of 30–50 cm sec–1 have the greatest effect on dispersal (Maude & Williams, 1983; Kerby et al., 2005; Clark et al., 2008; Foster & Keller, 2011), consistent with the results found here. Higher turbulence associated with increased water velocities could, however, increase orientation efficiency helping them find the food source (Moore & Grills, 1999). Field studies have highlighted the importance of water velocities and substrates as key factors affecting crayfishes in streams (Light, 2003; Bubb et al., 2004, 2005; Bobeldyk & Lamberti, 2008). The size of native crayfish did not differ between environments, but non-native crayfish were larger in the lakes than in streams. Individuals of O. rusticus were smaller in streams (Fig. 2) and larger individuals (> 40 mm carapace length) were rare. In contrast, the sizes of stream F. propinquus were not reduced relative to those in lakes possibly because their maximum size is smaller on average than O. rusticus and their chelae are shorter and broader (Tierney et al., 2000). Broad, short chelae were found in crayfishes from high-velocity habitats compared to those from low-velocity habitats and could be useful to deflect water when velocities increase (Perry et al., 2013). Although our study was not designed to examined differences within streams or the effect of cobble, we did observe larger individuals in low- flow areas and in areas with larger, more complex cobble substrates. Size differences of crayfishes have been shown to also differ between areas of different water velocities (e.g., Clark et al., 2008). We did not measure the chelae of individuals, but it is possible that the larger chelae of O. rusticus may be a disadvantage in streams relative to F. propinquus (Roth & Kitchell, 2005). The smaller size of O. rusticus observed in streams may decrease the competitive advantage of O. rusticus relative to other crayfishes in streams and may also reduce ecosystem effects compared to those observed in lakes. Although other field observations and laboratory trials have suggested that larger crayfish individuals are more negatively affected by flow compared to small crayfish (Light, 2003), we did not observe an effect of size in our experiments. Differences between performance of large (34–43 mm) versus small (17–28 mm) O. rusticus at the water velocities tested were not observed, and elevated water velocities affected both size classes significantly (Fig. 4). This is in contrast to laboratory studies of O. rusticus and F. propinquus that showed larger individuals experienced greater drag (Maude & Williams, 1983). In field studies of invasions of Pacifastacus leniusculus in streams, larger individuals were more negatively affected by flow and invasions tended to occur predominately downstream (Light, 2003; Bubb et al., 2004). The interaction of substrates and flow may favor small crayfish, such as Faxonius obscurus (Hagen, 1870), which are able to occupy refugia, unavailable to larger crayfish, allowing them to occupy areas of greater water velocities (Clark et al., 2008), but a heterogeneous distribution of substrates could still limit upstream dispersal because crayfish would be required to experience the full effect of flow in sand flats. Thus, carapace body size alone may not be a good indicator of susceptibility to flow. Factors other than carapace size could be more important, and size itself may be confounded by flow conditions in the habitat of origin. The larger body sizes that exist in lakes were not common in streams, thus our experiments may have used too small of a size range. The steams where these crayfish were collected did not have velocities in excess of 40 cm sec–1, but the large-size crayfish could be removed from these ecosystems during spring and fall floods when water velocities are much higher. More noteworthy is the possibility that the crayfish may have come from a flow environment that had predisposed them to dealing with flow. The absence of larger crayfish individuals in streams suggests elevated water velocity has an effect but because of their absence we could not experimentally test for an effect. Beyond body size, there are indications that the size of chelae might be an important factor. We used Form II individuals for the comparison between species of lake and stream crayfishes, and they had smaller chelae than Form I individuals. The use of Form II crayfish may explain why O. rusticus from streams performed better in elevated flow relative to individuals from the other two experiments, where Form I crayfish were used. Unfortunately, it is not possible to test differences between Form I and Form II crayfish because the two forms do not coexist in nature for long enough to use in experiments without the risk of molting affecting behavior. We did not observe differences in behavior between the two reproductive states, but this should be studied in future experiments. Because our results indicate that chelae size may play a role in the ability of crayfish to interact with elevated water velocity, this might mean that Form II crayfish are more capable of dispersal into higher flow environments. Support for the idea that crayfishes might differ in their ability to deal with flow depending on their habitat of origin is further exemplified by the performance differences between O. rusticus from streams and O. rusticus and F. propinquus from lakes (Fig. 5). In trials testing performance at 5 cm sec–1, O. rusticus from lakes took longer to reach the food source than other crayfishes but all individuals completed the trials significantly faster than in all other treatment (P < 0.05) (Fig. 5). Lake crayfish species took significantly longer than stream O. rusticus when water velocity was increased to 30 and 50 cm sec–1 We did not include results from the 66 cm sec–1 treatment because less than 10% of the lake crayfish species completed the trials. The most striking