2008 SOUTHEASTERN NATURALIST 7(3):413–428 Reproductive and Early Life History of Nonindigenous Red Shiner in the Chattahoochee River Drainage, Georgia Steven J. Herrington1,2,* and Dennis R. DeVries1 Abstract - This study quantified the reproductive and early life-history characteristics of nonindigenous populations of Cyprinella lutrensis (Red Shiner) introduced into two tributaries of the Chattahoochee River, GA. Red Shiners had a maximum age of at least two years and a peak breeding season from May through July, with intermittent spawning in both populations. The presence of small individuals late in the year suggests the potential for Red Shiners to spawn in their first summer of life in both study streams. Whereas these life histories are similar to those previously described for this species, these results suggest the potential for nonindigenous Red Shiners to successfully expand and establish populations in additional areas within the Chattahoochee River drainage. Introduction Cyprinella lutrensis Baird and Girard (Red Shiner) is a small cyprinid indigenous to the midwestern US (Page and Burr 1991), with nonindigenous populations recorded from at least 12 states (Fuller et al. 1999). Introductions have resulted from aquarium release (Jenkins and Burkhead 1994, Moore et al. 1976), bait release (Hubbs and Lagler 1964, Jennings and Saiki 1990, Wallace and Ramsey 1982), fish-farm/pond escape (Hubbs 1954), stocking as forage (Shapovalov et al. 1959), dispersal from other nonindigenous populations (Holden and Stalnaker 1975, Minckley 1973, Moyle 2002), and other unknown pathways (Fuller et al. 1999). The majority of these introductions have been in the western US, where Red Shiners have been found to prey upon (Brandenburg and Gido 1999, Ruppert et al. 1993), compete with (Douglas et al. 1994, Greger and Deacon 1988), and transmit parasites to (Deacon 1988, Heckmann et al. 1986, USFWS 1998) native fishes. Nonindigenous Red Shiners have recently established populations in southeastern US waters. In addition to the effects noted above, this species readily hybridizes with congeners (Etnier and Starnes 1993, Robison and Buchanan 1988, Smith 1979), occasionally leading to large hybrid swarms of continually backcrossing parentals and hybrids (Hubbs and Strawn 1956, Page and Smith 1970). This situation can lead to the eventual replacement of the hybrids and hybridizing parental species with Red Shiner (Page and Smith 1970). Nonindigenous Red Shiners have the potential to hybridize with at least eight native congeners in Alabama, Georgia, and North Carolina 1Department of Fisheries and Allied Aquacultures, Auburn University, AL 36849. 2Current address - The Nature Conservancy, 10394 NW Longleaf Drive, Bristol, FL 32321. Corresponding author - streamfishes@yahoo.com. 414 Southeastern Naturalist Vol.7, No. 3 waters where it currently has established populations (Boschung and Mayden 2004, Menhinick 1991). It has already been reported to hybridize with C. venusta Girard (Blacktail Shiner; Boschung and Mayden 2004), C. callitaenia Bailey and Gibbs (Bluestripe Shiner; Wallace and Ramsey 1982), and the federally threatened C. caerulea Jordan (Blue Shiner; Burkhead and Huge 2002) in the southeastern US. While nonindigenous Red Shiner populations have been well-studied in the western US since the mid-1950s (Douglas et al. 1994, Greger and Deacon 1988, Hubbs 1954, Karp and Tyus 1990), there has been virtually no research on its ecology and potential effects on native fishes in the southeastern US. Considering the high fish diversity in these waters (Lydeard and Mayden 1995), it is likely that Red Shiners interact with native fishes on some ecological level. A primary step in understanding these dynamics is examining the life history of the Red Shiner in its nonindigenous range. Here we describe the life cycle and reproductive ecology of two nonindigenous populations the species in the Chattahoochee River drainage in Georgia. Methods Review of Red Shiner life history The Red Shiner is a small (maximum total length [TL] = 9 cm) cyprinid with an average lifespan of 2–3 years (Becker 1983). It occurs in a variety of environments, ranging from small, headwater creeks, to large rivers and reservoirs, occupying habitats ranging from shallow, swift water to deep, backwater pools (Etnier and Starnes 1993, Herrington 2004, Matthews 1985). Red Shiners feed opportunistically on stream