BROADCAST spawning is the predominant reproductive

Transcription

1 Copeia 2009, No. 1, Effects of Streamflow and Intermittency on the Reproductive Success of Two Broadcast-spawning Cyprinid Fishes Bart W. Durham 1 and Gene R. Wilde 1 We studied daily growth-increment formation in the otoliths of early life history stages of Sharpnose Shiner, Notropis oxyrhynchus, and Smalleye Shiner, Notropis buccula, in the Brazos River, Texas to investigate the influence of streamflow and intermittency on the production of young. Both species successfully produced offspring throughout a four- to fivemonth period. Successful reproduction occurred over a longer period in 2004 than in The results of our study revealed that recruitment by N. oxyrhynchus and N. buccula populations in the Brazos River, Texas are related to streamflow in two principal ways. First, the greatest proportion of young-of-year produced during the reproductive season is associated with elevated streamflow events. Second, no young-of-year are successfully produced during periods of intermittency when the river is not flowing. Our results suggest that the focus of conservation efforts, which to date have primarily concentrated on creating proper streamflow conditions for spawning, should also be focused toward ensuring proper conditions for survival of ova and young larvae. BROADCAST spawning is the predominant reproductive mode among North American cyprinids and is exhibited by greater than 60% of species for which reproductive strategies have been described (Johnston and Page, 1992). Because broadcast-spawners release ova onto unmanipulated substrata, ova and developing larvae are susceptible to the vagaries of environmental conditions such as streamflow, temperature, and dissolved oxygen. Consequently, reproductive success among broadcastspawning species largely is determined by environmental conditions during the spawning season. Because most small cyprinid species are short-lived with only a two- to threeyear maximum life span (Winemiller and Rose, 1992; Bonner, 2000), a single year without successful reproduction would result in a significant decrease in population abundance in the following year. To reduce the likelihood of such an occurrence, fishes that inhabit extremely variable and unpredictable environments often spawn multiple clutches of ova throughout an extended reproductive season (Cohen, 1966; Hontela and Stacey, 1990; Lowerre-Barbieri et al., 1998). Early studies of the reproductive ecology of broadcastspawning cyprinids in Great Plains rivers of North America reported an apparent relationship between the recruitment of young-of-year fishes and increased streamflow conditions (Moore, 1944; Sliger, 1967; Bestgen et al., 1989). Consequently, elevated streamflow has been viewed as a necessary cue for the initiation of spawning among these species. This apparent relationship was based on sampling conducted only during periods of increased streamflow (Moore, 1944; Sliger, 1967) or from back-calculated estimates of spawning dates based on lengths of captured fish (Bestgen et al., 1989; Taylor and Miller, 1990). However, other evidence suggested that spawning was not initiated by increased streamflow. For example, detailed histological analysis of oocyte development in ovaries of Arkansas River Shiner, Notropis girardi, and Peppered Chub, Macrhybopsis tetranema, revealed that postovulatory follicles, which are remnants of recently spawned ova, were continuously present throughout the reproductive season and their abundance was not associated with the magnitude of streamflow (Bonner, 2000). Postovulatory follicles were present in the ovaries even during a month-long period when fish were confined to isolated streambed pools due to drought conditions. Further, Durham and Wilde (2006) found that successful reproduction among five cyprinid species in the Canadian River, Texas was continuous except during periods when the river was not flowing. The Sharpnose Shiner, Notropis oxyrhynchus, and Smalleye Shiner, Notropis buccula, are cyprinid fishes endemic to the Brazos River, Texas. Both species historically were found throughout the entire length of the river; however, extensive reservoir construction, groundwater extraction, and other anthropogenic modifications in the central portion of the basin (Anderson et al., 1983, 1995) have likely resulted in their extirpation from the lower two-thirds of the river. Both species now remain common only in the unmodified portion of the upper Brazos River. Given conflicting reports about the precise role that streamflow plays in the reproductive ecology of Great Plains cyprinids, additional study is needed to better understand the nature of the relationship between streamflow and reproduction and the possible impact of reduced streamflow on distribution and abundance of these species. Because