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.

Toxicity of herbicides to cyanobacteria and phytoplankton species of the San Francisco Estuary and Sacramento-San Joaquin River Delta, California, USA.

The herbicides glyphosate, imazamox and fluridone are herbicides, with low toxicity towards fish and invertebrates, which are applied to waterways to control invasive aquatic weeds. However, the effects of these herbicides on natural isolates of phytoplankton and cyanobacteria are unknown. Three species of microalgae found in the San Francisco Estuary (SFE)/Sacramento-San Joaquin River Delta (Delta) (Microcystis aeruginosa, Chlamydomonas debaryana, and Thalassiosira pseudonana) were exposed to the three herbicides at a range of concentrations in 96-well plates for 5-8 days. All three algal species were the most sensitive to fluridone, with IC50 of 46.9, 21, and 109 µg L-1 for M. aeruginosa, T. pseudonana and C. debaryana, respectively. Imazamox inhibited M. aeruginosa and T. pseudonana growth at 3.6 × 104 µg L-1 or higher, and inhibited C. debaryana growth at 1.0 × 105 µg L-1 or higher. Glyphosate inhibited growth in all species at ca. 7.0 × 104 µg L-1 or higher. Fluridone was the only herbicide that inhibited the microalgae at environmentally relevant concentrations in this study and susceptibility to the herbicide depended on the species. Thus, the application of fluridone may affect cyanobacteria and phytoplankton community composition in water bodies where it is applied.

Covariance of Phytoplankton, Bacteria, and Zooplankton Communities Within Microcystis Blooms in San Francisco Estuary.

Microcystis blooms have occurred in upper San Francisco Estuary (USFE) since 1999, but their potential impacts on plankton communities have not been fully quantified. Five years of field data collected from stations across the freshwater reaches of the estuary were used to identify the plankton communities that covaried with Microcystis blooms, including non-photosynthetic bacteria, cyanobacteria, phytoplankton, zooplankton, and benthic genera using a suite of analyses, including microscopy, quantitative PCR (qPCR), and shotgun metagenomic analysis. Coherence between the abundance of Microcystis and members of the plankton community was determined by hierarchal cluster analysis (CLUSTER) and type 3 similarity profile analysis (SIMPROF), as well as correlation analysis. Microcystis abundance varied with many cyanobacteria and phytoplankton genera and was most closely correlated with the non-toxic cyanobacterium Merismopoedia, the green algae Monoraphidium and Chlamydomonas, and the potentially toxic cyanobacteria Pseudoanabaena, Dolichospermum, Planktothrix, Sphaerospermopsis, and Aphanizomenon. Among non-photosynthetic bacteria, the xenobiotic bacterium Phenylobacterium was the most closely correlated with Microcystis abundance. The coherence of DNA sequences for phyla across trophic levels in the plankton community also demonstrated the decrease in large zooplankton and increase in small zooplankton during blooms. The breadth of correlations between Microcystis and plankton across trophic levels suggests Microcystis influences ecosystem production through bottom-up control during blooms. Importantly, the abundance of Microcystis and other members of the plankton community varied with wet and dry conditions, indicating climate was a significant driver of trophic structure during blooms.

Determining the Exposure Pathway and Impacts of Microcystis on Threadfin Shad, Dorosoma petenense, in San Francisco Estuary.

Blooms of the cyanobacterium Microcystis spp. could affect fish health through the ingestion of colonies as well as exposure to dissolved microcystins in the water column. The goal of the present study was to evaluate the dietary exposure pathway through which Microcystis spp. blooms may affect liver function and nutritional status using a novel approach involving multiple analytical methods to assess the potential risk. Our study was conducted using threadfin shad, Dorosoma petenense, which is a pelagic fish commonly exposed to Microcystis spp. blooms in the upper San Francisco Estuary. The approach incorporated published and optimized methods that offer multiple lines of evidence including in situ hybridization, immunohistochemistry, histopathology, condition factor indices, and nutritional profiles. Measurements of threadfin shad health and tissue condition were conducted at sites where Microcystis was present or absent during the 2007 bloom season. The results showed that dietary exposure to fish from Microcystis blooms resulted in the accumulation of microcystin in the gut and liver tissues of threadfin shad collected from the sites with blooms. Although toxicity endpoints were likely confounded by antecedent conditions, our findings demonstrate dietary exposure of Microcystis toxins to fish using a novel approach with multiple lines of evidence. Environ Toxicol Chem 2020;39:787-798. © 2020 The Authors. Environmental Toxicology and Chemistry published by Wiley Periodicals, Inc. on behalf of SETAC.

