Southeastern Naturalist 473 A.J. Edelman, J. Moran, T.J. Garrabrant, and K.C. Vorreiter 22001155 SOUTHEASTERN NATURALIST 1V4o(3l.) :1447,3 N–4o8. 33 Muskrat Predation of Native Freshwater Mussels in Shoal Creek, Alabama Andrew J. Edelman1,*, John Moran2, Timothy J. Garrabrant1, and Kaley C. Vorreiter1 Abstract - Widespread decline of native freshwater mussels has increased their susceptibility to extinction from environmental factors such as competition, disease, and predation. Mammals, in particular Ondatra zibethicus (Common Muskrat), are well documented as major predators of freshwater mussels. We assessed the impact of Common Muskrats on the native freshwater-mussel community in Shoal Creek, AL. We surveyed 12.7 km of Shoal Creek for signs of mussel predation by Common Muskrats. Based on the species composition of observed shell middens, Common Muskrats foraged on all 6 native mussel species in Shoal Creek, including federally listed threatened and endangered species (Hamiota altilis [Finelined Pocketbook] and Pleurobema georgianum [Southern Pigtoe], respectively). Common Muskrats appeared to feed on native mussels based on their natural availability rather than exhibiting strong size-selective predation. Introduction Freshwater mussels are some of the most diverse and endangered fauna in the continental US (Williams et al. 1993). This group has experienced a drastic decline in abundance and diversity over the last century (Bogan 1993, Downing et al. 2010). As a result, of the known freshwater-mussel species in the US, 6% are extinct, ~25% are federally listed as endangered or threatened, and 50% are considered species of special conservation concern (Williams et al. 1993, 2008). The southeastern US is considered a region of high diversity for freshwater mussels within North America and hosts 94% of US species and 95% of federally protected species (Lydeard and Mayden 1995, Williams et al. 2008). Decline of freshwater mussels is due to a variety of influences including habitat modification, invasive species, loss of host fish, pollution, and overharvesting (Bogan 1993, Downing et al. 2010, Williams et al. 1993). These factors have caused some freshwater-mussel populations to be composed mainly of older individuals with reduced reproductive output that are restricted to short stream reaches (Williams et al. 2008). The combination of these pressures has lowered the long-term viability of many freshwater-mussel populations, exposing them to increased likelihood of extinction caused by environmental factors such as competition, disease, and predation that typically are not a grave threat to the persistence of healthy populations (Downing et al. 2010, Williams et al. 1993). Localized predation may contribute to the decline of isolated freshwater-mussel populations (Kopij 2011, 1Department of Biology, University of West Georgia, Carrollton, GA 30118. 2National Forests in Alabama, US Forest Service, Montgomery, AL 36107. *Corresponding author - aedelman@westga.edu. Manuscript Editor: Roger D. Applegate Southeastern Naturalist A.J. Edelman, J. Moran, T.J. Garrabrant, and K.C. Vorreiter 2015 Vol. 14, No. 3 474 Neves and Odom 1989). Freshwater mussels are predated by a variety of mammalian species including Neovison vison (Schreber) (American Mink), Procyon lotor L. (Northern Raccoon), Lontra canadensis (Schreber) (Northern River Otter), and Ondatra zibethicus L. (Common Muskrat) (Williams et al. 2008). In particular, Common Muskrats (hereafter referred to as Muskrats) are well-documented as major predators of freshwater mussels, the effects of which are easily studied because they leave extensive midden piles of empty shells (Bovbjerg 1956, Diggins and Stewart 2000, Erickson 2001, Evermann and Clark 1920, Haag 2012, Hersey et al. 2013, Hoggarth et al. 1995, Lacki et al. 1990, Neves and Odom 1989, Owen et al. 2011, Tyrrell and Hornbach 1998, Watters 1995, Zahner-Meike and Hanson 2001). Muskrats are usually considered herbivores, but can feed heavily on freshwater bivalves in certain ecosystems or when fresh vegetation is seasonally scarce (Evermann and Clark 1920, Hersey et al. 2013, Lacki et al. 1990, Zahner-Meike and Hanson 2001). While healthy populations of mussels can often sustain high levels of predation, the effect of predation on endangered mussels can lead to further decline (Haag 2012, Hoggarth et al. 1995, Kopij 2011, Neves and Odom 1989). Our objective was to assess the scope of Muskrat predation on an isolated community of native freshwater mussels in Shoal Creek, AL, by examining shell remains in Muskrat middens. The freshwater-mussel community in Shoal Creek, similar to many other southeastern US rivers, is fragmented by lake impoundments and has been invaded by Corbicula fluminea (Müller) (Asiatic