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

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).


Introduction
Invasive species are becoming a worldwide epidemic and are triggering changes in the structure and function of invaded ecosystems (Ricciardi et al. 2000).One pair of global invaders, bighead, Hypophthalmichthys nobilis (Richardson, 1845), and silver carp, H. molitrix (Valenciennes, 1844), (collectively referred to as Asian carps) have been introduced intentionally and unintentionally throughout the world, mostly for aquaculture purposes (Kolar et al. 2007) as they are the most important aquaculture species in Asia and eastcentral Europe (Lieberman 1996;Penman et al. 2005).Bighead carp have been introduced to 74 countries and are reproducing in 19 and the silver carp has been introduced to 88 countries and are reproducing in 23 (Kolar et al. 2007).Both species of Asian carps are currently reproducing in the United States (Papoulias et al. 2006;DeGrandchamp et al. 2007;Lohmeyer and Garvey 2009;Deters et al. 2013).Asian carps were originally introduced into the southern United States in aquaculture ponds in the early 1970s where both species subsequently escaped and began their expansion through numerous dams on the Mississippi River and into associated tributaries (e.g., Missouri River, Illinois River, Ohio River; Kolar et al. 2007;USGS 2014).The northern extent of the Asian carps expansion is in the Mississippi River basin.They could potentially colonize the Great Lakes through the Chicago Shipping Canal (e.g., Lake Michigan) and the Illinois River, a tributary to the Mississippi River (Kocovsky et al. 2012).The eastern range includes the Ohio River where they threaten to enter the Great Lakes (e.g., Lake Erie) through the Wabash River, a tributary to the Ohio River, and the Maumee River, the second largest tributary to Lake Erie (Kocovsky et al. 2012).On the northwestern part of their expansion, Asian carps threaten to colonize three tributaries (e.g., James, Vermillion, and Big Sioux rivers) to the Missouri River below Gavins Point Dam, that serve as important fish habitat for many threatened and endangered fishes (Berry et al. 2007).These tributaries already face disturbance from current and present land use practices and natural physio-chemical and hydrologic fluctuations characteristic of prairie streams (Matthews 1988;Poff and Ward 1989;Hayer et al. 2014a).Prior to this study, the distribution and use by Asian carps of these three Missouri River Plains tributaries in South Dakota were unknown.However; one bighead carp was caught by an angler in the middle James River near Mitchell, South Dakota in 2008 and one silver carp was caught by an angler in the Big Sioux River near Canton, SD in 2004 (Kolar et al. 2005).The goal of this paper is to document the northwestern invasion front of adult, juvenile, and young-ofyear Asian carps in three prairie tributaries and other South Dakota waters (e.g., lakes) by providing the northern most latitude detection locations.

Methods
Three prairie tributaries in South Dakota converge with an unchannelized section (Galat et al. 2005a) of the Missouri River just downstream of Gavins Point Dam: the James, Vermillion and Big Sioux rivers.Gavins Point Dam is 23 m high hydroelectric dam and is the lower most dam on the Missouri River.No carp have been found upstream of this barrier.The three warmwater tributaries drain the Central Lowlands physiographic province in South Dakota (Galat et al. 2005b) and are characterized by low gradient streams of glacial origin (Hoagstrom et al. 2007).The James River (watershed area = 57,000 km 2 ) extends 760 Rkm from southeastern North Dakota through eastern South Dakota to its confluence with the Missouri River (Berry et al. 1993; Figure 1).The James River contains over 200 lowhead dams (approximately 1-2 meters) that are passable by fish during high water (Berry et al. 1993;Shearer and Berry 2003) and 28 meter high dam in the North Dakota part of the river (Berry et al. 1993).The Vermillion River, the smallest basin (watershed area = 5,800 km 2 ) extends 243 Rkm from the confluence of West and East Fork Vermillion rivers to its confluence with the Missouri River (Schmulbach and Braaten 1993; Figure 1).The Vermillion River contains one larger dam, East Vermillion Lake Dam, which creates Vermillion Lake and is 12 m high (Hayer et al. 2014b).The Big Sioux River (watershed area = 23,325 km 2 ) extends 470 Rkm from the Prairie Coteau of northeastern South Dakota to its confluence with the Missouri River at the South Dakota-Nebraska-Iowa border (Figure 1).The Big Sioux River contains a set of natural falls that are deemed impassable by fish (Dieterman and Berry 1998;Galat et al. 2005).The highest fall is 8 m high.
Standardized boat electrofishing occurred between 2009 and 2012 at five sites on the James River, two sites on the Vermillion River, and three sites on the Big Sioux River (Figure 1), all within South Dakota.Sampling consisted of three 10 minute electrofishing runs which generally covered three river kilometers.Sampling occurred once during each of three seasons: spring (May - June), summer (July -August), and fall (September -October).Additional non-standardized boat electrofishing occurred at various sites on the James River in North and South Dakota.Adult carps were considered to be greater than 600 mm TL (age 3+), juveniles were between 300 and 600 mm TL (ages 1 and 2), and age-0 were less than 300 mm TL.Life stage ages were verified by analyzing otoliths (Hayer et al. 2014b).

