Taxonomic status and distribution of the lamprey ichthyomyzon cf. gagei.
When Hubbs and Trautman (1957) described the southern brook lamprey, Ichthyomyzon gagei, during a revision of the genus Ichthyomyzon, they suggested that this nonparasitic species was derived from the parasitic chestnut lamprey I. castaneus, a suggestion that paralleled the proposed evolution of other nonparasitic Ichthyomyzon species from parasitic ancestors. They found no reason to assume, however, that each parasitic Ichthyomyzon species would give rise to only one nonparasitic form. They speculated that additional nonparasitic derivatives of I. castaneus might exist, and that I. gagei might have had a polyphyletic origin. Sixty years later, we consider these issues anew.
Cochran (1987) noted that there was no a priori reason to expect independent nonparasitic offshoots of Ichthyomyzon castaneus to be morphologically distinguishable from each other. However, that expectation might be modified if speciations occurred at different times. According to trends identified by Hubbs and Trautman (1957), older nonparasitic offshoots should have diverged more from I. castaneus and have a relatively shorter oral disk and snout and more degenerate teeth. The older nonparasitic offshoots might also have fewer teeth (Raney, 1952), although Potter (1980) suggested a tendency for tooth counts in nonparasitic species to first increase and then decrease evolutionarily. Finally, according to Hubbs and Trautman (1957), the older offshoots should be more similar to I. castaneus by having shorter relative branchial and tall lengths.
For many years, only three species of Ichthyomyzon were thought to occur in the upper Mississippi River basin in Wisconsin and Minnesota: the parasitic chestnut lamprey and the parasitic silver lamprey, I. unicuspis, and its nonparasitic derivative the northern brook lamprey, I. fossor. In the 1980s, a fourth species was discovered in the St. Croix River watershed of northwestern Wisconsin and northeastern Minnesota (Cochran, 1987; Cochran and Pettinelli, 1988). This nonparasitic species was morphologically similar to I. gagei, the nearest populations of which were 900 km to the S in southern Missouri. Cochran (1987) tentatively assigned the St. Croix specimens to I. gagei pending further analyses. However, he suggested that these specimens might represent a new taxon. More recently, individuals from Wisconsin and Minnesota have been referred to as I. cf. gagei (Cochran and Gripentrog, 1992; Lyons, 1992) to better reflect the uncertainty regarding their identity.
We present here a morphological comparison between Wisconsin populations of Ichthyomyzon cf. gagei and populations of I. gagei from the southern United States in order to clarify the taxonomic status of I. cf. gagei. We also provide updated information on the distribution of I. cf. gagei in the upper Mississippi River basin.
MATERIALS AND METHODS
For morphological comparisons, we made counts and measurements on museum specimens from throughout the range of Ichthyomyzon gagei and I. cf. gagei (see Material Examined). Counts were made for five meristic variables: number of trunk myomeres, number of pigmented sensory pores on the trunk, number of bicuspid circumoral teeth (both sides combined), number of teeth in the lateral row and number of supraoral cusps. Measurements were made to the nearest 0.1 mm for seven morphometric variables: total length, branchial length, body depth, disk length, eye length, snout length and tail length. We made counts and measurements on the left side following procedures in Hubbs and Trautman (1937).
Kott et al. (1988) suggested that the relative length of the urogenital papilla was of particular taxonomic value in nonparasitic lampreys. Accordingly, we measured urogenital papilla length in male Ichthyomyzon gagei and I. cf. gagei to the nearest 0.1 mm. We also measured samples of I. fossor and I. castaneus (see Material Examined) to check our consistency with Kott et al. (1988).
Ichthyomyzon cf. gagei and I. gagei were compared statistically using the Mann-Whitney U test for meristic variables and an analysis of covariance for natural log-transformed morphometric variables, with total length as the covariate (SAS, 1990). Differences were considered significant if P [less than] 0.05 (two-tailed tests). Principal components analyses of the five meristic variables (correlation matrix) and of the seven morphometric variables (sheared analysis of covariance matrix of natural log-transformed variables; Bookstein et al., 1985) were used to analyze morphological variation within and between the two putative taxa.
