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Reproductive Season, Fecundity, and Ovum Size of the Skygazer Shiner, Notropis uranoscopus, in Alabama.

INTRODUCTION

Notwithstanding decades of research on native fishes of North America, the natural history of many species remains largely, if not completely, unknown (Warren and Burr, 2014). In some cases these knowledge gaps are critical, given the ongoing habitat degradation and loss (Warren and Burr, 2014). The Skygazer Shiner, Notropis uranoscopus, is one species for which we have little information on natural history, aside from anecdotal comments in books devoted to the stale fish fauna (Mellee et ai. 1996; Boschung and Mayden, 2004). The purpose of this study was to document life-history data for this minnow, including reproductive phenology, clutch size, and ovum size.

The Skygazer Shiner, described by R. D. Suttkus (Suttkus, 1959), is a slender cyprinid with a flattened head and large eyes located near the lop of the head. It is a Mobile basin endemic found primarily below the Fall Line in the Cahaba, Alabama, and Tallapoosa rivers, as well as in the Uphapee Creek system (Mettee et al, 1996; Boschung and Mayden, 2004). The Skygazer Shiner is a true large-stream minnow, often inhabiting streams 25-100 m wide (Boschung and Mayden, 2004). As a benthic species, it is found along sand and gravel shoals having moderate to fast current (Mettee et al, 1996; Boschung and Mayden, 2004). Aggregations have been observed foraging over sand or gravel substrate in shallow riffle areas with moderate current (Pierson, pers. obs.). Although the Skygazer Shiner can be common in the main channels of the lower Tallapoosa and Cahaba rivers, it apparently has been eliminated from its historic range in the Alabama River system (Mettee et ai, 1996; Boschimg and Mayden, 2004).

MATERIALS AND METHODS

STUDY AREA

Samples were obtained from the Tallapoosa River about 16 km east-north-east of Montgomery, Alabama, in Elmore County (32.428301. -86.142311) and about 53 km downstream from the Thurlow Hydroelectric Project. At this point the river is about 61-76 m wide. The site includes large gravel-sand bars, islands, riffles and deep pools, as well as backwater areas. The substrate is primarily stable gravel or sand and the current in the main channel is between moderate and fast. The variety of habitats in the area has resulted in a diverse fish community, with 64 species of fishes having been collected from this site (Pierson, pers. obs.; also see Table 2.4, Boschung and Mayden, 2004). The Tallapoosa River is located in east-central Alabama and flows from headwaters in western Georgia. It flows in a south by southwesterly direction through the Piedmont before crossing the Fall Line and entering the Gulf Coastal Plain south of Tallassee, Alabama.

SAMPLING AND ANALYSIS

Collections of the Skygazer Shiner were made monthly or semimonthly in the main channel of the Tallapoosa River from March 1988 to May 1989. Specimens were taken with a nylon seine or Smith-Root backpack electrofisher. Following preservation in 10% formalin, specimens were stored in 50% isopropanol alcohol.

To determine the timing of the spawning season, periodic changes in the reproductive Condition of adult-size females from all of the samples were determined through visual examinations of ovaries and ova. An important aspect of our scheme is the presence or absence of a clutch of mature, follicular oocytes or ripe, ovulated eggs in the ovary. A clutch consists of oocytes or eggs that have undergone synchronous development that will be oviposited within a relatively short period of time (Heins and Rabito, 1986).

Females were classified into one of the following stages of ovarian condition, based on Heins and Rabito (1986): (1) Latent (IA)-ovaries very small, thin, flaccid, and transparent to slightly translucent. Larger, developing ova, if present, yolkless or vitellogenic but with nuclei visible. (2) Early maturing (EM)-ovaries small to moderate in size, translucent to white. Larger maturing oocytes relatively small but with nuclei obscured by yolk deposition, few in number to numerous, translucent to white. (3) Late maturing (LM)-ovaries white to cream in color. Larger maturing oocytes relatively large (often as large as mature ova) but not easily differentiated from smaller maturing oocytes, few in number to numerous, white or cream lo sometimes yellow. (4) Mature (MA)-ovaries cream to yellow. Mature oocytes present, unovulated, and easily differentiated from maturing oocytes on the basis of size and color, forming separate group of developing oocytes and being opaque cream to yellow in color, to translucent with small oil globules visible in mature-ripening females. (5) Ripe (RE)-ovaries white to yellow with ovulated, fully formed ripe ova concentrated posteriorly in the lumens of the ovaries in addition lo maturing oocytes in the follicles. Ripe ova ovulated, translucent with vitelline membranes elevated, white lo yellow. Females classified as LM through RE could display ovaries that may be small to greatly enlarged and filling a large portion of the body cavity. Ovaries from females classified as MA and RE may distend the abdomen when greatly enlarged.