Evaluation of water quality during successive severe drought years within Microcystis blooms using fish embryo toxicity tests for the San Francisco Estuary, California.

In the San Francisco Estuary, California, the largest estuary on the Pacific Coast of North America, the frequency and intensity of drought and associated cyanobacteria blooms are predicted to increase with climate change. To assess the impact of water quality conditions on estuarine fish health during successive severe drought years with Microcystis blooms, we performed fish embryo toxicity testing with Delta Smelt and Medaka. Fish embryos were exposed to filtered ambient water collected from the San Francisco Estuary during the Microcystis bloom season in 2014 and 2015, the third and fourth most severe recorded drought years in California. Medaka embryos incubated in filtered ambient waters exhibited high mortality rates (>77%), which was mainly due to bacterial growth. Medaka mortality data was negatively correlated with chloride, and positively correlated with water temperature, total and dissolved organic carbon, and ambient and net chlorophyll a concentration. Delta Smelt embryo mortality rates were lower (<42%) and no prominent seasonal or geographic trend was observed. There was no significant correlation between the Delta Smelt mortality data and water quality parameters. Aeromonas was the dominant bacteria that adversely affected Medaka. The growth of Aeromonas was suppressed when salinity was greater than or equal to 1psu and resulted in a significant reduction in mortality rate. Bacterial growth test demonstrated that the lysate of Microcystis cells enhanced the growth of Aeromonas. Toxin production by Microcystis is a major environmental concern, however, we conclude that dissolved substances released from Microcystis blooms could result in water quality deterioration by promoting growth of bacteria. Furthermore, a distinctive developmental deformity was observed in Medaka during the toxicity tests; somite formation was inhibited at the same time that cardiogenesis occurred and the functional heart was observed to be beating. The exact cause of the embryonic developmental deformity is still unknown.

Biodiversity of cyanobacteria and other aquatic microorganisms across a freshwater to brackish water gradient determined by shotgun metagenomic sequencing analysis in the San Francisco Estuary, USA.

Blooms of Microcystis and other harmful cyanobacteria can degrade water quality by producing cyanotoxins or other toxic compounds. The goals of this study were (1) to facilitate understanding of community structure for various aquatic microorganisms in brackish water and freshwater regions with emphasis on cyanobacteria, and (2) to test a hypothesis that Microcystis genotypes that tolerate higher salinity were blooming in brackish water environments during the severe drought, 2014. Shotgun metagenomic analysis revealed that cyanobacteria dominated the brackish water region while bacteria dominated the freshwater region. A group of cyanobacteria (e.g., Aphanizomenon, Microcystis, Planktothrix, Pseudanabaena), bacteria (e.g., Bacillus, Porphyrobacter), and diatoms (Phaeodactylum and Thalassiosira) were abundant in the brackish water region. In contrast, Hassallia (cyanobacteria) and green algae (Nannochloropsis, Chlamydomonas, and Volvox) were abundant in the landward freshwater region. Station variation was also apparent. One landward sampling station located downstream of an urbanized area differed substantially from the other stations in terms of both water chemistry and community structure, with a higher percentage of arthropods, green algae, and eukaryotes. Screening of the Microcystis internal transcribed spacer region revealed six representative genotypes, and two of which were successfully quantified using qPCR (Genotypes I and VI). Both genotypes occurred predominantly in the freshwater region, so the data from this study did not support the hypothesis that salinity tolerant Microcystis genotypes bloomed in the brackish water region in 2014.

Tidal day organic and inorganic material flux of ponds in the Liberty Island freshwater tidal wetland.

