Governing Ecological Connectivity in Cross-Scale Dependent Systems.

Ecosystem management and governance of cross-scale dependent systems require integrating knowledge about ecological connectivity in its multiple forms and scales. Although scientists, managers, and policymakers are increasingly recognizing the importance of connectivity, governmental organizations may not be currently equipped to manage ecosystems with strong cross-boundary dependencies. Managing the different aspects of connectivity requires building social connectivity to increase the flow of information, as well as the capacity to coordinate planning, funding, and actions among both formal and informal governance bodies. We use estuaries in particular the San Francisco Estuary, in California, in the United States, as examples of cross-scale dependent systems affected by many intertwined aspects of connectivity. We describe the different types of estuarine connectivity observed in both natural and human-affected states and discuss the human dimensions of restoring beneficial physical and ecological processes. Finally, we provide recommendations for policy, practice, and research on how to restore functional connectivity to estuaries.

Improving inference for nonlinear state-space models of animal population dynamics given biased sequential life stage data.

State-space models (SSMs) are a popular tool for modeling animal abundances. Inference difficulties for simple linear SSMs are well known, particularly in relation to simultaneous estimation of process and observation variances. Several remedies to overcome estimation problems have been studied for relatively simple SSMs, but whether these challenges and proposed remedies apply for nonlinear stage-structured SSMs, an important class of ecological models, is less well understood. Here we identify improvements for inference about nonlinear stage-structured SSMs fit with biased sequential life stage data. Theoretical analyses indicate parameter identifiability requires covariates in the state processes. Simulation studies show that plugging in externally estimated observation variances, as opposed to jointly estimating them with other parameters, reduces bias and standard error of estimates. In contrast to previous results for simple linear SSMs, strong confounding between jointly estimated process and observation variance parameters was not found in the models explored here. However, when observation variance was also estimated in the motivating case study, the resulting process variance estimates were implausibly low (near-zero). As SSMs are used in increasingly complex ways, understanding when inference can be expected to be successful, and what aids it, becomes more important. Our study illustrates (a) the need for relevant process covariates and (b) the benefits of using externally estimated observation variances for inference about nonlinear stage-structured SSMs.

Monitoring Turbidity in San Francisco Estuary and Sacramento-San Joaquin Delta Using Satellite Remote Sensing.

This study utilizes satellite data to investigate water quality conditions in the San Francisco Estuary and its upstream delta, the Sacramento-San Joaquin River Delta. To do this, this study derives turbidity from the European Space Agency satellite Sentinel-2 acquired from September 2015 to June 2019 and conducts a rigorous validation with in situ measurements of turbidity from optical sensors at continuous monitoring stations. This validation includes 965 matchup comparisons between satellite and in situ sensor data across 22 stations, yielding R 2 = 0.63 and 0.75 for Nephelometric Turbidity Unit and Formazin Nephelometric Unit (FNU) stations, respectively. This study then applies remote sensing to evaluate patterns in turbidity during the Suisun Marsh Salinity Control Gates Action ("Gates action"), a pilot study designed to increase habitat access and quality for the endangered Delta Smelt. The basic strategy was to direct more freshwater into Suisun Marsh, creating more low salinity habitat that would then have higher (and more suitable) turbidity than upstream river channels. For all seven acquisitions considered from June 29 to September 27, 2018, turbidity conditions in Bays and Sloughs subregions were consistently higher (and more suitable) (26-47 FNU) than what was observed in the upstream River region (13-25 FNU). This overall pattern was observed when comparing images acquired during similar tidal stages and heights.

Estuarine fish communities respond to climate variability over both river and ocean basins.

