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Life History of Campostoma oligolepis (Largescale Stoneroller) in Urban and Rural Streams
Eric J. South and William E. Ensign

Southeastern Naturalist, Volume 12, Issue 4 (2013): 781–789

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781 E.J. South and W.E. Ensign 22001133 SOUTSoHuEthAeSaTsEteRrnN NNaAtTurUaRliAstLIST 1V2o(4l.) :1728,1 N–7o8. 94 Life History of Campostoma oligolepis (Largescale Stoneroller) in Urban and Rural Streams Eric J. South1 and William E. Ensign1,* Abstract - We conducted a year-long investigation of the effect of watershed urbanization on the life history of Campostoma oligolepis Hubbs and Greene (Largescale Stoneroller). Lifehistory characteristics of separate populations of Largescale Stoneroller were compared by sampling two stream systems differing in urbanization in their upstream catchments. Both streams are located in the Etowah River drainage basin within the Piedmont ecoregion. We determined degree of urbanization by estimating the percent area of impervious catchment surfaces using ArcGIS, and we recorded stream temperatures with continuous-monitor probes. We sampled each stream system once a month during the spawning period and two additional months during the remainder of the year and recorded standard lengths, tuberculation, total weight, and gonadal weight for all retained specimens. Gonadosomatic index (GSI) values showed reproductively active individuals present in January in the urbanized system, one month before we found similar individuals in the non-urbanized system. Comparison of GSI values between systems suggested that reproductive maturity occurs at a larger size for females in the urbanized system. Comparison of standard lengths of reproductively active females indicated that growth rates are higher in the urban system. Introduction Streams in urbanized landscapes are often degraded. The symptoms that characterize the ecological degradation of urbanized lotic systems have been termed the urban-stream syndrome (Meyer et al. 2005, Walsh et al. 2005). One of the primary causes of the urban-stream syndrome is large amounts of stormwater runoff due to impervious surfaces and hydraulically efficient drainage systems (Walsh et al. 2005). Urban stormwater runoff alters stream hydrology, morphology, and water quality, all of which effect fish assemblages. Populations of sensitive fish taxa are often reduced or extirpated as a result of these habitat changes (Walsh et al. 2005). In contrast, tolerant species frequently persist in degraded stream environments and respond with increased abundance or dominance (Walsh et al. 2005). The purpose of this study was to investigate the effect of catchment urbanization on the life-history characteristics of Campostoma oligolepis Hubbs and Greene (Largescale Stoneroller). We compared populations of Largescale Stoneroller in two stream systems with differing levels of catchment urbanization. Previous research has shown that other Campostoma (stoneroller) species persist in urban environments (Waits et al. 2008). Spranza and Stanley (2000) observed increased juvenile growth rates and extended spawning seasons for Campostoma anomalum Rafinesque (Central Stoneroller) in non-urban systems with elevated temperatures and highly variable flow regimes. Urbanized stream 1Department of Biology and Physics, Kennesaw State University, Kennesaw, GA 30144. *Corresponding author - bensign@kennesaw.edu. E.J. South and W.E. Ensign 2013 Southeastern Naturalist Vol. 12, No. 4 782 systems typically have a higher percentage of increased impervious surface and a more open canopy than non-urban systems, which usually leads to warmer water due to stormwater runoff and increased insolation. Because water temperature and photoperiodicity influence spawning behavior in fishes (Bond 1996), we expected to find either a shifted or extended reproductive season for the urban stonerollers. While a shifted spawning season would likely be a response to changing thermal regimes, an extended spawning season could potentially be the result of a bet-hedging reproductive strategy that enhances juvenile survival rates in a variable environment (Spranza and Stanley 2000). Increased hydrologic variability (both in terms of intensity and periodicity) is also a common feature of urbanized streams (Roy et al. 2006). Stonerollers are primarily herbivores (Boschung and Mayden 2004); therefore, an increase in algal growth due to the warmer water temperatures and greater light availability may also contribute to increased adult and young-of-year (YOY) growth rates. Higher YOY growth rates and an earlier spawning season in the urban system could result in reproductive activity at a larger size. To test these ideas, we investigated four of the sixteen life-history characteristics of North American fishes described by Winemiller and Rose (1992), including length at maturation, duration of spawning season, YOY growth rates, and adult growth rates. We predicted that the more urbanized stream system would have a population of stonerollers with a longer spawning season, larger size at maturation, and higher adult and YOY growth rates. Study Area We collected Largescale Stonerollers from two stream systems located in the Etowah River drainage basin within the Piedmont ecoregion. The first collection site was an urban second-order tributary of Noonday Creek located in Cobb County, GA, approximately 10 km north of Atlanta. This stream was characterized by riffles and pools with a cobble substrate heavily embedded with silt and sand. Exposed bedrock substrate was present in some runs. The second site included two second-order confluent streams that were tributaries of