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Campostoma Anomalum) in a Heavily Urbanized Catchment

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Campostoma Anomalum) in a Heavily Urbanized Catchment Freshwater Biology (2008) 53, 2061–2075 doi:10.1111/j.1365-2427.2008.02030.x Source–sink dynamics sustain central stonerollers (Campostoma anomalum) in a heavily urbanized catchment ERIC R.WAITS, MARK J. BAGLEY, MICHAEL J. BLUM, FRANK H. MCCORMICK AND JAMES M. LAZORCHAK U.S. Environmental Protection Agency, National Exposure Research Laboratory, Ecological Exposure Research Division, Cincinnati, OH, U.S.A. SUMMARY 1. The influence of spatial structure on population dynamics within river–stream networks is poorly understood. Utilizing spatially explicit analyses of temporal genetic variance, we tested whether persistence of central stonerollers (Campostoma anomalum) reflects differences in habitat quality and location within a highly modified urban catchment in southwestern Ohio, U.S.A. 2. Estimates of genetic diversity did not vary with habitat quality. Nevertheless, evidence of weak but temporally stable genetic structure, location-dependent effective population sizes and rates of immigration among sites, together suggest that persistence of central stonerollers within the catchment may be attributable to source–sink dynam- ics driven by habitat heterogeneity. 3. Under this scenario, migrant-pool colonization from areas of relatively high habitat quality in the upper catchment sustains the presence of central stonerollers at degraded sites in the main stem and dampens population subdivision within the catchment. However, because intact habitat is restricted to the upper portion of the catchment, it is not possible to preclude net downstream dispersal as a mechanism contributing to source– sink dynamics. The slight genetic structure that persists appears to reflect weak isolation by distance diminished by high rates of immigration. 4. This study suggests that without a systems perspective of the conditions that sustain populations in degraded waterways, environmental assessments may underestimate levels of impairment. Conservation and management of stream fishes could be improved by maintaining habitat in areas that are net exporters of migrants or by remediation of impaired habitat. Keywords: aquatic biological assessment, conservation, effective population size, migration, popula- tion genetics Introduction Correspondence: Eric R. Waits, U.S. Environmental Protection Agency, National Exposure Research Laboratory, Molecular Relating local demographic processes to spatial struc- Ecology Research Branch, Cincinnati, OH 45268, U.S.A. ture (e.g. habitat heterogeneity) is essential for under- E-mail: [email protected] standing population and species persistence (Hanski Present address: Frank H. McCormick, U.S. Forest Service, & Gilpin, 1997; Fagan, 2002). Yet few studies have Pacific Northwest Research Station, Olympia, WA 98512, U.S.A. tested general hypotheses about the importance of Ó 2008 Blackwell Publishing Ltd. No claim to original US government works 2061 2062 E. R. Waits et al. spatial patterns in determining population dynamics examining both spatial and temporal genetic variance within river–stream networks (Lowe, Likens & Power, can be more informative (Tessier & Bernatchez, 1999; 2006). Metapopulation studies of stream biota such as Garant, Dodson & Bernatchez, 2000; Lundy, Rico & freshwater fishes often relate site occupancy to the Hewitt, 2000; Hansen et al., 2002; Heath et al., 2002; hierarchical structure of river–stream networks Alo & Turner, 2005). In addition to validating (Dunham & Rieman, 1999; Taylor & Warren, 2001), estimates of population genetic structure (Nielsen but rarely consider how colonization varies according et al., 1999), spatially explicit analysis of temporal to connectivity, dispersal geometry and spatial scale genetic variation allows more accurate estimation of (Pannell & Charlesworth, 1999; Fagan, 2002; Lowe effective population size (Ne) and immigration rates et al., 2006). Similarly, studies focusing on movement (m) (Waples, 1989). From a conservation standpoint, of stream fishes often identify habitat and conditions Ne and m are two of the most significant parameters that favour or constrain dispersal (Power, 1984; influencing genetic variation and therefore the sus- Skalski & Gilliam, 2000), but few effectively link tainability of populations in heterogeneous environ- movement patterns to the spatial distribution of ments (Allendorf & Leary, 1986; Pulliam, 1988; source and sink habitats (Lowe et al., 2006). Frankham, 1995; Newman & Pilson, 1997; Marr, Keller Urban catchments are natural laboratories for & Arcese, 2002; Vila et al., 2003). To monitor and examining population persistence and dispersal of assess populations, estimates of Ne and m can eluci- stream fishes. Runoff, physical habitat and flow date