difference between the lake and stream crayfishes was that stream individuals adopted a streamlined body posture, whereas lake crayfish individuals did not (Maude & Williams, 1983). These results suggest that there may be behavioral differences between these populations and success may be reduced if introductions occur with individuals from lakes to streams. Crayfishes from lakes, however, were observed standing with their bodies higher off the substrate and often moving their chelae in ways which increased drag on the individuals just prior to loss of contact with the substrate. These observations indicate that crayfishes may be preadapted to flow conditions in their habitat of origin and do not readily adjust to different flow environments. Our study provides a better understanding of the role of elevated water velocity on O. rusticus invasion dynamics by experimentally testing the effect of elevated water velocities on their performance. Our results provide valuable insight into the understanding of crayfish invasions in lotic versus lentic environments. In areas having numerous lakes, Short stream segments with low water velocities may act as corridors for invasion in areas having numerous lakes, whereas streams with culverts or high flow areas where there are limited refugia may limit dispersal (Puth & Allen, 2005). Because size is a key component for success in lakes, the abiotic effects of streams have the potential to alter O. rusticus invasions in lakes. Dispersal of large O. rusticus into lakes is thus likely to be limited by the high flow velocities experienced in streams, as well as lotic factors such as fish predation pressure (DiDonato & Lodge, 1993; Hill & Lodge, 1999), habitat availability (Hill & Lodge, 1995; 1999), and interactions with congeners (Hill & Lodge, 1994; 1995; 1999). The relative importance of factors explaining the success of O. rusticus invasions may shift from abiotic factors (such as water velocity or barriers) in high-gradient streams, to biotic factors (such as competition and predation) in low-gradient streams or lakes. This framework may provide new tools to limiting the spread of this and other benthic invasive species in freshwater ecosystems. ACKNOWLEDGEMENTS We acknowledge the comments and suggestions from Eric Peterson and Scott Sakaluk for their help in designing the experiment. We also thank Steve Juliano for his advice on statistical analyses. We are also grateful for suggestions and comments by Catherine O’Reilly and two anonymous reviewers, whose input dramatically improved the manuscript. Alboukadel Kassambara (Department of Biological Hematology, Montpellier, France) is acknowledged for his work on the pairwise tests of survival functions in the survminer R package. Jim Dunham was instrumental in helping design and build the flow chamber, without his help this would not have been possible. Funding for this project was in part from the Illinois State University Beta Lambda Chapter of the Phi Sigma Biological Honor Society. REFERENCES Bobeldyk, A.M. & Lamberti, G.A. 2008. A decade after invasion: Evaluating the continuing effects of rusty crayfish on a Michigan River. Journal of Great Lakes Research , 34: 265– 275. 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Effects of elevated water velocity on the invasive rusty crayfish (Orconectes rusticus Girard, 1852) in a laboratory mesocosm

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Abstract

Abstract Invasions of the rusty crayfish Orconectes rusticus (Girard, 1852) in lakes have led to the local extirpation of resident crayfishes and altered littoral communities. The spread of O. rusticus into streams poses an equally serious threat to the biodiversity of resident crayfishes and fishes. We found that O. rusticus in northern Wisconsin streams were significantly smaller than O. rusticus from lakes (P < 0.001) and not significantly different than Faxonius propinquus (Girard, 1852) (P < 0.001) from lakes or streams. We tested time to reach a limited food resource, performance, in 4 water velocities, 5, 30, 50, and 66 cm sec–1, in a laboratory flume. Performance of O. rusticus and F. propinquus did not differ within water velocities, but was reduced in water velocities of 50 and 66 cm sec–1. Performance also did not differ between large and small O. rusticus within water velocity treatments but was also reduced at 50 and 66 cm sec–1. Performance of O. rusticus and F. propinquus from lakes, however, was significantly lower than that of O. rusticus from streams (P < 0.05). In all experiments, performance of crayfish in the 66 cm sec–1 treatment was below 50%, suggesting that this is a critical water velocity for O. rusticus and F. propinquus. Our results also suggest that stream segments with high velocities may reduce upstream dispersal rates of O. rusticus from lakes thus potentially reducing the spread to upstream lake ecosystems. INTRODUCTION Spread of nonindigenous freshwater species poses a serious threat to resident species and changing aquatic ecosystems worldwide (Gurevitch & Padilla, 2004; Strayer, 2010). Studies of the dispersal of nonindigenous species with a free-swimming life stage have identified many factors limiting dispersal after establishment (Johnson & Carlton, 1996; Hrabik & Magnuson, 1999; Kocovsky et al., 2011). In contrast, dispersal of benthic species lacking a free-swimming life stage has received relatively little attention even though these species can have similar effects on invaded ecosystems (Covich et al., 1999; Schreiber et al., 2003; Bohonak & Jenkins, 2003; Hoffman et al., 2006; Sepulveda & Marczak, 2012). Crayfishes are often considered apex consumers or ecosystem engineers in streams and lakes and are capable of controlling the ecosystem structure and function of these systems (Olsen et al., 1991; Charlebois & Lamberti, 1996; Lodge et al., 1998; Covich et al., 1999; Hill & Lodge, 