Long-term monitoring of species assemblages provides a unique opportunity to test hypotheses regarding environmentally induced directional trajectories of freshwater species assemblages. We used 57 years of lockchamber fish rotenone and boat electrofishing survey data (1957–2014) collected by the Ohio River Valley Water Sanitation Commission (ORSANCO) to test for directional trajectories in taxonomy, trophic classifications, and life history strategies of freshwater fish assemblages in the Ohio River Basin. We found significant changes in taxonomic and trophic composition of freshwater fishes in the Ohio River Basin. Annual species richness varied from 31 to 90 species and generally increased with year. Temporal trajectories were present for taxonomic and trophic assemblages. Assemblage structure based on taxonomy was correlated with land use change (decrease in agriculture and increase in forest). Taxonomic assemblage structure was also correlated with altered hydrology variables of increased minimum discharge, decreased fall rate, and increased rise rate. Trophic composition of fish catch correlated with land use change (decrease in agriculture and increase in forest) and altered hydrology. Altered hydrology of increased minimum discharge, increased fall discharge, decreased base flows, and increased number of high pulse events was correlated with increased counts of herbivore-detritivores and decreased counts of piscivores and planktivores. We did not find directional changes in life history composition. We hypothesized a shift occurred from benthic to phytoplankton production throughout the basin that may have decreased secondary production of benthic invertebrates. This may also be responsible for lower trophic position of invertivore and piscivore fishes observed in other studies.
Citation: Pyron M, Mims MC, Minder MM, Shields RC, Chodkowski N, Artz CC (2019) Long-term fish assemblages of the Ohio River: Altered trophic and life history strategies with hydrologic alterations and land use modifications. PLoS ONE 14(4): e0211848. https://doi.org/10.1371/journal.pone.0211848
Editor: Hudson Tercio Pinheiro, California Academy of Sciences, UNITED STATES
Received: January 22, 2019; Accepted: March 22, 2019; Published: April 24, 2019
Copyright: © 2019 Pyron et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Data Availability: http://www.orsanco.org/data/
Funding: The authors received no specific funding for this work.
Competing interests: The authors have declared that no competing interests exist.
Anthropogenic threats to freshwater ecosystems are numerous and globally widespread. Rivers are altered by multiple factors including watershed land use, hydrologic alterations, municipal and industrial effluent, and water withdrawals . Conservation of water resources and increased water demands requires understanding historical and current effects of water and land use to help inform potential solutions via restoration or intervention ; key to this is the scale at which human activities affect biodiversity, and the patterns detectable across scales. Long-term monitoring data of biotic and abiotic factors, such as fish assemblages, provide an opportunity to test hypotheses regarding how environmental modifications affect the taxonomic, trophic, and life history compositions of aquatic organisms [3,4].
Land use changes from natural ecosystems to those dominated by intense agriculture, deforestation, or urbanization can dramatically alter fish biodiversity [5–7]. Modification from forest, grasslands, or wetlands to tillable agricultural land on a global scale provides numerous benefits to humans. Yet these activities are often unsustainable . When damaging agricultural practices are abandoned for best management or conservation goals, nutrient loading and pesticide contamination continue to affect stream ecosystems for years or decades, so-called the “ghost of land use past” .
The legacy of agriculture and land use is manifested in the Ohio River Basin, a watershed historically dominated by agriculture, but converted from agriculture to forest during the 1960s-80s . The Ohio River Basin was drastically modified via logging and draining of wetlands following European colonization . Urban and agricultural land use in the Ohio River basin were 13% and 74%, respectively, in 1930, exceeding critical threshold effects on water quality and aquatic health . In addition, the Ohio River hosts invasive species including Common Carp (Cyprinus carpio), Goldfish (Carassius auratus), Silver Carp (Hypophthalmichthys molitrix), Bighead Carp (Hypophthalmichthys nobilis), and zebra mussels .
Despite these challenges, Thomas et al.  identified improvements in fish assemblage metrics, including species richness and an index of well-being, in the most recent 50 years that were correlated with higher water quality after implementation of the US Clean Water Act. Yet the degree to which taxonomy, trophic classification, and life history strategies of fish assemblages throughout the basin have changed, and whether these changes are correlated with changes in land use and hydrology, remains unknown. Free of anthropogenic or other major disturbances, fish assemblages are expected to vary stochastically around an equilibrium structure, returning to average state with time over the long term [13,14]. Conversely, assemblages monitored over the long-term often exhibit directional trajectories in response to anthropogenic disturbance [15–17] or may transition to alternative community states .