We determined the distribution of Ichthyomyzon cf. gagei primarily from extensive fish sampling in Wisconsin and eastern Minnesota from 1982-1995. Vouchers of all lampreys collected were deposited in the University of Wisconsin Zoological Museum (UWZM), Madison; museum numbers and specific collection information are available from John Lyons. We also re-examined existing museum holdings of Ichthyomyzon from Wisconsin and Minnesota.
We found six significant morphological differences between Ichthyomyzon cf. gagei and I. gagei in univariate analyses. Ichthyomyzon cf. gagei had a significantly higher number of bicuspid teeth (Table 1) and longer branchial length, eye length and tail length, whereas I. gagei had a significantly longer snout (Table 2). Male I. cf. gagei had a relative urogenital papilla length significantly shorter than that of I. gagei. However, there was extensive overlap between the two taxa for all variables.
[TABULAR DATA FOR TABLE 1 OMITTED]
Principal components analysis of the five meristic variables revealed no major differences between I. cf. gagei and I. gagei. The first three principal components explained 69% of the variation. The first component loaded most heavily on number of bicuspid teeth (0.66) and supraoral cusps (0.59), the second on number of lateral teeth rows (0.72), and the third on number of trunk myomeres (0.85). Overlap was extensive between the two taxa on all three components.
Some separation between Ichthyomyzon cf. gagei and I. gagei was evident in the shared principal components analysis of the seven morphometric variables. The first three components combined accounted for 89% of the variation. The first component explained 61% of the variance and accounted for variation in size among specimens, with moderate loadings (0.32 to 0.44) on all seven variables. The second (18% of variance) and third components (9.5%) accounted for much of the variation in shape. The second component loaded most heavily on eye (-0.69), snout (0.54), and disk lengths (0.45). A plot of components one and two [ILLUSTRATION FOR FIGURE 1 OMITTED] showed that most I. gagei had high scores on component two, indicating that they had relatively short eyes and long snouts and disks, whereas most I. cf. gagei had low scores and thus had relatively large eyes and short snouts and disks. The third component loaded most heavily on disk (-0.60), eye (-0.46), and total lengths (0.40), and the two taxa overlapped extensively in scores for this component.
Ichthyomyzon cf. gagei was more widely distributed than previously known. We collected [TABULAR DATA FOR TABLE 2 OMITTED] I. cf. gagei from parts of three watersheds in the upper Mississippi basin [ILLUSTRATION FOR FIGURE 2 OMITTED]: the St. Croix River above St. Croix/Taylors Falls (Minnesota and Wisconsin), the Black River above Lake Arbutus (Wisconsin), and the Wisconsin River above the city of Wausau (Wisconsin). Ichthyomyzon cf. gagei was sometimes found with its close relative the parasitic I. castaneus, but never with other nonparasitic lamprey species. Ichthyomyzon cf. gagei and I. castaneus occurred together commonly in the St. Croix and rarely in the Wisconsin, but did not co-occur in the Black River drainage. The distribution of I. cf. gagei was complementary with I. fossor and American brook lamprey Lampetra appendix, the two other nonparasitic species in this region.
Our morphological analyses do not resolve the taxonomic status of Ichthyomyzon cf. gagei. Some evidence supports recognition of I. cf. gagei as a species distinct from I. gagei. We found six significant morphological differences between I. cf. gagei and I. gagei. Multivariate analyses indicated differences in shape between the two taxa. The greatly disjunct geographic ranges of I. cf. gagei and I. gagei and the extensive areas of unfavorable large-river habitat between the nearest populations of the two taxa make gene flow between them unlikely, further supporting specific status for I. cf. gagei. Conversely, other evidence argues against considering I. cf. gagei as a separate species. There was extensive overlap in all morphological characteristics between I. cf. gagei and I. gagei. Clearly, molecular genetic analyses will be necessary to help resolve the status of I. cf. gagei. In the meantime, we recommend continuing use of I. cf. gagei when referring to Wisconsin and Minnesota populations, to indicate their uncertain identity.
If the trends identified by Hubbs and Trautman (1937) are valid, then the morphological differences between I. cf. gagei and I. gagei are inconsistent with expectations if one were a substantially older offshoot of I. castaneus. The significantly shorter snout of I. cf. gagei would fit with it being the older derivative, but the significantly shorter branchial and tail lengths of I. gagei and its lower number of bicuspid circumoral teeth support the opposite conclusion.
