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USGS2016

Isotopic incorporation and the effects of fasting and dietary lipid content on isotopic discrimination in large carnivorous mammals

There has been considerable emphasis on understanding isotopic discrimination for diet estimation in omnivores. However, discrimination may differ for carnivores, particularly species that consume lipid-rich diets. Here, we examined the potential implications of several factors when using stable isotopes to estimate the diets of bears, which can consume lipid-rich diets and, alternatively, fast for weeks to months. We conducted feeding trials with captive brown bears ( Ursus arctos ) and polar bears ( Ursus maritimus ). As dietary lipid content increased to ∼90%, we observed increasing differences between blood plasma and diets that had not been lipid extracted (∆ 13 C tissue-bulk diet ) and slightly decreasing differences between plasma δ 13 C and lipid-extracted diet. Plasma Δ 15 N tissue-bulk diet increased with increasing protein content for the four polar bears in this study and data for other mammals from previous studies that were fed purely carnivorous diets. Four adult and four yearling brown bears that fasted 120 d had plasma δ 15 N values that changed by <±2‰. Fasting bears exhibited no trend in plasma δ 13 C. Isotopic incorporation in red blood cells and whole blood was ≥6 mo in subadult and adult bears, which is considerably longer than previously measured in younger and smaller black bears ( Ursus americanus ). Our results suggest that short-term fasting in carnivores has minimal effects on δ 13 C and δ 15 N discrimination between predators and their prey but that dietary lipid content is an important factor directly affecting δ 13 C discrimination and indirectly affecting δ 15 N discrimination via the inverse relationship with dietary protein content.

Physiological and Biochemical Zoology↗

USGS2018

Evaluating indices of lipid and protein content in lesser snow and Ross's geese during spring migration

Assessing nutrient stores in avian species is important for understanding the extent to which body condition influences success or failure in life‐history events. We evaluated predictive models using morphometric characteristics to estimate total body lipids (TBL) and total body protein (TBP), based on traditional proximate analyses, in spring migrating lesser snow geese ( Anser caerulescens caerulescens ) and Ross's geese ( A. rossii ). We also compared performance of our lipid model with a previously derived predictive equation for TBL developed for nesting lesser snow geese. We used external and internal measurements on 612 lesser snow and 125 Ross's geese collected during spring migration in 2015 and 2016 within the Central and Mississippi flyways to derive and evaluate predictive models. Using a validation data set, our best performing lipid model for snow geese better predicted TBL (root mean square error [RMSE] of 23.56) compared with a model derived from nesting individuals (RMSE = 48.60), suggesting the importance of season‐specific models for accurate lipid estimation. Models that included body mass and abdominal fat deposit best predicted TBL determined by proximate analysis in both species (lesser snow goose, R 2 = 0.87, RMSE = 23.56: Ross's geese, R 2 = 0.89, RMSE = 13.75). Models incorporating a combination of external structural measurements in addition to internal muscle and body mass best predicted protein values ( R 2 = 0.85, RMSE = 19.39 and R 2 = 0.85, RMSE = 7.65, lesser snow and Ross's geese, respectively), but protein models including only body mass and body size were also competitive and provided extended utility to our equations for field applications. Therefore, our models indicated the importance of specimen dissection and measurement of the abdominal fat pad to provide the most accurate lipid estimates and provide alternative dissection‐free methods for estimating protein.

Arkansas, Missouri, Nebraska, South Dakota↗

USGS1996

Lipid and water depletion in migrating passerines following passage over the Gulf of Mexico

Lipid depletion is currently believed to be the primary factor limiting flight duration of migrating birds in North America, while the influence of water loss is thought to be small. Three migrating species of passerines, wood thrush ( Hylocichla mustelina ), Swainson's thrush ( Catharus ustulatus ), and summer tanager ( Piranga rubra ) were captured during the 1993 spring migration just after crossing the Gulf of Mexico and examined for lipid and water depletion. The redwinged blackbird ( Agelaius phoeniceus ), a winter resident, was examined for comparison. Although some migrants had low levels of fat, most were not seriously fat-depleted and had much higher lipid levels than red-winged blackbirds. Migrants appeared dehydrated, usually having less than 60% body water and significantly less water than the blackbirds. Recaptured wood thrushes had significantly higher mass than when initially captured. Many of these birds were replenishing significant amounts of water, while the acquisition of lipid mass was dependent on the amount of time the birds spent on the study site. Migrants were significantly fatter but had significantly less water mass when captured during unfavorable weather than under favorable conditions. It appears that both dehydration and lipid depletion are major physiological constraints on migrating passerines.