The loss of inorganic and organic material export and habitat produced by freshwater tidal wetlands is hypothesized to be an important contributing factor to the long-term decline in fishery production in San Francisco Estuary. However, due to the absence of freshwater tidal wetlands in the estuary, there is little information on the export of inorganic and organic carbon, nutrient or phytoplankton community biomass and the associated mechanisms. A single-day study was conducted to assess the potential contribution of two small vegetated ponds and one large open-water pond to the inorganic and organic material flux within the freshwater tidal wetland Liberty Island in San Francisco Estuary. The study consisted of an intensive tidal day (25.5 h) sampling program that measured the flux of inorganic and organic material at three ponds using continuous monitoring of flow, chlorophyll a, turbidity and salt combined with discrete measurements of phytoplankton community carbon, total and dissolved organic carbon and nutrient concentration at 1.5 h intervals. Vegetated ponds had greater material concentrations than the open water pond and, despite their small area, contributed up to 81% of the organic and 61% of the inorganic material flux of the wetland. Exchange between ponds was important to wetland flux. The small vegetated pond in the interior of the wetland contributed as much as 72-87% of the total organic carbon and chlorophyll a and 10% of the diatom flux of the wetland. Export of inorganic and organic material from the small vegetated ponds was facilitated by small-scale topography and tidal asymmetry that produced a 40% greater material export on ebb tide. The small vegetated ponds contrasted with the large open water pond, which imported 29-96% of the inorganic and 4-81% of the organic material into the wetland from the adjacent river. This study identified small vegetated ponds as an important source of inorganic and organic material to the wetland and the importance of small scale physical processes within ponds to material flux of the wetland.

Sublethal dietary effects of Microcystis on Sacramento splittail, Pogonichthys macrolepidotus.

The presence of the toxic cyanobacterium Microcystis in the upper San Francisco Estuary (SFE) since 1999 is a potential but to date an unquantified threat to the health and survival of aquatic organisms, such as fish and zooplankton. The microcystins (MCs) predominantly in the LR-form (MC-LR) contained in Microcystis is hepatotoxic and a potential threat to the fishery. This study was conducted to determine the effects of dietary exposure of the endemic Sacramento splittail, Pogonichthys macrolepidotus in SFE to Microcystis and its toxin, MC-LR. Juvenile splittail (12.59 ± 0.7 g fish(-1)) were exposed to five diets for 28 d with MC-LR obtained from: (1) Microcystis harvested from the SFE and (2) a synthetic purified form of MC-LR. Three of the test diets contained 3.55 (D5), 9.14 (D10) and 17.13 (D20)mg MC-LR kg(-1) from Microcystis. The other two diets contained either purified MC-LR at 3.89 mg MC-LR kg(-1) (D5R) or no MC-LR (D0). The RNA/DNA ratio of fish muscle was significantly lower for all treatments fed test diets containing MC-LR compared to the control diet D0, suggesting Microcystis adversely affected nutritional status. Protein phosphatase 2A expression in the fish from the D5, D10 and D20 treatments were inversely affected by increasing concentrations of MC-LR. Cytoplasmic inclusion bodies and single cell necrosis were more prevalent and greater in severity in the fish exposed to the diets D10 and D20 compared to fish from the D0 treatment and indicate severe liver toxicity in splittail exposed to MC-LR. The sublethal effects on splittail characterized by this study suggest cyanobacterial blooms have the potential to affect splittail nutritional status and health in SFE.

Toxic threshold of dietary microcystin (-LR) for quart medaka.

This study was designed to estimate the toxic threshold of male and female fish to microcystins based on different biomarkers. Japanese medaka (Oryzias latipes) were fed dietary Microcystin-LR (0, 0.46, 0.85, 2.01 and 3.93 microg MC-LR/g dry diet for 8 weeks at 25 degrees C. The results revealed that dietary MC-LR inhibited growth at the end of 8 weeks. The survival of embryos and the RNA/DNA ratio of whole fish decreased significantly (P < 0.05) in fish fed 3.93 microg MC-LR/g dry diet. Heat shock protein (Hsp60) expression was induced in the liver of female and male fish fed diets containing > or =0.85 and 0.46 microg MC-LR/g diet, respectively. The activity of liver caspase 3/7 was significantly higher in female fish fed 3.93 microg MC-LR/g diet and in males fed 2.01 MC-LR microg/g dry diet than fish fed the control diet. The threshold for inhibition of liver protein phosphatase expression was lower in female (2.01 microg/g diet) than that in male fish (3.93 microg/g diet). Histopathological examination showed significant single-cell necrosis in female and male medaka fed diets containing 0.85 and 3.93 microg MC-LR/g diet, respectively. Based on different biomarkers, this study demonstrated that dietary MC-LR is toxic to Medaka and the effects are gender dependent.