Food webs depict trophic interactions between consumers and resources and allow analyses of community structure, stability, and ecosystem processes . Yet, complex drivers of ecosystem variation and food web modification are difficult to identify . For example, flow regimes influence freshwater food webs in complex and frequently contradicting manners. Hydrologic alterations due to construction of dams and levees in the Upper Mississippi River caused increased hydrogeomorphic complexity . Increased complexity resulted in more diverse food sources for fish production, and increased variation in food sources for invertivore and piscivore fishes . Yet, in the Ohio River, similar correlations between hydrologic alterations and changing food webs were not observed. Bowes  found that mean trophic positions of fishes decreased after dam construction, but trophic position was not correlated with hydrologic variables. Delong and Thoms  identified major changes in carbon sources for the Ohio River, and increased variation in mean nitrogen stable isotope ratios of fishes, following flow modifications that occurred from 1950–55. Bowes  identified carbon sources for fishes from the Ohio River collected from 1931–1970 and found that autochthonous algae was the major contributor. Food webs can also be influenced by biotic factors such as aquatic invasive species  that replace or supplement native species and can shift energy sources. We were interested if hydrologic alterations in the Ohio River resulted in modifications of trophic structure in fish assemblages.
Fish assemblages are often controlled by hydrologic regimes [25–27], considered the “master variable” for ecological integrity of lotic ecosystems . Hydrologic regimes are a significant contributor to habitat variation, the habitat template (or “templet”, sensu Southwood ) upon which life history strategies evolve in response to environmental filtering . Winemiller and Rose  proposed three general endpoint life history strategies for fishes based on generation time, fecundity, and juvenile survivorship–referred to as the trivariate continuum model. Equilibrium strategists are characterized by late maturity, low fecundity, and high juvenile survivorship; they are predicted to occur in stable environments. Periodic strategists are characterized by late maturity, high fecundity, and low juvenile survivorship; periodic stream fishes are predicted to occur in environments with predictable seasonal hydrology. Opportunistic strategists are characterized by early maturity, low fecundity, low juvenile survivorship; they are predicted to occur in harsh environments with unstable hydrology . Mims and Olden  validated hydrology-life history expectations for fishes across the United States, finding that the proportion of opportunistic strategists increased with flow variability, the proportion of periodic strategists increased with hydrology seasonality, and equilibrium strategists were weakly associated with hydrologic variability and predictability. Perkin et al.  tested for temporal variation in Sabine River, USA, fish assemblages as a result of dam construction and subsequent hydrologic alteration. Built upon the trilateral continuum model applied by Mims and Olden , Perkin et al.  characterized species into four life history strategy categories: equilibrium, periodic, and opportunistic, as well as intermediate for species that are not strongly associated with one of the three endpoint strategies. Perkin et al.  found that dam construction resulted in reduced hydrologic variability and predicted changes in life history trait composition of the fishes: opportunistic strategist richness decreased and intermediate strategist richness was constant. We predicted similar patterns for life history trait composition in the Ohio River.
In the present study, we predicted basin-scale, long-term directional shifts in the taxonomic, trophic, and life history characteristics of fish assemblages of the Ohio River Basin. We tested for temporal changes by taxonomic classification, trophic traits, and life history strategies for fish assemblages. Combining taxonomic analyses with trait-based analyses links ecological functions to environmental variation at assemblage-level scales [33,34]. Our predictions were that assemblage composition varied predictably and directionally with hydrologic alterations caused by dams and land use variation such that 1) the fish assemblage will vary temporally with hydrologic alterations and land use change, 2) benthic invertivores decrease and planktivores increase with time, corresponding with the prevalence of algae in Ohio River foodwebs , and 3) variation in catch by life history strategies are correlated with hydrologic alteration.
Materials and methods
Fish assemblage and taxonomic data
The Ohio River Valley Water Sanitation Commission (ORSANCO) was founded in 1948 to monitor water quality and curb pollution throughout the Ohio River Basin (ORB). ORSANCO personnel surveyed the Ohio River and its tributaries via biological and chemical assessments. Biological assessments include July to October lockchamber rotenone surveys from 1957–2005 (www.orsanco.org). Rotenone is a natural chemical that kills fish by block cellular uptake of oxygen and has been used extensively in fisheries management . These surveys allow for analysis in long-term assemblage shifts for fish communities in the ORB . Rotenone collections (377 surveys, 59 locations) were in lockchambers at dams located near the Mississippi River confluence (river km 10) upstream to lock #53 (Fig 1, river km 1,549.8), and are described in detail by Thomas et al. . Boat electrofishing surveys (1864 surveys, 1362 locations) at 0.5 km reaches were conducted from 1990–2014 at river locations that differed from rotenone lockchamber collections. Our preliminary analyses of overlapping years of rotenone and electrofishing collections resulted in different assemblage structure (unpubl. results), thus we analyzed rotenone and electrofishing collections separately. In order to explore temporal patterns of variation in fish assemblages at the basin-scale, we aggregated data into annual CPUE counts for each taxon. CPUE units are number of individuals per lock survey or number of individuals per 0.5 km river distance electrofished. Several taxonomic groups were identified only to genus or family in the ORSANCO database (details in Thomas et al. ) and were not included in analyses (S1 Appendix).