Our results for relative urogenital papilla length were only partially concordant with those of Kott et al. (1988). We have expressed our results relative to total length for consistency with our other analyses, unlike Kott et al. (1988), who related urogenital papilla length to branchial length. Our value for the mean ratio of urogenital papilla length to branchial length for Ichthyomyzon gagei (22.1) was lower than any of the values for this species reported by Kott et al. (1988), and our range of values was much wider, although there was substantial overlap (11.0-38.7, N = 23 vs. 22.7-33.3, N = 6). Our mean value for I. fossor (11.6) was similar to that (10.5) of Kott et al. (1988), although our range was narrower (10.5-13.1, N = 5 vs. 6.7-21.7, N = 25). All of our values were greater than Kott's for I. castaneus (8.0-14.2, N = 7 vs. 5.3, N = 1).
Ichthyomyzon cf. gagei is more widespread in Wisconsin than previous literature indicated, not because of a recent expansion in range but rather because earlier studies of fish distribution either failed to sample suitable habitats effectively or did not recognize I. cf. gagei when it was captured. Many museum specimens of I. cf. gagei from the upper Black River drainage had been misidentified as I. castaneus, and specimens from the upper Wisconsin River drainage had been misidentified as I. fossor (Lee et al., 1980; Becker, 1983; Fago, 1983, 1992). The larval "I. castaneus" from the Prairie River, upper Wisconsin River drainage, used in the analyses and depicted in Lanteigne (1988; [ILLUSTRATION FOR FIGURE 4 OMITTED]) were probably I. cf. gagei; I. cf. gagei was abundant at this locality and I. castaneus was rare. Within its range, I. cf. gagei is common in appropriate habitat, occurring in moderate to large-sized streams (mean width 5-50 m) of low to moderate gradient (0.3 to 3 m/km) with predominantly sand and gravel or cobble substrates. It is most numerous in streams with cool summer water temperatures (maximum daily mean typically 22-24 c), and often is found with salmonids, although it is absent from the coldest streams. However, I. cf. gagei is an inconspicuous species that spends most of its life buried in the stream bottom, and is difficult to capture without specialized equipment except when individuals emerge during late spring to spawn.
The distribution of Ichthyomyzon cf. gagei suggests that it was the first nonparasitic lamprey species to colonize the upper Mississippi basin after deglaciation and that it persists in the basin today as a relict. Ichthyomyzon cf. gagei is the nonparasitic lamprey that occurs farthest upstream in the St. Croix, Black and Wisconsin river watersheds [ILLUSTRATION FOR FIGURE 2 OMITTED]. Fago (1986, 1992) reported I. fossor from two sites within the area of the St. Croix watershed occupied by I. cf. gagei, but these two records were ammocoetes (UWZM 9981, 9982), and from our examination cannot be identified to species with certainty. Ichthyomyzon fossor and L. appendix occur downstream in the St. Croix, Black and Wisconsin River watersheds, and are also found farther North in the Lake Superior basin [ILLUSTRATION FOR FIGURE 2 OMITTED]. However, I. fossor and Lampetra appendix are believed to have colonized the Lake Superior basin from the S through the Lake Michigan basin rather than directly from the upper Mississippi River basin (Bailey and Smith, 1981). In the Black and Wisconsin River watersheds, populations of I. cf. gagei are found within a few kilometers of populations of I. fossor and Lampetra appendix, with I. cf. gagei occurring upstream of historical waterfalls or large rapids (now mostly obliterated by dams).
The distribution pattern of Ichthyomyzon cf. gagei implies that barriers to upstream movement may have prevented I. fossor and Lampetra appendix from successfully colonizing the areas currently occupied by I. cf. gagei. Although I. cf. gagei probably reached the upper Mississippi River basin first, it may have been replaced as I. fossor and L. appendix entered the basin. Ichthyomyzon cf. gagei apparently has been able to persist only in areas that I. fossor and L. appendix have been unable to colonize. From our observations, there is substantial overlap in the habitats of I. cf. gagei, I. fossor, and L. appendix, so differences in ecological requirements are unlikely to account for the observed complementary distribution pattern. Ichthyomyzon fossor and L. appendix occur together at many localities in Wisconsin [ILLUSTRATION FOR FIGURE 2 OMITTED]. Interestingly, I. gagei occasionally has been found together with L. appendix or L. aepyptera in the southern United States (Lee et al., 1980). The ranges of I. gagei and I. fossor do not overlap.