the present condition and project future vulner- regime modifications can lead to highly altered abilities of populations (Bagley et al., 2002). Thus, an stream fish assemblages reflecting heterogeneous loss understanding of the role of Ne and m in maintaining of diversity and persistence of pollution-tolerant population genetic structure can be critical to species (Roy et al., 2005). Variation in assemblage management and conservation, especially for small structure can be examined to relate site occupancy to populations inhabiting marginal habitats that are habitat quality and spatial location (Power, 1984; likely to be affected by stochastic events (Pulliam, Taylor, 1997; Gotelli & Taylor, 1999). Even in the most 1988; Alo & Turner, 2005). degraded and biologically depauperate ecosystems, it We undertook this study of a moderately pollu- is possible to learn more about persistence and tion-tolerant stream fish within a heavily urbanized colonization from patterns of genetic variation among catchment to improve basic understanding of meta- populations of remaining pollution-tolerant fishes. population dynamics in environmentally heteroge- Urbanization can influence genetic variation of pol- neous river–stream networks. Utilizing spatially lution-tolerant species by altering levels of genetic explicit analysis of temporal genetic variance, we drift, migration, and natural selection (Bickham et al., tested whether population persistence reflects habi- 2000; Theodorakis, 2003). Patterns of genetic variation tat quality and location within the catchment. We may subsequently bear signatures of population first examined whether levels of genetic diversity persistence and colonization relative to habitat qual- were lower at impaired sites compared to unim- ity, connectivity, dispersal geometry and spatial scale. paired locations. Since genetic differences should For example, habitat modifications that reduce pas- reflect influences of selection, gene flow or genetic sage and restrict gene flow (Hebert et al., 2000) can drift, we then assessed whether the distribution of increase genetic drift within subdivided populations genetic variance was related to habitat quality, and divergence among populations (Pannell & geographic proximity of sites, or stream connectivity Charlesworth, 1999) at varying spatial scales. Expo- patterns. We also estimated Ne and m at sites that sure to urban runoff can select against less tolerant were sampled multiple times over an 8-year period, genotypes and consequently alter the size, viability, with the expectation that estimates of Ne would be and genetic diversity of populations (Fox, 1995; smaller and estimates of m would be higher in Cimmaruta et al., 2003). degraded areas. Finally, we examined spatial and Prior studies have demonstrated that measurement temporal patterns of population subdivision as well of spatial genetic variance is a useful approach for as spatial variation in estimates of Ne and m to infer examining metapopulation dynamics in stream fishes patterns of connectivity and dispersal at different (Fontaine et al., 1997; McElroy et al., 2003), but spatial scales. Ó 2008 Blackwell Publishing Ltd. No claim to original US government works, Freshwater Biology, 53, 2061–2075 Central stoneroller dynamics in an urbanized catchment 2063 Methods catchment are mostly intact and in-stream habitats are characterized by coarse substrates and moderate Study location and sample collection cover. Biotic diversity and abundance are highest in The Mill Creek catchment covers 274 km2 in south- these upper tributaries and head waters. Downstream western Ohio, USA. The basin crosses approximately of the head waters, the catchment contains more 45 km of the Cincinnati (OH) urban corridor from its residential, urban and light industrial development; headwaters to the confluence at the Ohio River fine substrates, stream embeddedness and entrench- (Fig. 1). Over 500 000 people live in the drainage area ment increase, channel sinuosity decreases, and and development is continuing throughout the basin. in-stream cover is reduced due to narrow riparian Mill Creek has been designated a highly impaired borders. Further downstream, sections of the catch- waterbody for Aquatic Life Use, Recreation (Primary ment are heavily industrialized. Former municipal Contact) and Fish Consumption Advisories (Ohio and industrial landfills, including five Superfund sites EPA, 2004a). The system is heavily impacted by (abandoned hazardous waste sites which pose a threat industrial and municipal point source discharges, to local ecosystems or people and have been identified uncontrolled storm water runoff, sewer overflows, for priority clean-up), as well as more than 100 and contaminated sediment from industrial dis- combined sewer overflows and 50 sanitary sewer charges, landfills and toxic waste sites (American
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