Evaluating top-down, bottom-up, and environmental drivers of pelagic food web dynamics along an estuarine gradient.

Identification of the key biotic and abiotic drivers within food webs is important for understanding species abundance changes in ecosystems, particularly across ecotones where there may be strong variation in interaction strengths. Using structural equation models (SEMs) and four decades of integrated data from the San Francisco Estuary, we investigated the relative effects of top-down, bottom-up, and environmental drivers on multiple trophic levels of the pelagic food web along an estuarine salinity gradient and at both annual and monthly temporal resolutions. We found that interactions varied across the estuarine gradient and that the detectability of different interactions depended on timescale. For example, for zooplankton and estuarine fishes, bottom-up effects appeared to be stronger in the freshwater upstream regions, while top-down effects were stronger in the brackish downstream regions. Some relationships (e.g., bottom-up effects of phytoplankton on zooplankton) were seen primarily at annual timescales, whereas others (e.g., temperature effects) were only observed at monthly timescales. We also found that the net effect of environmental drivers was similar to or greater than bottom-up and top-down effects for all food web components. These findings can help identify which trophic levels or environmental factors could be targeted by management actions to have the greatest impact on estuarine forage fishes and the spatial and temporal scale at which responses might be observed. More broadly, this study highlights how environmental gradients can structure community interactions and how long-term data sets can be leveraged to generate insights across multiple scales.

Evaluating environmental DNA detection of a rare fish in turbid water using field and experimental approaches.

Detection sensitivity of aquatic species using environmental DNA (eDNA) generally decreases in turbid water but is poorly characterized. In this study, eDNA detection targeted delta smelt (Hypomesus transpacificus), a critically endangered estuarine fish associated with turbid water. eDNA sampling in the field was first paired with a trawl survey. Species-specific detection using a Taqman qPCR assay showed concordance between the methods, but a weak eDNA signal. Informed by the results of field sampling, an experiment was designed to assess how turbidity and filtration methods influence detection of a rare target. Water from non-turbid (5 NTU) and turbid (50 NTU) estuarine sites was spiked with small volumes (0.5 and 1 mL) of water from a delta smelt tank to generate low eDNA concentrations. Samples were filtered using four filter types: cartridge filters (pore size 0.45 µm) and 47 mm filters (glass fiber, pore size 1.6 µm and polycarbonate, pore sizes 5 and 10 µm). Prefiltration was also tested as an addition to the filtration protocol for turbid water samples. eDNA copy numbers were analyzed using a censored data method for qPCR data. The assay limits and lack of PCR inhibition indicated an optimized assay. Glass fiber filters yielded the highest detection rates and eDNA copies in non-turbid and turbid water. Prefiltration improved detection in turbid water only when used with cartridge and polycarbonate filters. Statistical analysis identified turbidity as a significant effect on detection probability and eDNA copies detected; filter type and an interaction between filter type and prefilter were significant effects on eDNA copies detected, suggesting that particulate-filter interactions can affect detection sensitivity. Pilot experiments and transparent criteria for positive detection could improve eDNA surveys of rare species in turbid environments.

Striped bass (Morone saxatilis) migration timing driven by estuary outflow and sea surface temperature in the San Francisco Bay-Delta, California.

The influence of climate on the timing of large-scale animal migrations is a major ecological and resource management concern. Anadromous fish migrations can have broad scale impacts on human communities and marine, aquatic and terrestrial food webs. However, isolating the effects of climate change on the timing of life stage transitions for anadromous fish species is challenging. Striped bass (Morone saxatilis) exhibit striking variation in migration patterns within their natural range, including migratory behaviors that change with latitude, and climate-induced temperature changes are predicted to drive future habitat and distribution changes. Here we explore the linkages between migration and multiple components of coastal and inland aquatic ecosystems impacted by climate change. By leveraging environmental and fisheries monitoring which began in 1969, we describe the upstream migration timing of non-native adult Striped bass influenced by estuary outflow and sea surface temperature in the San Francisco Bay-Delta, California. Striped bass migrated later in years when Delta outflow was greater and sea surface temperature was cooler. It is likely that temperature thresholds in the ocean during the springtime provide a cue for Striped bass to initiate migration, but sea surface temperature may also represent composite climatic trends influencing Striped bass. Further, the observed variation in migration timing of adult Striped bass has implications for predation risk on the seaward-migration of juvenile Chinook salmon.