Clam). Six native freshwater mussel species inhabit Shoal Creek, and most of them are considered species of conservation concern (Dolloff et al. 2012, Mirarchi et al. 2004): federally endangered Pleurobema georgianum (Lea) (Southern Pigtoe), federally threatened Hamiota altilis (Conrad) (Finelined Pocketbook), and 3 Alabama state species of conservation concern including Strophitus connasaugaensis (Lea) (Alabama Creekmussel), Villosa nebulosa (Conrad) (Alabama Rainbow), and V. umbrans (Lea) (Coosa Creekshell). Villosa vibex (Conrad) (Southern Rainbow) also inhabits Shoal Creek, but is not of conservation concern (Dolloff et al. 2012). Significant predation of freshwater mussels by Muskrats in Shoal Creek has been anecdotally documented during stream surveys (Warren et al. 2004). In addition, native mussel species at this locality are impacted by the fragmented nature of the river system, which may decrease genetic diversity and recruitment within each segment. Both of the federally protected species in Shoal Creek are highly localized in their distribution and require intact river systems for long-term survival (Dolloff et al. 2012, Williams et al. 2008). We expected that Muskrats in Shoal Creek would selectively feed on the larger species and individuals as reported in other studies (reviewed in Owen et al. 2011). Field-Site Description Our study system, Shoal Creek, is ~32 km long and drains an area of 122 km2 in Cleburne and Calhoun counties, AL. The Shoal Creek watershed is primarily forested, and except for a 4-km segment at its mouth, is almost completely contained within the Shoal Creek Ranger District of the Talladega National Forest. Southeastern Naturalist 475 A.J. Edelman, J. Moran, T.J. Garrabrant, and K.C. Vorreiter 2015 Vol. 14, No. 3 Four public roads cross Shoal Creek, and the Pinhoti Trail and Pine Glen Recreation Area occur along its banks. Within the Talladega National Forest, there are 3 free-flowing, but fragmented segments of Shoal Creek created by man-made impoundments (Fig. 1): (1) above Sweetwater Lake (10 km in length), (2) between Sweetwater Lake and Highrock Lake (9.6 km in length), and (3) between Highrock Lake and Whiteside’s Mill Lake (5.5 km in length). Villosa nebulosa, V. umbrans, and V. vibex have been documented in all 3 segments of Shoal Creek. Strophitus connasaugaensis and H. altilis are only known to occur in the 2 upper segments Figure 1. Location of sampled Muskrat middens along Shoal Creek, AL. The winter/spring stream survey extent is marked by the thick, black line. Southeastern Naturalist A.J. Edelman, J. Moran, T.J. Garrabrant, and K.C. Vorreiter 2015 Vol. 14, No. 3 476 of Shoal Creek from Highrock Lake to above Sweetwater Lake, whereas P. georgianum only occurs between Sweetwater and Highrock lakes (Dolloff et al. 2012, Warren et al. 2004). Methods We visually searched for signs of mussel predation by Muskrats at Shoal Creek during 2 survey periods (summer and winter/spring). One day each month during the summer period, we surveyed a stretch of Shoal Creek beginning at the Forest Road 500 crossing near the Pine Glen Recreation Area and traveling upstream (n = 3 surveys, conducted on 20 June, 16 July, and 24 August 2012). The survey on 20 June 2012 extended 1.2 km upstream, and the 16 July and 24 August 2012 surveys extended 650 m upstream (Fig. 1). The summer survey period occurred as part of a larger monitoring effort of the mussel population in association with bridge construction at the road crossing near the Pine Glen Recreation Area. The summer survey period was relatively informal (we did not map locations) and consisted of 1 person (J. Moran) walking along the streambed and collecting any observable predated native mussels (paired valves only). We collected only native species and recorded neither the number of middens nor the number of shells in middens during the summer survey period. The winter/spring survey period occurred periodically from 14 December 2012 to April 6 2013, during which we inspected a 12.7-km stretch of Shoal Creek from 3.2 km upstream of Highrock Lake to just below Coleman Lake (Fig. 1). At these survey locations, Shoal Creek is considered a second-order stream with widths of ~5–8 m (Dolloff et al. 2012). Unlike the summer survey, we inspected each stream stretch only once during the winter/spring survey. For the winter/spring survey period, we developed a more formalized survey methodology and included multiple simultaneous observers. We surveyed by walking line transects with observers spaced ~2–3 m apart along the stream channel. We proceeded slowly upstream as a group while visually searching for mussel-shell middens along the immediate stream banks, partially submerged and emerged logs and rocks, and streambed (Erb and