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Host Usage and Evidence of Chestnut Lamprey Distribution in Selected Arkansas Streams
Jeremiah M. Salinger and Ronald L. Johnson

Southeastern Naturalist, Volume 18, Issue 2 (2019): 303–313

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Southeastern Naturalist 303 J.M. Salinger and R.L. Johnson 22001199 SOUTHEASTERN NATURALIST 1V8o(2l.) :1380,3 N–3o1. 32 Host Usage and Evidence of Chestnut Lamprey Distribution in Selected Arkansas Streams Jeremiah M. Salinger1,* and Ronald L. Johnson2 Abstract - We documented distributional evidence of the parasitic fish Ichthyomyzon castaneus (Chestnut Lamprey) in selected Arkansas streams to provide information on host usage and selection of attachment sites. The species was at one point considered common in Arkansas streams, yet our sampling using boat electrofishing during late summer and fall collected Chestnut Lampreys in only 3 of the 12 streams for a total of just 8 individuals. We found evidence of Chestnut Lamprey parasitism in 7 of the 12 streams. Of the 2166 nonlamprey fishes collected, 11 individuals (0.5%) from 4 species bore evidence of Chestnut Lamprey parasitism. The most frequently parasitized host was the large-bodied, non-native Cyprinus carpio (Common Carp). There were no obvious patterns in the attachment/wound site location of parasitized fish. Further surveys of Arkansas streams are needed to evaluate trends in Chestnut Lamprey abundance and distribution. Introduction Parasitic lampreys have acquired a negative reputation throughout North America owing to the historically catastrophic damage inflicted on sportfish populations of the Great Lakes by invasive Petromyzon marinus L. (Sea Lamprey; Irwin et al. 2012, Madenjian et al. 2008, Szalai et al. 2005). Consequently, conservation of native parasitic lamprey species, other than Entosphenus tridentatus (Richardson) (Pacific Lamprey; PLTW 2017), historically has not been a high priority, although conservation attention for lampreys has increased in recent years (Maitland et al. 2015). Lack of conservation emphasis carries significant implications for both lampreys (Mesa and Copeland 2009) and indigenous peoples with economic and sociocultural interests in lampreys (Close et al. 2002, Wang and Schaller 2015). For example, lampreys have historically been a component of subsistence fisheries for Native Americans (Buklis 2002, Close et al. 2002) and are still commonly consumed outside of North America (Beaulaton et al. 2008). Species conservation efforts are likely to be ineffective without basic knowledge of identifying morphological characteristics (Neave et al. 2007), life history (Mesa and Copeland 2009), and regional distribution (Robison et al. 2011a). To illustrate the latter, only recently has the second of the 2 parasitic lamprey species found in Arkansas, Ichthyomyzon unicuspis Hubbs and Trautman (Silver Lamprey), been documented in Arkansas (Robison et al. 2011a). On the other hand, the commonly occurring I. castaneus Girard (Chestnut Lamprey) has been known from Arkansas since 1928 (Salinger et al. 2018). 1Department of Aquaculture and Fisheries, University of Arkansas at Pine Bluff, Pine Bluff, AR 71601. 2Department of Biological Sciences, Arkansas State University, State University, AR 72467. *Corresponding author - Manuscript Editor: Hayden Mattingly Southeastern Naturalist J.M. Salinger and R.L. Johnson 2019 Vol. 18, No. 2 304 Although the Chestnut Lamprey is a parasite of a variety of fishes (Cochran 2014), its impact on host populations has not been well-studied. This species is known to occur throughout eastern North America west of the Appalachian Mountains, in Canada from Manitoba in the northwest to Québec in the east, and in the US as far south as Louisiana and northwestern Alabama (Mayden et al. 1989, Renaud 2011, Renaud and de Ville 2000, Robison and Buchanan 1988). Parasitism by this species has been studied to some degree in northern areas of its range (Cochran 2014, Hall 1963, Morman 1979). Curiously, they are considered threatened in Iowa, Kansas, and Nebraska, yet few studies have been conducted focusing on lamprey distribution in these areas (Flammang and Olson 2010, Mesa and Copeland 2009, Steffensen 2015). Additionally, this species is considered data deficient in areas of its Canadian distribution and is believed to be threatened by