1999; Lodge et al., 2000; Nystrom et al., 2001). The primary source of crayfish introduction may be due to the bait and aquarium sales (DiStefano et al., 2009; Mrugała et al., 2014). In lake districts in the northern Midwestern USA, crayfish introductions likely occur in lakes with subsequent dispersal into streams (Byron & Wilson, 2001; Puth & Allen, 2005; Foster & Keller, 2011). The spread of nonindigenous crayfishes, such as the rusty crayfish, Orconectes rusticus (Girard, 1852), in lakes is affected by a combination of abiotic and biotic factors. The dispersal of crayfish after establishment in lakes is restricted to the littoral zone with limited dispersal through the cold, low-oxygen waters of the hypolimnion (Wilson et al., 2004; Jansen et al., 2009). Increased refuge availability, e.g., cobble, large woody debris, or macrophytes, leads to increased invasion rates which can be as high as 0.68 km yr–1 (Wilson et al., 2004). Spread through the littoral zone is reduced in areas where refugia provided by cobble, large woody debris, or macrophytes is limited, potentially due to the risk of fish predation (Kershner & Lodge, 1995). Resident species may persist in marginal habitats not preferred by O. rusticus after an invasion (Garvey et al., 2003). The biotic factors affecting invasion success of O. rusticus in lakes have been attributed primarily to the larger average size relative to residents (DiDonato & Lodge, 1993; Hill & Lodge, 1995; 1999; Lodge et al., 2000). Larger average crayfish size increases reproductive output of females relative to residents and young O. rusticus have faster growth rates with higher survivorship (Hill et al., 1993). When competing for food and shelter, similar sized O. rusticus and native Faxonius propinquus (Girard, 1852) (formerly listed as Orconectes propinquus but recently placed in FaxoniusOrtmann, 1905 by Crandall & De Grave, 2017) are competitively equal, but O. rusticus is dominant if the carapace length is as little as 3 mm larger than F. propinquus (Hill & Lodge, 1999). Risk of predation is also decreased as crayfish size increases (Garvey et al., 1994; Hill & Lodge, 1999). Size may be the determining factor explaining the success of O. rusticus and other crayfishes in lake invasions. Invasion of streams by crayfish may differ from lakes, with a greater importance of abiotic factors compared to biotic factors. Abiotic forces, particularly flow and substrate composition, strongly influence invasion success of introduced fishes and crayfishes, as in Pacifastacus leniusculus (Dana, 1852) in European and North American streams (Moyle & Light, 1996a; 1996b; Light, 2003; Bubb et al., 2004; Marchetti et al., 2004; Leprieur et al., 2006; Propst et al., 2008; Clark et al., 2013). High flow often reduces upstream dispersal abilities of crayfishes and likely limits invader abundance (Light, 2003; Bubb et al., 2006; Cruz & Rebelo, 2007). High flow events can alter substrates and reduce the impacts of nonindigenous crayfish on prey by reducing invader abundances and may limit invasion success (Poff & Ward, 1989; Moyle & Light, 1996a, b; Gamradt & Kats, 1996; Light, 2003; Kerby et al., 2005; Marchetti & Moyle, 2010). In Europe, crayfish barriers allowed upstream migration of pelagic fishes, but reduced dispersal of benthic fishes and crayfishes (Frings et al., 2013). The upstream movement of benthic fishes and crayfishes was not affected by slope or roughness of the barrier but by a critical stream-flow velocity (0.65 cm sec–1) (Frings et al., 2013). There was a negative correlation in stream studies between stream flow velocity and the abundance of F. propinquus (Kutka et al., 1996). The effect of culverts on crayfish did not necessarily create barriers, but elevated flow velocities altered crayfish behavior and slowed and perhaps prevented upstream movement in some cases (Puth & Allen, 2005; Foster & Keller, 2011). Thus, elevated velocities combined with substrate characteristics may be key factors affecting invasion rates and successes. While conducting surveys in lakes and streams in northern Wisconsin and the Upper Peninsula of Michigan, we observed that O. rusticus were less common in higher flow streams and were often absent upstream of culverts or areas of elevated water velocity (WLP, pers. obs.). We also observed that O. rusticus in streams appeared smaller than O. rusticus in lakes particularly where substratum was sparse and water velocities were high. We hypothesized that elevated velocities may be affecting both the upstream dispersal and the size frequency distribution of O. rusticus. Based on these observations, we experimentally tested the hypothesis that size-matched O. rusticus and F. propinquus differed in their ability to perform in elevated water velocities. We then tested whether the size of O. rusticus affected performance in flow. We finally examined if O. rusticus and F. propinquus from lakes differed from O. rusticus from streams differed in their ability to deal with increased water velocities. MATERIALS AND METHODS Comparison of size frequency distributions in lakes and streams To test for differences in the size of crayfish individuals between lake and stream populations, we measured crayfish carapace lengths of O. rusticus from 12 lakes and 13 streams and F. propinquus from 6 lakes and 5 streams during the summers of 2003 to 2005 (Table 1). The length of carapaces was measured to the nearest 0.1 mm with Mitutoyo digital calipers (Mitutoyo, Aurora, IL, USA) and sex and reproductive form were recorded. Male crayfish alternate between a non-reproductive form (Form II: gonopods inflexible and white) in early summer to a reproductive from (Form I: gonopods threadlike and often orange) from late summer to spring. We used a mixed two-way analysis of variance with fixed effects of species (O. rusticus or F. propinquus), sex (male and female), and habitat type (lake or stream), and