And Silver Carp, H. Molitrix (Valenciennes, 1844) Range Expansion on the Northwestern Front of the Invasion in North America

Rapid Communication

Adult, juvenile and young-of-year bighead, Hypophthalmichthys nobilis (Richardson, 1845) and silver carp, H. molitrix (Valenciennes, 1844) range expansion on the northwestern front of the invasion in North America

Cari-Ann Hayer*, Brian D.S. Graeb and Katie N. Bertrand South Dakota State University, Department of Natural Resource Management, Box 1240B, NPB 138, Brookings, SD 57006 USA E-mail: [email protected] (CAH), [email protected] (BDSG), [email protected] (KNB) *Corresponding author

Received: 2 June 2014 / Accepted: 14 August 2014 / Published online: 23 September 2014

Handling editor: Vadim Panov

Abstract

Asian carps (bighead and silver carp) were collected with boat electrofishing over four years in three South Dakota tributaries to the Missouri River at the beginning of their invasion into this region. This paper documents their annual movement upstream into these tributaries and identifies differences in distribution by age-0, juvenile, and adults. By the end of this study in 2012, Asian carps dispersion was slowed or halted in these tributaries due to artificial and natural barriers. These records represent the northern most records of Asian carps in North America (46.931042, -98.708975). Key words: South Dakota, prairie streams, flooding, establishment, reproduction

Introduction through numerous dams on the Mississippi River and into associated tributaries (e.g., Missouri River, Invasive species are becoming a worldwide Illinois River, Ohio River; Kolar et al. 2007; epidemic and are triggering changes in the USGS 2014). The northern extent of the Asian structure and function of invaded ecosystems carps expansion is in the Mississippi River basin. (Ricciardi et al. 2000). One pair of global invaders, They could potentially colonize the Great Lakes bighead, Hypophthalmichthys nobilis (Richardson, through the Chicago Shipping Canal (e.g., Lake 1845), and silver carp, H. molitrix (Valenciennes, Michigan) and the Illinois River, a tributary to the 1844), (collectively referred to as Asian carps) have Mississippi River (Kocovsky et al. 2012). The been introduced intentionally and unintentionally eastern range includes the Ohio River where they throughout the world, mostly for aquaculture threaten to enter the Great Lakes (e.g., Lake purposes (Kolar et al. 2007) as they are the most Erie) through the Wabash River, a tributary to important aquaculture species in Asia and east- the Ohio River, and the Maumee River, the second central Europe (Lieberman 1996; Penman et al. largest tributary to Lake Erie (Kocovsky et al. 2005). Bighead carp have been introduced to 74 2012). On the northwestern part of their expansion, countries and are reproducing in 19 and the silver Asian carps threaten to colonize three tributaries carp has been introduced to 88 countries and are (e.g., James, Vermillion, and Big Sioux rivers) to reproducing in 23 (Kolar et al. 2007). Both species the Missouri River below Gavins Point Dam, that of Asian carps are currently reproducing in the serve as important fish habitat for many threatened United States (Papoulias et al. 2006; DeGrandchamp and endangered fishes (Berry et al. 2007). These et al. 2007; Lohmeyer and Garvey 2009; Deters et tributaries already face disturbance from current al. 2013). Asian carps were originally introduced and present land use practices and natural into the southern United States in aquaculture physio-chemical and hydrologic fluctuations ponds in the early 1970s where both species characteristic of prairie streams (Matthews 1988; subsequently escaped and began their expansion Poff and Ward 1989; Hayer et al. 2014a).

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Figure 1. Study area with standardized sampling sites (circles) spanning the James, Vermillion, and Big Sioux Rivers in the eastern part of North and South Dakota. Large barriers represent dams that presumably Asian carp cannot pass. 1= Gavins Point Dam, 23 m high, 2 = Jamestown Dam, 28 meters high, 3 = Vermillion Lake Dam, 12 m high, 4 = Sioux Falls, 8 m high. A = Shue creek, b = Lake Byron, c = Milltown, SD, d = Mitchell, SD.