We quantified clutch size (i.e., clutch fecundity or clutch number) using mature, follicular oocytes from reproductively mature females (Wallace and Selman, 1981; Heins and Rabito, 1986; Heins and Baker, 1988) from April 1988. This month was used given a relatively large number of mature females was available early in the spawning season. Using mature females allows accurate determination of clutch size (Heins and Rabito, 1986; Heins and Baker, 1993). Moreover, in minnows, ripe eggs are rarely obtained from field-caught samples (Heins, pers. obs.), and mature oocytes appear to demonstrate accurately variation in the size of ripe eggs (Heins and Baker, 1988).

Both ovaries were removed from each of 17 adult females after digital calipers were used to measure standard length (SL, tip of snout to base of caudal fin) of each specimen to the nearest 0.1 mm. Each clutch was separated from the ovaries, and the number of eggs in the clutch was counted. The diameter of three randomly chosen ova in each clutch was measured lo the nearest 0.05 mm using an ocular micrometer in a dissecting microscope. Mean ovum diameter (DIAM) was calculated as the mean diameter of the three eggs. Because the preserved ova were rarely spherical, all diameters were determined by averaging measurements of the largest and smallest dimensions. Ten randomly chosen eggs from each clutch were then dried al 40C for 24-28 h and weighed on an electronic balance; the mean ovum mass was calculated for each female by dividing the total d it mass by the number of dried eggs.

RESULTS AND DISCUSSION

Female Sky-gazer Shiners were found to have clutches of eggs from April-August (Table 1). Heretofore, we had only anecdotal statements about the reproductive season of the Skygazer Shiner. Mettee et al. (1996) stated reproduction occurred from April to June, and Boschung and Mavden (2004) reported reproductive females from May to July. Therefore this report presents data lo support a longer spawning season than previously known.

Clutch sizes of 17 MA females (40.4-46.2 mm SL) captured in April 1988 ranged in size from 336-582 eggs (Fig. 1). There was a significant relationship between female body size and clutch size (r = 0.600; df = 1, 15; P = 0.011). The relationship of SL and CS was expressed by the following equation: CS = -722.478 + 26.704*SL.

Reproductively mature females contained two groups of yolk-bearing oocytes or eggs in their ovaries. A complement of larger mature oocytes was easily separated by size (primarily) and color from a complement of smaller maturing oocytes. Such a bimodal distribution of yolk-bearing oocytes is indicative of a long reproductive season during which a number of clutches of eggs are released in successive bouts (Hickling and Rulenberg, 1936; MacGregor, 1970; Heins and Rabilo, 1986). Because our egg counts represent clutch sizes, the total number of eggs produced in one reproductive season, hence reproductive effort, is expected to be much greater.

Ovum diameter ranged from 0.84-0.92 mm and averaged 0.87 mm, whereas ovum dry weights ranged from 110-140 [micro]g and averaged 128 [micro]g. Neither egg diameter (r = 0.122, P = 0.642) or egg weight (r = 0.074, P = 0.778) were significantly related to fish SL. Ovum diameter and weight showed a significant relationship (r = 0.536, P = 0.027): WT = -48.871 +204.133*DIAM. The loss of lipids in specimens stored in alcohol needs to be considered when any comparisons of data from different studies are made (Heins and Baker, 1999).

In summary this report presents data supporting the conclusion of a long spawning season extending from April through August. Clutch size is relatively large and egg size small for a small-bodied, stream-dwelling minnow (Boschung and Mayden, 2004). The Skygazer Shiner appears to show characteristics of an "opportunistic" life-history strategy (e.g., extended reproductive season, repeated spawning, high reproductive effort, small eggs) typical of species able to repopulate habitats despite consistently high levels of ongoing adult mortality or following disturbances (Winemiller and Rose, 1992). This strategy' is consistent with what we know about the ecological role of the Skygazer Shiner.

Acknowledgments.--RP completed the lab work for this report as part of a senior undergraduate project with the assistance of DCH. The stud)' was initiated when JMP contacted DCH to inquire about study of the Skygazer Shiner from samples he had available. Unfortunately, this study was not completed in JMP's lifetime. It is dedicated to JMP who was an avid naturalist and dear friend.