site (the stream or lake) as a random effect. All statistical analyses of carapace lengths were conducted using the R (R Core Team, 2017) and the car (Fox & Weisberg, 2011) and nlme (Pinheiro et al., 2017) packages. Pairwise comparisons of least squares means were performed with a Bonferroni correction using the LSMEANS package (Lenth, 2016). Table 1. Locations where Faxonius propinquus and Orconectes rustics were collected. Species  Location  Lat. (N)  Long. (W)  Number of individuals collected  Faxonius propinquus  Allequash Lake, WI  46o02ʹ  89o37ʹ  47    Little John Lake, WI  46°00ʹ  89°38ʹ  39    Long Lake, WI  45°50ʹ  88°40ʹ  51    Plum Lake, WI  45o59ʹ  89o31ʹ  10    South Turtle, WI  46°12ʹ  89°53ʹ  49    Trout Lake, WI  46°01ʹ  89°40ʹ  99    Allequash Creek, WI  46°01ʹ  89°39ʹ  57    Cisco Branch Ontonagon River, MI  46o17ʹ  89o04ʹ  42    Manitowish River, WI  46o07ʹ  89o39ʹ  47    Mill Creek, MI  42°09ʹ  86o15ʹ  36    Plum Creek, WI  45°58ʹ  89°32ʹ  70  Orconectes rusticus  Big Lake, WI  46°09ʹ  89°45ʹ  21    Birch Lake, WI  46o13ʹ  89o50ʹ  22    Bond Falls Flowage, MI  46o23ʹ  89o06ʹ  18    Little John Lake, WI  46°00ʹ  89°38ʹ  19    Papoose Lake, WI  46°10ʹ  89°48ʹ  20    Plum Lake, WI  45o59ʹ  89o31ʹ  50    Presque Isle Lake, WI  46°13ʹ  89°46ʹ  33    Star Lake, WI  46o01ʹ  89o28ʹ  22    South Turtle Lake, WI  46°12ʹ  89°53ʹ  32    Trout Lake, WI  46°01ʹ  89°40ʹ  265    Van Vliet Lake, WI  46o11ʹ  89o45ʹ  31    White Sand Lake, WI  46o05ʹ  89o35ʹ  20    Allequash Creek, WI  46°01ʹ  89°39ʹ  31    Bank Lick Creek, KY  39o02ʹ  84o29ʹ  19    Big Blue River, IN  39o20ʹ  85o59ʹ  19    Brandywine Creek, MI  41o57ʹ  86o23ʹ  16    Cherry Fork Creek, OH  38o55ʹ  83o39ʹ  51    Cisco Branch Ontonagon River, MI  46°21ʹ  89°04ʹ  54    Garrison Creek, KY  39o06ʹ  84o48ʹ  50    Manitowish River, WI  46o07ʹ  89o39ʹ  35    Plum Creek, WI  45o59ʹ  89o33ʹ  31    Middle Branch Ontonagon River, MI  46o14ʹ  89o09ʹ  21    Prairie River, WI  45o13ʹ  89o38ʹ  25    Roselawn Creek, MI  46o24ʹ  89o10ʹ  36    Wisconsin River, WI  44o54ʹ  89o29ʹ  42  Species  Location  Lat. (N)  Long. (W)  Number of individuals collected  Faxonius propinquus  Allequash Lake, WI  46o02ʹ  89o37ʹ  47    Little John Lake, WI  46°00ʹ  89°38ʹ  39    Long Lake, WI  45°50ʹ  88°40ʹ  51    Plum Lake, WI  45o59ʹ  89o31ʹ  10    South Turtle, WI  46°12ʹ  89°53ʹ  49    Trout Lake, WI  46°01ʹ  89°40ʹ  99    Allequash Creek, WI  46°01ʹ  89°39ʹ  57    Cisco Branch Ontonagon River, MI  46o17ʹ  89o04ʹ  42    Manitowish River, WI  46o07ʹ  89o39ʹ  47    Mill Creek, MI  42°09ʹ  86o15ʹ  36    Plum Creek, WI  45°58ʹ  89°32ʹ  70  Orconectes rusticus  Big Lake, WI  46°09ʹ  89°45ʹ  21    Birch Lake, WI  46o13ʹ  89o50ʹ  22    Bond Falls Flowage, MI  46o23ʹ  89o06ʹ  18    Little John Lake, WI  46°00ʹ  89°38ʹ  19    Papoose Lake, WI  46°10ʹ  89°48ʹ  20    Plum Lake, WI  45o59ʹ  89o31ʹ  50    Presque Isle Lake, WI  46°13ʹ  89°46ʹ  33    Star Lake, WI  46o01ʹ  89o28ʹ  22    South Turtle Lake, WI  46°12ʹ  89°53ʹ  32    Trout Lake, WI  46°01ʹ  89°40ʹ  265    Van Vliet Lake, WI  46o11ʹ  89o45ʹ  31    White Sand Lake, WI  46o05ʹ  89o35ʹ  20    Allequash Creek, WI  46°01ʹ  89°39ʹ  31    Bank Lick Creek, KY  39o02ʹ  84o29ʹ  19    Big Blue River, IN  39o20ʹ  85o59ʹ  19    Brandywine Creek, MI  41o57ʹ  86o23ʹ  16    Cherry Fork Creek, OH  38o55ʹ  83o39ʹ  51    Cisco Branch Ontonagon River, MI  46°21ʹ  89°04ʹ  54    Garrison Creek, KY  39o06ʹ  84o48ʹ  50    Manitowish River, WI  46o07ʹ  89o39ʹ  35    Plum Creek, WI  45o59ʹ  89o33ʹ  31    Middle Branch Ontonagon River, MI  46o14ʹ  89o09ʹ  21    Prairie River, WI  45o13ʹ  89o38ʹ  25    Roselawn Creek, MI  46o24ʹ  89o10ʹ  36    Wisconsin River, WI  44o54ʹ  89o29ʹ  42  View Large Effects of water velocity on performance in flow To test for effects of elevated water velocities on crayfish we used a laboratory recirculating flume where the time for crayfish to successfully move from a refugium to a food source was timed and used as an estimate of performance in flow (Fig. 1). Crayfish used in the experiment were collected from lakes and streams in northern Illinois and northern Wisconsin in late summer 2005 (Table 1). Streams from which crayfish were collected had mid-channel water velocities of approximately 25 cm sec–1 with maximum water velocities in faster flowing areas of 40 cm sec–1 during the summer. Crayfish were maintained in 15 large species-specific flow-through aquaria (115 l) with excess shelters and a 12:12h photoperiod. The effect of housing stream crayfish in non-flowing aquaria does not affect them in subsequent experiments (Pecor et al., 2008). Water temperatures were maintained at 20 oC and water velocities were less than 5 cm sec–1. Crayfish were fed an ad libitum diet of calcium enriched guinea pig food (Teklad GP Diet 7006) (Teklad, Indianapolis, IN, USA). Crayfish were acclimated to captive conditions for at least five days prior to experimental trials. No crayfish were held in captivity for more than 45 days. Figure 1. View largeDownload slide Recirculating flow chamber showing overhead view (A) and side view (B). Figure 1. View largeDownload slide Recirculating flow chamber showing overhead view (A) and side view (B). The recirculating laboratory flume consisted of two independent, parallel channels that were 157 cm long by 36 cm wide with collimators (mesh size = 1 cm) at the upstream and downstream ends of the channel. Water depth was maintained at 41 cm. The water was recirculated through two 30 cm diameter PVC pipes using two ¾ HP 90 volt DC motors controlled with a variable speed controller and three-blade propeller in the outflow pipe of the chamber. Water velocities could be controlled from 0 to 80 cm sec–1. In the trials, we used four fixed velocities: 5 cm sec–1, 30 cm sec–1, 50 cm sec–1, and 66 cm sec–1 measured in the center of the flume channels 2 cm above the substratum using a March McBirney Flo-Mate 2000 flow meter (Hach, Loveland, CO, USA). We also measured the water velocity across the chamber and the water velocity in the center: 50% of the channel was within 10% of the tested water velocity and this was the region most crayfish moved. The 33 cm sec–1 water velocity represented a commonly observed near-bed water velocities in the streams we sampled and is close to the slip speed of O. rusticus and F. propinquus (Maude & Williams, 1983). We used the 50 cm sec–1 water velocity because this as an upper summer velocity in our study streams having low crayfish populations, and the 66 cm sec–1 water velocity because this was the velocity at which the substrate in the flume was not mobile and was later shown to limit upstream dispersal in weirs (Frings et al., 2013). Due to the inability to collect sufficient numbers of crayfish during the experiment, we used a subset of these velocities in some experiments. The substrate in the chamber was composed a 10 cm layer of gravel (1.5 cm average diameter) with a gradual slope on the sides to ensure even water velocity across the chamber. To standardize hunger levels, crayfish were starved for 24 h (Hill & Lodge, 1999) and then placed in the experimental channel with the opening facing downstream and covered with a plexiglas plate prior to the start of the trial. A limited food item (5 ± 0.5 g piece of chicken liver) was placed upstream and the crayfish were allowed to exit the shelter. The time it took a crayfish to move from the downstream shelter to the upstream food source within a 60 min period was recorded. Initial tests revealed that the ability to reach the food source did not increase with longer trial durations. Each crayfish was used only once and then euthanized. Water velocity effects on O. rusticus and F. propinquus from streams To test for species-specific differences in the time required to successfully reach an upstream food item, male (Form I) O. rusticus and F. propinquus were tested on gravel substrates. Crayfish carapace lengths (CL), measured from tip of the rostrum to the end of the carapace, ranged 33–36 mm CL. Time required to reach the upstream food source was tested at four water velocities: 5 cm sec–1 (N = 24 O. rusticus, N = 26 F. propinquus), 30 cm sec–1 (N = 13 O. rusticus and N = 9 F. propinquus), 50 cm sec–1 (N = 23 O. rusticus and N = 22 F. propinquus), and 66 cm sec–1 (N = 10 O. rusticus and N = 5 F. propinquus). Comparison of time required to reach upstream food item in large and small O. rusticus To examine the elevated water velocity on size of male (Form I) O. rusticus, we determined the time required to reach an upstream food source for small (17–28 mm CL, N = 32) and large (34–43 mm CL, N = 32) O. rusticus. These size categories were one standard deviation larger and smaller than the mean sizes observed in streams. These tests were conducted in the experimental flume in four water velocities: 5 cm sec–1, 30 cm sec–1, 50 cm sec–1, and 66 cm sec–1. Comparison of the time required for O. rusticus and F. propinquus from lakes with O. rusticus from streams to reach the upstream food item To compare O. rusticus and F. propinquus from lakes with O. rusticus from streams in the time required to reach the upstream food item, we used water velocities of 5 cm sec–1, 30 cm sec–1, and 50 cm sec–1. We did not use the 66 cm sec–1 water velocity treatment due to the limited number of crayfish and poor performance at this velocity. Form II or non-reproductive male crayfish were used because we were not able to collect Form I males when the experiment was conducted. We used O. rusticus (N = 32) from Little John Lake and F. propinquus (N = 32) (26–38 mm CL) from Allequash Lake and O. rusticus from Allequash Creek (N = 24) in the three water velocities. No F. propinquus from streams were run in this experiment due to an inability to find enough individuals. Statistical analyses of movement rates in the flume We used the R survival package (Therneau, 2017) to perform a Kaplan-Meier survival analysis. Survival analysis allows for the use of censored data, observations where the event of interest (success in reaching the food source) did not occur by the end of an experimental trial. We allowed crayfish 60 min to reach the food source before the trial was ended. Omission of censored observations can cause bias when making comparisons or calculating medians and 95% confidence intervals from the time failure functions, but only for cases where > 50% of the individuals completed the trial. Confidence intervals are not symmetric due to the inclusion of censored values. Survival analysis provides a failure-time function of the proportion of crayfish that have reached the upstream food source. The analysis also allows an estimation of the restricted mean and standard error of the survival function while accounting for the censored data. We used the R survminer package (Kassambara & Kosinski, 2017) to perform a pairwise log-rank test with a Bonferroni correction on all pairwise combinations of treatments. A log-rank test is a nonparametric test used to compare pairwise right-skewed and censored data in the survival functions. RESULTS Mean crayfish size in streams versus lakes There was a significant interaction between species and lake or stream (F1,33 = 8.306, P = 0.0069). Orconectes rusticus from streams were significantly smaller than O. rusticus from lakes (P < 0.05) and not significantly different than F. propinquus from streams (P > 0.05) (Fig. 2). Figure 2. View largeDownload slide Box and whisker plot showing the median (horizontal line) and quartiles from lakes and streams where Orconectes rusticus and Faxonius propinquus were collected (Table 1). Orconectes rusticus and F. propinquus males in lakes and streams. Orconectes rusticus from lakes were significantly larger than O. rusticus from streams and also significantly larger than F. propinquus in lakes and streams (P < 0.05). Figure 