and terrestrial invertebrates, as well as algae and other plant material (Herrington 2004, Ross 2002, Sublette et al. 1990). The Red Shiner matures rapidly and can reproduce within its first summer of life (Marsh-Matthews et al. 2002). It is moderately fecund (Becker 1983, Burkhead and Huge 2002), but maximizes its reproductive potential with an extended spawning season from late April through October, allowing for rapid population increases (Farringer et. al. 1979, Jennings and Saiki 1990, Moyle 2002). The Red Shiner is also reproductively plastic, having the ability to broadcast spawn in riffl es (Minckley 1972) or in vegetation and brush (Smith 1979), crevice spawn (Gale 1986), and spawn over sunfish nests (Minckley 1959, Pfl ieger 1997). It tolerates environmental extremes such as low oxygen, high temperature, high acidity, and high turbidity better than most North American cyprinids (Matthews and Hill 1977, Matthews and Maness 1979). These life-history traits allow the Red Shiner to thrive in harsh environmental conditions that preclude more sensitive species (Smith 1979, Sublette et al. 1990). In addition, it is considered a behaviorally aggressive species (Karp and Tyus 1990, Minckley 1973) that can hybridize with congeners (Etnier and Starnes 1993) and may out-compete native fishes in degraded ecosystems (Page and Smith 1970). 2008 S.J. Herrington and D.R. DeVries 415 Study sites Red Shiners were collected from Proctor Creek (Fulton County, GA, 33°47'39"N, 84°28'28"W) and Nickajack Creek (Cobb County, GA, 33°48'12"N, 84°31'17"W), both tributaries of the Chattahoochee River in Georgia. Both streams are in the Piedmont physiographic province (Mettee et al. 1996) and are separated from one another by 8 km. Proctor Creek is a second-order stream at 231 m above sea level with a drainage area of 35 km2. It is characterized by clear water and sand substrates, with distinct riffle and pool habitats averaging 6 m wide and 0.6 m deep. Proctor Creek flows through a residential and urban landscape with a history of chemical and sewage waste pollution from the surrounding industry of Atlanta, GA (DeVivo 1995). Nickajack Creek is a third-order stream at 227 m above sea level with a drainage area of 81.6 km2. It is characterized by clear water and sand and gravel substrates, with distinct riffle and pool habitats averaging 10 m wide and 0.9 m deep. Nickajack Creek flows through primarily residential landscape in greater northwest Atlanta, GA (DeVivo 1995). Fish diversity varies markedly between the two streams. Proctor Creek has low fish diversity (≈10 spp.), with Red Shiner dominant and often the only cyprinid captured in recent surveys (Couch et al. 1995, DeVivo 1995). In contrast, Nickajack Creek has relatively high fish diversity (≈23 spp.; Herrington 2004). Although Red Shiners are numerically dominant, five other cyprinid species are common to Nickajack Creek, including Campostoma pauciradii Burr and Cashner (Bluefin Stoneroller), Nocomis leptocephalus Girard (Bluehead Chub), Luxilus zonistius Jordan (Bandfin Shiner), Notropis buccatus Cope (Silverjaw Minnow), and Notropis longirostris Hay (Longnose Shiner) (Couch et al. 1995). Reproductive and somatic characteristics Red Shiners were collected monthly from each stream from 0900 to 1200 hours in all available habitats (i.e., riffl es, pools, and instream structure) between May 2002 and May 2003 using a backpack electrofisher (Model LR-24; Smith-Root, Inc. Water temperature was measured on the day of fish collection using a digital thermometer. Fish were euthanatized in MS-222 (tricaine methanesulfonate), fixed in a 10% unbuffered formalin solution, and stored in 70% ethanol for 6–9 days before being transferred to Gilson’s Fluid (see below). Sex, standard length (SL), and mass were quantified in the laboratory. Sex was determined by examining gonads of dissected specimens. The SL of all specimens was measured (nearest 0.1 mm) using digital calipers. Total, eviscerated somatic, and gonad wet masses of specimens >30 mm SL were determined by blotting them dry and weighing them (nearest 0.1 mg). Seasonal changes in gonad mass for both sexes were quantified using the gonadosomatic index (GSI), calculated as 100 times the gonad mass of 416 Southeastern Naturalist Vol.7, No. 3 a specimen divided by its eviscerated somatic mass (Strange 1996). After dissection, ovaries were stored separately in modified Gilson’s Fluid