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California Roach (Hesperoleucus Symmetricus)Intheeel River of Northwestern California: Native Or Introduced?

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California Roach (Hesperoleucus Symmetricus)Intheeel River of Northwestern California: Native Or Introduced? Environ Biol Fish (2019) 102:771–781 https://doi.org/10.1007/s10641-019-00870-x California roach (Hesperoleucus symmetricus)intheEel River of northwestern California: native or introduced? Andrew P. Kinziger & Rodney J. Nakamoto & Andy Aguilar & Bret C. Harvey Received: 26 September 2018 /Accepted: 3 March 2019 /Published online: 15 March 2019 # Springer Nature B.V. 2019 Abstract To explore the history of California roach findings for two other California cyprinids introduced (Hesperoleucus symmetricus) in the Eel River, we com- into the Eel River from adjacent drainages, Sacramento piled mitochondrial DNA data for the putatively intro- pikeminnow (Ptychocheilus grandis) and speckled dace duced Eel River population and comparative collections (Rhinichthys osculus). from throughout the native range. Consistent with an introduction scenario, we found that: 1) one haplotype Keywords Invasion genetics . Mitochondrial DNA . occurred at high frequency in the Eel River, Russian Genetic diversity. Introduced species . California roach . River and Clear Lake populations, making the Russian Hesperoleucus symmetricus River and Clear Lake likely source areas, and 2) the introduced population exhibited reduced haplotype di- versity in comparison to populations from the native Introduction range. However, we also detected four private haplo- types in the putatively introduced population, despite Efforts to slow the rate of fish introductions would examining 269 individuals from the likely source areas. benefit from better understanding of invasion pathways. Extrapolation of the haplotype richness of the likely Much effort has focused on intercontinental introduc- source population suggested that even with the large tions. However, particularly for drainages with relative- sample size, many haplotypes in the source population ly few species, the possibility of introductions from remained uncollected. The most parsimonious conclu- vicinal sources also deserves consideration. Even in sion of our results is a recent introduction of a small cases of likely introduction from nearby sources, deter- number of California roach to the Eel River of Califor- mining if a species is native or introduced, and identifi- nia from a nearby drainage. This result aligns with cation of source populations, can be surprisingly diffi- cult. Historic field surveys can inform questions about A. P. Kinziger (*) species’ introductions, but these are subject to the prob- Department of Fisheries Biology, Humboldt State University, One lem of imperfect detection (e.g., MacKenzie et al. 2003). Harpst Street, Arcata, CA 95521, USA Modern genetic methods have greatly facilitated the e-mail: [email protected] identification of introduced species, but in some cases R. J. Nakamoto : B. C. Harvey their application has left substantial uncertainty about U.S. Forest Service, Pacific Southwest Research Station, 1700 whether a species is native or introduced (e.g., Scott Bayview Drive, Arcata, CA 95521, USA et al. 2009; Rezansoff et al. 2015; see also Carlton A. Aguilar 1996). Department of Biological Sciences, California State University, The presence of California roach (Heperoleucus 5151 State University Drive, Los Angeles, CA 90032, USA symmetricus) in the Eel River of northwestern 772 Environ Biol Fish (2019) 102:771–781 California represents the challenges that can arise in (Lock et al. 2006), providing a possible colonization efforts to explain current freshwater fish distributions opportunity. Also, the native range of California roach from observational data. The species is currently abun- includes several smaller coastal drainages south of the dant and broadly distributed in the Eel Drainage. But Eel River and north of the Russian River (Moyle 2002). California roach were not detected by a foundational We studied mitochondrial DNA variation in Califor- study of fish distributions in coastal Oregon and north- nia roach from the Eel River and surrounding native ern California at the end of the nineteenth Century populations in an attempt to clarify the origin of the Eel (Snyder 1908), nor by a variety of surveys conducted River population. First, we estimated genetic distances in the 1930s and 1950s in many portions of the Eel and constructed statistical parsimony networks to re- River drainage with water temperature suitable for Cal- solve genetic relationships and identify the likely source ifornia roach (e.g., CDFG 1934, 1959a). In 1959, Cal- populations. Second, we compared the genetic diversity ifornia Department of Fish and Game personnel record- of the Eel River population to surrounding native pop- ed Bunidentified