Louisiana↗

USGS2021

Effect of temperature, nitrate concentration, pH and bicarbonate addition on biomass and lipid accumulation in the sporulating green alga PW95

The mixed effects of temperature (20 °C, 25 °C and 30 °C), nitrate concentration (0.5 mM and 2.0 mM), pH buffer, and bicarbonate addition (trigger) on biomass growth and lipid accumulation were investigated in the environmental alga PW95 during batch experiments in standardized growth medium. PW95 was isolated from coal-bed methane production water and classified as a Chlamydomonas -like species by morphological characterization and phylogenetic analysis (18S, ITS, rbc L). A factorial experimental design tested the mixed effects on PW95 before and after nitrate depletion to determine a low cost, high efficiency combination of treatments for biomass growth and lipid accumulation. Results showed buffer addition affected growth for most of the treatments and bicarbonate trigger had no statistically significant effect on growth and lipid accumulation. PW95 displayed the highest growth rate and chlorophyll content at 30 °C and 2.0 mM nitrate and there was an inverse relation between biomass accumulation and lipid accumulation at the extremes of nitrate concentration and temperature. The combination of higher temperature (30 °C) and lower nitrate level (0.5 mM) without the use of a buffer or bicarbonate addition resulted in maximal daily biomass accumulation (5.30 × 10 6 cells/mL), high biofuel potential before and after nitrate depletion (27% and 20%), higher biofuel productivity (16 and 15 mg/L/d, respectively), and desirable fatty acid profiles (saturated and unsaturated C16 and C18 chains). Our results indicate an important interaction between low nitrate levels, temperature, and elevated pH for trade-offs between biomass and lipid production in PW95. This work serves as a model to approach and advance the study of physiological responses of novel microalgae to diverse culture conditions that mimic environmental changes for outdoor biofuel production. The most promising conditions for growth and biofuel production were identified for PW95 and this approach can be implemented for other microalgal production systems.

Algal Research↗

USGS2004

The influence of diet, consumption and lipid use on recruitment of white bass

The abundance of white bass ( Morone chrysops ) in Lake Erie has declined in recent years, sparking interest in mechanisms influencing its recruitment. We evaluate two mechanisms affecting recruitment: diet and the potential for competition, and storage of lipid energy reserves and the relationship to overwinter survival. The fish in our study were characteristic of white bass in the northern portion of their range, feeding predominantly on zooplankton. Only the largest age-0 white bass ate fish as a significant portion of their diet. Over the summer sampling period, we found decreasing ration sizes, expressed as a percentage of maximum ration, as the summer progressed with a concomitant decrease in the relative amount of lipid storage. In laboratory experiments, age-0 white bass held at 5°C and given food ad libitum did feed, but at rates that were insufficient to maintain body weight. Loss in weight was accompanied with a loss in lipids at a rate of 2.8 mg of lipids per gram of body weight per day. Based on our data, we concluded that age-0 white bass in Lake Erie were food-limited. Food limitation resulted in reduced growth rates, presumably related to competition with other planktivorous fishes. Reduced growth results in increased mortality and, ultimately, low recruitment through increased risk of predation by larger piscivorous fishes, reduced ability for white bass to switch to more energetically profitable piscivory and the increased likelihood of higher overwinter mortality because of reduced lipid stores.

Michigan, New York, Ohio, Pennsylvania↗

USGS2009

Lipid reserves of Lesser Scaup ( Aythya affinis ) migrating across a large landscape are consistent with the "Spring Condition" hypothesis