Estuaries are dynamic environments at the land-sea interface that are strongly affected by interannual climate variability. Ocean-atmosphere processes propagate into estuaries from the sea, and atmospheric processes over land propagate into estuaries from watersheds. We examined the effects of these two separate climate-driven processes on pelagic and demersal fish community structure along the salinity gradient in the San Francisco Estuary, California, USA. A 33-year data set (1980-2012) on pelagic and demersal fishes spanning the freshwater to marine regions of the estuary suggested the existence of five estuarine salinity fish guilds: limnetic (salinity = 0-1), oligohaline (salinity = 1-12), mesohaline (salinity = 6-19), polyhaline (salinity = 19-28), and euhaline (salinity = 29-32). Climatic effects propagating from the adjacent Pacific Ocean, indexed by the North Pacific Gyre Oscillation (NPGO), affected demersal and pelagic fish community structure in the euhaline and polyhaline guilds. Climatic effects propagating over land, indexed as freshwater outflow from the watershed (OUT), affected demersal and pelagic fish community structure in the oligohaline, mesohaline, polyhaline, and euhaline guilds. The effects of OUT propagated further down the estuary salinity gradient than the effects of NPGO that propagated up the estuary salinity gradient, exemplifying the role of variable freshwater outflow as an important driver of biotic communities in river-dominated estuaries. These results illustrate how unique sources of climate variability interact to drive biotic communities and, therefore, that climate change is likely to be an important driver in shaping the future trajectory of biotic communities in estuaries and other transitional habitats.

Effects of incubation temperature on the upper thermal tolerance of the imperiled longfin smelt (Spirinchus thaleichthys).

Upper thermal limits in many fish species are limited, in part, by the heart's ability to meet increased oxygen demand during high temperatures. Cardiac plasticity induced by developmental temperatures can therefore influence thermal tolerance. Here, we determined how incubation temperatures during the embryonic stage influence cardiac performance across temperatures during the sensitive larval stage of the imperiled longfin smelt. We transposed a cardiac assay for larger fish to newly hatched larvae that were incubated at 9°C, 12°C or 15°C. We measured heart rate over increases in temperature to identify the Arrhenius breakpoint temperature (TAB), a proxy for thermal optimum and two upper thermal limit metrics: temperature when heart rate is maximized (Tpeak) and when cardiac arrhythmia occurs (TArr). Higher incubation temperatures increased TAB, Tpeak and TArr, but high individual variation in all three metrics resulted in great overlap of individuals at TAB, Tpeak and TArr across temperatures. We found that the temperatures at which 10% of individuals reached Tpeak or TArr and temperatures at which number of individuals at TAB relative to Tpeak (ΔN(TAB,Tpeak)) was maximal, correlated more closely with upper thermal limits and thermal optima inferred from previous studies, compared to the mean values of the three cardiac metrics of the present study. Higher incubation temperatures increased the 10% Tpeak and TArr thresholds but maximum ΔN(TAB,Tpeak) largely remained the same, suggesting that incubation temperatures modulate upper thermal limits but not Topt for a group of larvae. Overall, by measuring cardiac performance across temperatures, we defined upper thermal limits (10% thresholds; Tpeak, 14.4-17.5°C; TArr, 16.9-20.2°C) and optima (ΔN(TAB,Tpeak), 12.4-14.4°C) that can guide conservation strategies for longfin smelt and demonstrated the potential of this cardiac assay for informing conservation plans for the early life stages of fish.

Effects of turbidity, temperature and predation cue on the stress response of juvenile delta smelt.

The San Francisco Estuary (SFE) is one of the most degraded ecosystems in the United States, and organisms that inhabit it are exposed to a suite of environmental stressors. The delta smelt (Hypomesus transpacificus), a small semi-anadromous fish endemic to the SFE and considered an indicator species, is close to extinction in the wild. The goal of this study was to investigate how environmental alterations to the SFE, such as reductions in turbidities, higher temperatures and increased prevalence of invasive predators affect the physiology and stress response of juvenile delta smelt. Juvenile delta smelt were exposed to two temperatures (17 and 21°C) and two turbidities (1-2 and 10-11 NTU) for 2 weeks. After the first week of exposure, delta smelt were exposed to a largemouth bass (Micropterus salmoides) predator cue at the same time every day for 7 days. Fish were measured and sampled on the first (acute) and final (chronic) day of exposures to predator cues and later analyzed for whole-body cortisol, glucose, lactate, and protein. Length and mass measurements were used to calculate condition factor of fish in each treatment. Turbidity had the greatest effect on juvenile delta smelt and resulted in reduced cortisol, increased glucose and lactate, and greater condition factor. Elevated temperatures reduced available energy in delta smelt, indicated by lower glucose and total protein, whereas predator cue exposure had negligible effects on their stress response. This is the first study to show reduced cortisol in juvenile delta smelt held in turbid conditions and adds to the growing data that suggest this species performs best in moderate temperatures and turbidities. Multistressor experiments are necessary to understand the capacity of delta smelt to respond to the multivariate and dynamic changes in their natural environment, and results from this study should be considered for management-based conservation efforts.