N. oxyrhynchus and N. buccula appear to have many of the same life history and reproductive traits that have been described for other Great Plains cyprinids that broadcast-spawn drifting semibuoyant eggs (Platania and Altenbach, 1998), an investigation of their recruitment patterns would help support a broader understanding of the relationship between streamflow and reproduction in these species. In this study, we inspected daily growth increment formation in the otoliths of young-of-year N. oxyrhynchus and N. buccula in the Brazos River, Texas to investigate the influence of streamflow and intermittency on recruitment. MATERIALS AND METHODS Study area and field techniques. The Brazos River is located at the southern edge of the North American Great Plains ecosystem. Its headwaters form in western Texas, and the river flows east and south through Texas for approximately 2000 km before discharging into the Gulf of Mexico at Freeport. Two major tributaries, the Salt Fork and Double 1 Department of Biological Sciences, Texas Tech University, Mail Stop 3131, Lubbock, Texas ; (BWD) bart.durham@ lcu.edu; and (GRW) gene.wilde@ttu.edu. Send reprint requests to BWD. Submitted: 7 August Accepted: 17 June Associate Editor: J. W. Snodgrass. F 2009 by the American Society of Ichthyologists and Herpetologists DOI: /CE

2 22 Copeia 2009, No. 1 microhabitats to ensure that a representative sample of available young-of-year fish was obtained. Young-of-year fish were identified by their small size compared to adults and were readily identifiable as young-of-year fish throughout the reproductive season. All young-of-year fish collected were preserved in 95% ethanol. Voucher specimens were reposited in the Texas Natural Science Center Ichthyology Collection (TNHC ) at the University of Texas in Austin. To assess the effects of variation in reproductive effort on recruitment, adult fish were also collected at each site on each date for inspection of reproductive condition. Adult fish were collected with a m seine (5-mm mesh) and preserved in 10% buffered formalin. Fig. 1. Study area and location of sampling sites on the upper Brazos River, Texas. Mountain Fork (DMF), combine to form the Brazos River mainstem at their confluence in northeastern Stonewall County, Texas (Fig. 1). In this portion of the Brazos River, precipitation during the year is sporadic and localized, leading to variable and erratic stream discharge (Fig. 2; Echelle et al., 1972; Ostrand and Wilde, 2002). Although there can be considerable variation in the timing of precipitation from year to year, most precipitation is a result of convective thunderstorms that occur primarily in late spring and again in early fall. As spring precipitation decreases, the upper portion of the Brazos River and its tributaries often experience periods of intermittency during the typically warm and dry summer months. Three sampling sites in the upper Brazos River Basin were selected based on location, accessibility, and potential species composition (Fig. 1). Site 1 was located on the mainstem of the Brazos River in Baylor County, Texas (33u34990N, 99u16910W). Site 2 was located on the mainstem of the Brazos River in Knox County, Texas (33u309030N, 99u48910W). Site 3 was located on the DMF of the Brazos River in Fisher County, Texas (32u55980N, 100u29930W). We obtained streamflow data for all sites from the United States Geological Survey surface water monitoring station nearest to each site. For the two sites on the Brazos River mainstem, streamflow data were obtained from the same USGS station, USGS number , which is located at site 1 and is approximately 50 km downstream from site 2. Consequently, all data collected at these two sites were combined for analyses. Data for the DMF were obtained from station number , which is located approximately 30 km downstream from the sampling site. We collected young-of-year fish with a m seine (1-mm mesh) monthly at each site from April 2003 through March 2005, except during May through September (the approximate spawning season) when samples were taken twice each month. At each site, we sampled for approximately one hour and collected fish from all available Laboratory techniques. In the laboratory, all young-of-year fish were identified to species. Because many samples contained large numbers of fish (.500), a sub-sample of individuals of each species collected from each site on each date was selected for otolith removal and analysis of otolith microstructure. Individual fish in sub-samples were chosen indiscriminately, except that we intentionally included all sizes of fish collected so that the full range of lengths present in the original sample would also be represented in the sub-sample. In a study using the same fish selection procedure, Durham and Wilde (2006) used t- tests to assess the assumption of no