for approximately three months to aid in egg separation before subsequent measurement and counting (Kelso and Rutherford 1996). All mature ova were counted, and sizes were measured from a sample of mature females from each study stream. Ovaries were removed from the Gilson’s Fluid, rinsed with tap water, and transferred to Petri dishes. Mature and immature ova were separated using forceps and fine dissection probes. Ova were considered mature if they were large, opaque, and yellowish in color; in contrast, immature ova were small, thin, and translucent in color (sensu Heins and Baker 1993). Once separated, mature ova were positioned so as not to be touching one another and photographed using a digital camera with Win/TV 4.05 image capture software (Happauge Computer Works 1996). Images were analyzed using ImageTool 2.0 (UTHSCSA 1996) to calculate the total number of eggs and diameter of each ovum per image. Diameters of mature ova were estimated by averaging maximum and minimum dimensions, as ova were occasionally irregularly shaped due to preservation (sensu Heins and Baker 1993). Data analyses Deviations of the stream-specific sex ratio of Red Shiners from 1:1 and differences in sex ratios between streams were tested with chi-square analyses with Yate’s correction for continuity. Length-frequency distributions were used to estimate age-classes and the presence of age-0 recruits to the populations (MacDonald 1987). Between-stream differences in breeding and non-breeding season GSI values were analyzed using separate 2-way ANOVAs with Bonferroni’s multiple comparison tests for males and females. Breeding season was determined by examining trends in gonad development and GSI for both sexes. Months with mature gonads and high GSI values for fish were considered the breeding season, while months with immature gonad development and low GSI values were considered the non-breeding season. Differences in total number of mature ova per specimen between study streams was analyzed using ANCOVA with SL as a covariate to account for differences in total mature ova related to fish size. To quantify the relationship between mean ovum diameter and SL, we first averaged the 30 largest mature ova of 19 and 27 female Red Shiners from Proctor and Nickajack creeks, respectively, resulting in one mean diameter value per specimen, which we regressed on SL. Between-stream differences in mean ovum diameters of Red Shiners were analyzed using either a t-test or an ANCOVA with SL as a covariate. Differences in eviscerated somatic body mass per stream were log10+1 transformed to achieve normality and then analyzed using ANCOVA with SL as a covariate. All statistical comparisons were performed with SPSS 11.5 (SPSS Inc. 2002) and Programs for Ecological Methodology 6.1 (Kenney and Krebs 2002) at the P ≤ 0.05 significance level. 2008 S.J. Herrington and D.R. DeVries 417 Results Reproductive biology Both sexes of Red Shiner from both streams were captured in shallow, swift-fl owing riffl es during April 2002 through November 2002, then in deeper, slower-fl owing water in pooling areas during December 2002 through March 2003, and again in riffl es during April 2003 through May 2003. Water temperatures were similar between streams over the sample period (Fig. 1). A total of 1540 and 612 Red Shiners were collected from Proctor and Nickajack creeks, respectively, of which 926 and 404, respectively, were dissected and sexed during the study period. The male-to-female sex ratio did not differ from 1:1 (chi-square = 0.57, P > 0.50) in Proctor Creek; but was significantly skewed towards females in Nickajack Creek (at 0.63:1, chi-square = 19.60, P < 0.001). Sex ratios differed significantly between streams (chi-square = 16.91, P < 0.001). The largest Red Shiner individuals (SL) collected were 75.9 mm in Proctor Creek (June 2002) and 67.7 mm in Nickajack Creek (May 2003). The smallest Red Shiners (SL) collected were 12.3 mm in Proctor Creek (August 2002) and 12.8 mm in Nickajack Creek (January 2003). Sexually mature males had prominent breeding colors, tubercles, and enlarged, opaque white testes, consistent with descriptions for central Great Plains US populations Figure 1. Monthly temperature of Proctor and Nickajack Creeks between May 2002 and May 2003. 