We used land use information for the Ohio River watershed  that included 1957–2014 at a resolution of 0.5° x 0.5°. Land use was summarized by year and tested for correlation with year and for prediction of fish assemblages in ordinations (below). Impoundments were initially constructed over 100 years ago and have been frequently modified since . We used daily discharge data from a downstream USGS site, at Louisville, OH (station number 03294500; referred to here as “Louisville”) and an upstream USGS site at Sewickley, PA (station number 03086000; referred to here as “Sewickley”) to analyze variation using the Indicators of Hydrologic Alteration (IHA) software . We selected the default IHA parameters to identify altered variables, and for a single time period (same time period as fish data). Altered hydrology variables were defined by significant regressions with time (alpha = 0.05). We used a principal components analysis (PCA) to summarize dominant gradients of hydrologic variability as altered hydrology variables for each river location. We retained principal components (PC) with the largest eigenvalues from a scree plot and included in constrained ordinations with CPUE counts of fishes by taxonomy, trophic traits, and life history strategies. We tested PC axes from IHA for serial autocorrelation with time with a Durbin-Watson statistic followed by examination of autocorrelation function plots .
Life history and trophic traits
Fishes were classified into the life history strategies defined by Winemiller and Rose  using the database originally published by Mims et al.  and recently modified to include updated traits data, including trophic information (Julian D. Olden, unpublished data). We calculated Euclidean distance in trivariate life history space from each species location to each of three life history strategy endpoints (opportunistic, periodic, equilibrium) and an intermediate strategy when species did not fit an endpoint (defined as strategy weights < 0.60), following Perkin et al. . Euclidean distances were normalized between 0 and 1, and the inverse resulted in a “strategy weight” for each of the three life history gradients. We classified trophic traits (Julian D. Olden, unpublished data; ), which included adult feeding mode based on published diet analyses and we assigned each species to a trophic category (herbivore-detritivore, invertivore, invertivore-piscivore, omnivore, and piscivore).
Analyses of basin-wide taxonomic, trophic, and life history composition through time
We used log (x + 1) transformed correlation analyses to examine species richness variation by year for CPUE counts by taxonomic, trophic, and life history categories. Additionally, we used a series of multivariate ordinations to explore taxonomic, trophic, and life history composition of fishes throughout the Ohio River Basin. Rare species (< 5 occurrences) were removed, and data were transformed by log (x + 1) or arcsine (percentage data). We used nonmetric multidimensional scaling (NMDS) with Bray-Curtis distance measure to explore directional shifts in the fish assemblage classified by taxonomy, trophic traits and life history strategy. We also used redundancy analysis (RDA), a constrained ordination, to test for relationships for hydrology and land use variables with taxonomic, trophic, and life history composition of fish assemblages. RDA and NMDS analysis were performed in Canoco 5 , and NMDS ordination plots were created in R (R Development Core Team 2011). We used the forward selection of variables for a regression model option in Canoco, that uses a Monte Carlo permutation test for significance (alpha = 0.05). We tested species richness and ordination axes (that were correlated with year) for serial autocorrelation with time with a Durbin-Watson statistic followed by examination of autocorrelation function plots . If strong autocorrelation was identified we used linear regressions and specified an autoregressive moving average (ARIMA) correlation structure in the model in Minitab 18 (Minitab, Inc).
Long-term freshwater fish assemblages and environmental variation in the Ohio River Basin ORSANCO rotenone collections included a total of 89 species (2,389,722 individuals). Boat electrofishing collections included a total of 90 species (651,956 individuals). The complete combined dataset included 135 species (not including hybrids) across 19 families. Annual species richness of the combined dataset, excluding rare taxa (< 5 occurrences total), varied from 31 to 90 and increased with year. The Durbin-Watson statistic for species richness indicated positive autocorrelation, and the moving average regression model explained high variation in species richness (R2 = 0.50), indicating increased species richness with year. Similar patterns were present for rotenone or electrofishing collections with year. The species with the 10 highest rank counts in the combined dataset were Gizzard Shad (Dorosoma cepedianum), Emerald Shiner (Notropis atherinoides), Freshwater Drum (Aplodinotus grunniens), Channel Shiner (Notropis wickliffi), Channel Catfish (Ictalurus punctatus), Threadfin Shad (Dorosoma petenense), Skipjack Herring (Alosa chrysochloris), Common Carp, Bluegill (Lepomis macrochirus), and White Bass (Morone chrysops). The trophic trait categories with the highest percent counts were herbivore-detritivores (0.34), invertivores (0.19), invertivore-piscivores (0.33), omnivores (0.36), and piscivores (0.09). Life history classifications resulted in 79 opportunistic, 11 equilibrium, 4 periodic, and 41 intermediate species (S1 Appendix).
Land use changes during the 1957–2014 period resulted in increased forest land use with year (r = 0.98, p < 0.001) and decreased agriculture land use. The IHA for Louisville resulted in significant temporal trends in hydrology for 10 variables that were in four of the five statistics groups defined in IHA software (Table 1). All hydrology variables except fall rate increased during the period. The IHA for Sewickley resulted in significant hydrologic alterations for 10 variables that were in four of the five statistics IHA groups (Table 1). All hydrology variables except 7-day maximum increased. A PCA of Sewickley IHA variables resulted in four PC axes with the first axis correlated with 1-day to 90-day maximum discharge, the second axis correlated with 7-day maximum and reversals, the third axis correlated with December discharge and reversals, and the fourth axis was correlated with December discharge and reversals (Table 2). A PCA of Louisville IHA variables resulted in four PC axes with the first axis correlated with 1-day to 30-day discharge, rise rate, and fall rate, the second axis correlated with November and December discharge, base flow, and high pulse number, the third axis correlated with September, November, and October discharge and base flow, and the fourth axis correlated with September and December discharge (Table 2). None of the IHA PC axes resulted in strong Durbin-Watson D statistics, indicating a lack of strong temporal autocorrelation.