difference in mean length between field samples and sub-samples used for otolith analysis. They found that sub-samples differed from field samples in only two out of 200 instances for five cyprinid species in the Canadian River, Texas. Thus, we are confident that sub-sampled fish used for otolith analysis were representative of the total catch. We measured each fish to standard length (SL) and removed lapilli. Procedures for otolith preparation and counting of daily growth increments followed those of Durham and Wilde (2005, 2006). Using a dissecting microscope, we removed both lapilli otoliths. We attached one to a glass microscope slide with thermoplastic cement and stored the remaining otolith for future reference. Two readers independently counted daily growth increments for all otoliths using a compound light microscope at 100X magnification. If growth increment counts from the two readers were within 10% of each other, they were accepted and a final daily age was assigned as the mean of the two counts. When the two initial readings differed by more than 10%, a third reader counted growth increments for that otolith. We excluded from analysis all otoliths for which counts could not be reconciled to within 10%. The final number of useable otoliths for N. oxyrhynchus was 150 in 2003 (7% excluded) and 124 in 2004 (3% excluded). The final number of useable otoliths for N. buccula was 253 in 2003 (8% excluded) and 280 in 2004 (3% excluded). Prior to this study, we used alizarin complexone to validate the daily deposition of growth increments in the lapilli of young-of year N. oxyrhynchus, N. buccula, and Plains Minnow, Hybognathus placitus (Durham and Wilde, 2008). We immersed fish in a solution of alizarin complexone to induce a chemical reference mark on the otoliths. The number of daily growth increments outside the reference mark was compared to the number of days since treatment over a 30-day period. Otoliths were removed, prepared, and read using the same protocols described above. Regression models revealed a high correspondence between the

3 Durham and Wilde Intermittent streamflow and recruitment 23 Fig. 2. Mean daily streamflow for Brazos River study sites between April 2003 and March number of daily growth increments and the number of days since alizarin complexone treatment for N. oxyrhynchus (r ; n 5 65) and N. buccula (r ; n 5 64). In addition, slopes of regression lines did not differ from 1.0 (t-test, P, 0.05), indicating that growth increments are deposited daily in both species. To determine spawning dates from assigned ages, we added three days to each final daily age estimate to account for the period of egg incubation and early embryonic development, which Moore (1944), Bottrell et al. (1964), and Sliger (1967) estimated to be between one and three days for N. girardi, M. tetranema, and H. placitus, respectively. We assumed three days to allow for the formation of the first daily growth increment after hatching. We identified adult fish to species and determined sex by macroscopic inspection of the gonads. For each site and date, we removed ovaries from up to five females of each species containing mature ovaries (Durham, 2007). Occasionally, samples contained fewer than five females with mature ovaries. We embedded each ovary in paraffin and sectioned them longitudinally at a thickness of 5 7 mm. We fixed the sections to microscope slides and stained them with Weigert s hematoxylin and eosin. We viewed slides under a compound microscope at 40X magnification and classified all differentiated oocytes in one complete section into one of the following groups: cortical alveoli, early vitellogenic, or late vitellogenic. We assessed variation in reproductive effort by calculating the mean proportion of late vitellogenic oocytes for each site and date. Data analyses. We assessed the relationship between Brazos River streamflow and recruitment, defined here as the successful hatching and survival of young-of-year, for N. oxyrhynchus and N. buccula with a generalized linear model. We modeled the number of fish spawned on each day (dependent variable) as a function of streamflow (independent variable) with a negative binomial error distribution, a negative binomial dispersion parameter, and a log-link function to control for the overdispersion common in biological count and catch data (White and Bennetts, 1996; Power and Moser, 1999). Because generalized linear models are fit to data using maximum likelihood methods, significance of individual species and site comparison models was based on an analysis of deviances, which are distributed as X 2 variates. We conducted separate analyses for each year and site combination for each species. We used SAS statistical software and the GENMOD procedure to