The “spring condition” hypothesis (SCH) states that nutrition during spring migration affects survival, reproductive success, and, ultimately, population size of migratory birds. The North American population of Lesser Scaup ( Aythya affinis ) has experienced a marked decline, apparently because of poor recruitment. An important prediction of the SCH is that female Lesser Scaup have low lipid reserves during spring migration. We previously reported that lipid reserves and body mass of females collected on migratory stopover areas in northwestern Minnesota in springs 2000–2001 were lower than those on the same areas in the 1980s and markedly lower than those collected at Pool 19 of the Mississippi River in 2000–2001, an important preceding stopover area. However, it was unclear whether these findings represented a site-specific result or a landscape-scale phenomenon. Accordingly, we examined lipid and body mass of 641 female Lesser Scaup migrating across seven eco-physiographic regions of Iowa, Minnesota, and North Dakota during springs 2003–2005. We found that lipids and body mass of females throughout the Upper Midwest were similar to or less than the low values documented in northwestern Minnesota in springs 2000–2001 and markedly lower than those of females at Pool 19 in springs 2000–2001. Accordingly, our results are consistent with a prediction of the SCH, because lipid and body mass of females are low throughout this large landscape, lower than at an important preceding stopover area, and lower than all historical values. Finally, our results suggest the potential for cross-seasonal influences of nutrition on recruitment and that a stronger management focus on spring migration habitats may be necessary for conservation and recovery of declining migratory birds, especially Lesser Scaup.

The Auk↗

USGS1981

Body lipids and pesticide burdens of migrant blue-winged teal

Blue-winged Teal were collected before and after their migration to wintering grounds in Latin America. Pesticide burdens, body weights, and lipid levels of carcasses were determined. Only DDE and dieldrin were detected in a small proportion of the samples and then at concentrations far below known-effect levels. Residue loads, because of their infrequency, were not significantly correlated with overall body weight and percent lipid. Body weights among most age and sex classes did not differ in either fall or spring, nor did percent lipid in any instance. However, body weights and lipid levels were significantly correlated; as body weight increased so did percent lipid. Thus, the extreme variability in body weight appears to be a function of the amount of fat present and not overall body size, age, or sex.

Journal of Field Ornithology↗

USGS1990

Effects of dietary a-linolenic acid on n-3 fatty acids of rainbow trout lipids

The effects of α-linolenic acid enriched diets on the lipid composition of rainbow trout ( Oncorhynchus mykiss ) muscle and liver were determined. Diets containing 0, 4, 10 or 20% (wt/wt) linseed oil were fed to 280 trout for up to 64 days. Linolenic acid levels in total lipid, neutral lipid and phospholipid of liver and muscle increased with duration of intake. The linolenic acid content of total lipid in muscle increased from 10 mg to 355 mg/100 g flesh. There was no significant increase in the elongated desaturated products, i.e., eicosapentaenoic or docosahexaenoic acids, in either tissue during the feeding period.

Lipids↗

USGS2021

Lipidomics reveals specific lipid molecules associated with cold stress syndrome in the Florida manatee (Trichechus manatus latirostris)

Cold stress syndrome (CSS) in the Florida manatee ( Trichechus manatus latirostris) results in perturbations to many physiological pathways, often leading to further illness or death. In this study, we applied a non-targeted lipidomics approach with ultra-high performance liquid chromatography and high-resolution tandem mass spectrometry to characterize changes related to CSS in the lipidomic profiles of manatee plasma. Lipidomic analyses were conducted on healthy manatee (control) and cold-exposed manatee plasma samples with varying concentrations of Serum Amyloid A (SAA), an acute-phase protein that is associated with inflammatory disease. Control manatees ( n = 10) were compared to all manatees exposed to cold temperatures ( n = 17), and a subset of those manatees with SAA values > 120 μg/mL ( n = 9). Increased SAA values were associated with higher levels of various acylcarnitine lipids, while several triacylglycerols and oxidized triacylglycerols were significantly lower in manatees with cold exposure. These identified lipids are critical molecules involved in the maintenance of energy homeostasis and could potentially be examined in conjunction with current physical parameters to characterize cold stress. The ability to detect such differences highlights the addition of lipidomics as a valuable tool in understanding cold stress and potentially other illnesses in manatees. Further investigation into the function of the altered lipids could greatly increase our understanding of lipid metabolism in physiologically stressed manatees as well as other marine mammals and inform future management recovery strategies.