Prior to this study, the distribution and use by South Dakota to its confluence with the Missouri Asian carps of these three Missouri River Plains River (Berry et al. 1993; Figure 1). The James River tributaries in South Dakota were unknown. contains over 200 lowhead dams (approximately However; one bighead carp was caught by an 1–2 meters) that are passable by fish during high angler in the middle James River near Mitchell, water (Berry et al. 1993; Shearer and Berry 2003) South Dakota in 2008 and one silver carp was and 28 meter high dam in the North Dakota part caught by an angler in the Big Sioux River near of the river (Berry et al. 1993). The Vermillion Canton, SD in 2004 (Kolar et al. 2005). The goal River, the smallest basin (watershed area = 5,800 of this paper is to document the northwestern km2) extends 243 Rkm from the confluence of invasion front of adult, juvenile, and young-of- West and East Fork Vermillion rivers to its year Asian carps in three prairie tributaries and confluence with the Missouri River (Schmulbach other South Dakota waters (e.g., lakes) by and Braaten 1993; Figure 1). The Vermillion providing the northern most latitude detection River contains one larger dam, East Vermillion locations. Lake Dam, which creates Vermillion Lake and is 12 m high (Hayer et al. 2014b). The Big Sioux 2 Methods River (watershed area = 23,325 km ) extends 470 Rkm from the Prairie Coteau of northeastern Three prairie tributaries in South Dakota converge South Dakota to its confluence with the Missouri with an unchannelized section (Galat et al. 2005a) River at the South Dakota-Nebraska-Iowa border of the Missouri River just downstream of Gavins (Figure 1). The Big Sioux River contains a set of Point Dam: the James, Vermillion and Big Sioux natural falls that are deemed impassable by fish rivers. Gavins Point Dam is 23 m high hydro- (Dieterman and Berry 1998; Galat et al. 2005). electric dam and is the lower most dam on the The highest fall is 8 m high. Missouri River. No carp have been found upstream Standardized boat electrofishing occurred of this barrier. The three warmwater tributaries between 2009 and 2012 at five sites on the James drain the Central Lowlands physiographic province River, two sites on the Vermillion River, and in South Dakota (Galat et al. 2005b) and are three sites on the Big Sioux River (Figure 1), all characterized by low gradient streams of glacial within South Dakota. Sampling consisted of three origin (Hoagstrom et al. 2007). The James River 10 minute electrofishing runs which generally (watershed area = 57,000 km2) extends 760 Rkm covered three river kilometers. Sampling occurred from southeastern North Dakota through eastern once during each of three seasons: spring (May –

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Figure 2. Northern most collections of silver and bighead carp adults. Adults are 3 years old or more and greater than 600 mm TL.

June), summer (July – August), and fall (September Silver carp have also only been collected in the – October). Additional non-standardized boat Big Sioux River at the confluence with the electrofishing occurred at various sites on the Missouri River and were last collected on August James River in North and South Dakota. Adult 17, 2012 (N = 5; TL = 634–783 mm; 3260–6123 g; carps were considered to be greater than 600 mm Figure 2). One adult bighead carp was collected TL (age 3+), juveniles were between 300 and near Mitchell (August, 31 2010) on the James 600 mm TL (ages 1 and 2), and age-0 were less River (TL = 1001, 9072 g) and no adults have than 300 mm TL. Life stage ages were verified been collected in the Vermillion or the Big Sioux by analyzing otoliths (Hayer et al. 2014b). Rivers (Figure 2).

Results Juveniles

Our data suggest that Asian carps dispersion has Twelve juvenile silver carp were collected from been slowed or halted in these Missouri River Shue Creek, a tributary to the James River north tributaries due to artificial and natural barriers. of Huron on September 27, 2011 (TL = 409 – These barriers are the most upstream collections 507; 768 – 1474 g; Figure 3). One juvenile silver within these river basins (Figure 1) where carp (450 mm, 1088 g) was subsequently collected bighead and silver carp were detected (Figures 2 in North Dakota on the James River in the –4). These findings represent the northernmost Jamestown Reservoir tailrace (Figures 3, 4) on Asian carps detections in North America October 12, 2011. This is the first record of (46.931042, -98.708975). silver carp in North Dakota. Fifteen silver carp (TL = 311–369 mm, 299–656 g) were collected from the Vermillion River below East Lake Adults Vermillion dam on August 11, 2011 and nineteen One adult silver carp was collected as far upstream were collected in the Big Sioux River at the as Milltown on the James River (TL = 752,4958 g) confluence with the Missouri River (TL = 384 – 474 on August 2, 2012 (Figure 2) and have not been mm; 510 – 1191; Figure 3) on August 17, 2012. collected above the confluence of the Vermillion Six juvenile bighead carp (415 – 509 mm TL, River with the Missouri River where nine silver 822 – 1389 g) were first collected from Firesteel carp were last collected on August 16, 2012 (TL Creek, a tributary to the James River near Mitchell