Growth, osmoregulation and ionoregulation of longfin smelt (Spirinchus thaleichthys) yolk-sac larvae at different salinities.

Longfin smelt (Spirinchus thaleichthys) is a threatened anadromous fish species that spawns in freshwater to moderately brackish (i.e. 5-10 ppt) reaches of the upper San Francisco Estuary and has declined to ~1% of its pre-1980s abundances. Despite 50+ years of population monitoring, the efficacy of 10+ years of conservation efforts for longfin smelt remain uncertain due to a limited understanding of how the species responds to environmental variation, such as salinity. For example, high mortality during larval stages has prevented culture efforts from closing the life cycle in captivity. Here, we investigated the effects of salinity on longfin smelt yolk-sac larvae. Newly hatched larvae from four single-pair crosses were acutely transferred to and reared at salinities of 0.4, 5, 10, 20 or 32 ppt. We compared whole-body water and sodium ion (Na+) content, notochord length and yolk-sac volume at 12, 24, 48, 72, and 96 hours post-transfer for each salinity treatment. We found that larvae maintained osmotic and ionic balance at 0.4-10 ppt, whereas salinities ˃10 ppt resulted in decreased water and increased whole-body Na+ content. We also found that larvae grew largest and survived the longest when reared at 5 and 10 ppt, respectively, and that yolk resorption stalled at 0.4 ppt. Finally, there were significant but small interclutch variations in responses to different salinities, with clutch accounting for <8% of the variance in our statistical models. Overall, our results indicate that longfin smelt yolk-sac larvae likely perform best at moderately brackish conditions, thus yielding a mechanism that explains their distribution in field surveys and providing key information for future conservation efforts.

Multi-scale trend analysis of water quality using error propagation of generalized additive models.

Effective stewardship of ecosystems to sustain current ecological status or mitigate impacts requires nuanced understanding of how conditions have changed over time in response to anthropogenic pressures and natural variability. Detecting and appropriately characterizing changes requires accurate and flexible trend assessment methods that can be readily applied to environmental monitoring datasets. A key requirement is complete propagation of uncertainty through the analysis. However, this is difficult when there are mismatches between sampling frequency, period of record, and trends of interest. Here, we propose a novel application of generalized additive models (GAMs) for characterizing multi-decadal changes in water quality indicators and demonstrate its utility by analyzing a 30-year record of biweekly-to-monthly chlorophyll-a concentrations in the San Francisco Estuary. GAMs have shown promise in water quality trend analysis to separate long-term (i.e., annual or decadal) trends from seasonal variation. Our proposed methods estimate seasonal averages in a response variable with GAMs, extract uncertainty measures for the seasonal estimates, and then use the uncertainty measures with mixed-effects meta-analysis regression to quantify inter-annual trends that account for full propagation of error across methods. We first demonstrate that nearly identical descriptions of temporal changes can be obtained using different smoothing spline formulations of the original time series. We then extract seasonal averages and their standard errors for an a priori time period within each year from the GAM results. Finally, we demonstrate how across-year trends in seasonal averages can be modeled with mixed-effects meta-analysis regression that propagates uncertainties from the GAM fits to the across-year analysis. Overall, this approach leverages GAMs to smooth data with missing observations or varying sample effort across years to estimate seasonal averages and meta-analysis to estimate trends across years. Methods are provided in the wqtrends R package.

Antimicrobial Drug-Resistant Gram-Negative Saprophytic Bacteria Isolated from Ambient, Near-Shore Sediments of an Urbanized Estuary: Absence of ß-Lactamase Drug-Resistance Genes.