418 Southeastern Naturalist Vol.7, No. 3 (see Matthews 1995). Males exhibited breeding conditions as early as April and as late as November in both streams. The smallest mature males (SL) were 30.1 mm in Proctor Creek (May 2002) and 31.6 mm in Nickajack Creek (June 2002). Females were considered sexually mature if mature ova were Figure 2 (above and opposite page). Monthly length-frequency histograms of Cyprinella lutrensis (Red Shiner) in Proctor and Nickajack Creeks between May 2002 and May 2003. 2008 S.J. Herrington and D.R. DeVries 419 present in their ovaries. Females were sexually mature as early as April and as late as September in both streams. The smallest mature females (SL) were 30.5 mm in Proctor Creek (May 2003) and 34.1 mm in Nickajack Creek (August 2002). Length-frequency distributions indicated two age-0 modes in both streams in certain months, though their appearance differed by location (Fig. 2). In Proctor Creek during August 2002, one mode was near 16 mm 420 Southeastern Naturalist Vol.7, No. 3 while the other was near 22 mm. The first mode appeared in early July 2002, indicating that spawning began in June, while the second mode appeared in early August 2002, indicating a second distinct spawning event that occurred in July. Age-0 modes were not apparent in Nickajack Creek until October 2002, with one near 20 mm and another near 32 mm. These size classes roughly matched those in Proctor Creek in October 2002, so it is likely that these modes were present but undetected in Nickajack Creek from June 2002 through September 2002 samples. Therefore, spawning events likely occurred during similar times in both streams. Length-frequency histograms also showed a maximum age of at least two years for Red Shiners in both streams, with presence of age-1 and age-2 year classes best exhibited in 2 May 2002 histograms (Fig. 2). Analysis of GSI values for both sexes indicate at least a three-month breeding season in both streams. GSI values were high relative to other months from May 2002 through July 2002 (i.e., the breeding season) (Fig. 3). These GSI values decreased in August 2002 through early September, and remained low until the following March (i.e., the non-breeding season). GSI values subsequently increased in April 2003 and again in May 2003 (Fig. 3). May through July was considered the breeding season and September through March was considered the non-breeding season for subsequent breeding- season analyses. August 2002 and April 2003 were transitional months in gonadal development for Red Shiners and therefore were not included in the analyses. Although temporal patterns of gonadal investment were similar for Red Shiners in both streams, proportional investment differed by both stream and season. Females from Proctor Creek had significantly higher mean GSI values during both the breeding (p < 0.001) and non-breeding (p < 0.001) seasons than those from Nickajack Creek (F3, 18 = 94.2, p < 0.001). Similarly, males from Proctor Creek had significantly higher mean GSI values during both the breeding (p < 0.01) and non-breeding (p < 0.05) seasons than those from Nickajack Creek (F3, 18 = 80.1, p < 0.05). Females contained three distinct size classes of ova: (1) very small, thin, and translucent (immature ova); (2) small and semi-translucent (immature ova); and (3) large, opaque, and yellowish (mature ova). The total number mass, and diameter of mature ova differed by stream. The mean number of mature ova per female (adjusted for SL) was higher in Proctor Creek (mean = 925, SD = 374, range = 365–1542) than Nickajack Creek (mean = 305, SD = 119, range = 127–591) (ANCOVA: F1, 43 = 128.7, P < 0.001). Ova mass per female (adjusted for SL) also was higher in Proctor Creek (mean = 0.43 g, SD = 0.17) than Nickajack Creek (mean = 0.14 g, SD = 0.06) (ANCOVA: F1, 43 = 130.0, P < .001). There was no relationship between mean ovum diameter and SL from Proctor (F = 0.80; P = 0.384) or Nickajack Creek (F = 0.09; P = 0.770). Ovum diameters per female were ≈7% larger in Nickajack Creek (mean = 0.70 mm, SE = 0.01) than Proctor Creek (mean = 0.65 mm, SE = 0.01) (t1, 45 = 5.60, P = 0.022). 2008 S.J. Herrington and D.R. DeVries 421 Somatic characteristics Eviscerated somatic masses (ESMs) of Red Shiners differed between streams and between seasons. Females from Proctor Creek had higher SL-adjusted ESMs during the breeding (mean = 2.22 g, SD = 1.31) than Figure 3. Monthly gonadosomatic index (GSI) values of female and male Cyprinella lutrensis (Red Shiner) from Proctor and Nickajack Creeks between May 2002 and May 2003. Error bars indicate standard deviations. 