2. View largeDownload slide Box and whisker plot showing the median (horizontal line) and quartiles from lakes and streams where Orconectes rusticus and Faxonius propinquus were collected (Table 1). Orconectes rusticus and F. propinquus males in lakes and streams. Orconectes rusticus from lakes were significantly larger than O. rusticus from streams and also significantly larger than F. propinquus in lakes and streams (P < 0.05). Experimental water velocity effects on O. rusticus and F. propinquus from streams The time required for crayfishes to reach the upstream food item increased significantly (P < 0.05) as water flow increased above 30 cm sec–1 (Fig. 3). Crayfish tended to walk in the middle section of the flume the majority of the time and did not use the edges due in part to the gravel added to the edges. There was, however, no significant difference (P > 0.05) between crayfish species within water velocity treatments (Fig. 3). The number of censored individuals increased dramatically at higher water velocities with only 2 of 10 O. rusticus and 2 out of 5 F. propinquus reaching the food resource preventing the calculation of median times as less than 50% reached the food source. Figure 3. View largeDownload slide Comparison of time required for size matched Orconectes rusticus and Faxonius propinquus to reach a food source at 4 water velocities using Kaplan-Meier survival probability (A). Median time (± 95% CI) at which 50% of the individuals have reached the limited food source (B). At higher water velocities, less than 50% of the crayfish reached the food source so no median is reported. A pairwise Log-Rank test was used to test for significant differences between groups using a Bonferroni adjusted p value using the survminer package (Kassambara & Kosinski 2017). Figure 3. View largeDownload slide Comparison of time required for size matched Orconectes rusticus and Faxonius propinquus to reach a food source at 4 water velocities using Kaplan-Meier survival probability (A). Median time (± 95% CI) at which 50% of the individuals have reached the limited food source (B). At higher water velocities, less than 50% of the crayfish reached the food source so no median is reported. A pairwise Log-Rank test was used to test for significant differences between groups using a Bonferroni adjusted p value using the survminer package (Kassambara & Kosinski 2017). Experimental water velocity effects on large and small O. rusticus The time required for large and small O. rusticus to reach the limited food resource increased significantly from 5 to 50 and to 66 cm sec–1 (P < 0.05) (Fig. 4). There were, however, no significant differences between these size classes of O. rusticus within water velocity treatments (P < 0.05). At 66 cm sec–1, 70% of the small O. rusticus were successful, whereas only 45% of the large individuals were successful (Fig. 4). Figure 4. View largeDownload slide Comparison time required for large (34–43 mm CL) versus small (17–28 mm CL) Orconectes rusticus to reach a food source at four water velocities using Kaplan-Meier survival probability (A). Median time (+/- 95% CI) at which 50% of the individuals reached the limited food source (B). At higher water velocities, less than 50% of the crayfish reached the food source so no median is reported. A pairwise Log-Rank test was used to test for significant differences between groups using a Bonferroni adjusted p value using the survminer package (Kassambara & Kosinski, 2017). Figure 4. View largeDownload slide Comparison time required for large (34–43 mm CL) versus small (17–28 mm CL) Orconectes rusticus to reach a food source at four water velocities using Kaplan-Meier survival probability (A). Median time (+/- 95% CI) at which 50% of the individuals reached the limited food source (B). At higher water velocities, less than 50% of the crayfish reached the food source so no median is reported. A pairwise Log-Rank test was used to test for significant differences between groups using a Bonferroni adjusted p value using the survminer package (Kassambara & Kosinski, 2017). Experimental water velocity effects on O. rusticus and F. propinquus from lakes and streams Form II male O. rusticus from streams reached the food source significantly faster than O. rusticus and F. propinquus from lakes at 30 and 50 cm sec–1 (P < 0.05) (Fig. 5). Orconectes rusticus from lakes took significantly longer than F. propinquus from lakes and O. rusticus from streams to reach the food source in the 5 cm sec–1 treatment (P < 0.05) (Fig. 5). Orconectes rusticus and F. propinquus from lakes did not differ significantly in their performance in flow at 30 and 50 cm sec–1 as in the prior experiment (P > 0.05) (Fig. 5). Orconectes rusticus and F. propinquus from lakes took significantly longer to reach the food source as water velocity was increased from 5 to 30 and 30 to 50 cm sec–1 (P < 0.05) (Fig. 5). The number of individuals from lakes reaching the limited food source at 66 cm sec–1 was less than 35% for both O. rusticus and F. propinquus, thus median times are unavailable but were significantly longer than O. rusticus from streams (P < 0.05) (Fig. 5). Figure 5. View largeDownload slide Comparison of the time required for size matched Orconectes rusticus and Faxonius propinquus from lakes and O. rusticus from streams to reach a food source at 4 water velocities using Kaplan-Meier survival probability (A). Median time (± 95% CI) at which 50% of the individuals reached the limited food source (B). At higher water velocities, less than 50% of the crayfish reached the food source so no median is reported. A pairwise Log-Rank test was used to test for significant differences between groups using a Bonferroni adjusted P value using the survminer package (Kassambara & Kosinski, 2017). Figure 5. View largeDownload slide Comparison of the time required for size matched Orconectes rusticus and