cyprinids^ in the Eel River between ulations to determine if there were reductions in genetic Cape Horn Dam and Van Arsdale Dam, the first docu- diversity consistent with expectations for introduced mentation of cyprinids in the basin (CDFG 1959b). The populations. Population genetics predicts that intro- first record of California roach in the Eel River drainage duced species should experience founder effects as in- comes from an October 1967 collection in Yager Creek dicated by shifts in haplotype frequency and reductions analyzed by W. I. Follett, then the Curator of Fishes at in diversity in comparison to the source population the California Academy of Sciences (Follett 1968). Cal- (Dlugosch and Parker 2008). We included collections ifornia roach were not found at this site in a survey from the entire geographic range of California roach conducted three years earlier (CDFG 1964). In 1968, because the accuracy of assignment of sources popula- cyprinids were recorded from Bull Creek, a tributary of tions depends upon having sampled all potential sources the lower South Fork Eel River (California Department as well as the degree of genetic differentiation among of Fish and Game (CDFG) Field Note 1968); 1973 and them (Muirhead et al. 2008). 1974 surveys of the same tributary specifically identify California roach (CDFG Field Note 1973, 1974). Addi- tional surveys in the 1970’s suggest a broadening distri- Materials and methods bution of California roach in the Eel River. The species was apparently encountered at multiple sites in the Van We compiled mitochondrial DNA sequence data from a Duzen and South Fork Eel rivers in 1971 and was total of 541 individuals, combining 164 individuals abundant at South Fork Eel River sites in 1972 (Fite from Aguilar and Jones (2009)withan additional 377 1973). However, California roach apparently remained individuals collected and sequenced for this study absent in the early 1970s from parts of the drainage (Fig. 1,Table 1). Samples used in this study were where they are now abundant, such as the North Fork collected across a 12 year span, ranging from 2004 to of the Eel River (e.g., CDFG 1972a, b). Also, as might 2016. Aguilar and Jones (2009) conducted a phyloge- be expected for an introduced population, California netic analysis of samples from throughout the range of roach in the Eel River are not found in reaches above a California roach, providing a description of mitochon- barrier to upstream migration on the Van Duzen River drial variation in eight putative subspecies. However, that support Sacramento sucker (Catostomus Aguilar and Jones (2009) did not include the Eel River occidentalis), an obligate freshwater species apparently in their study. We analyzed 108 individuals from the Eel native to the basin. A recent range-wide genomics study River and bolstered samples sizes from possible source of California roach has concluded that California roach populations by adding 249 individuals from the Russian in the Eel Drainage were introduced (Baumsteiger et al. River (259 total), 12 individuals from the Sacramento 2017). River (67 total), and eight individuals from the Navarro Several other observations make the apparent non- River (18 total). We collected specimens for this study native status of California roach in the Eel River intrigu- by seining or backpack electrofishing. Whole specimens ing. Geologic evidence indicates that approximately 2 or tissue were preserved in 95% ethanol. All whole million years ago, portions of the current Eel River specimens were deposited into the Humboldt State Uni- drainage flowed southward into the Russian River versity Fish Collection. Environ Biol Fish (2019) 102:771–781 773 Fig. 1 The distribution of collection locations used for mitochondrial DNA analysis of California roach Whole genomic DNA was extracted from fin tissue DNA data that included 322 base pairs of the NADH- using chelex methods (Walsh et al. 1991). We se- 2 subunit and 293 base pairs of control region. Ampli- quenced a 615-base-pair fragment of mitochondrial fication primers, thermocycling temperatures and times, 774 774 Table 1 Group, sample location, number of fish sequenced, longitude, latitude and accession numbers for Humboldt State University (HSU) Fish Collection when available for California roach used for mitochondrial DNA analysis Group Location N Longitude Latitude Accession number Eel Bull Creek 8 −124.014 40.35151 HSU 5408 Eel East Branch South Fork 8 −123.781 40.07403 HSU 5402 Eel South Fork Eel River 21 −123.814 40.21778 HSU 5404 Eel Van Duzen River 18 −123.963 40.48444 HSU 5403 Eel Williams Creek 5 −123.144 39.83133 Eel Black Butte River 6 −123.084 39.82355 Eel Outlet Creek 19 −123.381 39.59460 HSU 5400 Eel North Fork Eel River 19 −123.350 39.93772 HSU 5405 Eel Salt Creek 4 −123.366 40.13139 Russian East Fork Russian River 1 −123.123 39.24722 HSU 5410 Russian Russian River 6
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