Marine Biology↗

USGS2024

Perfluorohexanesulfonic acid (PFHxS) impairs lipid homeostasis in zebrafish larvae through activation of PPARα

Perfluorohexanesulfonic acid (PFHxS), an emerging short-chain per- and polyfluoroalkyl substance, has been frequently detected in aquatic environments. Adverse outcome pathway studies have shown that perfluorinated compounds impair lipid homeostasis through peroxisome proliferator activated receptors (PPARs). However, many of these studies were performed at high concentrations and may thus be a result of overt toxicity. To better characterize the molecular and key events of PFHxS to biota, early life-stage zebrafish ( Danio rerio ) were exposed to concentrations detected in the environment (0.01, 0.1, 1, and 10 μg/L). Lipidomic and transcriptomic evaluations were integrated to predict potential molecular targets. PFHxS significantly impaired lipid homeostasis by the dysregulation of glycerophospholipids, fatty acyls, glycerolipids, sphingolipids, prenol lipids, and sterol lipids. Informatic analyses of the lipidome and transcriptome indicated alterations of the PPAR signaling pathway, with downstream changes to retinol, linoleic acid, and glycerophospholipid metabolism. To assess the role of PPARs, potential binding of PFHxS to PPARs was predicted and animals were coexposed to a PPAR antagonist (GW6471). Molecular simulation indicated PFHxS had a 27.1% better binding affinity than oleic acid, an endogenous agonist of PPARα. Antagonist coexposures rescued impaired glycerophosphocholine concentrations altered by PFHxS. These data indicate PPARα activation may be an important molecular initiating event for PFHxS.

Environmental Science & Technology↗

USGS2011

Mercury distribution and lipid oxidation in fish muscle: Effects of washing and isoelectric protein precipitation

Nearly all the mercury (Hg) in whole muscle from whitefish ( Coregonus clupeaformis ) and walleye ( Sander vitreus ) was present as methyl mercury (MeHg). The Hg content in whole muscle from whitefish and walleye was 0.04–0.09 and 0.14–0.81 ppm, respectively. The myofibril fraction contained approximately three-fourths of the Hg in whitefish and walleye whole muscle. The sarcoplasmic protein fraction (e.g., press juice) was the next most abundant source of Hg. Isolated myosin, triacylglycerols, and cellular membranes contained the least Hg. Protein isolates prepared by pH shifting in the presence of citric acid did not decrease Hg levels. Addition of cysteine during washing decreased the Hg content in washed muscle probably through the interaction of the sulfhydryl group in cysteine with MeHg. Primary and secondary lipid oxidation products were lower during 2 °C storage in isolates prepared by pH shifting compared to those of washed or unwashed mince from whole muscle. This was attributed to removing some of the cellular membranes by pH shifting. Washing the mince accelerated lipid peroxide formation but decreased secondary lipid oxidation products compared to that of the unwashed mince. This suggested that there was a lipid hydroperoxide generating system that was active upon dilution of aqueous antioxidants and pro-oxidants.

Journal of Agricultural and Food Chemistry↗

USGS2023

Lipid metabolites index habitat quality for Canvasbacks on stopover areas during spring migration

Nutrients acquired by ducks on spring migratory stopover areas influence survival and subsequent reproduction. Accordingly, wetland loss and degradation on stopover areas can lead to reduced refueling efficiency and have demographic consequences. Lipid metabolite concentrations in blood provide a useful index of daily mass change in wild birds and can be used to make inferences about quality of stopover areas for refueling. We experimentally validated a model that uses lipid metabolites to predict daily mass change, and then we used those predictions to make inferences about foraging habitat quality for Canvasbacks ( Aythya valisineria ) at important stopover sites of the upper Mississippi and Illinois Rivers, USA. We measured plasma lipid metabolites and daily mass change of 60 wild Canvasbacks held in short-term captivity and subjected to feeding and fasting treatments. Respectively, triglyceride and β-hydroxybutyrate concentrations were positively and negatively related to mass change ( R 2 = 0.58). On average, Canvasbacks collected experimentally across our study area had positive index values indicating sufficient forage resources to allow energy acquisition. However, predicted daily mass increases were greater at more northerly pools of the Mississippi River (Pools 7–8 and 13) compared to more southerly locations (Pool 19 of the Mississippi River and the Illinois River Valley), which was likely due, in part, to more abundant submerged aquatic vegetation at more northerly pools. Our results affirm that lipid metabolites are useful predictors of daily mass change that in turn can provide inferences about habitat quality. Lower daily mass increases of Canvasbacks at Pool 19 are concerning because that area is considered a critically important spring stopover area for migratory diving ducks. Considering the challenges of managing large rivers for multiple uses, targeting restoration of wetlands isolated or isolatable from river systems could provide stopover areas with necessary forage for optimal mass gain.