422 Southeastern Naturalist Vol.7, No. 3 the non-breeding season (mean = 1.19, SD = 0.96); (ANCOVA: F1, 310 = 22.35, P < 0.001). However, there was no significant difference in SLadjusted ESMs between the breeding (mean = 1.80 g, SD = 1.37) and non-breeding (mean = 1.86 g, SD = 0.73) seasons for females from Nickajack Creek (ANCOVA: F1, 176 = 0.22, P = 0.637). Males from Proctor Creek had higher SL-adjusted ESMs during the breeding (mean = 2.55g, SD = 1.72) than the non-breeding (mean = 1.06 g, SD = 0.57) season (ANCOVA: F1, 252 = 41.5, P < 0.001). Similarly, males from Nickajack had higher SLadjusted ESMs during the breeding (mean = 1.80 g, SD = 0.42) than the non-breeding (mean = 1.57 g, SD = 0.84) season (ANCOVA: F1, 125 = 27.2, P < 0.001). Females from Proctor Creek had higher SL-adjusted ESMs than those from Nickajack Creek during the breeding season (ANCOVA: F1, 237 = 68.9, P < 0.001) as well as during the non-breeding season (ANCOVA: F1, 249 = 12.1, P = .001). Although males from Proctor Creek had higher SL-adjusted ESMs than those from Nickajack Creek during the breeding season (ANCOVA: F1, 179 = 60.8, P < 0.001), males from Nickajack Creek had higher SL-adjusted ESMs than those from Proctor Creek during the non-breeding season (ANCOVA: F1, 198 = 17.3, P < .001). Discussion The reproductive and early life histories of Red Shiners in Proctor and Nickajack creeks were similar to those previously reported elsewhere for this species (Farringer et. al. 1979, Jennings and Saiki 1990, Marsh-Matthews et al. 2002). Although direct observations of reproductive behavior were not made, spawning probably occurred in riffl es given that reproductively mature Red Shiners were almost exclusively captured in this habitat during the breeding season (Herrington 2004). Red Shiners likely broadcast-spawned over gravel substrates in riffl es, as reproductively mature individuals were almost never found in pools, and riffl es seldom contained debris needed for typical crevice spawning . In addition, eggs (presumably Red Shiner, based on size and appearance) were present in substrate samples examined from riffl es during the breeding season in both streams (Herrington 2004). This spawning mode is relatively uncommon for Red Shiner in its native (Pfl ieger 1997) and introduced (Minckley 1972) ranges. Where known, all members of the genus Cyprinella spawn in crevices (Mayden 1989). Because many of the Cyprinella spp. that currently are or may become sympatric with Red Shiner in the southeastern US have only been reported to spawn in crevices, it is possible that sympatric congeners may not be susceptible to hybridization resulting from reproductive segregation from broadcast-spawning Red Shiners described herein. However, a hybrid between Red Shiner and Bluestripe Shiner, a species of Cyprinella only reported to spawn in crevices (Wallace and Ramsey 1981), has been described from the Chattahoochee River (Wallace and Ramsey 1982). In spawning substrate choice experiments, Vives (1993) reported that Red Shiners do not preferentially crevice spawn over other spawning modes. 2008 S.J. Herrington and D.R. DeVries 423 Vives (1993) also proposed that other Cyprinella spp. only known to spawn in crevices may have the ability to spawn in other ways, citing previously unreported observations of broadcast spawning of C. formosa Girard (Beautiful Shiners) and C. spiloptera Cope (Spotfin Shiners). Hybridization of natives with nonindigenous Red Shiner therefore appears possible given the previously reported hybrids, reproductive plasticity of Red Shiner, and potential reproductive plasticity of other Cyprinella species. Although the Red Shiner population in Proctor Creek had a 1:1 sex ratio, the population from Nickajack Creek was skewed towards females. Skewed sex ratios can result from factors such as sexual differences in activity (Semlitsch et al. 1981), habitat use (Keenlyne 1972), and sampling error or bias. Red Shiners appeared to have a maximum age of at least two years and an extended spawning season, with peak spawning periods from early May through July. These results are similar to other native and introduced populations throughout its range (Becker 1983, Farringer et al. 1979, Moyle 2002, Ross 2002, Smith 1979). April was a period of gonadal investment while August was a period of gonadal reduction; however, it was possible