Fish assemblage composition and environmental correlates through time: 1957–2005 rotenone surveys
No single trophic category or life history strategy count was correlated with year, however ordinations did provide evidence of temporal trends. The NMDS analysis using taxonomic counts resulted in a final stress of 0.09 and two axes that explained 83% of variation (Fig 2A). The second NMDS axis was significantly correlated with year (r = 0.64, p < 0.001, Fig 2B), resulting in a directional trajectory. The Durbin-Watson statistic for taxonomic counts indicated no autocorrelation was present. The NMDS analysis of trophic counts resulted in a final stress of 0.07 and two axes that explained 88% of variation (Fig 2A). The second NMDS axis was significantly correlated with year (r = - 0.41, p = 0.02, Fig 2B), resulting in a directional trajectory. The Durbin-Watson statistic for trophic counts indicated no autocorrelation was present. The NMDS analysis using life history strategies resulted in a final stress of 0.07 and two axes that explained 87% of variation (Fig 2A). Neither life history strategy NMDS axis was significantly correlated with year. The RDA analyses of taxonomic, trophic and life history composition of assemblages did not result in significant ordinations with hydrology and land use variables.
Nonmetric multidimensional scaling ordination of rotenone (left panels) and electrofishing collections (right panels): taxonomic counts (top), trophic counts (middle), and life history strategist counts (bottom). Final stress values for rotenone collection analyses were 0.09, 0.09, and 0.07 from top to bottom. Final stress values for electrofishing collection analyses were 0.06, 0.05, and 0.01 from top to bottom. Lines connecting years represent temporal trajectories. Highest loading variables are listed on axes.
Fish assemblage composition and environmental correlates through time: 1990–2014 electrofishing surveys
Trophic categories that increased in count through time included herbivore-detritivores (r = 0.58, p = 0.003), invertivores (r = 0.45, p = 0.03), invertivore-piscivores (r = 0.51, p = 0.01), and omnivores (r = 0.47, p = 0.02) (Fig 3). No other trophic trait counts or life history strategies were significantly related to year. NMDS analyses revealed temporal directional trajectories for taxonomic and trophic composition, but not life history composition of assemblages. NMDS analysis of taxonomic composition of assemblages through time resulted in two axes that explained 89% variation (final stress = 0.06; Fig 2C). The Durbin-Watson statistic for taxonomic counts indicated positive autocorrelation, and the moving average regression model explained high variation in taxonomic counts (R2 = 0.79), indicating significant patterns with year. The first NMDS axis was significantly correlated with year (r = 0.89, p < 0.001; Fig 2D). NMDS analysis of trophic composition of assemblages through time resulted in two axes that explained 86% of variation (final stress = 0.05; Fig 2C). The first NMDS axis was significantly correlated with year (r = - 0.89, p < 0.001; Fig 2D). The Durbin-Watson statistic for trophic composition indicated no autocorrelation was present. Finally, NMDS analysis of life history composition of assemblages through time explained 98% of variation (final stress = 0.01; Fig 2C). Neither NMDS axis was significantly correlated with year.
Redundancy analysis of taxonomic composition of assemblages resulted in two significant axes that explained 29% of variation (all canonical axes were significant, p = 0.004). Forest land use was significantly correlated with the first RDA axis, and fishes with higher counts in later years were River Carpsucker (Carpiodes carpio), Silver Carp, and Spotfin Shiner (Cyprinella spiloptera) (Fig 4A). Fishes with higher counts in earlier years with decreased forest land use were Goldfish, Channel Darter (Percina copelandi), and Slenderhead Darter (Percina phoxocephala) (Fig 4A). The second RDA axis was significantly correlated with two hydrology PC axes: the first PC axis from the Louisville IHA represented increased minimum discharge, decreased fall rate and increased rise rate (Table 2). Fishes with higher counts in these years were Bighead Carp, Mississippi Silvery Minnow (Hybognathus nuchalis), and Spotted Gar (Lepisosteus oculatus) (Fig 4A). Fishes in lower counts during these years were Smallmouth Bass, Spotted Bass, and Bluegill (Fig 4A).
Redundancy analysis using taxonomic counts from electrofishing collections, with significant environmental vectors on bottom (A, B). Axes explained 22.4% and 6.4% of variation. PC axes represent altered hydrology variables (loadings are in Table 2). Species or trophic traits with highest loadings on axes are listed. Redundancy analysis using trophic counts from electrofishing collections, with significant environmental vectors on bottom (C, D). Axes explained 25.6% and 13.2% of variation. PC axes represent altered hydrology variables. Species or trophic traits with highest loadings are listed on axes.