= 681 – 784 mm; 3203 – 7285 g; Figure 2). on September 29, 2011 and were last collected

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Figure 3. Northern most collections of silver and bighead carp juveniles. Adults are 1–2 years old and between 300 and 600 mm TL.

Figure 4. Juvenile silver carp collected in North Dakota on the James River below Jamestown Dam. Photograph by G. VanEeckhout.

in the Big Sioux River (N = 5; TL = 349–470 mm; was collected on October 20, 2010 in the Big 288–1389 g) on October 6, 2011 at the confluence Sioux River below the falls (TL = 298 mm, 301 g; with the Missouri River (Figure 3). Four bighead Figure 6). carp (309–372 mm TL, 299–565 g) were first collected from the Vermillion River below the Lakes East Vermillion Lake Dam on August 11, 2011 (Figure 3). Two bighead carp and one silver carp (TL Age-0 approximately between 400 and 460 mm) were collected by a commercial fisherman with a seine Two age-0 silver carp were collected on Sept 29, pull on November 2, 2012 from Lake Byron 2011 in Shue Creek at the confluence with the which is the first confirmed lentic record in James River (TL = 170, 174 mm; 44, 51 g; South Dakota (South Dakota Game Fish and Figures 5,6). One young-of-year bighead carp Parks, personal communication).

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Figure 5. Northern most collections of age-0 silver and bighead carp. Age-0 carps were born the year of collection and are less than 300 mm TL.

Figure 6. Two young of year silver carps collected in Shue Creek, a tributary to the James River. Photograph by C Hayer.

Discussion but they also represent invasion into new habitats (e.g., smaller watersheds, limited backwaters and The James River has over 230 low head dams floodplain lakes; Coulter et al. 2013) which are which may impede movement during normal or atypical for established populations elsewhere low water years (Berry et al. 1993; Shearer and (e.g., Illinois River, Ohio River, middle Berry 2003); however, record discharge and Mississippi River; Tucker et al. 1996; Kolar et flooding in all basins in late 2010 and early 2011 al. 2007; DeGrandchamp et al. 2008). It is difficult (United States Geological Survey 2012) may to determine where these Asian carp populations have allowed for, and facilitated their unimpeded are in the invasion process (e.g., dispersal, movement and dispersal upstream and into colonization, establishment, self-sustaining) as we normally unconnected lakes. Additionally, these have not confirmed reproduction in these basins; records not only represent a range expansion, however, the presence of young-of-year silver and the northernmost records in North America, carp in the middle to upper James River suggests