that reproduction continued late into the summer as sexually mature individuals of both sexes were present, albeit sporadically, in September collections from both streams. Interestingly, Red Shiners <15 mm were collected as late as December 2002 in Nickajack Creek. According to Saksena (1962), Red Shiner eggs hatch in 3–4 days and larvae reach 15 mm SL in 34 days under laboratory conditions between 25 and 27.8 °C. The temperatures of Nickajack Creek on 8 September and 8 October 2002 were 26 and 23 °C, respectively, and a dramatic decrease in temperature was not measured until November 2002. Small individuals collected in December 2003 thus might have hatched between September and October 2002. Similar suggestions of late autumnal spawning in natural populations have been made by Fausch and Bestgen (1997) and Matthews (1998) based on collections of individuals 14–15 mm SL in late winter and early spring. Marsh-Matthews et al. (2002) found newly-hatched Red Shiner larvae in experimental stream tanks in Oklahoma as late as 25 October 1999 at a temperature of 15 °C, approximately the temperature recorded in Nickajack Creek on 7 November 2002. Those offspring were parented by Red Shiners hatched earlier that season (18–19 May 1999) that had reached sexual maturity by 29 August 1999, of which three females, 28–31 mm SL, contained mature to ripe ova (Marsh-Matthews et al. 2002). Because similar-sized, sexually mature Red Shiners were present in both Proctor and Nickajack creeks by September 2002 (Fig. 2), it is possible that age-0 Red Shiners can spawn within their first summer of life in these streams. The presence of three size classes of ova suggests intermittent spawning throughout the breeding season, a typical pattern for the genus and species (Boschung and Mayden 2004, Mayden 1989). Average batch fecundity of Red Shiners (i.e., number of mature ova) in this study was similar to those reported throughout its native range. For example, Laser and Carlander 424 Southeastern Naturalist Vol.7, No. 3 (1971) examined Red Shiners in Iowa and reported batch fecundity to be 485–684 eggs, whereas Red Shiners from Texas had a range of 164–912 (Islam 1972), similar to the range of 127–591 for Red Shiners from Nickajack Creek. Although Red Shiners from Proctor Creek often had considerably higher values (range = 365–1542) than these native populations, fecundities were variable and their ranges overlapped substantially. Average egg diameters in Proctor and Nickajack creeks were smaller compared to those in its native range. Red Shiners had average mature ovum diameters of 0.8 mm in Kansas (Cavin 1962), 1.0 mm in Missouri (Gale 1986), and 1.2 mm in New Mexico populations (Sublette et al. 1990), compared with 0.65 and 0.70 mm in Proctor and Nickajack creeks, respectively. These differences probably refl ect preservation effects (which differed across studies) as storage media such as concentrated alcohol can significantly reduce mass (and therefore size) of ova in fishes (Heins and Baker 1999). Red Shiners from Proctor Creek had higher GSI values, egg masses, total number of mature ova, and ESMs than those from Nickajack Creek during both the breeding and non-breeding seasons. As expected, ESMs for Red Shiners in both streams were generally higher in breeding versus non-breeding seasons, given that available food resources (i.e., aquatic and terrestrial invertebrates) tend to be more abundant in warmer than cooler months (Merritt and Cummins 1996). Although the differences in somatic masses were generally small, differences for GSI values, egg masses, and total number of mature ova were large. These results suggested that Red Shiners from Proctor Creek were in better physiological condition than those from Nickajack Creek during all seasons. Nonindigenous Red Shiners occur in at least seven tributaries in the upper Chattahoochee River drainage (Couch et al. 1995) and appear to be expanding in distribution (S.J. Herrington, unpubl. data). Considering its generalist ecology, this species might be able to establish populations in both high- and low-diversity systems within this drainage, and will likely spread farther south into new areas. Given their current persistence and success in the upper Chattahoochee River system, Red Shiners pose a serious conservation threat to the high diversity of fishes in the southeastern US. 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