Resistance and resilience of pelagic and littoral fishes to drought in the San Francisco Estuary.

Many estuarine ecosystems and the fish communities that inhabit them have undergone substantial changes in the past several decades, largely due to multiple interacting stressors that are often of anthropogenic origin. Few are more impactful than droughts, which are predicted to increase in both frequency and severity with climate change. In this study, we examined over five decades of fish monitoring data from the San Francisco Estuary, California, USA, to evaluate the resistance and resilience of fish communities to disturbance from prolonged drought events. High resistance was defined by the lack of decline in species occurrence from a wet to a subsequent drought period, while high resilience was defined by the increase in species occurrence from a drought to a subsequent wet period. We found some unifying themes connecting the multiple drought events over the 50-yr period. Pelagic fishes consistently declined during droughts (low resistance), but exhibit a considerable amount of resiliency and often rebound in the subsequent wet years. However, full recovery does not occur in all wet years following droughts, leading to permanently lower baseline numbers for some pelagic fishes over time. In contrast, littoral fishes seem to be more resistant to drought and may even increase in occurrence during dry years. Based on the consistent detrimental effects of drought on pelagic fishes within the San Francisco Estuary and the inability of these fish populations to recover in some years, we conclude that freshwater flow remains a crucial but not sufficient management tool for the conservation of estuarine biodiversity.

Inter-population differences in salinity tolerance of adult wild Sacramento splittail: osmoregulatory and metabolic responses to salinity.

The Sacramento splittail (Pogonichthys macrolepidotus) is composed of two genetically distinct populations endemic to the San Francisco Estuary (SFE). The allopatric upstream spawning habitat of the Central Valley (CV) population connects with the sympatric rearing grounds via relatively low salinity waters, whereas the San Pablo (SP) population must pass through the relatively high-salinity Upper SFE to reach its allopatric downstream spawning habitat. We hypothesize that if migration through SFE salinities to SP spawning grounds is more challenging for adult CV than SP splittail, then salinity tolerance, osmoregulatory capacity, and metabolic responses to salinity will differ between populations. Osmoregulatory disturbances, assessed by measuring plasma osmolality and ions, muscle moisture and Na+-K+-ATPase activity after 168 to 336 h at 11‰ salinity, showed evidence for a more robust osmoregulatory capacity in adult SP relative to CV splittail. While both resting and maximum metabolic rates were elevated in SP splittail in response to increased salinity, CV splittail metabolic rates were unaffected by salinity. Further, the calculated difference between resting and maximum metabolic values, aerobic scope, did not differ significantly between populations. Therefore, improved osmoregulation came at a metabolic cost for SP splittail but was not associated with negative impacts on scope for aerobic metabolism. These results suggest that SP splittail may be physiologically adjusted to allow for migration through higher-salinity waters. The trends in interpopulation variation in osmoregulatory and metabolic responses to salinity exposures support our hypothesis of greater salinity-related challenges to adult CV than SP splittail migration and are consistent with our previous findings for juvenile splittail populations, further supporting our recommendation of population-specific management.

Role of freshwater floodplain-tidal slough complex in the persistence of the endangered delta smelt.

Seasonal floodplain wetland is one of the most variable and diverse habitats found in coastal ecosystems, yet it is also one of the most highly altered by humans. The Yolo Bypass, the primary floodplain of the Sacramento River in California's Central Valley, USA, has been shown to provide various benefits to native fishes when inundated. However, the Yolo Bypass exists as a tidal dead-end slough during dry periods and its value to native fishes has been less studied in this state. During the recent drought (2012-2016), we found higher abundance of the endangered Delta Smelt (Hypomesus transpacificus), than the previous 14 years of fish monitoring within the Yolo Bypass. Meanwhile, Delta Smelt abundance elsewhere in the estuary was at record lows during this time. To determine the value of the Yolo Bypass as a nursery habitat for Delta Smelt, we compared growth, hatch dates, and diets of juvenile Delta Smelt collected within the Yolo Bypass with fish collected among other putative nursery habitats in the San Francisco Estuary between 2010 and 2016. Our results indicated that when compared to other areas of the estuary, fish in the Yolo Bypass spawned earlier, and offspring experienced both higher quality feeding conditions and growth rates. The occurrence of healthy juvenile Delta Smelt in the Yolo Bypass suggested that the region may have acted as a refuge for the species during the drought years of 2012-2016. However, our results also demonstrated that no single region provided the best rearing habitat for juvenile Delta Smelt. It will likely require a mosaic of habitats that incorporates floodplain-tidal sloughs in order to promote the resilience of this declining estuarine fish species.