4 24 Copeia 2009, No. 1 conduct regression analyses. If a general relationship exists between streamflow and recruitment, we would expect regression slopes to be positive, regardless of statistical significance. If there were no relationship, we would expect half of the regression slope estimates to be positive and half to be negative. We used a binomial test (Siegel, 1956) to determine if an excess of positive estimates existed. RESULTS Mean length (SL, mm) and age (days) of N. oxyrhynchus youngof-year for which otoliths were analyzed was mm (range mm) and days (range days), respectively in 2003, and mm (range mm) and days (range days) in Mean length and age of N. buccula young-of-year was mm (range mm) and days (range days), respectively in 2003, and mm (range mm) and days (range days) in Streamflow during 2003 was low in both the Brazos River mainstem and the DMF with only a few moderate peaks in streamflow occurring during the reproductive season (Fig. 3). In the Brazos River mainstem, streamflow ranged from 0.0 m 3?s m 3?s 21 but was, 1.0 m 3?s 21 on 72% of days during the reproductive season. In the DMF, streamflow ranged from 0.0 m 3?s m 3?s 21 and was, 1.0 m 3?s 21 on 81% of days during the 2003 reproductive season. Streamflow was absent in the Brazos River between 7 August and 29 August, and absent in the DMF between 20 July and 29 August during the 2003 reproductive season. During these periods, fish were confined to isolated pools. Streamflow during the 2004 reproductive season also was variable, but was consistently greater than in the previous year and the river never ceased to flow (Fig. 3). Streamflow in 2004 ranged from 0.31 m 3?s m 3?s 21 but was. 1.0 m 3?s 21 on 82% of days in the Brazos River mainstem. Streamflow ranged from 0.25 m 3?s m 3?s 21 in the DMF and was. 1.0 m 3?s 21 on 73% of days during the 2004 reproductive season. Notropis oxyrhynchus and N. buccula successfully produced offspring between April and September during periods of high and low streamflow (Figs. 3, 4). However, the absence of streamflow in the river at both sites during portions of July and August in 2003 appeared to preclude successful recruitment by both species (Figs. 3, 4). Of the 493 individuals for which otoliths were analyzed in 2003, none had back-calculated hatch dates that corresponded to the period during which the river did not flow. In 2004 when the river flowed continuously, no interruption in recruitment was observed. Recruitment of N. oxyrhynchus and N. buccula occurred over a longer period in 2004 than in For N. oxyrhynchus in the Brazos River, recruitment occurred from late April through July in 2003 and from late March through August in 2004 (Fig. 3). In the DMF, recruitment by N. oxyrhynchus occurred from late May through mid-july in 2003 and from mid-april through mid-august in For N. buccula in the Brazos River, recruitment occurred from late April through early August in 2003 and from mid-april through early September in In the DMF, recruitment by N. buccula occurred from late April through mid July in 2003 and from May through mid August in 2004 (Fig. 4). Increases in the proportion of fish produced on a given day in both years appeared to coincide with, or occur a few days after, increases in streamflow, indicating that some Fig. 3. Mean daily streamflow for Brazos River study sites in 2003 and 2004 (solid line) and the proportion of all young-of-year N. oxyrhynchus collected that were spawned on each date during the reproductive season (circles). Spawning dates were determined by back-calculating the number of daily growth increments on otoliths. Shaded areas indicate periods during which the river did not flow. association between recruitment and streamflow exists (Figs. 3, 4). A statistically significant (P, 0.05) relationship between streamflow and the number of fish produced on each date was found for only two of the eight species, site, and year combinations (Table 1). Both significant relationships were observed in the Brazos River mainstem in 2003, indicating that the number of young-of-year recruited by both species at this site during 2003 was positively related to the level of streamflow. Slopes of regression variable estimates were positive for seven of the eight species, site, and year combinations (Table 1), further suggesting the presence of a general positive relationship between recruitment and streamflow (binomial test, P ). The proportion of late vitellogenic oocytes ranged from 0.32 to 0.78 in the ovaries of N. oxyrhynchus and from 0.09 to 0.73 in N. buccula. In both species, the proportion of late vitellogenic oocytes decreased in samples taken after increases in streamflow occurred (Figs. 5, 6) indicating that synchronized spawning events within the population were associated with increases in streamflow. The only exception to this pattern was for N. buccula in the DMF in In that case, there was only a slight decrease in the proportion of late vitellogenic oocytes after the largest peak in streamflow in early June, and the biggest decrease was observed in August and was not associated with elevated streamflow. Although