287 C.-A. Hayer et al. reproduction may be occurring within the James Dieterman D, Berry Jr. CR (1998) Fish community and water River. Reproduction has been reported in the quality changes in the Big Sioux River. The Prairie Naturalist 30: 199–224 lower Missouri River (Shrank et al. 2001; Klumb Galat DL, Berry CR Jr., Peters EJ, White RG (2005a) Missouri 2007; Stukel et al. 2007), but as of November River. In: Benke AC, Cushing CE (eds), Rivers of North 2012 has not been reported in the Missouri River America. Elsevier, Oxford, pp 427–480, http://dx.doi.org/10. 1016/B978-012088253-3/50013-4 in South Dakota or Nebraska. As a direct result Galat DL, Berry CR Jr., Gardner WM, Hendrickson JC, Mestl of the rapid expansion and increasing abundance GE, Power GJ, Stone C, Winston MR (2005b) Spatio- of Asian carps in South Dakota (Hayer et al. temporal patterns and changes in Missouri River fishes. In: 2014a), the South Dakota Game, Fish and Parks Rinne JN, Hughes RM, Calamusso R (eds), Historical changes in fish assemblages of large American Rivers. Department issued an emergency regulation in American Fisheries Society Symposium, pp 249–291 2012 that closed these tributaries to commercial Hayer C-A, Howell J, Graeb BDS, Bertrand KN (2014a) An or recreational harvest of all bait fish in order to historical watershed level perspective on the persistence and prevent further spread of Asian carps. South occupancy of fishes in prairie streams. PhD dissertation, South Dakota State University, Brookings, Sd, 253 pp Dakota Missouri River tributaries support valuable Hayer C-A, Bertrand KN, Graeb BDS (2014b) Population fisheries and provide habitat for several threatened dynamics of bighead and silver carp on the northwestern and endangered species (Berry et al. 2007). front of their North American invasion. Aquatic Invasions 9: Continued monitoring and research on this newly 289–303, http://dx.doi.org/10.3391/ai.2014.9.3.05 Hoagstrom CW, Wall SS, Kral JG, Blackwell BG, Berry CR invading population of Asian carps will provide (2007) Zoogeographic patterns and faunal change of South invaluable insight into complex invasive species, Dakota fishes. Western North American Naturalist 67: 161– assist with understanding Asian carps population 184, http://dx.doi.org/10.3398/1527-0904(2007)67[161:ZPAFCO]2.0.CO;2 dynamics during an invasion, and expose the Klumb RA (2007) Shallow water fish communities in the Missouri River downstream of Fort Randall and Gavins Point negative impacts Asian carps may be having on dams in 2003 and 2004 with emphasis on Asian carps, Pierre prairie stream ecosystems. South Dakota, 156 pp Kocovsky PM, Chapman DC, McKenna JE (2012) Thermal and hydrologic suitability of Lake Erie and its major tributaries Acknowledgements for spawning of Asian carps. Journal of Great Lakes Research 38: 159–166, http://dx.doi.org/10.1016/j.jglr.2011.11.015 We would like to thank the South Dakota Game Fish and Parks Kolar CS, Chapman D, Courtenay W, Housel C, Williams J, and for their continued support of this project and specifically M. Jennings D (2007) Bigheaded carps: a biological synopsis Smith and G. VanEeckhout for continued updates on Asian carps and environmental risk assessment, Special publication 33. within the states. Additionally we would like to thank J Howell American Fisheries Society, Bethesda, 204 pp for assistance with field work. We would like to thank two Kolar CS, Chapman D, Courtenay W, Housel C, Williams J, anonymous reviewers for their improvements upon this Jennings D (2005) Asian carps of the genus Hypophthaly- manuscript. michthys (Pisces, Cyprinidae) – a biological synopsis and environmental risk assessment. Report to the U.S. Fish and References Wildlife Service. U.S. Geological Survey, LaCrosse, Wisconsin, 184 pp Berry CR Jr, Duffy WG, Walsh R, Kubeny S, Schumacker D, Lieberman DM (1996) Use of Silver carp (Hypophthalmichthys Van Eeckout G (1993) In: Hesse LW, Stalnaker CB, Benson molitrix) and Bighead carp (Aristichthys nobilis) for algae NG, Zuboy JR (eds), The James River of the Dakotas. control in a small pond: changes in water quality. Journal of Restoration Planning for the Rivers of the Mississippi River Freshwater Ecology 11: 391–397, http://dx.doi.org/10.1080/02705 060.1996.9664466 Ecosystem, Biological Report 19, National Biological Lohmeyer AM, Garvey JE (2009) Placing the North American Survey, Washington, D.C., pp 70–86 invasion of Asian carp in a spatially explicit context. Berry CR, Higgins KF, Willis DW, Chipps SR (eds) (2007) Biological Invasions 11: 905–916, http://dx.doi.org/10.1007/s105 History of fisheries and fishing in South Dakota. 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Hydrobiologia 571: 355– DeGrandchamp KL, Garvey JE, Colombo RE (2008) Movement 360, http://dx.doi.org/10.1007/s10750-006-0260-7 and habitat selection by invasive Asian carps in a large river. Poff NL, Ward JV (1989) Implications of streamflow variability Transactions of the American Fisheries Society 137: 45–56, and predictability for lotic community structure: a regional http://dx.doi.org/10.1577/T06-116.1 analysis of streamflow patterns. Canadian Journal of Deters JE, Chapman DC, McElroy B (2013) Location and timing Fisheries and Aquatic Sciences 46:1805–1818, http://dx.doi.org/ of Asian carp spawning in the lower Missouri River. 10.1139/f89-228 Environmental Biology of Fishes 96: 617–629, http://dx.doi.org/ 10.1007/s10641-012-0052-z