Pumpkinvine Creek. The streams were located in a forested area of Paulding County, GA, approximately 30 km west of Noonday Creek. Collecting from the upper Pumpkinvine system presented some challenges during the latter part of this study: we discovered that the stream we initially chose for the rural system, Hulseytown Branch, had no above-ground flow in August, with surface-water limited to isolated pools. Consequently, we substituted a second stream, Brushy Branch (confluent with Hulseytown Branch), for the remaining three sampling collections. The last collection from Brushy Branch, in January, yielded a small sample consisting of only ten juveniles and four adults. An obstruction at a downstream culvert which had formed since our penultimate collection, in November, markedly altered habitat at the Brushy Branch site, eliminating the majority of the erosional habitat units where we had captured stonerollers in the previous two samples. Both streams have riffle and pool morphology similar to Noonday Creek, but the substrate is primarily cobble, pebble, and gravel with little embeddedness. We determined the level 783 E.J. South and W.E. Ensign 2013 Southeastern Naturalist Vol. 12, No. 4 of urbanization in the watersheds above the study areas by evaluating impervious surface from the 2006 National Land Cover database (Fry et al. 2011) using Arc- GIS. We identified Noonday Creek (watershed area approximately 9.8 km2) as the more urbanized stream system, with impervious surface covering of 26.3% of the total area. We classified the upper Pumpkinvine streams (watershed area approximately 7.0 km2) as the less impacted stream system, with only 3.4% of the total surface area impervious. Methods We used a backpack electroshocker (Smith-Root Model LR-24) and dip nets to make monthly collections of specimens from both stream systems from February to June 2011, and once each in August 2011, November 2011, and January 2012. We anesthetized all fish with tricaine methanesulfonate, measured them with dial calipers to obtain standard length (SL) and total length to the nearest 0.1 mm, and assessed each one for the presence or absence of tuberculation. We preserved approximately 20 fish per stream from each collection for further study in the lab; all other individuals were allowed to recover before release. We initially preserved retained specimens in 95% ethanol (ETOH) and subsequently transferred them to 70% ETOH. We used some of the collected fish for a concurrent study on age and growth using otoliths, so we used ETOH rather than fixing the specimens in a 10% formaldehyde solution because formaldehyde decalcifies otoliths and would have rendered the specimens useless for the aging study (Cailliet et al. 1986). Of a total of 396 captured fish, we retained 323 for laboratory examination. In addition to the fish collections, we also measured water temperature at each site on each collection date. We secured temperature loggers in each stream to record hourly water temperatures from May through August. Although this period was outside the spawning season, we used the temperature logger data to assess the relative difference in temperature regimes between the two streams. Once in the lab, we placed each fish in water for 10 minutes to allow partial tissue rehydration before processing. We then blotted each fish dry and recorded the total weight to the nearest milligram. We used an opti-visor and digital dial calipers to measure SL and total length to the nearest 0.1 millimeter. SL measurements were taken by removing the lateral musculature at the caudal peduncle and exposing the hypural plate. We removed the gonads, blotted them dry, and weighed them to the nearest milligram. We recorded the presence or absence of tuberculation for males. We examined the gonads of all individuals with a dissecting scope to ensure correct gender assignment, and estimated gonadosomatic index (GSI) by dividing the gonadal tissue weight by the total weight of each individual, and multiplying this value by 100. We used GSI values to categorize individuals into one of two levels of reproductive activity. We assumed that individuals preparing for reproductive activity would undergo a rapid increase in GSI. In contrast, we expected that non-reproductive individuals (juveniles and post-spawn fish) would make limited investments of energy into the production and maintenance of reproductive E.J. South and W.E. Ensign 2013 Southeastern Naturalist Vol. 12, No. 4 784 biomass, resulting in a relatively stable GSI. Thus, we identified a baseline GSI and classified individuals with GSI values that showed evidence of rapid increase above the baseline as reproductively active (RA), and individuals with GSI values near the baseline as reproductively inactive (RI). To differentiate RA from RI individuals, we rank-ordered GSI values from lowest to highest in each gender category for all individuals collected from all sites and dates. The difference between each successive observation was then calculated and used as a measure of the relative increase in the investment in reproductive products. We employed a nonparametric deviance method proposed by Qian et al. (2003) to identify the threshold value where GSI begins to increase rapidly. In this technique, we determined the overall deviance of individual values for a response variable around the group mean. We then created two subsets of data and calculated the deviance of each of the subsets from their respective mean. The sum of the subset deviances will always be less than the group deviance, and the threshold value for the overall data set is defined as the value separating the two subsets that produces the greatest difference between the overall deviance