We assessed the prevalence of antimicrobial resistance and screened for clinically relevant ß-lactamase resistance determinants in Gram-negative bacteria from a large urbanized estuary. In contrast to the broad literature documenting potentially hazardous resistance determinants near wastewater treatment discharge points and other local sources of aquatic pollution, we employed a probabilistic survey design to examine ambient, near-shore sediments. We plated environmental samples from 40 intertidal and shallow subtidal areas around San Francisco Bay (California, USA) on drug-supplemented MacConkey agar, and we tested isolates for antimicrobial resistance and presence of clinically relevant ß-lactamase resistance determinants. Of the 74 isolates identified, the most frequently recovered taxa were Vibrio spp. (40%), Shewanella spp. (36%), Pseudomonas spp. (11%), and Aeromonas spp. (4%). Of the 55 isolates tested for antimicrobial resistance, the Vibrio spp. showed the most notable resistance profiles. Most (96%) were resistant to ampicillin, and two isolates showed multidrug-resistant phenotypes: V. alginolyticus (cefotaxime, ampicillin, gentamicin, cefoxitin) and V. fluvialis (cefotaxime, ampicillin, cefoxitin). Targeted testing for class 1 integrons and presence of ß-lactam-resistance gene variants TEM, SHV, OXA, CTX-M, and Klebsiella pneumonia carbapenemase (KPC) did not reveal any isolates harboring these resistance determinants. Thus, while drug-resistant, Gram-negative bacteria were recovered from ambient sediments, neither clinically relevant strains nor mobile ß-lactam resistance determinants were found. This suggests that Gram-negative bacteria in this well-managed, urbanized estuary are unlikely to constitute a major human exposure hazard at this time.

Demography of the salt marsh harvest mouse (Reithrodontomys raviventris halicoetes) and associated rodents in tidal and managed wetlands.

Suisun Marsh (Solano County, California) is the largest contiguous marsh remaining on the West Coast of the United States, and makes up approximately 10% of the wetlands remaining in the San Francisco Estuary. Suisun Marsh has been safeguarded from development through the operation of over 100 privately owned waterfowl hunting clubs, which manage for diked waterfowl habitat. However, this management-and the subsequent loss of tidal influence-has been considered harmful for some species, including the endangered salt marsh harvest mouse (SMHM; Reithrodontomys raviventris). To determine the value of tidal wetlands relative to those managed for waterfowl, we performed periodic surveys for rodents in managed and tidal wetlands over 5 years, and used capture-mark-recapture analyses to estimate demographic parameters and abundance for the three most common rodents-the northern SMHM (R. r. halicoetes), the western harvest mouse (a sympatric native species; R. megalotis, WHM), and the house mouse (a sympatric invasive species; Mus musculus). Wetland type had no effect on detection, temporary emigration, or survival for any of these species. However, fecundity and population growth for all three species were affected by an interaction of season and wetland type, although none of these parameters was consistently superior in either habitat type. Estimated abundance of SMHM and Mus was similar in both wetland types, whereas WHM were more abundant in managed wetlands. Salt marsh harvest mice also showed no affinity for any microhabitat characteristics associated with tidal wetlands. Managed wetlands in Suisun Marsh support SMHM and Mus equally, and abundances of WHM were greater than in tidal wetlands, suggesting managed wetlands may be superior in terms of supporting native rodents. As climate change and sea level rise are predicted to threaten coastal marshes, these results suggest the recovery strategy for SMHM could incorporate managed wetlands.

A novel and versatile flash-freezing approach for evaluating the health of Delta Smelt.