5 Durham and Wilde Intermittent streamflow and recruitment 25 Fig. 4. Mean daily streamflow for Brazos River study sites in 2003 and 2004 (solid line) and the proportion of all young-of-year N. buccula collected that were spawned on each date during the reproductive season (circles). Spawning dates were determined by back-calculating the number of daily growth increments on otoliths. Shaded areas indicate periods during which the river did not flow. there is no clear explanation for why the reproductive pattern differed in this case, streamflow at site 3 in 2003 was the lowest for the longest period of time during the study and may have affected reproductive output. With this single exception, reproductive output clearly intensified during or just after increases in streamflow. DISCUSSION Based on gonadosomatic indices, oocyte size-distribution histograms, and histological analysis of ovaries of mature Fig. 5. Mean proportion (6SE) of late vitellogenic oocytes in the ovaries of N. oxyrhynchus from the Brazos River at each site and sampling date plotted with mean daily discharge for Brazos River study sites in 2003 and females, Durham (2007) showed that N. oxyrhynchus and N. buccula spawn multiple times over a protracted reproductive period that spans approximately six months, April through September. These same analyses demonstrate that ovaries of individual fish contain oocytes in all stages of development throughout the reproductive season including a continuous supply of late vitellogenic oocytes ready to be spawned. Spawning within populations of both species occurs continuously at a low intensity and is asynchronous during periods of low streamflow, but spawning becomes synchronized and more intense during periods of increased streamflow (Durham, 2007). Analyses of otolith microstructure used in this study revealed that ova successfully hatch and young-of-year fish can be produced over a similar protracted Table 1. Generalized Linear Models Describing the Relationship between Recruitment of Notropis oxyrhynchus and Notropis buccula and Streamflow in the Brazos River Mainstem and Double Mountain Fork of the Brazos River (DMF) in 2003 and Species Year River n Fish Slope Intercept X 2 P-value N. oxyrhynchus 2003 Brazos DMF Brazos DMF N. buccula 2003 Brazos DMF Brazos DMF

6 26 Copeia 2009, No. 1 Fig. 6. Mean proportion (6SE) of late vitellogenic oocytes in the ovaries of N. buccula from the Brazos River at each site and sampling date plotted with mean daily discharge for Brazos River study sites in 2003 and period. In addition, our study revealed that recruitment by N. oxyrhynchus and N. buccula populations in the Brazos River are related to the magnitude of streamflow in two principal ways. First, the greatest proportion of young-ofyear fish produced during the reproductive season is associated with elevated streamflow events. Second, no young-of-year are successfully produced during periods of intermittency when the river is not flowing. The observed increase in the proportion of young-of-year successfully produced during periods of increased streamflow in both years of the study is likely a result of both the greater number of ova that are spawned when streamflow increases and the favorable conditions for survival of drifting ova and young larvae that result from a greater volume of water in the river. Increased water levels aid in suspension and transport of ova as they develop and provide abundant nursery habitat along channel margins for emergent larvae. In a number of cases, there was a short lag-time between the increase in streamflow and the increase in the proportion of offspring produced. Reasons for this lag are not clear; however, based on our knowledge of their reproductive ecology, we suggest two possible explanations. First, the synchronized spawning episodes, which are cued by a rising hydrograph (Durham, 2007; this study), may not occur immediately as streamflow increases. If this is the case, a similar lag between streamflow and production of young-of-year would be expected; however, a narrower sampling window is required to confirm this possibility. Alternatively, the lag may be a sampling artifact resulting from rapid transport of ova and young larvae downstream and away from the sampling sites until streamflow recedes to a magnitude that young-of-year fish are capable of colonizing. The negative effects of no- and low-flow conditions on spawning by adults and survival of ova likely explain why recruitment of N. oxyrhynchus and N. buccula during the 2003 reproductive season was noticeably restricted in time compared to recruitment during In the most extreme case, recruitment by