various anthropogenic activities (COSEWIC 2010). Within Arkansas, Chestnut Lampreys are historically considered to be common (Robison and Buchanan 1988). They have been found in 43 streams of the Arkansas, Ouachita, Red, St. Francis, and White river drainages, the Mississippi River, and 4 lakes (DeGray, Hamilton, Norfork, and Webb) in Arkansas (Buchanan et al. 2003, Connior et al. 2011, Robison and Buchanan 1988, Robison et al. 2006, Salinger et al. 2018, Tumlison and Robison 2010). Apart from aspects of its spawning behavior in the Antoine River (Robison et al. 1983), biological information for Chestnut Lampreys in Arkansas has been limited to incidental captures occurring during qualitative fish sampling of streams. The objectives of our study were to (1) evaluate host usage of the Chestnut Lamprey in a state where the species has been understudied and (2) investigate evidence of its distribution using boat electrofishing in selected streams with historical records of Chestnut Lamprey presence. Field-Site Description We sampled a total of 29 river km located in 12 Arkansas streams (Fig. 1) from mid-July to early November 2015, during a time of year when Chestnut Lampreys are most actively feeding (Robison and Buchanan 1988). Streams were selected for sampling if they had a record of Chestnut Lamprey presence (Salinger et al. 2018) and availability of boat access. Streams were excluded from consideration if they had any records of Silver Lampreys (e.g., the upper White River drainage of northwest Arkansas; Robison et al. 2011a). We avoided streams with confirmed presence of the Silver Lamprey because of difficulties in differentiating wounds between lamprey species. In an attempt to representatively sample all of Arkansas’s ecoregions, we selected streams from 5 of the state’s 6 ecoregions (Cadron Creek and Little Red River from the Arkansas River Valley; Little Missouri River and Sulphur River from the Gulf Coastal Plain; Black River, Current River, and St. Francis River from the Mississippi Alluvial Plain; Fourche LaFave River, Ouachita River, and Petit Jean River from the Ouachita Mountains; and Spring River and Strawberry River from the Ozark Mountains). We did not sample Crowley’s Ridge Ecoregion due to its longitudinal narrowness and lack of higher-order streams. We selected ten 250-m reaches on each stream except Little Missouri River for sampling, with at least 1 km separating sampling reaches. Only 6 reaches were sampled in the Little Southeastern Naturalist 305 J.M. Salinger and R.L. Johnson 2019 Vol. 18, No. 2 Missouri River at the request of the Arkansas Game and Fish Commission to avoid electrofishing in sensitive trout-stocked areas. We excluded reaches from sampling if they were inaccessible or too shallow. All streams sampled were mid-order streams (Strahler numbers 4–6; Strahler 1957). The streams exhibit a diversity of habitats throughout the state, varying from the rocky substrate of the cold tailwaters of the Little Red River, to the sandy-bottomed, warmwater Strawberry River. Land use surrounding our field sites was similarly variable, varying from forested (Petit Jean River) and agricultural areas (St. Francis River) to relatively urban areas (Ouachita and Spring rivers). Methods We conducted electrofishing during daylight hours via single-pass, 60–120-Hz pulsed DC boat electrofishing using a 6-m aluminum-framed boat equipped with a 50-hp generator and GPP 5.0 electrofishing unit (Smith-Root, Inc., Vancouver, Figure 1. Ovals indicate sections of Arkansas streams sampled by boat electrofishing for evidence of Chestnut Lampreys, July-November 2015. Southeastern Naturalist J.M. Salinger and R.L. Johnson 2019 Vol. 18, No. 2 306 WA). Stunned fishes estimated to have a standard length (SL) greater than 127 mm (smallest known host size of Chestnut Lampreys; Cochran 1985) were held in an aerated 200-L live-well. The live-well was supplemented with Prime Water Conditioner (SeaChem Laboratories, GA) at a ratio of 0.1 mL/L of water to encourage mucus layer growth and protection (Harnish et al. 2011). We obtained SL (mm) and mass (g) for each captured fish immediately following the end of a reach. At the same time, we identified fish to species and examined them for the presence of lamprey wounds (Fig. 2). Lamprey wound locations on the host were assigned using a subtle modification of the system developed by Lennon (1954). Unlike Lennon (1954), we subdivided regions I and VI into dorsal (A) and ventral (B) sections (Fig. 3). Other body regions were consistent with Lennon (1954). Once measurements were taken, we released fish in the same reach in which they were captured. We measured parasitic lampreys for SL to the nearest mm, identified to species, noted as attached or free-swimming, photographed, and released them. Parasitic lampreys were determined to be Chestnut Lampreys if they possessed 6 bicuspid inner lateral teeth (COSEWIC 2010, Renaud 2011, Robison and Buchanan 1988). Figure 2. A Chestnut Lamprey wound on the dorsal fin of a Common Carp. This places the wound in Lennon’s (1954) Region II. Southeastern Naturalist 307 J.M. Salinger and R.L. Johnson 2019 Vol. 18, No. 2 Results We captured 2166 fishes representing 13 families and 58 species (Table 1). Of these, 11 individuals (0.5%) from 4 species displayed wounds attributable to a parasitic lamprey (Table 2; Figs. 2, 3). Seven of these wounded fishes were mature adult Common Carp, with a mean (± SE) SL of 621.1 ± 33.5 mm and mass of 3778.6 ± 607.7 g. No other host species had more than 2 parasitized individuals captured (Table 2, Fig. 3). No consistent positional wounding pattern was identified. Six of the 11 wounded fishes were wounded dorsally, with 2 Common Carp wounded on the dorsal fin, whereas the remainder were wounded ventrally, including 1 wounded on a pectoral fin. Wounds on 2 Common Carp occurred cranially (Table 2, Fig. 3). Eight Chestnut Lampreys were captured from 3 of the streams sampled in northeastern Arkansas (Black, Current, and Spring rivers; Fig. 1). Mean (± SE) SL of Table 1. Fishes >127 mm SL captured in 12 Arkansas streams by boat electrofishing in 2015 with evidence of Chestnut Lamprey parasitism, grouped by family. # of individuals with Number of Number of evidence of Chestnut Family species captured individuals captured Lamprey parasitism Amiidae 1 21 0 Anguillidae 1 8 0 Catostomidae 15 673 2 Centrarchidae 17 527 2 Clupeidae 3 152 0 Cyprinidae 3 125 7 Esocidae 1 1 0 Ictaluridae 5 245 0 Lepisosteidae 4 131 0 Moronidae 3 17 0 Percidae 3 4 0 Salmonidae 3 70 0 Sciaenidae 1 192 0 Figure 3. Position of attachment for fishes with evidence of Chestnut Lamprey parasitism in selected Arkansas streams, July–November 2015 (modified from Lennon 1954). Key: CC = Common Carp, RR = River Redhorse, SB = Spotted Bass, SS = Spotted Sucker. Southeastern Naturalist J.M. Salinger and R.L. Johnson 2019 Vol. 18, No. 2 308 the 8 captured lampreys was 205.0 ± 17.9 mm. Of these, 4 were captured while attached to hosts (all Common Carp) or self-dislodged from their hosts upon or after capture (Table 2). Mean self-dislodged lamprey SL was 236.2 ± 16.2 mm. No Silver Lampreys were captured. We collected parasitized fishes from 7 of the 12 streams sampled, including 1 from Cadron Creek (Arkansas River drainage); 3 from Black River, 1 from Current River, 3 from Spring River, and 1 from Strawberry River (Black River drainage); 1 from Little Missouri River (Ouachita River drainage); and 1 from Little Red River (White River drainage) (T able 3, Fig. 1). Table 2. Lamprey-wounded fishes captured in 12 Arkansas streams (July–November 2015) by boat electrofishing, grouped by species. Individuals marked with an asterisk were captured with an attached Chestnut Lamprey. Attachment site or wound locations are illustrated in Figure 3. Attachment site Host species or wound location SL (mm) Mass (g) Stream Common Carp II 493 1830 Current River Common Carp* IA 505 1640 Black River Common Carp* II 630 3530 Spring River Common Carp II 660 4080 Black River Common Carp* II 660 4100 Spring River Common Carp VIB 670 4500 Spring River Common Carp* IA 730 6770 Black River River Redhorse III 480 900 Little Missouri River Spotted Bass II 260 200 Strawberry River Spotted Bass III 162 100 Cadron Creek Spotted Sucker II 263 202 Little Red River Mean (± SE) 501 (56) 2532 (633) Table 3. Twelve streams located in 5 ecoregions sampled for Ichthyomyzon castaneus (Chestnut Lamprey) by boat electrofishing, July–November 2015, to assess host usage and distribution. Chestnut Lamprey attached to a host fish was considered to be direct evidence of parasitism, whereas a wounded host without a lamprey attached at the time of the host’s capture was considered indirect evidence. Evidence of Chestnut Chestnut Lamprey Parasitism