Perry 2003, Zahner-Meike and Hanson 2001). We bypassed deep pools due to our inability to see the streambed. All observers wore polarized sunglasses to reduce glare and used view buckets to look at promising locations under the water surface. When a shell midden was identified, we centered one to four 0.25-m2 quadrats on the site (number of quadrats depended on size of area covered by the midden) and collected all visible, empty shells within each quadrat (both native and invasive species). We mapped all shell-midden locations using a global positioning system (GPS) receiver. We identified to species all shells collected during the summer and winter/spring survey periods and measured the length on the longest shell-axis. In addition, for shells collected during the winter/spring surveys, we classified shells as either recent or older predation events (e.g., intact periostracum and shiny nacre indicated recent event), and examined them for signs of predation (e.g., broken shells and incisor and claw marks). Muskrats typically feed on mussels by inserting their Southeastern Naturalist 477 A.J. Edelman, J. Moran, T.J. Garrabrant, and K.C. Vorreiter 2015 Vol. 14, No. 3 incisors between the valves and prying upward leaving characteristic teeth and claw marks. This action can break the shell of thinner-shelled mussel species, but leaves thicker-shelled species intact (Dillon 2000, Erb and Perry 2003, Haag 2012, Zahner-Meike and Hanson 2001). Given that older predated shells were difficult to identify to species, we only used recently predated shells (as described above) in all analyses of the winter/spring survey period. To avoid counting individuals more than once in the winter/spring survey period, we assigned unpaired valves a value of 0.5 in all counts. We quantified prey selection of Muskrats during the winter/ spring survey period by examining Manly’s selection and standardized selection ratios (Manly et al. 2002) for native mussel species. We calculated the selection ratio (wi) as the proportion of the species eaten divided by the proportion of the species available. If wi > 1, then the species was eaten more than expected by availability, and less than expected if wi < 1. The standardized selection ratio (β, ranges from 0 to 1) usually provides a less-biased estimate, and we calculated it as wi divided by the sum of wi for all species. For each species, we compared β to the baseline value (1 divided by the number of species) to determine if a species was over- (β > baseline) or under-utilized (β < baseline). We determined the availability and distribution of shell lengths of native species in Shoal Creek based on a previous survey for live mussels conducted on the same stream segments in 2011 (Dolloff et al. 2012). We pooled data from the Dolloff et al. (2012) survey for both the quantitative and qualitative surveys at all sites. We tested for evidence of prey selection overall with a log-likelihood chi-squared test and for each species by examining Bonferroni-corrected 95% confidence intervals for selection ratios (Manly et al. 2002). We employed R package adehabitatHS software (Calenge 2006) to conduct the selection analysis. We compared the frequency distributions of shell lengths (paired valves only) between the winter/spring survey period and the Dolloff et al. (2012) survey data with a 2-sample Kolmogorov-Smirnov test to determine if sizeselective predation occurred. Previous surveys of Shoal Creek have demonstrated that mussel abundance is highly variable in this study system even in spatially adjacent sites (Dolloff et al. 2012). Thus, given the less-rigorous survey methodology and more spatially restricted nature of the summer-survey period which likely contributed to a less-representative sample, we did not compare these data directly with the winter/spring survey period data or the Dolloff et al. (2012) survey data. Results Summer survey period During the summer survey period, we found 54 shells in June, 23 shells in July, and 67 shells in August. In general, we frequently found larger-sized predated mussels in piles on top of submerged and emerged large rocks and logs. We often found smaller-sized mussel shells in scattered piles located in shallows (less than 20 cm water depth) with a mix of small gravel and sand substrates that appeared to have been recently disturbed. We collected predated shells from 6 native mussel species (Table 1) with the federally endangered and threatened species (H. altilis and P. georgianum) accounting for about 15% and the state species of conservation Southeastern Naturalist A.J. Edelman, J. Moran, T.J. Garrabrant, and K.C. Vorreiter 2015 Vol. 14, No. 3 478 concern (S. connasaugaensis, V. nebulosa, and V. umbrans) accounting for about 62% (Table 1). Winter/spring