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Ricciardi A, Steiner WWM, Mack RN, Simberloff D (2000) Stukel S, Kral J, LaBay S (2007) 2006 Annual Report Pallid Toward a global information system for invasive species. Sturgeon Population Assessment and Associated Fish BioScience 50: 239–244, http://dx.doi.org/10.1641/0006-3568(20 Community Monitoring for the Missouri River: Segment 7. 00)050[0239:TAGISF]2.3.CO;2 South Dakota Game Fish and Parks, Yankton, South Dakota. Schmulbach JC, Braaten PJ (1993) The Vermillion River. Neither Prepared for the U.S. Army Corps of Engineers, Missouri red nor dead. In: Hesse LW, Stalnaker CB, Benson NG, River Recovery Program, March 2007, 129 pp Zuboy JR (eds), Proceedings of the symposium on restoration Tucker JK, Cronin FA, Hrabik RA, Peterson MD, Herzog DP planning for rivers of the Mississippi River ecosystem, pp (1996) The bighead carp (Hypophthalmichthys nobilis) in the 57–69 Mississippi River. Journal of Freshwater Ecology 11: 241– Schrank SJ, Braaten PJ, Guy CS (2001) Spatiotemporal variation 243, http://dx.doi.org/10.1080/02705060.1996.9663484 in density of larval bighead carp in the lower Missouri River. United States Geological Survey (2012) USGS current water data Transactions of the American Fisheries Society 130:809–814, for the nation. URL: http://waterdata.usgs.gov/nwis/rt? Accession http://dx.doi.org/10.1577/1548-8659(2001)130<0809:SVIDOL>2.0.CO;2 date September 13, 2014 Shearer JS, Berry CR Jr. (2003) Fish community persistence in United States Geological Survey (2014) Silver carp http://nas.er. eastern North and South Dakota rivers. Great Plains usgs.gov/queries/factsheet.aspx?speciesID=549 (Accessed September Research 13: 139–159 13, 2014)

Supplementary material

Table S1. First collection records for adult, juvenile, and young-of year silver and bighead carps for North and South Dakota.

Record Coordinates Number Life Stage Species State Location Record Date Reference Collected Latitude Longitude (N) (W) Adult Silver Carp 1 SD James River at Milltown 43.428253 -97.802089 2 August 2012 Current Study

Vermillion River confluence Silver Carp 9 SD 42.73362 -96.88918 16 August 2012 Current Study with the Missouri River Big Sioux River confluence Silver Carp 5 SD 42.51066 -96.47855 17 August 2012 Current Study with the Missouri River Bighead Carp 1 SD James River near Mitchell 43.70212 -97.96766 31 August 2010 Current Study Shue Creek confluence with 27 September Juvenile Silver Carp 12 SD 44.441792 -98.115286 Current Study the James River 2011 North Dakota James River below 12 October Silver Carp 1 ND 46.931042 -98.708975 Game Fish and Jamestown Dam 2011 Parks Vermillion River below East Silver Carp 15 SD 43.587875 -97.173394 11 August 2011 Current Study Lake Vermillion Dam Big Sioux River confluence Silver Carp 19 SD 42.51066 -96.47855 17 August 2012 Current Study with the Missouri River Firesteel Creek confluence 29 September Bighead Carp 6 SD 43.70212 -97.96766 Current Study with the James River 2011 Big Sioux River confluence Bighead Carp 5 SD 42.51066 -96.47855 6 October 2011 Current Study with the Missouri River Vermillion River below East Bighead Carp 4 SD 43.587875 -97.173394 11 August 2011 Current Study Lake Vermillion Dam South Dakota 2 November Silver Carp 1 SD Lake Byron 44.566761 -98.142442 Game Fish and 2012 Parks South Dakota 2 November Bighead Carp 2 SD Lake Byron 44.566761 -98.142442 Game Fish and 2012 Parks Shue Creek confluence with 29 September Age-0 Silver Carp 2 SD 44.441792 -98.115286 Current Study the James River 2011 Big Sioux River below 20 October Bighead Carp 1 SD 43.43759 -96.59552 Current Study Sioux Falls 2010

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