Stream Ecoregion Lamprey collected? Direct Indirect Cadron Creek Arkansas River Valley No No Yes Little Red River Arkansas River Valley No No Yes Little Missouri River Gulf Coastal Plain No No Yes Sulphur River Gulf Coastal Plain No No No Black River Mississippi Alluvial Plain Yes Yes Yes Current River Mississippi Alluvial Plain Yes No Yes St. Francis River Mississippi Alluvial Plain No No No Fourche LaFave River Ouachita Mountains No No No Ouachita River Ouachita Mountains No No No Petit Jean River Ouachita Mountains No No No Spring River Ozark Mountains Yes Yes Yes Strawberry River Ozark Mountains No No Yes Southeastern Naturalist 309 J.M. Salinger and R.L. Johnson 2019 Vol. 18, No. 2 Discussion Robison and Buchanan (1988) stated that the Chestnut Lamprey was common in Arkansas. However, the results of our study and other studies may indicate otherwise (Buchanan et al. 2003, Connior et al. 2011; McAllister et al. 2010; Robison et al. 2006, 2011b; Tumlison and Robison 2010). However, it must be noted that our study was of limited geographic scope (i.e., only 12 streams were sampled), did not sample stream sections lower than 4th order or higher than 6th order, and was performed during late summer and fall, which may limit its utility in drawing conclusions about the distribution and abundance of Chestnut Lampreys. Sampling during the spring spawning migration of the Chestnut Lamprey may be more informative, but heavy rainfall resulting in high flows and turbidity during this time may prohibit effective sampling. We documented evidence of Chestnut Lampreys from only 7 of 12 study streams, with only sporadic evidence of lamprey attacks in central or southern Arkansas. Each Chestnut Lamprey individual that we collected was from northeastern Arkansas. It is plausible that some wounded fishes reported in Table 2 were parasitized by Silver Lampreys, despite our avoidance of streams in northwestern Arkansas where Silver Lampreys have been documented. The presence of the Silver Lamprey in Arkansas was only recently established (Robison et al. 2011a), and its statewide distribution has not been adequately studied. Particularly notable was the lack of evidence of Chestnut Lampreys from the Ouachita River, where 27 of the 250 Arkansas Chestnut Lamprey collection records occur (Salinger et al. 2018). Chestnut Lampreys have been collected over a 44-year period from this stream, and as recently as 2013. Therefore, we find it unlikely that the species has been extirpated from the Ouachita River. Of the 177 fishes collected in the Ouachita River, none were parasitized by lampreys, yet the sample included several species (e.g., Hypentelium nigricans Lesueur [Northern Hog Sucker], Ictalurus punctatus Rafinesque [Channel Catfish], Micropterus salmoides Lacepède [Largemouth Bass], and assorted Moxostoma spp. [redhorse suckers]) previously identified as Chestnut Lamprey hosts (Cochran 2014). Further, only 1 parasitized fish was collected from southern Arkansas (Little Missouri River), despite a recent documented southern range expansion for the Chestnut Lamprey in Arkansas (Robison et al. 2006). Despite a low number of captures, the frequency of fish parasitized in the present study (0.5%) is similar to that of Hubley (1961), who observed 0.2% of fishes in the Upper Mississippi River in Wisconsin to be parasitized by Chestnut Lampreys. In contrast, Hall (1963) noted that up to one-third of Salvelinus fontinalis Mitchill (Brook Trout) and S. namaycush Walbaum in Artedi (Lake Trout) observed during field sampling and creel surveys in Michigan’s Manistee River were parasitized by Chestnut Lampreys. None of the 70 salmonids, primarily Oncorhynchus mykiss Walbaum (Rainbow Trout), we captured in the Little Red River were parasitized. It must be noted that the sampling in this section was performed in hypolimnetic waters, which severely alters and restricts species diversity (Johnson et al. 2006), and may possibly limit the local presence of the Chestnut Lamprey. Southeastern Naturalist J.M. Salinger and R.L. Johnson 2019 Vol. 18, No. 2 310 Three of the four fish species parasitized have previously been identified in the literature as serving as Chestnut Lamprey hosts (Common Carp, Moxostoma carinatum Cope [River Redhorse], and Minytrema melanops Rafinesque [Spotted Sucker]; Cochran 2014; Flammang and Olson 2010; Hubley 1961; Mayden et al. 1989; Ryon