survey period We found 10 middens during the winter/spring survey period, 3 between Highrock Lake and Sweetwater Lake and 7 between Sweetwater Lake and Coleman Lake (Fig. 1). Middens tended to be located in shallows, and we frequently found them on or next to submerged and emerged rocks and logs. Middens contained a total of 552 whole shells and 827 half shells. The number of shells in middens ranged from 2 to 434.5 (mean ± SE = 96.6 ± 174.1 shells). We observed predation signs on about 27% (259.5 of 965.5 shells) of all collected shells. We collected shells from 7 different species; the invasive C. fluminea accounted for ~88% of total shells (851.5 of 965.5 shells). Paired valves of C. fluminea found in middens were shorter in length (21.8 ± 0.4 mm, n = 130) than paired valves of all native mussel species combined (58.6 ± 1.3 mm, n = 89; 2-tailed t-test: t = -27.0, P < 0.001). Of the native species shells collected (n = 114), the federally endangered and threatened species accounted for less than 6% and the state species of conservation concern accounted for about 69% (Table 2). There was no indication of size-selective predation of native mussels by Muskrats. The pooled paired-valve lengths from all native species did not exhibit any difference in frequency distributions between midden- and stream-survey samples (2-sample Kolmogorov-Smirnov test, D = 0.10, P = 0.60; Fig. 2). There was no Table 2. Mean shell length (± SE), number, percentage, and prey-selection ratios of freshwater mussels found in all Muskrat middens during the winter/spring survey period at Shoal Creek, AL. Shell length calculated from paired valves only. Stream availability (SA) based on 2011 survey of live mussels (n = 203) in Shoal Creek (Dolloff et al. 2012). wi 95% CI = 95% Bonferroni confidence interval; intervals that span 1 indicate random prey selection. Shell length Midden SA Species (mm) n % % wi ± SE wi 95% CI β Hamiota altilis 55.7 ± 7.0 4.5 3.9 5.2 0.76 ± 0.42 -0.25–1.77 0.12 Pleurobema georgianum 36.1 ± 7 2.0 1.8 1.0 1.68 ± 1.67 -2.32–5.69 0.27 Strophitus connasaugaensis 62.4 ± 1.3 46.0 40.4 34.9 1.16 ± 0.17 0.74–1.57 0.18 Villosa nebulosa 51.5 ± 3.0 20.5 18.0 25.0 0.72 ± 0.17 0.31–1.13 0.11 Villosa umbrans 51.9 ± 2.9 12.5 11.0 13.0 0.84 ± 0.27 0.19–1.50 0.13 Villosa vibex 64.8 ± 2.5 28.5 25.0 20.8 1.2 ± 0.26 0.58–1.82 0.19 Table 1. Mean shell length (± SE), number, and percentage of freshwater mussels found in all Muskrat middens during the summer-survey period at Shoal Creek, AL. Species Shell length (mm) n Midden % Hamiota altilis 49.3 ± 3.8 9 6.3 Pleurobema georgianum 39.2 ± 1.7 13 9.0 Strophitus connasaugaensis 58.9 ± 1.9 29 20.1 Villosa nebulosa 37.9 ± 1.2 26 18.1 Villosa umbrans 41.6 ± 1.0 34 23.6 Villosa vibex 55.0 ± 1.0 33 22.9 Southeastern Naturalist 479 A.J. Edelman, J. Moran, T.J. Garrabrant, and K.C. Vorreiter 2015 Vol. 14, No. 3 evidence of prey selection by Muskrats based on relative abundances of native mussel species in middens (χ2 = 3.5, df = 5, P = 0.63). Examination of selection ratios for each native species indicated that prey selection was random (95% CI for all wi included 1; Table 2). The standardized selection ratios also revealed a similar pattern of random predation for each species (all β values close to baseline value of 0.167; Table 2). Discussion Based on shells collected at middens, Muskrats appeared to prey on native mussels according to their relative abundances in Shoal Creek. The prey-selection ratios for each native mussel species were near values predicted if Muskrats captured species based on natural availability (Table 2). Our results did not indicate that larger species or individuals were preyed upon at higher rates than expected by availability (Table 2, Fig. 2). These findings are in contrast to several other studies that reported size-selective or species-selective predation on freshwater mussels by Muskrats based on similar midden-sampling techniques (Diggins and Stewart 2000, Erickson 2001, Jokela and Mutikainen 1995, Neves and Odom 1989, Owen et al. 2011, Tyrrell and Hornbach 1998, Watters 1995, Zahner-Meike and Hanson 2001). This discrepancy between our results and those of other studies may be due to differences in habitat and mussel communities of sampled sites. The previous studies occurred in larger aquatic habitats (rivers and lakes) that often had greater Figure 2. Shell-length frequency (grouped into 10-mm size classes) for all native freshwater mussels (paired valves only) found in Muskrat middens during the winter/spring survey period (dark gray bars, n = 89) and stream-survey samples from Dolloff et al. 2012 (light gray bars, n = 173) at Shoal Creek, AL. Southeastern Naturalist A.J. Edelman, J. Moran, T.J. Garrabrant, and K.C. Vorreiter 2015 Vol. 14, No. 3 480 