Illinois, Wisconsin↗

USGS2014

An assessment of morphometric indices, blood chemistry variables and an energy meter as indicators of the whole body lipid content in Micropterus dolomieu , Sander vitreus and Ictalurus punctatus

The effectiveness of several non-lethal techniques as indicators of total lipid content in smallmouth bass Micropterus dolomieu , walleye Sander vitreus and channel catfish Ictalurus punctatus was investigated. The techniques included (1) the Fulton and relative condition factors, (2) relative mass, (3) plasma indicators of nutritional status (alkaline phosphatase, calcium, cholesterol, protein, triglycerides and glucose) and (4) readings from a hand-held, microwave energy meter. Although simple linear regression analysis showed that lipid content was significantly correlated with several predictor variables in each species, the r 2 values for the relations ranged from 0·17 to 0·50 and no single approach was consistent for all species. Only one model, between energy-meter readings and lipid content in I. punctatus , had an r 2 value (0·83) high enough to justify using it as a predictive tool. Results indicate that no single variable was an accurate and reliable indicator of whole body lipid content in these fishes, except the energy meter for I. punctatus .

Journal of Fish Biology↗

USGS2011

Identification of marine-derived lipids in juvenile coho salmon and aquatic insects through fatty acid analysis

The energetic benefits enjoyed by consumers in streams with salmon runs depend on how those benefits are accrued. Adult Pacific salmon Oncorhynchus spp. deliver significant amounts of nutrients (i.e., nitrogen and phosphorus) and carbon to streams when they spawn and die; these nutrient additions can have demonstrable effects on primary production in streams. Consumption of carcass tissues or eggs provides for direct energy subsidies to consumers and may have significant effects on their condition. In this study, comparisons of juvenile coho salmon O. kisutch and aquatic insects exposed to terrestrial and marine energy sources demonstrated that direct consumption of marine-derived lipids had a significant effect on the lipid reserves of consumers. Direct consumption of marine-derived tissues was verified through fatty acid analysis. Selected aquatic insects and juvenile coho salmon were reared for 6 weeks in experimental streams supplied with terrestrial or marine energy sources. Chironomid midges, nemourid stoneflies, and juvenile coho salmon exposed to the marine energy source altered their fatty acid compositions by incorporating the long-chain polyunsaturated fatty acids that are characteristic of marine fish. The fatty acid composition of baetid mayflies was unaffected. The direct movement of specific fatty markers indicated that direct consumption of marine-derived tissues led to increased energy reserves (triacylglycerols) in consumers. Similar results were obtained for juvenile coho salmon sampled from natural streams before and after the arrival of adult salmon runs. These data indicate that marine-derived lipids from anadromous fish runs are an important source of reserve lipids for consumers that overwinter in streams.

Transactions of the American Fisheries Society↗

USGS2006

Association of polychlorinated biphenyls (PCBs) with live algae and total lipids in rivers - A field-based approach

The association of PCBs and live algal cells in rivers was studied at four locations during four seasons in two Wisconsin rivers. Positive relations between particle-associated PCBs and both chlorophyll-a and algal carbon concentrations indicated that live algal cells were a significant sorption phase for dissolved PCBs. Large Pennate diatoms (Navicula, Synedra, Pinnularia, Diatoma, and Cocconeis), or more rarely, Euglenoids (Trachelomonas sp.), dominated most sample assemblages on an algal carbon basis. These assemblages made up the highest percentage of total SOC during spring (average=50%) and lowest during summer (average=15%). At the three impounded sites, most individual PCB congeners were relatively enriched in samples characterized by: (1) high concentrations of algal carbon (as a percent of SOC), (2) algal assemblages dominated (or co-dominated) by Euglenoids, and (3) high concentrations of total lipids. Despite relatively higher masses of sorbed PCBs in the most lipid-rich samples, there was no robust correlation between total lipid content and particle-associated PCBs when aggregating all samples from the study. A possible explanation is that PCBs are associated with other structural components in live algae and (or) departure from chemical equilibrium in the river due to algal growth kinetics. A kinetic uptake model was used to calculate the mass of PCBs associated with the total organic carbon content of live algae. Based on this model, PCBs were enriched in algal cells during bloom seasons (spring and fall) compared to non-bloom seasons (summer and winter). Further, although individual PCB congener partition coefficients (log) to live algal cells (range=5.3-6.4) overlapped to those for detritus (range=3.6-7.4), PCBs tended to be enriched in detrital carbon pools during non-bloom conditions. The larger range of estimated PCB partition coefficients for detritus likely reflects the more heterogeneous nature of this material compared to live algal cells.

