Histopathological assessment of seven year-classes of Delta Smelt.

The Delta Smelt (Hypomesus transpacificus) is an imperiled, annual fish endemic to the Sacramento-San Joaquin Delta and San Francisco Estuary. This study examined the severity and prevalence of liver and gill lesions of juvenile through adult Delta Smelt from 2011 through 2017 collected from five regions throughout its habitat (n = 1,053). The first and last years of the study were wet, but bracketed an extreme drought in CA (2012-2016), during which the Delta Smelt population reached historical lows. Overall, the three most common lesions were gill ionocyte hyperplasia, liver lipidosis, and gill aneurysm. Individuals with higher fork lengths exhibited increased gill and liver lesion score (summations of the severity scores), suggesting that Delta Smelt accumulate lesions through their lives, and that larger individuals were more tolerant of liver and gill lesions. Liver lesion score showed significant regional differences, while salinity was a better predictor of gill lesions than region, with lower gill lesion scores associated with higher salinities. Largely consistent with previously reported histopathology patterns, Delta Smelt collected from the Confluence and Suisun Marsh had the lowest liver lesion score, while Delta Smelt collected from Cache Slough and Suisun Bay had the highest lesion scores, and Suisun Marsh had the lowest glycogen depletion, suggesting heterogeneous levels of exposure to environmental stressors across regions. Gill and liver lesion score also varied significantly with year-class. The highest gill lesion score occurred in the 2015/16 year-class, and the lowest occurred in the 2017/18 year-class, a 2.8-fold difference. Controlling for size and regional effects, individuals with comparatively high liver lesion scores were prevalent in the population until the 2014/15 year-class. In the two subsequent year-classes, Delta Smelt livers were in the best condition, coinciding with peak drought conditions and record low abundances.

Sensitivities of an endemic, endangered California smelt and two non-native fishes to serial increases in temperature and salinity: implications for shifting community structure with climate change.

In many aquatic systems, native fishes are in decline and the factors responsible are often elusive. In the San Francisco Estuary (SFE) in California, interactions among native and non-native species are key factors contributing to the decline in abundance of endemic, endangered Delta Smelt (Hypomesus transpacificus). Climate change and drought-related stressors are further exacerbating declines. To assess how multiple environmental changes affect the physiology of native Delta Smelt and non-native Mississippi Silverside (Menidia beryllina) and Largemouth Bass (Micropterus salmoides), fishes were exposed to serial exposures of a single stressor (elevated temperature or salinity) followed by two stressors (elevated temperature and salinity) to determine how a single stressor affects the capacity to cope with the addition of a second stressor. Critical thermal maximum (CTMax; a measure of upper temperature tolerance) was determined after 0, 2, 4 and 7 days following single and multiple stressors of elevated temperature (16°C vs. 20°C) and salinity (2.4 vs. 8-12 ppt, depending on species). Under control conditions, non-native fishes had significantly higher CTMax than the native Delta Smelt. An initial temperature or salinity stressor did not negatively affect the ability of any species to tolerate a subsequent multiple stressor. While elevated salinity had little effect on CTMax, a 4°C increase in temperature increased CTMax. Bass experienced an additive effect of increased temperature and salinity on CTMax, such that CTMax further increased under multiple stressors. In addition, Bass demonstrated physiological sensitivity to multiple stressors demonstrated by changes in hematocrit and plasma osmolality, whereas the physiology of Silversides remained unaffected. Non-native Bass and Mississippi Silversides showed consistently higher thermal tolerance limits than the native Delta Smelt, supporting their abundance in warmer SFE habitats. Continued increases in SFE water temperatures predicted with climate change may further impact endangered Delta Smelt populations directly if habitat temperatures exceed thermal limits.

Foraging and metabolic consequences of semi-anadromy for an endangered estuarine fish.

Diadromy affords fish access to productive ecosystems, increasing growth and ultimately fitness, but it is unclear whether these advantages persist for species migrating within highly altered habitat. Here, we compared the foraging success of wild Delta Smelt-an endangered, zooplanktivorous, annual, semi-anadromous fish that is endemic to the highly altered San Francisco Estuary (SFE)-collected from freshwater (<0.55 psu) and brackish habitat (≥0.55 psu). Stomach fullness, averaged across three generations of wild Delta Smelt sampled from juvenile through adult life stages (n = 1,318), was 1.5-fold higher in brackish than in freshwater habitat. However, salinity and season interacted, with higher fullness (1.7-fold) in freshwater than in brackish habitat in summer, but far higher fullness in brackish than freshwater habitat during fall/winter and winter/spring (1.8 and 2.0-fold, respectively). To examine potential causes of this interaction we compared mesozooplankton abundance, collected concurrently with the Delta Smelt, in freshwater and brackish habitat during summer and fall/winter, and the metabolic rate of sub-adult Delta Smelt acclimated to salinities of 0.4, 2.0, and 12.0 psu in a laboratory experiment. A seasonal peak in mesozooplankton density coincided with the summer peak in Delta Smelt foraging success in freshwater, and a pronounced decline in freshwater mesozooplankton abundance in the fall coincided with declining stomach fullness, which persisted for the remainder of the year (fall, winter and spring). In brackish habitat, greater foraging 'efficiency' (prey items in stomachs/mesozooplankton abundance) led to more prey items per fish and generally higher stomach fullness (i.e., a higher proportion of mesozooplankton detected in concurrent trawls were eaten by fish in brackish habitat). Delta Smelt exhibited no difference in metabolic rate across the three salinities, indicating that metabolic responses to salinity are unlikely to have caused the stomach fullness results. Adult migration and freshwater spawning therefore places young fish in a position to exploit higher densities of prey in freshwater in the late spring/summer, and subsequent movement downstream provides older fish more accessible prey in brackish habitat. Thus, despite endemism to a highly-altered estuary, semi-anadromy provided substantial foraging benefits to Delta Smelt, consistent with other temperate migratory fish.

Physiological effects of salinity on Delta Smelt, Hypomesus transpacificus.

Abiotic factors like salinity are relevant to survival of pelagic fishes of the San Francisco Bay Estuary. We tested the effects of 4 parts per thousand (ppt) salinity increases on Delta Smelt (DS) in a laboratory experiment simulating salinity increases that might occur around the low-salinity zone (LSZ) (<6 ppt). Adult DS, fed 2% body mass per day, starting at 0.5 ppt [freshwater (FW)], were exposed to weekly step-increases of 4 ppt to a maximum of 10 ppt saltwater (SW) over 19 days, and compared to FW controls. DS (n = 12/treatment per sampling) were sampled at 24, 72, and 96 h (1, 3, and 4 days) post-salinity increase for analyses of hematocrit, plasma osmolality, muscle water content, gill chloride cell (CC) Na(+)/K(+)-ATPase (NKA) and apoptosis after being weighed and measured (n = 3 tanks per treatment). No apparent increase in length or weight occurred nor did a difference in survival. Following step-increases in SW, hematocrit increased over time. Other fish responses generally showed a pattern; specifically plasma osmolality became elevated at 1 day and diminished over 4 days in SW. Percent muscle water content (%) did not show significant changes. CCs showed increased NKA, cell size and apoptosis over time in SW, indicating that CCs turnover in DS. The cell renewal process takes days, at least over 19 days. In summary, DS are affected by salinities of the LSZ and ≤10 ppt, though they employ physiological strategies to acclimate.

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.