and Loar 1988; Sever and Mould 1981; Tumlison and Robison 2010). If the wounds we observed were indeed caused by Chestnut Lamprey, Micropterus punctulatus Rafinesque (Spotted Bass) would represent a new host record for the Chestnut Lamprey, although other members of the genus Micropterus have been previously identified as hosts (Cochran 2014). The most frequently parasitized fish in our study were mature Common Carp. A small sample size limits conclusions resulting from these findings. However, one potential explanation could be selection for larger hosts maximizing blood meal size, as demonstrated by laboratory feeding experiments (Cochran 1985). However, we collected other equally large-sized potential hosts such as Ictiobus spp. (buffalo; Cochran 2014) and Atractosteus and Lepisosteus spp. (gars; Cochran 2004), yet none of these were documented as hosts in our study. A second potential explanation for the more frequent parasitism of Common Carp is its non-native status. Other studies have documented native lamprey species often feeding on non-native hosts (Hume et al. 2013, Inger et al. 2010, Lubinski et al. 1986, Weitkamp et al. 2015). This occurrence may be an example of behavioral plasticity leading to host-switching (Bush 2009, Hoberg and Brooks 2008), a hypothesis that merits further study. It is possible that we would have found more evidence of Chestnut Lampreys if we had attempted to sample with other gear types as suggested by Moser et al. (2007); however, many of the traditionally used methods for sampling lampreys were either unavailable to us or impractical for logistical reasons. As we were sampling mid-order streams, we were limited to sampling using boat electrofishing. We would suggest that future researchers attempt to use multiple gear types. Future researchers may also find it beneficial to incorporate sampling techniques not traditionally used in aquatic biology research, such as pheromone-baited traps (Johnson et al. 2005, Yun et al. 2014) or environmental DNA sampling (Gingera et al. 2016, Takahara et al. 2012). Finally, we would also encourage future researchers to describe the occurrence of Chestnut Lampreys in relation to stream habitat variables, as this aspect of Chestnut Lamprey ecology remains understudied. Acknowledgments This research was conducted under Arkansas Game and Fish Commission Scientific Collection Permit #051420151, issued to J.M. Salinger. This research would not have been possible without the assistance of our field technicians, Joshua Lukac and Taylor Mackey, as well as Justin Stroman, Kyle Swallow, Brian Wagner, and the many other members of the Arkansas Game and Fish Commission’s Fisheries Division, past and present, who have put forth the time and effort to make this research possible. The Arkansas Department of Environmental Quality generously allowed us access to several Chestnut Lamprey records heretofore unavailable to us, which were indispensable in selection of study sites. We are Southeastern Naturalist 311 J.M. Salinger and R.L. Johnson 2019 Vol. 18, No. 2 also indebted to Jennifer Bouldin and Jerry Farris for loaning us equipment used during the field season, as well as to Casey Cox and Tracy Klotz for their invaluable boat maintenance advice. Helpful input from Richard Grippo, Paul Sikkel, and the late Philip Cochran improved the design of the study. Shannon Smith and Douglas Zentner assisted in the construction of Figure 1. A review of the manuscript by Steve Lochmann improved the te final manuscript product. Lastly, we are grateful to the faculty and staf f, particularly Pablo Bacon, of the L.A. Logan Biological Field Station, Southern Arkansas University, for housing the research team during part of its field season. Literature Cited Beaulaton, L., C. Taverny, and G. Castelnaud. 2008. Fishing, abundance, and life-history traits of the anadromous Sea Lamprey (Petromyzon marinus) in Europe. Fisheries Research 92:90–101. Buchanan, T.M., D. Wilson, L.G. Claybrook, and W.G. Layher. 2003. Fishes of the Red River in Arkansas. Journal of the Arkansas Academy of Science 57:18–26. Buklis, L.S. 2002. Subsistence fisheries management on federal public lands in Alaska. Fisheries 27:10–18. Bush, S.E. 2009. Does behavioural flexibility facilitate host switching by parasites? Functional Ecology 23:578–586. Close, D.A., M.S. 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