Redundancy analysis of trophic composition of fish assemblages resulted in two significant axes that explained 38.8% of variation (all canonical axes were significant, p = 0.03). Forest land use was significantly and negatively correlated with the first RDA axis in recent years (Fig 4D). Trophic categories with higher counts in these years were herbivore-detritivores. Piscivores and herbivore-detritivores had lower counts during these years. The second RDA axis was strongly correlated with hydrology PC axes. The first PC axis, positively correlated with the second RDA axis, captured increased minimum discharge from both gages (Fig 4D, Table 2). The second PC axis, negatively correlated with the second RDA axis, captured years with increased fall discharge, decreased base flows, and increased number of high pulse events from the Louisville gage (Fig 4D, Table 2). The second RDA axis was also positively correlated with increased counts of herbivore-detritivores and negatively correlated with counts of piscivores (Fig 4D). The RDA of life history composition did not result in a significant ordination.
At the scale of the complete Ohio River mainstem, we found directional shifts in taxonomic and trophic composition of freshwater fish assemblages over multiple decades. Our findings may stem from basin-wide changes over the temporal duration of our study, including water quality improvements following the Clean Water Act, which can influence freshwater assemblages, food webs, and the environmental selection pressures that influence them. Additionally, the inability to detect a change in life history composition of freshwater assemblages at a basin scale may reflect the importance of local scale in considering hydrologic alteration and its effects on freshwater fish assemblages. Our results differed for rotenone and electrofishing data, likely because the rotenone collections were at fewer sites and were not made in all years. In addition, biases in each of these collection methods likely differ among taxa and habitats based upon responses to boat electrofishing or presence in lockchambers.
Temporal trends of taxonomic composition of fish assemblages in the Ohio River Basin We found increases in species richness and counts over the duration of this study throughout the Ohio River Basin. Thomas et al.  utilized an index of well-being (MIWB) on this same dataset and reported an increase in count of sensitive taxa and biomass score for fish assemblage quality. Our results and Thomas et al.  provide evidence that management of watersheds for improved water quality may influence fish assemblages and can be detected at a basin scale. Similar patterns were found for the Illinois River fish assemblage responses to land use and hydrologic alteration, where recovery appeared to result after the Clean Water Act .
The commercial fish catch yield from the Illinois River declined drastically following construction of navigation dams and locks in the 1930s, compared to historic catches, likely from combined effects of agriculture and hydrologic alteration . Commercial fishing has also likely affected the composition of freshwater fish assemblages in the Ohio River Basin over the course of the study. Paddlefish (Polyodon spathula), Silver Carp, Bighead Carp, Flathead Catfish (Pylodictis olivaris), Channel Catfish, and Blue Catfish (Ictalurus furcatus) are current Ohio River commercial fisheries [43,44], and commercial fishing likely had an effect on fish assemblages in the past 50 years. Commercial fishing records are sparse due to lack of reporting, and detailed analysis of commercial fishing effects are difficult. Paddlefish accounted for 85% of the 2008 commercial harvest of Ohio River fishes in Indiana and were the most valuable fishery due to egg harvest . In the Indiana section of the Ohio River in 2000, approximately 16,000 kg of catfish were harvested commercially, but by 2014 harvest decreased to approximately 4,500 kg. Size limits for these catfish allowed sexually immature fish to be collected after 2000. Reduced counts of omnivores (including catfish), detected in this study, likely contributed to the reductions in commercial catch rates for catfish.
Environmental correlates of changes to trophic composition of fish assemblages
We found increased piscivore count (electrofishing collections) associated with increased lentic conditions that occurred after lock and dam construction , and we hypothesize that increased phytoplankton productivity may be the mechanism (although planktivore count did not increase). Enhanced phytoplankton productivity can result in bottom-up effects, with increased count of consumers  and piscivores . We assume that decreased turbidity occurred with decreasing agricultural land use in the Ohio River Basin over the study period may also have indirect effects on piscivores that capture prey using vision. This is in contrast to invertivores such as some catfish that rely on tactile or taste perception and thrive in turbid habitats .
Bowes  found a 10-year increase in carbon from terrestrial plants (C3) in tissues of invertivore and piscivore fishes in 1960, that coincided with increased forest land use. Phytoplankton contributions to fish tissue covaried less predictably with terrestrial C3 during these time periods . We suggest increased forest land use in the watershed during this period resulted in increased secondary food sources, partial restoration of natural hydrology, and decreased turbidity. Sediment storage upstream of dams and invasive Dreissena spp. bivalve molluscs may contribute additionally to decreased turbidity . These turbidity modifications could result in an increased ability of prey to avoid visual predators, facilitating niche development and reduced feeding specialization of consumers. Following an increase in turbidity during early settlement of the Ohio River Basin associated with forest cutting and wetland drainage, turbidity has decreased in the second half of the 21st century, likely due to the conversion of agriculture to forested lands .
Altered hydrology variables representing minimum mean discharge and rise and fall rates were correlated with fish composition. These axes were also correlated with decreased counts of piscivores and planktivores, and increased counts of herbivore-detritivores. Increased discharge variability can have negative effects on fishes through life cycle disruption, altered assemblages, and loss of sensitive species . We do not find an obvious mechanistic explanation for these correlations.