N. oxyrhynchus at the DMF site in 2003 began a month later and ended a month before recruitment at the same site in Extreme drought conditions prevailed in the region during much of 2003; whereas, in 2004, the region received record high precipitation. Similar inter-annual variation in reproductive condition and recruitment of Red Shiner, Cyprinella lutrensis, populations in central Texas and Oklahoma were reported by Farringer et al. (1979), which they attributed to a combination of differences in streamflow, turbidity, and temperature. Cyprinid fishes in both the Brazos and Canadian rivers release ova (i.e., spawn) in isolated pools when streamflow is absent (Bonner, 2000; Durham, 2007); however, there is no evidence that young-of-year in either river are successfully produced from these ova (Durham and Wilde, 2006; this study). The ultimate fate of ova spawned in pools, or of any young-of-year fish resulting from those ova, is unknown but they likely succumb to the stressful conditions that occur in drying streambed pools (Tramer, 1977; Matthews and Maness, 1979; Mundahl, 1990; Capone and Kushlan, 1991; Ostrand and Wilde, 2001) or are consumed by adult fish (Ruppert et al., 1993; Vives, 1993; Gido et al., 1999). Although we found no evidence that ova spawned within pools successfully hatch (Durham and Wilde, 2006; this study), questions remain about how periods of intermittency affect survival and growth trajectories of young-of-year that are present in the river prior to pool formation. Growthincrement data from otoliths of cyprinids in the Canadian River, Texas indicate that fish spawned prior to periods of intermittent streamflow are capable of surviving pooled conditions (Durham and Wilde, 2006). However, the dynamics that determine which individuals survive in pools, how growth rates might differ between fish that experience pooled conditions and those that never become trapped in pools, or if size-selective overwinter mortality occurs for these species (Durham and Wilde, 2005) is unknown. Effective conservation and management of imperiled cyprinids is often hindered by a general lack of basic biological information (Johnston and Page, 1992; Johnston, 1999), particularly regarding their reproductive ecology and the biology of early life-history stages. The present study helps clarify the role that streamflow plays in the basic reproductive biology and recruitment of N. oxyrhynchus and N. buccula. In addition, our study identifies an important consideration for the conservation of imperiled Great Plains cyprinids, that the focus of conservation efforts, which to date have primarily concentrated on creating proper streamflow conditions for spawning, should be equally focused toward ensuring proper conditions for survival of ova and young-of-year individuals. Extended periods of intermittency are detrimental to recruitment and negatively affect survival and growth of ova and young-of-year fish. Despite the loss of some reproductive output when conditions are unfavorable for recruitment (i.e., when fish are trapped in

7 Durham and Wilde Intermittent streamflow and recruitment 27 isolated pools), the protracted reproductive season and multiple spawning strategy exhibited by many cyprinid species allows populations to persist in variable stream environments. However, as river systems become increasingly fragmented and the frequency of intermittent streamflow increases, reproductive failure could become more common among these species and may be the source of recent population declines observed for several broadcast spawning species (Anderson et al., 1995; Pigg et al., 1999; Bonner and Wilde, 2000). Thus, additional fragmentation of streams and rivers with reservoirs or other modifications that reduce the volume of water in the river should be avoided if possible. However, in particularly dry years, such as occurred in 2003, water releases from existing reservoirs could be used to reduce the frequency of intermittent streamflow and improve recruitment and growth for young, if such contingencies were in place. ACKNOWLEDGMENTS We thank P. Bean, B. Gaines, M. Laman, and C. Stennett for field assistance, and C. Chizinski and D. Knabe for laboratory assistance and reading otoliths. All fish were collected legally under the authority of valid public fishing permits issued by the Texas Parks and Wildlife Department. All field and laboratory procedures were reviewed and approved by the Texas Tech University Animal Care and Use Committee, and work was conducted under protocol number Helpful reviews of earlier drafts of this manuscript were graciously provided by R. Patiño, K. Pope, L. Smith, and R. Strauss. Funding for this project was provided in part by the Texas Parks and Wildlife Department and the United States Fish and Wildlife Service. 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