A common approach used to assess environmental impacts in aquatic environments is to measure indicators of stress (biomarkers) and condition of fish within ecosystems. Particularly in estuarine ecosystems with multiple stressors, it is often desirable to quantify a suite of biological endpoints that (1) reflect fish condition at several levels of biological organization and time scales and (2) are sensitive to a range of environmental stressors. However, established methods of preservation and processing of fish for specific endpoints are often incompatible. Here, we developed a novel flash-freezing approach for assessing the health of a small, sensitive fish, the endangered Delta Smelt (Hypomesus transpacificus) after collections from the San Francisco Estuary (SFE). We assess whether flash-freezing the entire fish ensures effective preservation of multiple tissues for subsequent biomarker analyses by comparing measurements of fresh to frozen tissue. Tissues included brain, gill, and liver for enzyme activity, kidney and spleen for pathogens, and gills, liver, and gonads for histopathology and reproduction. Although flash-freezing in liquid nitrogen altered the length, weight, and condition factor of Delta Smelt, the percent changes were small (<1.5%). Histological analyses of the cellular morphology of gills, liver, and gonads were similar between both methods. Freezing artefacts were observed in ovaries, but did not hinder the identification and interpretation of cell types and oocyte stages. Freezing did not alter bacterial isolation or the activities of ethoxyresorufin-0-deethylase (EROD) or acetylcholinesterase (AChE), but had a small, negative influence on sodium potassium adenosine triphosphatase (ATPase) activity. Thus, flash-freezing in the field is a versatile preservation method for Delta Smelt, allowing for multiple tissue collections and bioassays from an individual tiny fish exposed to a wide range of natural and anthropogenic stressors. Similar methodology may be applicable to other species for which a range of biological endpoints and histopathology data are needed.

Contaminant and food limitation stress in an endangered estuarine fish.

The abundance of Delta Smelt (Hypomesus transpacificus), a fish species endemic to the upper San Francisco Estuary (SFE), is declining. Several causes for the population decline have been proposed, including food limitation and contaminant effects. Here, using juvenile Delta Smelt collected from throughout their range, we measured a suite of indices across three levels of biological organization (cellular, organ, individual) that reflect fish condition at temporal scales ranging from hours to weeks. Using these indices, the relative conditions of fish collected from five regions in the SFE were compared: Cache Slough, Sacramento River Deep Water Ship Channel, Confluence, Suisun Bay and Suisun Marsh. Fish sampled from Suisun Bay and, to a lesser extent the Confluence, exhibited relatively poor short-term nutritional and growth indices and morphometric condition, while fish from the freshwater regions of the estuary, and Cache Slough in particular, exhibited the most apparent histopathological signs of contaminant exposure. In contrast, fish from the Suisun Marsh region exhibited higher short-term nutrition and growth indices, and better morphometric and histopathological condition. For instance, fish collected from Suisun Marsh had a mean stomach fullness, expressed as a percentage of fish weight, that was 3.4-fold higher than fish collected from Suisun Bay, while also exhibiting an incidence of histopathological lesions that was 11-fold lower than fish collected from Cache Slough. Thus, our findings support the hypothesis that multiple stressors, including food limitation and contaminants, are contributing to the decline of Delta Smelt, and that these stressors influence Delta Smelt heterogeneously across space.

Henneguya sp. in yellowfin goby Acanthogobius flavimanus from the San Francisco Estuary.

Myxozoan spores were observed in yellowfin goby Acanthogobius flavimanus collected from Suisun Marsh, San Francisco Estuary (SFE). Although histopathological changes associated with the parasite were not observed, the spores formed plasmodia that partially blocked the gastric and intestinal mucosa and gut lumen and may affect the perfomance and survival of the yellowfin goby. Morphological features of the spores resembled Henneguya sp. and molecular analysis of the 18S ribosomal DNA (Domain III) confirmed close similarity to H. rhinogobii and H. pseudorhinogobii isolated from the Japanese freshwater goby. The yellowfin goby myxozoan however, is likely an undescribed species based on phylogenetic analysis and morphologic features. Detailed description of vegetative and spore stages are currently lacking for proposal to a new species of Henneguya. A specific PCR test was developed, which confirmed a 100% prevalence of the parasite among randomly collected gobies in group 1 (N = 30) and group 2 (N = 15) at termination of the study at one month in captivity. The myxozoan was also detected from 18 gobies (12%) that died in the first group within two weeks in captivity. Apparently healthy gobies that served as controls did not reveal the presence of the myxozoan by PCR. This study documents the occurrence of a potentially new species of myxozoan in the yellowfin goby and underscores the detection of a parasitic infection in an introduced fish in the SFE. Although the pathogenesis of the myxozoan was not assessed and the prevalence as reported here is restricted to a comparatively small collection site in Suisun slough, the reemergence, identification, and ecological relevance of the parasite on goby populations in the SFE may be investigated in the future using the specific diagnostic tool developed in this study.