mussel-species diversity and size ranges (reviewed in Owen et al. 2011) compared to Shoal Creek. Muskrats preferentially prey on mussels that range from 20 to 90 mm in length (Diggins and Stewart 2000, Erickson 2001, Jokela and Mutikainen 1995, Neves and Odom 1989, Owen et al. 2011, Zahner-Meike and Hanson 2001). Muskrats may avoid mussels >90 mm in length because they are too energetically costly to extract, whereas mussels less than 20 mm are likely difficult to find (Owen et al. 2011). All 6 native mussel species and sampled individuals in Shoal Creek were within the preferred size range of Muskrats, which may account for the lack of a strong difference between shell sizes observed in the middens and available in the stream (Fig. 2). Predation by Muskrats can influence the local community structure of native mussels, most obviously by reducing the abundance of preferred-size individuals or species (Diggins and Stewart 2000, Erickson 2001, Jokela and Mutikainen 1995, Zahner-Meike and Hanson 2001). Muskrats are primarily herbivores, but the percentage of their diet derived from carnivory varies depending on habitat (Willner et al. 1980). In marsh habitats with abundant wetland vegetation, very little of their diet consists of animal matter (Lacki et al. 1990). However, in stream habitats with little vegetation or when vegetation is seasonally scarce, animal matter may constitute the majority of the Muskrat’s diet (Evermann and Clark 1920, Hersey et al. 2013, Zahner-Meike and Hanson 2001). Shoal Creek is a small, second-order stream with little aquatic vegetation. Thus, Muskrats at this location likely derive a significant proportion of their diet from animal matter including freshwater mussels. Our results, confirmed that Muskrats preyed on all native mussel species in Shoal Creek. Predation by Muskrats of the rare and federally listed H. altilis and P. georgianum is of greatest conservation concern given these species’ highly restricted distributions and low population sizes (Dolloff et al. 2012, Warren et al. 2004). The extent to which predation is contributing to the overall decline of freshwater mussels is uncertain, but other processes such as pollution and habitat destruction are considered greater threats (Downing et al. 2010). Although healthy populations of freshwater mussels may be able to sustain high levels of predation, further loss of individuals in declining or low-abundance populations via localized predation may pose a serious threat (Neves and Odom 1989). Mussel communities at Shoal Creek exhibit relatively low abundances most likely because of the low productivity of the headwater stream system (Warren et al. 2004), a characteristic that may place this community at greater risk of decline from predation. Low abundance coupled with isolation of stream segments by human-made impoundments on Shoal Creek may reduce probability of recolonization of sites by mussels after intense predation by Muskrats and other predators. Invasive C. fluminea were very common in middens at Shoal Creek even though their shell size averaged near the lower range preferred by Muskrats. Density of C. fluminea has not been measured at Shoal Creek, but this species is more abundant than all other native mussel species combined and is highly visible on the streambed (A.J. Edelman, pers. observ.) likely making them easy for Muskrats and other predators to find. Given the high fecundity of C. fluminea (Sousa et al. Southeastern Naturalist 481 A.J. Edelman, J. Moran, T.J. Garrabrant, and K.C. Vorreiter 2015 Vol. 14, No. 3 2008), populations of this species can presumably sustain intense levels of predation. However, the impact of this additional and highly abundant food source may indirectly alter the predator–prey dynamics between Muskrats and native mussels and should be the subject of future study. It has been demonstrated in other ecological systems, that introduced-prey species can have negative and positive indirect effects on native prey species via the mechanisms of apparent competition and indirect facilitation (Jaworski et al. 2013, Roemer et al. 2002, White et al. 2006). Temporary control of Muskrat populations at Shoal Creek through removals could be considered as a potential option to aid in the recovery of native mussel populations (Neves and Odom 1989). Limited removal of Muskrats may be most effective at locations of high mussel-diversity or during reintroduction efforts. Future studies could examine how Muskrat removal affects freshwater-mussel communities to determine whether this is an effective management strategy. Acknowledgments We thank Jonathan Stober for technical assistance with this project and 2 anonymous reviewers for their helpful comments. 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