value and the sum of the two subset deviance values (Qian et al. 2003). We used an iterative replacement approach in Excel to determine the threshold value that maximized the difference in overall and subset deviances. We used the non-parametric Mann-Whitney U test for all statistical analyses because biological data sample sizes were small and we could not assume data normality. We compared average GSI values of RA individuals between the two stream systems for each monthly collection. We also compared mean SL of RA individuals between the two stream systems for each month and collectively across months during which reproductive activity might be expected based on data presented in other studies of Campostoma spawning periods (February–May; Etnier and Starnes 1993, Miller 1962). We compared daily water temperature averages for each stream from 6:00 AM and 6:00 PM readings using a paired t-test. Because this was an exploratory study in which we wished to elucidate trends rather than make strong inferences, we chose to set our significance level for al l comparisons at P = 0.10. For the same reason, we did not use corrections for multiple comparisons in our comparisons of monthly values. Results Temperature differences between the two stream systems were highly significant (AM: P < 0.001, PM: P < 0.001). There was a 1.9 ºC difference in temperature at 6:00 AM and a 2.0 ºC difference at 6:00 PM. Noonday Creek temperatures were consistently higher across times and dates. Using the nonparametric deviance method, we identified a threshold value between 0.976 and 0.990 to separate female Largescale Stonerollers. Consequently, we defined RA females as those individuals with GSI values of 0.990 and above, and RI females as those individuals with GSI values of 0.976 and below. We defined RA and RI males by a similar process using the GSI values of 0.192 and above, and 0.175 and below, respectively. 785 E.J. South and W.E. Ensign 2013 Southeastern Naturalist Vol. 12, No. 4 We observed elevated female GSI values from January through May (Fig. 1). High RA female GSI values through May as well as a precipitous drop in those values in June indicated that the completion of the spawning season for both stream systems was concurrent. Additionally, the males collected in June showed low GSI values and no tuberculation. GSI values for RA females were significantly higher in Noonday Creek than Pumpkinvine Creek for the month of February (P = 0.088; Fig. 1); the median Noonday Creek value exceeded the maximum value from Pumpkinvine Creek. From March through May, there was no difference in either median value or range (Fig. 1). RA males had significantly higher GSI values in Pumpkinvine Creek than those in Noonday Creek during March (P = 0.024). Based on analysis of monthly data, our results indicated significant differences in SL of RA females between the two stream systems (Fig. 2). RA females were significantly longer in the urban system in January, February, April, and May (P = 0.034, 0.004, 0.004, and 0.077 for the January, February, April, and May collections, respectively). When we combined data from February through May, differences in length of RA females between Noonday and Pumpkinvine creeks were highly significant (P = less than 0.0001). We found no significant length differences for RA males. For most monthly collections, we were unable to determine age classes based on the length-frequency distributions. However, the length-frequency distributions in June and August were of interest. In June, no YOY were collected in the Figure 1. Gonadosomatic index (GSI) values for reproductively active female Largescale Stonerollers collected monthly from Noonday and upper Pumpkinvine stream systems in 2011 and January 2012. Horizontal bars represent median GSI values and vertical lines represent ranges of GSI values. E.J. South and W.E. Ensign 2013 Southeastern Naturalist Vol. 12, No. 4 786 Pumpkinvine system. However, a 23-mm individual was collected from Noonday Creek. The August collection showed well-defined YOY cohorts for both streams (Fig. 3). The urban system had fifteen YOY ranging from 38.7–56.0 mm SL, and the rural system had seven YOY ranging from 27.6–39.5 mm SL. All but two of the YOY in Noonday Creek were larger than the YOY in upper Pumpkinvine Creek, and the largest YOY individuals from Noonday Creek were equal in size to the smallest age 1 individuals in Pumpkinvine Creek. The August collection also showed well-defined second modes at 72.5 mm in Noonday Creek and at 57.5 mm for the Pumpkinvine system that can be reasonably interpreted a s age 1+ fishes. Discussion As predicted, our results suggested an extended spawning season for Largescale Stoneroller in the urbanized system. The increased GSI values we observed for Noonday Creek females in January, and the significant difference in RA female GSI values between Noonday and Pumpkinvine creeks in February suggested that females in the Noonday stream were building reproductive biomass earlier than females in the upper Pumpkinvine streams. The presence of some heightened GSI values for RA females in both stream systems through the end of May indicates that the end of the spawning season was synchronous in both stream systems. Although the median value for Noonday Creek had declined to lower levels by May, the single highest female GSI value recorded during the study also came from the Figure 2. SL (mm) of reproductively active female Largescale Stonerollers collected monthly (February–November 2011 and January 2012) from Noonday and upper Pumpkinvine stream systems. Horizontal bars represent median lengths, and vertical lines represent length ranges. 