A Conservation Hatchery Population of Delta Smelt Shows Evidence of Genetic Adaptation to Captivity After 9 Generations.

Genetic adaptation to captivity is a concern for threatened and endangered species held in conservation hatcheries. Here, we present evidence of genetic adaptation to captivity in a conservation hatchery for the endangered delta smelt (Fish Conservation and Culture Laboratory, University of California Davis; FCCL). The FCCL population is genetically managed with parentage analysis and the addition of wild fish each year. Molecular monitoring indicates little loss of genetic variation and low differentiation between the wild and conservation populations. Yet, we found an increase in offspring survival to reproductive maturity during the subsequent spawning season (recovery rate) in crosses that included one or both cultured parents. Crosses with higher levels of hatchery ancestry tend to produce a greater number of offspring that are recovered the following year. The recovery rate of a cross decreases when offspring are raised in a tank with fish of high levels of hatchery ancestry. We suggest changes in fish rearing practices at the FCCL to reduce genetic adaptation to captivity, as delta smelt numbers in the wild continue to decline and the use of FCCL fish for reintroduction becomes more likely.

Evidence of a Shift in the Littoral Fish Community of the Sacramento-San Joaquin Delta.

Many estuarine and freshwater ecosystems worldwide have undergone substantial changes due to multiple anthropogenic stressors. Over the past two decades, the Sacramento-San Joaquin Delta (Delta) in California, USA, saw a severe decline in pelagic fishes, a shift in zooplankton community composition, and a rapid expansion of invasive aquatic vegetation. To evaluate whether major changes have also occurred in the littoral fish community, we analyzed a beach seine survey dataset collected from 1995 to 2015 from 26 sites within the Delta. We examined changes in the Delta fish community at three different ecological scales (species, community, and biomass), using clustering analyses, trend tests, and change-point analyses. We found that the annual catch per effort for many introduced species and some native species have increased since 1995, while few experienced a decline. We also observed a steady pattern of change over time in annual fish community composition, driven primarily by a steady increase in non-native Centrarchid species. Lastly, we found that littoral fish biomass has essentially doubled over the 21-year study period, with Mississippi Silverside Menidia audens and fishes in the Centrarchidae family driving most of this increase. The changes in the catch per effort, fish community composition, and biomass per volume indicate that a shift has occurred in the Delta littoral fish community and that the same factors affecting the Delta's pelagic food web may have been a key driver of change.

Inter-population differences in salinity tolerance and osmoregulation of juvenile wild and hatchery-born Sacramento splittail.

The Sacramento splittail (Pogonichthys macrolepidotus) is a minnow endemic to the highly modified San Francisco Estuary of California, USA and its associated rivers and tributaries. This species is composed of two genetically distinct populations, which, according to field observations and otolith strontium signatures, show largely allopatric distribution patterns as recently hatched juveniles. Juvenile Central Valley splittail are found primarily in the nearly fresh waters of the Sacramento and San Joaquin rivers and their tributaries, whereas San Pablo juveniles are found in the typically higher-salinity waters (i.e. up to 10‰) of the Napa and Petaluma Rivers. As the large salinity differences between young-of-year habitats may indicate population-specific differences in salinity tolerance, we hypothesized that juvenile San Pablo and Central Valley splittail populations differ in their response to salinity. In hatchery-born and wild-caught juvenile San Pablo splittail, we found upper salinity tolerances, where mortalities occurred within 336 h of exposure to 16‰ or higher, which was higher than the upper salinity tolerance of 14‰ for wild-caught juvenile Central Valley splittail. This, in conjunction with slower recovery of plasma osmolality, but not ion levels, muscle moisture or gill Na(+),K(+)-ATPase activity, in Central Valley relative to San Pablo splittail during osmoregulatory disturbance provides some support for our hypothesis of inter-population variation in salinity tolerance and osmoregulation. The modestly improved salinity tolerance of San Pablo splittail is consistent with its use of higher-salinity habitats. Although confirmation of the putative adaptive difference through further studies is recommended, this may highlight the need for population-specific management considerations.