Studies at smaller scales (e.g., the Wabash River) offer a comparison to trophic composition of freshwater fish assemblages and environmental attributes of the Ohio River Basin reported here. Anthropogenic influences on the Wabash River and its watershed include hydrologic alterations, land use, historical industrial wastes , and the Asian carp invasion in the 1990s . Pyron et al.  suggested that changes in Wabash River watershed agriculture nutrient management and Asian carp invasion were contributors to observed fish assemblage variation. These changes include decreased planktivore/detritivores and omnivores, and increased benthic invertivores . The Ohio River watershed has undergone similar agricultural land use modifications, but some differences from the Wabash River remain (e.g., the dominant land use changed from rowcrop agriculture to forest). Intensive rowcrop agricultural land use can influence abundances of generalist fishes (i.e., invertivores) that do not require specialized habitats and prey through nutrient and hydrologic modifications. This may explain trends in trophic composition in the Ohio River basin during this study, including omnivore and invertivore-piscivore dominance during the entire time period.
In addition to changes in trophic composition of fish assemblages found in this study, intraspecific changes may also be occurring that are not detectable at the resolution of static, species-specific trait data. Delong and Thoms  identified major changes in carbon sources, and increased variation in mean nitrogen stable isotope ratios of fishes, following flow modification of the Ohio River in 1950–1955. Bowes  found decreased trophic position of Ohio River fishes over the past century. Piscivores may switch from traditional planktivore prey (Gizzard Shad) to larval fish, zooplankton, or benthic invertebrates following decreased turbidity; this provides a potential explanation for recent decreased trophic level in piscivores. Bowes  showed that Ohio River fish species were more closely packed in isotopic niche space after dams were installed. Contributions of algae to fish tissue carbon increased with dam construction, and the contribution of terrestrial carbon sources decreased. The mean trophic position of Ohio River fishes also decreased following dam construction. Bowes  interpreted the causes as a reduction in the relative amount of shallow areas where light can reach the benthos, and thus a reduction in benthic algal productivity. This likely caused a shift from benthic to phytoplankton production, decreased secondary productivity of benthic invertebrates, and decreased trophic position of invertivore and piscivore fishes.
Primary flow alterations of the Ohio River are from dams constructed to enable lockchamber use for barges, resulting in modification of the channel from flowing to lentic conditions . Over the period of the study, we detected signals of increased variability in discharge, decreased seasonality, and generally less stable discharge regimes. We thus expected increased opportunistic and intermediate strategists and decreased equilibrium strategists with decreased stability in discharge regimes in the Ohio River. Yet, we did not detect changes in counts of life-history strategies through time at the scale of the Ohio River Basin. Fish assemblage variation in the Ohio River and other rivers likely have different patterns at different locations, and at different spatial scales . Indeed, changes in hydrology differed to some degree between the two gages. In this case, our study design relating data from two stream gages to assemblage data throughout the basin revealed trends in taxonomic and trophic composition through time, but it may not reveal the scale at which flow regimes filter for life history strategies. Furthermore, changes in trophic composition through time have stronger hypothesized linkages to land use and other basin-wide changes than hydrology, which may have stronger mechanistic links to taxonomy and life history. Previous studies supporting relationships between life history strategies and flow regimes have linked assemblages with stream flow data at more local scales (e.g., within stream reaches) rather than across an entire basin (e.g., ). At large spatial scales, the ability of hydrology alone to explain life history composition in fish assemblages is likely limited .
We found detectable, directional changes through time in taxonomic and trophic composition of freshwater fish assemblages throughout the Ohio River Basin. Furthermore, we found evidence of relationships between environmental attributes (land use, hydrology) and taxonomic and trophic composition of assemblages. Yet, we did not find detectable temporal changes in life history composition of assemblages at a basin scale. Future land use modifications, climate change, and altered biotic interactions could continue to contribute to complex and directional patterns of change in freshwater fish assemblages in the Ohio River. Continued efforts to incorporate spatial and temporal scales will help reveal patterns of fish assemblage composition and its environmental correlates across scales, from basins to reaches.
S1 Appendix. Life history classifications based on Mims and Olden  and Perkin et al. .
Strategy weights are log-transformed and classified into opportunistic (Opp), periodic (Per), and equilibrium (Equ), and hard classification (Class) includes intermediate classifications.
We are grateful to ORSANCO for data access and Jeff Thomas for his assistance in this manuscript. Julian Olden provided helpful contributions and comments in early versions of this manuscript. Keith Gido suggested the serial autocorrelation analysis. The manuscript was improved with suggestions from Jay Stauffer, Sally Thompson, and an anonymous reviewer. We have no conflicts of interest as no funding was used for this research.
- 1. Craig LS, Olden JD, Arthington AH, Entrekin S, Hawkins CP, Kelly JJ, et al. Meeting the challenge of interacting threats in freshwater ecosystems: a call to scientists and managers. Elementa Science of the Anthropocene 2017; 5:72. http://doi.org/10.1525/elementa.256
- 2. Poff LN. Beyond the natural flow regime? Broadening the hydro-ecological foundation to meet environmental flows challenges in a non-stationary world. Freshwater Biology 2018; 63:1011–1021.