787 E.J. South and W.E. Ensign 2013 Southeastern Naturalist Vol. 12, No. 4 May Noonday Creek sample, indicating reproductively active individuals were still present in the system. Additionally, the YOY size differences that we detected in our August collections suggest that spawning season may begin earlier in Noonday Creek than in Pumpkinvine Creek. Previous studies have shown that increased water temperatures in freshwater habitats due to anthropogenic influence initiate early spawning behavior in temperate fishes (Cooke et al. 2003, Paller and Saul 1996). Similarly, our findings suggested that elevated water temperatures in an urbanized stream system corresponded to early spawning activity in a freshwater temperate-zone cyprinid. Peak spawning activity for Central Stoneroller has been reported to occur when water temperatures are 12–14 °C (Etnier and Starnes 1993). In this study’s initial February sampling from the Noonday stream, we recorded a water temperature of 12 °C, and collected RA female Largescale Stonerollers with high GSI values. Spawning behavior of Central Stoneroller has been observed to cease when temperatures drop to 10.6 °C (Miller 1962). In the February sampling in Hulseytown Branch, we collected RA female Largescale Stoneroller with low GSI values and recorded a water temperature of 9.5 °C. Spranza and Stanley (2000) found that Central Stonerollers in a stream environment with elevated water temperatures extended their spawning activity beyond the Figure 3. Length-frequency histograms for all Largescale Stonerollers captured in the Noonday and Pumpkinvine stream systems in August 2011. E.J. South and W.E. Ensign 2013 Southeastern Naturalist Vol. 12, No. 4 788 spawning season observed for stonerollers in a lower water temperature environment. Our study suggests that urbanized Largescale Stonerollers invested energy in reproductive products earlier in the year than the stonerollers in the rural system. In each of these studies, the entire spawning season for stonerollers in an elevated water-temperature environment was not shifted or truncated, but extended earlier or later than the spawning season of the stonerollers in the lower temperature environment. An extended spawning season may enhance the ability of stonerollers to persist in thermally enriched environments by producing offspring over a longer period of time. The extended production of offspring may buffer the effects of stochastic events and increase the number of reproductively active adults available for subsequent reproduction, and thereby promote persistence of the population. We also predicted that Largescale Stoneroller growth rates would be higher in the urban system than in the rural system. If we assume that females reached reproductive maturity at the same age in both stream systems, then the significant length differences we observed in RA females in January, February, April, and May suggest that females grew faster in the urban system. Furthermore, the difference in the putative modal values for age 1+ Central Stonerollers in August (Fig. 3) also indicates higher growth rates in the urban system. Increased size is associated with increased reproductive output in fishes; therefore, more eggs will likely be produced by the urban stream females. There was also evidence that YOY fish in the urban system were larger in August (Fig. 3). The larger size of YOY individuals collected in August from Noonday Creek could have been a function of the earlier initiation of spawning in the urban stream than in the rural stream, or higher growth rates associated with higher water temperatures and increased food supplies. Regardless of the causal factor, it is clear that Noonday Creek YOY were larger than Pumpkinvine Creek YOY as the end of the summer arrived. A number of studies have shown that larger size is associated with increased overwinter survival (Shuter et al. 1980, Thompson et al. 1991). The higher female GSI values in the Noonday Creek February collection and the presence of RA females in May suggest an extended spawning season and higher growth rate for Largescale Stoneroller in urbanized Etowah basin streams. The significantly longer SL of reproductively active females collected from the Noonday Creek system provides strong evidence of higher growth rates in the urban setting. The larger YOY individuals collected in the urban system in the August sample suggest an increased likelihood of survival overwinter, and may also indicate higher growth rates in the urban system. Each of these characteristics should contribute to Largescale Stonerollers’ ability to persist in urbanized systems. Acknowledgments We appreciate field assistance provided by Chris Yates and John Bremner and technical assistance from David Neely. Logistic and financial support from the Department of Biology and Physics at Kennesaw State University allowed the senior author to conduct an undergraduate-directed study project that culminated in this manuscript. 789 E.J. South and W.E. Ensign 2013 Southeastern Naturalist Vol. 12, No. 4 Literature Cited Bond, C.E. 1996. Biology of Fishes, 2nd Edition. Saunders College Publishing, Orlando, FL. 750 pp. Boschung, H.T., and R.L. Mayden. 2004. Fishes of Alabama. Smithsonian Institute, Washington, DC. 736 pp. Cailliet, G.M., M.S. Love, and A.W. Ebeling. 1986. Fishes: A Field and Laboratory Manual on their Structure, Identification, and Natural History. Waveland Press, Inc., Long Grove, IL. 194 pp. Cooke, S.J. 2003. Nesting activity, parental care behavior, and reproductive success of Smallmouth Bass, Micropterus dolomieu, in an unstable thermal environment. Journal of Thermal Biology 28:445–456. Etnier, D.A., and W.C. Starnes. 1993. The Fishes of Tennessee. 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