Recent analyses of several N temperate fish taxa, including sticklebacks, Gasterosteus species (Schluter and McPhail, 1992), whitefishes, Coregonus species (Bernatchez et al., 1996) and salmon, Oncorhynchus nerka (Taylor et al., 1996) have revealed the potential for multiple, parallel divergences between life history forms. What Hubbs and Trautman (1937) envisioned as possible for I. gagei may also be true for I. cf. gagei; either or both may represent a collection of populations independently derived from Ichthyomyzon castaneus. It is conceivable that the I. cf. gagei populations isolated in the upper St. Croix, Black and Wisconsin river watersheds had independent origins. This issue begs for a molecular genetic analysis.
Material examined. - Ichthyomyzon cf. gagei: UMMZ (University of Michigan Museum of Zoology) 211769, 211771, 211772, UWZM 8435, 8438, 9969, Namekagon River, St. Croix drainage, Wisconsin (N = 37); UWZM 8433, Wood River, St. Croix drainage, Wisconsin (1); UWZM 9736, Moose River, St. Croix drainage, Wisconsin (1); UWZM 9808, Wisconsin River, Wisconsin (16); UWZM 9809, Plum Creek, Wisconsin River drainage, Wisconsin (9); UWZM 9970, Yellow River, St. Croix drainage, Wisconsin (9); UWZM 10580, Black River, Wisconsin (13).
Ichthyomyzon gagei: NMC (National Museums of Canada, Canadian Museum of Nature) 86-0824B, Mitchell Creek, Texas, (4); UAIC (University of Alabama Ichthyological Collection) 1248.10, 1250.01, 1251.01, Wercher Creek system, Georgia (4); UAIC 2895.10, Hamm Creek, Alabama (1); UAIC 4706.11, tributary to Oakmulaee Creek, Alabama (1); UAIC 6098.01, Hail Creek, Alabama (2); UAIC 8404.02, Blue Girth Creek, Alabama (1); UAIC 8496.01, Crooked Creek, Alabama (1); UAIC 8822.01, Cahaba River, Alabama (2); UMMZ 64494, tributary of Tagiphoa River, Louisiana (3); UMMZ 107043, 181968, Dry Prong, Louisiana (9); UMMZ 119976, Barren Fork, Oklahoma (1); UMMZ 143018, Nacogdoches Creek, Texas (1); UMMZ 157706, Chaelafaula Creek, Alabama (4); UMMZ 163536, Big Escambia Creek, Alabama (1); UMMZ 173427, Upper Gasconade River, Missouri (1); UWZM 9627, Tallapoosa River, Alabama (2); UWZM 9944, Chatafalla Creek, Alabama (1).
Ichthyomyzon fossor. UWZM 10720, Bear Creek, Chippewa River drainage, Wisconsin (5).
Ichthyomyzon castaneus:. UWZM 10721, 10723, 10726, Namekagon River, St. Croix River drainage, Wisconsin (5); Uncatalogued, unknown locality, Wisconsin (2).
Acknowledgments. - We thank B. Kuhajda, D. Nelson, C. Renaud and G. Seegert for providing preserved specimens. S. Bellrichard, A. Gripentrog, J. Hagar, M. Kaminski, P. Kanehl and T. Simonson helped collect fresh specimens. Many of the specimens were collected during fish sampling funded by the Sport Fish Restoration Program, Projects F-83-R and F-95-P, Study RS043 and RS046, and the U.S. Forest Service, North Central Forest Experiment Station, Wildlife and Fish Habitat Research Unit NC-4202. Direct funding for this study was provided by the Wisconsin Department of Natural Resources, Bureau of Research, the Lois Almon Fund, and the St. Norbert College faculty development program. M. Sheen is grateful to St. Norbert College for the support of undergraduate research.
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|Author:||Lyons, J.; Cochran, P.A.; Sneen, M.E.|
|Publication:||The American Midland Naturalist|
|Date:||Jul 1, 1997|
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