Science of the Total Environment↗

USGS2002

Partition coefficients of organic compounds in lipid-water systems and correlations with fish bioconcentration factors

Triolein-water partition coefficients (KtW) have been determined for 38 slightly water-soluble organic compounds, and their magnitudes have been compared with the corresponding octanol-water partition coefficients (KOW). In the absence of major solvent-solute interaction effects in the organic solvent phase, the conventional treatment (based on Raoult's law) predicts sharply lower partition coefficients for most of the solutes in triolein because of its considerably higher molecular weight, whereas the Flory-Huggins treatment predicts higher partition coefficients with triolein. The data are in much better agreement with the Flory-Huggins model. As expected from the similarity in the partition coefficients, the water solubility (which was previously found to be the major determinant of the KOW) is also the major determinant for the Ktw. When the published BCF values (bioconcentration factors) of organic compounds in fish are based on the lipid content rather than on total mass, they are approximately equal to the Ktw, which suggests at least near equilibrium for solute partitioning between water and fish lipid. The close correlation between Ktw and Kow suggests that Kow is also a good predictor for lipid-water partition coefficients and bioconcentration factors.

Environmental Science & Technology↗

USGS2014

Lipid and moisture content modeling of amphidromous Dolly Varden using bioelectrical impedance analysis

The physiological well-being or condition of fish is most commonly estimated from aspects of individual morphology. However, these metrics may be only weakly correlated with nutritional reserves stored as lipid, the primary form of accumulated energy in fish. We constructed and evaluated bioelectrical impedance analysis (BIA) models as an alternative method of assessing condition in amphidromous Dolly Varden Salvelinus malma collected from nearshore estuarine and lotic habitats of the Alaskan Arctic. Data on electrical resistance and reactance were collected from the lateral and ventral surfaces of 192 fish, and whole-body percent lipid and moisture content were determined using standard laboratory methods. Significant inverse relationships between temperature and resistance and reactance prompted the standardization of these data to a constant temperature using corrective equations developed herein. No significant differences in resistance or reactance were detected among spawning and nonspawning females after accounting for covariates, suggesting that electrical pathways do not intersect the gonads. Best-fit BIA models incorporating electrical variables calculated from the lateral and ventral surfaces produced the strongest associations between observed and model-predicted estimates of proximate content. These models explained between 6% and 20% more of the variability in laboratory-derived estimates of proximate content than models developed from single-surface BIA data and 32% more than models containing only length and weight data. While additional research is required to address the potential effects of methodological variation, bioelectrical impedance analysis shows promise as a way to provide high-quality, minimally invasive estimates of Dolly Varden lipid or moisture content in the field with only small increases in handling time.

Alaska↗

USGS2022

Factors affecting interannual variation in diet and body lipid content of age-0 Scaphirhynchus sturgeon in the lower Missouri River, USA

The ability of young fish to find and consume food during early life history is an important factor affecting survival and recruitment. While dietary assessments for age-0 Scaphirhynchus sturgeon (shovelnose sturgeon and pallid sturgeon) in the Missouri River, USA have received increased attention over the last 15 years, there is currently limited information available to evaluate long-term trends in prey consumption and body condition. To better understand interannual factors during early-life history, we examined foraging and body condition of age-0 (<12.0 cm) Scaphirhynchus in relation to discharge and the availability of hypothesized foraging and food-producing habitats at a single reach (Lexington) of the Missouri River over a span of five years (2014–2018). Relatively high discharge in 2015 led to concomitant maxima in foraging and lipid levels for age-0 sturgeon. However, lower water levels in 2014 did not see declines in lipid content as would be expected given the low level of foraging observed that year. Additionally, the availability of hypothesized foraging and food-producing habitats had little effect on age-0 sturgeon prey consumption and condition in the Lexington Reach. Our results suggest that other factors in addition to river discharge may affect age-0 sturgeon foraging and condition and more research focused on understanding the flow-habitat relationships would be critical.

Missouri↗