Lifetime Chronicles of Selenium Exposure Linked to Deformities in an Imperiled Migratory Fish.

Aquatic ecosystems worldwide face growing threats from elevated levels of contaminants from human activities. Toxic levels of selenium (Se) shown to cause deformities in birds, fish, and mammals can transfer from parents to progeny during embryonic development or accumulate through Se-enriched diets. For migratory species that move across landscapes, tracking exposure to elevated Se is vital to mitigating vulnerabilities. Yet, traditional toxicological investigations resolve only recent Se exposure. Here, we use a novel combination of X-ray fluorescence microscopy and depositional chronology in a biomineral to reveal for the first time provenance, life stage, and duration of toxic Se exposure over the lifetime of an organism. Spinal deformities observed in wild Sacramento Splittail (Pogonichthys macrolepidotus), an imperiled migratory minnow, were attributed to elevated Se acquired through maternal transfer and juvenile feeding on contaminated prey. This novel approach paves the way for diagnosing sources, pathways, and potential for a cumulative exposure of Se relevant for conservation.

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.

Analysis of pelagic species decline in the upper San Francisco Estuary using multivariate autoregressive modeling (MAR).

Four species of pelagic fish of particular management concern in the upper San Francisco Estuary, California, USA, have declined precipitously since ca. 2002: delta smelt (Hypomesus transpacificus), longfin smelt (Spirinchus thaleichthys), striped bass (Morone saxatilis), and threadfin shad (Dorosoma petenense). The estuary has been monitored since the late 1960s with extensive collection of data on the fishes, their pelagic prey, phytoplankton biomass, invasive species, and physical factors. We used multivariate autoregressive (MAR) modeling to discern the main factors responsible for the declines. An expert-elicited model was built to describe the system. Fifty-four relationships were built into the model, only one of which was of uncertain direction a priori. Twenty-eight of the proposed relationships were strongly supported by or consistent with the data, while 26 were close to zero (not supported by the data but not contrary to expectations). The position of the 2 per thousand isohaline (a measure of the physical response of the estuary to freshwater flow) and increased water clarity over the period of analyses were two factors affecting multiple declining taxa (including fishes and the fishes' main zooplankton prey): Our results were relatively robust with respect to the form of stock-recruitment model used and to inclusion of subsidiary covariates but may be enhanced by using detailed state-space models that describe more fully the life-history dynamics of the declining species.

Bayesian change point analysis of abundance trends for pelagic fishes in the upper San Francisco Estuary.

We examined trends in abundance of four pelagic fish species (delta smelt, longfin smelt, striped bass, and threadfin shad) in the upper San Francisco Estuary, California, USA, over 40 years using Bayesian change point models. Change point models identify times of abrupt or unusual changes in absolute abundance (step changes) or in rates of change in abundance (trend changes). We coupled Bayesian model selection with linear regression splines to identify biotic or abiotic covariates with the strongest associations with abundances of each species. We then refitted change point models conditional on the selected covariates to explore whether those covariates could explain statistical trends or change points in species abundances. We also fitted a multispecies change point model that identified change points common to all species. All models included hierarchical structures to model data uncertainties, including observation errors and missing covariate values. There were step declines in abundances of all four species in the early 2000s, with a likely common decline in 2002. Abiotic variables, including water clarity, position of the 2 per thousand isohaline (X2), and the volume of freshwater exported from the estuary, explained some variation in species' abundances over the time series, but no selected covariates could explain statistically the post-2000 change points for any species.

Resolving selenium exposure risk: Spatial, temporal, and tissue-specific variability of an endemic fish in a large, dynamic estuary.

Estuaries provide critical habitat for a vast array of fish and wildlife but are also a nexus for core economic activities that mobilize and concentrate contaminants that can threaten aquatic species. Selenium (Se), an essential element and potent reproductive toxin, is enriched in parts of the San Francisco Estuary (SFE) to levels known to cause toxicity, yet the risk of Se to species that inhabit the SFE is not well understood. We quantified Se concentrations in muscle, liver and ovary of the demersal cyprinid Sacramento Splittail from six regions in the SFE at three time points to evaluate Se exposure risk. Selenium levels exceeded proposed EPA criteria in ovary and thresholds of concern for liver in 15% and 20%, respectively, of fish collected in the fall of 2010, preceding the discovery of juvenile Splittail displaying a high incidence (>40%) of spinal deformities characteristic of Se toxicity, and again in 2011. No exceedances were detected in muscle tissue. Selenium concentrations varied significantly among regions for muscle (F5,113 = 20.49, p < 0.0001), liver (F5,113 = 28.4, p < 0.0001) and ovary (F5,112 = 19.3, p < 0.0001) but did not vary between the wet and dry years, nor were they influenced by foraging trophic level or prey selection. Foraging location along the salinity gradient, defined by δ34S values, explained regional Se exposures in Splittail. Relationships between tissues varied among regions for muscle and liver and muscle and ovary, but a single global relationship could be defined for ovary and liver Se concentrations. Our results suggest that the proposed EPA Se criteria for muscle tissue in Splittail may be under-protective as it would not have predicted exceedances in liver or ovary tissue and that the relationship between muscle tissue and ovary and liver may be Se concentration and seasonal dependent.

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.

SmeltCam: underwater video codend for trawled nets with an application to the distribution of the imperiled delta smelt.

Studying rare and sensitive species is a challenge in conservation biology. The problem is exemplified by the case of the imperiled delta smelt Hypomesus transpacificus, a small delicate fish species endemic to the San Francisco Estuary, California. Persistent record-low levels of abundance and relatively high sensitivity to handling stress pose considerable challenges to studying delta smelt in the wild. To attempt to overcome these and other challenges we have developed the SmeltCam, an underwater video camera codend for trawled nets. The SmeltCam functions as an open-ended codend that automatically collects information on the number and species of fishes that pass freely through a trawled net without handling. We applied the SmeltCam to study the fine-scale distribution of juvenile delta smelt in the water column in the upper San Francisco Estuary. We learned that during flood tides delta smelt were relatively abundant throughout the water column and that during ebb tides delta smelt were significantly less abundant and occurred only in the lower half and sides of the water column. The results suggest that delta smelt manipulate their position in the water column to facilitate retention in favorable habitats. With the application of the SmeltCam we increased the survival of individual delta smelt by 72% compared to using a traditional codend, where all of the fish would have likely died due to handling stress. The SmeltCam improves upon similar previously developed silhouette photography or video recording devices and demonstrates how new technology can be developed to address important questions in conservation biology as well as lessen the negative effects associated with traditional sampling methods on imperiled species.