LITERATURE CITED

BOSCHUNG H. T., JR. AND R. L. MAIDEN. 2004. Fishes of Alabama. Smithsonian Books, Washington, D. C. 960 p.

HEINS, D. C. AND J. A. BAKER. 1993. Clutch production in the darter Etheostoma lynceum Hay and its implications for life-history study. J. Fish Biol., 42:819-829.

HEINS, D. C. AND J. A. BAKER. 1988. Egg sizes in fishes: Do mature oocytes accurately demonstrate size statistics of ripe ova? Copeia, 1988:238-240.

--AND --. 1999. Evaluation of ovum storage techniques for reproductive studies of fishes Ecol. Freshw. Fish, 8:65-69.

--AND F. G. RABITO, JR. 1986. Spawning performance in North American minnows: direct evidence of the occurrence of multiple clutches in the genus Notropis.J. Fish Biol.. 28:343-357.

HICKLING, C. F. AND E. RUTENBERG. 1936. The ovary as an indicator of the spawning period in fishes. J. Mar. Biol. Assoc. U. K. 21:311-318.

MACGREGOR, J. S. 1970. Fecundity, multiple spawning, and description of the gonads in Sebaslodes. U. S. Fish Wildl. Serv. Spec. Sci. Rep., Fish., 596:1-12.

METTEE, M. F., P. E. O'NEIL, AND J. M. PIERSON. 1996. Fishes of Alabama and the Mobile Basin. Oxmoor House. Birmingham, Alabama 820 p.

SUTTKUS, R. D. 1959. Notropis uranoscopus, a new cyprinid fish from the Alabama River system. Copeia, 1959:7-11.

WALLACE, R.A. AND K. SELMAN. 1981. Cellular and dynamic aspects of oocyte growth in teleosts. Am. Zool., 21:325-343.

WARREN M. L., JR. AND B. M. BURR. 2014. Freshwater Fishes of North America: Volume 1: Petromyzontidae to Catostomidae. Johns Hopkins University Press. Baltimore, Maryland 664 p.

WINEMILLER, K. O. AND K. A. ROSE. 1992. Patterns of life-history diversification in North American fishes: implications for population regulation. Can. J. Fish. Aquat. Sci., 49:2196-2218.

DAVID C. HEINS (1), Department of Ecology and Evolutionary Biology, Tulane University, New Orleans, Louisiana 70118; ROBERT PASHKIN (2), Department of Ecology and Evolutionary Biology, Tulane University, New Orleans, Louisiana 701148, and J. MALCOLM PIERSON (3), Alabama Power Company, 600 North 18th Street, Birmingham 35291. Submitted 18 April 2019; Accepted 14 June 2019

(1) Corresponding author: E-mail: heins@tulane.edu

(2) Present address: 30 Evergreen Ave., Port Jefferson Station, New York 11776; E-mail: ripashkin@gmail.

(3) Deceased

Caption: FIG. 1.--Scatter plot showing relationship between clutch size (number) and standard length (mm) of Skygazer Shiner females in April 1988. The data are untransformed
TABLE 1.--Reproductive condition of Skygazer Shiner females sampled
monthly or bimonthly from March 1988 to May' 1989 from the Tallapoosa
River, Alabama. Data shown are percentages of females in each stage
of reproductive condition for a given sample date (n, number examined):
LA, latent; EM, early maturing; LM, late maturing, and Clutch,
clutch-bearing inclusive of mature, ripening and ripe females.
Empty cells represent samples for which no females in those
ovarian stages were captured

Year   Month and day     n    LA     EM    LM   Clutch

1988      Mar. 24       25           76    24
          Apr. 19       46            9    24     74
          Apr. 28       39                 54     46
          May 2         58            2           98
          Jun. 6        36                 17     83
          Jun. 29       41                       100
          Jul. 26       57                 63     37
          Aug. 16       45                 33     67
          Sep. 26       43    100
          Oct. 17       76    100
          Nov. 29      186    100
          Dec. 21       19    100
1989      Jan. 19       38    100
          Feb. 27       50          100
          Mar. 27       56           57    46
          Apr. 17       45           26    36     38
          May 15        66                 32     68
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Title Annotation:Notes and Discussion Piece
Author:Heins, David C.; Pashkin, Robert; Pierson, J. Malcolm
Publication:The American Midland Naturalist
Date:Oct 1, 2019
Words:2110
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