- 3. Olden JD, Poff NL, Bestgen KR. Life-history strategies predict fish invasions and extirpations in the Colorado River Basin. Ecological Monographs 2006; 76:25–40.
- 4. Perkin JS, Knorp NE, Boersig TC, Gebhard AE, Hix LA, Johnson TC. Life history theory predicts long-term fish assemblage response to stream impoundment. Canadian Journal of Fisheries and Aquatic Sciences 2017; 74:228–239.
- 5. Lammert M, Allan JD. Assessing biotic integrity of streams: effects of scale in measuring the influence of land use/cover and habitat structure on fish and macroinvertebrates. Environmental Management 1999; 23:257–270. pmid:9852191
- 6. Zimmerman JK, Vondracek B, Westra J. Agricultural land use effects on sediment loading and fish assemblages in two Minnesota (USA) watersheds. Environmental Management 2003; 32:93–105. pmid:14703915
- 7. Allan JD. Landscapes and riverscapes: the influence of land use on stream ecosystems. Annual Reviews in Ecology, Evolution and Systematics 2004; 35:257–284.
- 8. Foley JA, DeFries R, Asner GP, Barford C, Bonan G, Carpenter SR, et al. Global consequences of land use. Science 2005; 309:570–574. pmid:16040698
- 9. Harding JS, Benfield EF, Bolstad PV, Helfman GS, Jones EBD. Stream biodiversity: the ghost of land use past. Proceedings of the National Academy of Sciences 1998; 95:14843–14847.
- 10. Tayyebi A, Pijanowski BC, Pekin BK. Land use legacies of the Ohio River Basin: Using a spatially explicit land use change model to assess past and future impacts on aquatic resources. Applied Geography 2015; 57:100–111.
- 11. Thomas JA, Emery EB, McCormick FH. Detection of temporal trends in Ohio River fish assemblages based on lock chamber surveys (1957–2001). American Fisheries Society Symposium 2005; 45:431–450.
- 12. Angradi TR, Bolgrien DW, Jicha TM, Pearson MS, Taylor DL, Moffett MF., et al. An assessment of stressor extent and biological condition in the North American mid-continent great rivers (USA). River Systems 2011; 19:143–163.
- 13. Grossman GD, Ratajcak RE Jr, Crawford M, Freeman MC. Assemblage organization in stream fishes: effects of environmental variation and interspecific interactions. Ecological Monographs 1998l 68:395–420.
- 14. Matthews WJ, Marsh-Matthews E. Dynamics of an upland stream fish community over 40 years: trajectories and support for the loose equilibrium concept. Ecology 2016; 97:706–719. pmid:27197397
- 15. Pyron M, Lauer TE, Gammon JR. Stability of the Wabash River fish assemblages from 1974 to 1998. Freshwater Biology 2006; 51:1789–1797.
- 16. Beugly J, Pyron M. Temporal and spatial variation in the long-term functional organization of fish assemblages in a large river. Hydrobiologia 2010; 654:215–226.
- 17. Gido KB, Probst DL, Olden JD, Bestgen KR. Multidecadal responses of native and introduced fishes to natural and altered flow regimes in the American Southwest. Canadian Journal of Fisheries and Aquatic Sciences 2013; 70:554–564.
- 18. Scheffer M, Carpenter SR. Catastrophic regime shifts in ecosystems: linking theory to observation. Trends in Ecology and Evolution 2003; 18:648–656.
- 19. DeAngelis DL, Mulholland PJ, Palumbo AV, Steinman AD, Huston MA, Elwood JW. Nutrient dynamics and food-web stability. Annual Reviews in Ecology and Systematics 1989; 20:71–95.
- 20. DeLong MD, Thoms MC. Changes in the trophic status of fish feeding guilds in response to flow modification. Journal of Geophysical Research: Biogeosciences 2016; 121:949–964.
- 21. Thorp JH, Bowes RE. Carbon sources in riverine food webs: new evidence from amino acid isotope techniques. Ecosystems 2017; 20:1029–1041.
- 22. Thorp JH, Thoms MC, DeLong MD. The riverine ecosystem synthesis: biocomplexity in river networks across space and time. River Research and Applications 2006; 22:123–147.
- 23. Bowes RE. Temporal Analysis of River Food Webs. Lawrence: University of Kansas, 2016, Dissertation.
- 24. Vander Zanden MJ, Chandra S, Allen BC, Reuter JE, Goldman CR. Historical food web structure and restoration of native aquatic communities in the Lake Tahoe (California-Nevada) basin. Ecosystems 2003; 6:274–288.
- 25. Poff LN, Allan JD. Functional organization of stream fish assemblages in relation to hydrological variability. Ecology 1995; 76:606–627.
- 26. Jackson DA, Peres-Neto PR, Olden JD. What controls who is where in freshwater fish communities: the roles of biotic, abiotic and spatial factors? Canadian Journal of Fisheries and Aquatic Science 2001; 58:157–170.
- 27. Mims MC, Olden JD. Life history theory predicts fish assemblage response to hydrologic regimes. Ecology 2012; 93:35–45. pmid:22486085
- 28. Poff LN, Allan JD, Bain MB, Karr JR, Prestegaard KL, Richter BD, et al. The natural flow regime. Bioscience 1997; 47:769–784.