Faxonius propinquus from lakes and O. rusticus from streams to reach a food source at 4 water velocities using Kaplan-Meier survival probability (A). Median time (± 95% CI) at which 50% of the individuals reached the limited food source (B). At higher water velocities, less than 50% of the crayfish reached the food source so no median is reported. A pairwise Log-Rank test was used to test for significant differences between groups using a Bonferroni adjusted P value using the survminer package (Kassambara & Kosinski, 2017). DISCUSSION Our results show that Orconectes rusticus in streams are smaller than those in lakes we sampled in northern Wisconsin. Our results also suggest that both O. rusticus and F. propinquus have limited abilities to tolerate water velocities in excess of 50 cm sec–1. In particular, lake individuals had a reduced ability to tolerate water velocities greater than 30 cm sec–1. In northern Wisconsin, O. rusticus introductions likely occur in lakes with the potential for subsequent dispersal through streams to other lakes. The existence of higher flow areas, especially in culverts or natural high flow areas, could have the potential to reduce, but not prevent the rate, of the spread of O. rusticus through streams. The larger size of O. rusticus in lakes is largely responsible for the success of O. rusticus, but in streams this size difference is absent. The effect of higher water velocities on crayfish combined with the smaller average size of O. rusticus has the potential to reduce the success of O. rusticus in streams. The idea that elevated water velocities could alter dispersal in streams is especially well known for fishes and has been used to limit dispersal of nonindigenous crayfishes in Europe (Frings et al., 2013). Fish dispersal is significantly reduced in areas of elevated water velocities and culvert pipes, particularly for benthic fishes (Wheeler et al., 2006; Noonan et al., 2011). European resource managers have attempted to utilize structures that increase water velocity over smooth surfaces to control the dispersal of invasive crayfishes to new habitats (Kerby et al., 2005; Frings et al., 2013). The effectiveness of these structures has been dependent on maintaining water velocity greater than 60 cm sec–1 and other factors, e.g., roughness of surfaces and slope, were found to be less important (Frings et al., 2013). Field studies have also shown that dispersal of crayfish species appears to be strongly influenced by elevated water velocities and in particular flood events (Light, 2003; Bubb et al., 2004). It is noteworthy that these studies have shown that water velocities in excess of 30–50 cm sec–1 have the greatest effect on dispersal (Maude & Williams, 1983; Kerby et al., 2005; Clark et al., 2008; Foster & Keller, 2011), consistent with the results found here. Higher turbulence associated with increased water velocities could, however, increase orientation efficiency helping them find the food source (Moore & Grills, 1999). Field studies have highlighted the importance of water velocities and substrates as key factors affecting crayfishes in streams (Light, 2003; Bubb et al., 2004, 2005; Bobeldyk & Lamberti, 2008). The size of native crayfish did not differ between environments, but non-native crayfish were larger in the lakes than in streams. Individuals of O. rusticus were smaller in streams (Fig. 2) and larger individuals (> 40 mm carapace length) were rare. In contrast, the sizes of stream F. propinquus were not reduced relative to those in lakes possibly because their maximum size is smaller on average than O. rusticus and their chelae are shorter and broader (Tierney et al., 2000). Broad, short chelae were found in crayfishes from high-velocity habitats compared to those from low-velocity habitats and could be useful to deflect water when velocities increase (Perry et al., 2013). Although our study was not designed to examined differences within streams or the effect of cobble, we did observe larger individuals in low- flow areas and in areas with larger, more complex cobble substrates. Size differences of crayfishes have been shown to also differ between areas of different water velocities (e.g., Clark et al., 2008). We did not measure the chelae of individuals, but it is possible that the larger chelae of O. rusticus may be a disadvantage in streams relative to F. propinquus (Roth & Kitchell, 2005). The smaller size of O. rusticus observed in streams may decrease the competitive advantage of O. rusticus relative to other crayfishes in streams and may also reduce ecosystem effects compared to those observed in lakes. Although other field observations and laboratory trials have suggested that larger crayfish individuals are more negatively affected by flow compared to small crayfish (Light, 2003), we did not observe an effect of size in our experiments. Differences between performance of large (34–43 mm) versus small (17–28 mm) O. rusticus at the water velocities tested were not observed, and elevated water velocities affected both size classes significantly (Fig. 4). This is in contrast to laboratory studies of O. rusticus and F. propinquus that showed larger individuals experienced greater drag (Maude & Williams, 1983). In field studies of invasions of Pacifastacus leniusculus in streams, larger individuals were more negatively affected by flow and invasions tended to occur predominately downstream (Light, 2003; Bubb et al., 2004). The interaction of substrates and flow may favor small crayfish, such as Faxonius obscurus (Hagen, 1870), which are able to occupy refugia, unavailable to larger crayfish, allowing them to occupy areas of greater water velocities (Clark et al., 2008), but a heterogeneous distribution of substrates could still limit upstream dispersal because crayfish would be required to experience the full effect of flow in sand flats. Thus, carapace body size alone may