Results
Our data suggest that Asian carps dispersion has been slowed or halted in these Missouri River tributaries due to artificial and natural barriers.These barriers are the most upstream collections within these river basins (Figure 1) where bighead and silver carp were detected (Figures 2  -4).These findings represent the northernmost Asian carps detections in North America (46.931042, -98.708975).

Adults
One adult silver carp was collected as far upstream as Milltown on the James River (TL = 752,4958 g) on August 2, 2012 (Figure 2) and have not been collected above the confluence of the Vermillion River with the Missouri River where nine silver carp were last collected on August 16, 2012 (TL = 681 -784 mm; 3203 -7285 g; Figure 2).Silver carp have also only been collected in the Big Sioux River at the confluence with the Missouri River and were last collected on August 17, 2012 (N = 5; TL = 634-783 mm; 3260-6123 g; Figure 2).One adult bighead carp was collected near Mitchell (August, 31 2010) on the James River (TL = 1001, 9072 g) and no adults have been collected in the Vermillion or the Big Sioux Rivers (Figure 2).

Juveniles
Twelve juvenile silver carp were collected from Shue Creek, a tributary to the James River north of Huron on September 27, 2011 (TL = 409 -507; 768 -1474 g; Figure 3).One juvenile silver carp (450 mm, 1088 g) was subsequently collected in North Dakota on the James River in the Jamestown Reservoir tailrace (Figures 3, 4) on October 12, 2011.This is the first record of silver carp in North Dakota.Fifteen silver carp (TL = 311-369 mm, 299-656 g) were collected from the Vermillion River below East Lake Vermillion dam on August 11, 2011 and nineteen were collected in the Big Sioux River at the confluence with the Missouri River (TL = 384 -474 mm; 510 -1191; Figure 3) on August 17, 2012.
Six juvenile bighead carp (415 -509 mm TL, 822 -1389 g) were first collected from Firesteel Creek, a tributary to the James River near Mitchell on September 29, 2011 and were last collected  in the Big Sioux River (N = 5; TL = 349-470 mm; 288-1389 g) on October 6, 2011 at the confluence with the Missouri River (Figure 3).Four bighead carp (309-372 mm TL, 299-565 g) were first collected from the Vermillion River below the East Vermillion Lake Dam on August 11, 2011 (Figure 3).

Lakes
Two bighead carp and one silver carp (TL approximately between 400 and 460 mm) were collected by a commercial fisherman with a seine pull on November 2, 2012 from Lake Byron which is the first confirmed lentic record in South Dakota (South Dakota Game Fish and Parks, personal communication).

Discussion
The James River has over 230 low head dams which may impede movement during normal or low water years (Berry et al. 1993;Shearer and Berry 2003); however, record discharge and flooding in all basins in late 2010 and early 2011 (United States Geological Survey 2012) may have allowed for, and facilitated their unimpeded movement and dispersal upstream and into normally unconnected lakes.Additionally, these records not only represent a range expansion, and the northernmost records in North America, but they also represent invasion into new habitats (e.g., smaller watersheds, limited backwaters and floodplain lakes; Coulter et al. 2013) which are atypical for established populations elsewhere (e.g., Illinois River, Ohio River, middle Mississippi River; Tucker et al. 1996;Kolar et al. 2007;DeGrandchamp et al. 2008).It is difficult to determine where these Asian carp populations are in the invasion process (e.g., dispersal, colonization, establishment, self-sustaining) as we have not confirmed reproduction in these basins; however, the presence of young-of-year silver carp in the middle to upper James River suggests reproduction may be occurring within the James River.Reproduction has been reported in the lower Missouri River (Shrank et al. 2001;Klumb 2007;Stukel et al. 2007), but as of November 2012 has not been reported in the Missouri River in South Dakota or Nebraska.As a direct result of the rapid expansion and increasing abundance of Asian carps in South Dakota (Hayer et al. 2014a), the South Dakota Game, Fish and Parks Department issued an emergency regulation in 2012 that closed these tributaries to commercial or recreational harvest of all bait fish in order to prevent further spread of Asian carps.South Dakota Missouri River tributaries support valuable fisheries and provide habitat for several threatened and endangered species (Berry et al. 2007).Continued monitoring and research on this newly invading population of Asian carps will provide invaluable insight into complex invasive species, assist with understanding Asian carps population dynamics during an invasion, and expose the negative impacts Asian carps may be having on prairie stream ecosystems.

Figure 1 .
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.

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

Figure 3 .
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 .
Figure 4. Juvenile silver carp collected in North Dakota on the James River below Jamestown Dam.Photograph by G. VanEeckhout.

Figure 5 .
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 .
Figure 6.Two young of year silver carps collected in Shue Creek, a tributary to the James River.Photograph by C Hayer.