- 29. Southwood TRE. Habitat, the templet for ecological strategies? Journal of Animal Ecology 1977; 46:337–365.
- 30. Lytle DA, Poff NL. Adaptation to natural flow regimes. Trends in Ecology and Evolution 2004; 19:94–100. pmid:16701235
- 31. Winemiller KO, Rose KA. Patterns of life history diversification in North American fishes: implication for population regulation. Canadian Journal of Fisheries and Aquatic Sciences 1992; 49:2196–2218.
- 32. Winemiller KO. Life history strategies, population regulation and implications for fisheries management. Canadian Journal of Fisheries and Aquatic Sciences 2005; 62:872–885.
- 33. Poff LN. Landscape filters and species traits: towards mechanistic understanding and prediction in stream ecology. Freshwater Science 1997; 16:391–409.
- 34. Pyron M, Williams L, Beugly J, Jacquemin SJ. The role of trait-based approaches in understanding stream fish assemblages. Freshwater Biology 2011; 56:1579–1592.
- 35. Robertson DR, Smith-Vaniz WF. Rotenone: an essential but demonized tool for assessing marine fish diversity. Bioscience 2008; 58:165–170.
- 36. Meiyappan P, Jain AK. Three distinct global estimates of historical land-cover change and land-use conversions for over 200 years. Frontiers in Earth Science 2012; 6:122–139.
- 37. Richter BD, Baumgartner JV, Powell J, Braun DP. A method for assessing hydrologic alteration within ecosystems. Conservation Biology 1996; 10:1163–1174.
- 38. Gido KB, Propst DL. Long-term dynamics of native and nonnative fishes in the San Juan River, New Mexico and Utah, under a partially managed flow regime. Transactions of the American Fisheries Society; 141:645–659.
- 39. Mims MC, Olden JD, Shattuck ZR, Poff NL. Life history trait diversity of native freshwater fishes in North America. Ecology of Freshwater Fish 2010; 19:390–400.
- 40. Giam X, Olden JD. Environment and predation govern fish community assembly in temperate streams. Global Ecology and Biogeography 2016; 19:390–400.
- 41. ter Braak CJF, Šmilauer P. Canoco reference manual and user’s guide: software for ordination, version 5.0. Ithaca, New York: Microcomputer Power, 2012.
- 42. Gibson-Reinemer DK, Sparks RE, Parker JL, DeBoer JA, Fritts MW, McClelland MA, et al. Ecological recovery of a river fish assemblage following the implementation of the clean water act. Bioscience 2017; 67:957–970.
- 43. Sindt T. 2012 Ohio River Angler Survey, Hebron, Ohio: Report for Ohio Department of Natural Resources, 2012.
- 44. Indiana Natural Resources Commission (NRC). Economic Impact Statement LSA Document #14–510. Indiana Register, 2017.
- 45. Stefanavage T. Summary of Reported Harvest and License Sales for Indiana’s Ohio River Commercial Fisheries, 2007. Indianapolis, Indiana: Indiana Department of Natural Resources Report, 2009.
- 46. Power ME. Top-down and bottom-up forces in food webs: do plants have primacy? Ecology 1992; 73:733–746.
- 47. Barbiero RP, Lesht BM, Warren GJ. Evidence for bottom-up control of recent shifts in the pelagic food web of Lake Huron. Journal of Great Lakes Research 2011; 37:78–85.
- 48. Gerking SD. Feeding Ecology of Fish. San Diego: Academic Press, 2014.
- 49. Thorp JH, Delong MD, Casper AF. In situ experiments on predatory regulation of a bivalve mollusc (Dreissena polymorpha) in the Mississippi and Ohio Rivers. Freshwater Biology 1998; 39:649–661.
- 50. Poff LN, Zimmerman JKH. Ecological responses to altered flow regimes: a literature review to inform the science and management of environmental flows. Freshwater Biology 2010; 55:194–205.
- 51. Gammon JR.The Wabash River Ecosystem, Bloomington, Indiana: Indiana University Press, 1998.
- 52. Pyron M, Becker JC, Broadway KJ, Etchison L, Minder M, DeColibus D, et al. Are long-term fish assemblage changes in a large US river related to the Asian carp invasion? Test of the hostile take-over and opportunistic dispersal hypotheses. Aquatic Sciences 2017; 79:631–642.
- 53. Broadway KJ, Pyron M, Gammon JR, Murry BA. Shift in a large river fish assemblage: body-size and trophic structure dynamics. PLoS One 2015; 10: pmid:25902144
- 54. Fausch KD, Torgersen CE, Baxter CV, Li HW. Landscapes to riverscapes: bridging the gap between research and conservation of stream fishes: a continuous view of the river is needed to understand how processes interacting among scales set the context for stream fishes and their habitat. Bioscience 2002; 52:483–498.
- 55. McManamay RA, Frimpong EA. Hydrologic filtering of fish life history traits across the US and implications for streamflow alterations. Ecological Applications 2015; 25:243–263. pmid:26255371