not be a good indicator of susceptibility to flow. Factors other than carapace size could be more important, and size itself may be confounded by flow conditions in the habitat of origin. The larger body sizes that exist in lakes were not common in streams, thus our experiments may have used too small of a size range. The steams where these crayfish were collected did not have velocities in excess of 40 cm sec–1, but the large-size crayfish could be removed from these ecosystems during spring and fall floods when water velocities are much higher. More noteworthy is the possibility that the crayfish may have come from a flow environment that had predisposed them to dealing with flow. The absence of larger crayfish individuals in streams suggests elevated water velocity has an effect but because of their absence we could not experimentally test for an effect. Beyond body size, there are indications that the size of chelae might be an important factor. We used Form II individuals for the comparison between species of lake and stream crayfishes, and they had smaller chelae than Form I individuals. The use of Form II crayfish may explain why O. rusticus from streams performed better in elevated flow relative to individuals from the other two experiments, where Form I crayfish were used. Unfortunately, it is not possible to test differences between Form I and Form II crayfish because the two forms do not coexist in nature for long enough to use in experiments without the risk of molting affecting behavior. We did not observe differences in behavior between the two reproductive states, but this should be studied in future experiments. Because our results indicate that chelae size may play a role in the ability of crayfish to interact with elevated water velocity, this might mean that Form II crayfish are more capable of dispersal into higher flow environments. Support for the idea that crayfishes might differ in their ability to deal with flow depending on their habitat of origin is further exemplified by the performance differences between O. rusticus from streams and O. rusticus and F. propinquus from lakes (Fig. 5). In trials testing performance at 5 cm sec–1, O. rusticus from lakes took longer to reach the food source than other crayfishes but all individuals completed the trials significantly faster than in all other treatment (P < 0.05) (Fig. 5). Lake crayfish species took significantly longer than stream O. rusticus when water velocity was increased to 30 and 50 cm sec–1 We did not include results from the 66 cm sec–1 treatment because less than 10% of the lake crayfish species completed the trials. The most striking difference between the lake and stream crayfishes was that stream individuals adopted a streamlined body posture, whereas lake crayfish individuals did not (Maude & Williams, 1983). These results suggest that there may be behavioral differences between these populations and success may be reduced if introductions occur with individuals from lakes to streams. Crayfishes from lakes, however, were observed standing with their bodies higher off the substrate and often moving their chelae in ways which increased drag on the individuals just prior to loss of contact with the substrate. These observations indicate that crayfishes may be preadapted to flow conditions in their habitat of origin and do not readily adjust to different flow environments. Our study provides a better understanding of the role of elevated water velocity on O. rusticus invasion dynamics by experimentally testing the effect of elevated water velocities on their performance. Our results provide valuable insight into the understanding of crayfish invasions in lotic versus lentic environments. In areas having numerous lakes, Short stream segments with low water velocities may act as corridors for invasion in areas having numerous lakes, whereas streams with culverts or high flow areas where there are limited refugia may limit dispersal (Puth & Allen, 2005). Because size is a key component for success in lakes, the abiotic effects of streams have the potential to alter O. rusticus invasions in lakes. Dispersal of large O. rusticus into lakes is thus likely to be limited by the high flow velocities experienced in streams, as well as lotic factors such as fish predation pressure (DiDonato & Lodge, 1993; Hill & Lodge, 1999), habitat availability (Hill & Lodge, 1995; 1999), and interactions with congeners (Hill & Lodge, 1994; 1995; 1999). The relative importance of factors explaining the success of O. rusticus invasions may shift from abiotic factors (such as water velocity or barriers) in high-gradient streams, to biotic factors (such as competition and predation) in low-gradient streams or lakes. This framework may provide new tools to limiting the spread of this and other benthic invasive species in freshwater ecosystems. ACKNOWLEDGEMENTS We acknowledge the comments and suggestions from Eric Peterson and Scott Sakaluk for their help in designing the experiment. We also thank Steve Juliano for his advice on statistical analyses. We are also grateful for suggestions and comments by Catherine O’Reilly and two anonymous reviewers, whose input dramatically improved the manuscript. Alboukadel Kassambara (Department of Biological Hematology, Montpellier, France) is acknowledged for his work on the pairwise tests of survival functions in the survminer R package. Jim Dunham was instrumental in helping design and build the flow chamber, without his help this would not have been possible. Funding for this project was in part from the Illinois State University Beta Lambda Chapter of the Phi Sigma Biological Honor Society. REFERENCES Bobeldyk, A.M. & Lamberti, G.A. 2008. A decade after invasion: Evaluating the continuing effects of rusty crayfish on a Michigan River. Journal of Great Lakes Research , 34: 265– 275. 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