Validation of a microwave energy meter to non-lethally estimate energetic reserves in adult sturgeon.

Whole-body (WB) energetic reserves influence fish survival, growth, and reproduction but are typically quantified using lethal methods (i.e. proximate analyses) or interpreted through body condition indices. Energetic reserves can impact population dynamics through influences on growth rates, age-at-first-reproductive-maturity, and spawning periodicity at the individual-fish level, especially in long-lived sturgeon species. Therefore, a non-lethal tool to track the energetic reserves of endangered sturgeon populations could inform adaptive management and further our understanding of the sturgeon's biology. The Distell Fatmeter is a microwave energy meter that has been validated to non-lethally estimate energetic reserves in some fish species, but never successfully for sturgeon. Here, stepwise linear regressions were applied to test commonly monitored body metrics and Fatmeter measurements at nine different anatomical sites on captive adult pallid sturgeon (Scaphirhynchus albus; total length of 790-1015 mm; WB lipid of 13.9-33.3%) compared with WB lipid and energy content determined by proximate analyses. Fatmeter measurements alone explained approximately 70% of the variation in WB energetic reserves, which outperformed models considering body metrics alone by a margin of approximately 20%. The top-ranked models based on AICc score (second-order Akaike Information Criterion) included a combination of body metrics and Fatmeter measurements and accounted for up to 76% of the variation in WB lipid and energy. We recommend the incorporation of Fatmeter measurements at a single site located dorsally to the lateral scutes at the posterior end of the fish above the pelvic fins (U-P) into conservation monitoring programs for adult pallid sturgeon (total length [TL] ≥ 790 mm; fork length [FL] ≥ 715 mm) and the cautious application of Fatmeter measurements for sturgeon between 435 and 790 mm TL (375-715 mm FL). Measurements at this U-P site combined with body mass explained approximately 75% of the variation in WB lipid and energy.

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.

Divergent transcriptomic signatures in response to salinity exposure in two populations of an estuarine fish.

In estuary and coastal systems, human demand for freshwater, climate change-driven precipitation variability, and extreme weather impact salinity levels, reducing connectivity between mesohaline coastal fish populations and potentially contributing to genomic divergence. We examined gill transcriptome responses to salinity in wild-caught juveniles from two populations of Sacramento splittail (Pogonichthys macrolepidotus), a species of conservation concern that is endemic to the San Francisco Estuary, USA, and the lower reaches of its tributaries. Recent extreme droughts have led to salinities above the tolerance limits for this species, creating a migration barrier between these populations, which potentially contributed to population divergence. We identified transcripts involved in a conserved response to salinity; however, the more salinity-tolerant San Pablo population had greater transcriptome plasticity (3.6-fold more transcripts responded than the Central Valley population) and a response consistent with gill remodeling after 168 hr of exposure to elevated salinity. The reorganization of the gill in response to changing osmotic gradients is a process critical for acclimation and would facilitate enhanced salinity tolerance. We detected an upregulation of receptors that control the Wnt (wingless-type) cell signaling pathway that may be required for an adaptive response to increases in salinity, patterns not observed in the relatively salinity-sensitive Central Valley population. We detected 62 single nucleotide polymorphisms (SNPs) in coding regions of 26 transcripts that differed between the populations. Eight transcripts that contained SNPs were associated with immune responses, highlighting the importance of diversity in immune gene sequences as a defining characteristic of genomic divergence between these populations. Our data demonstrate that these populations have divergent transcriptomic responses to salinity, which is consistent with observed physiological differences in salinity tolerance.

Diel cycling hypoxia enhances hypoxia tolerance in rainbow trout (Oncorhynchus mykiss): evidence of physiological and metabolic plasticity.

Many fish naturally encounter a daily cycle of hypoxia, but it is unclear whether this exposure hardens hypoxia-intolerant fish to future hypoxia or leads to accumulated stress and death. The rainbow trout (Oncorhynchus mykiss) is a putatively hypoxia-sensitive species found in rivers and estuaries that may routinely experience hypoxic events. Trout were exposed to one of four 135 h treatments in a swim-tunnel respirometer: (1) air-saturated control (20.7 kPa PO2 ); (2) diel cycling O2 (20.7-4.2 kPa PO2  over 24 h); (3) acute hypoxia (130 h at 20.7 kPa PO2  followed by 5 h at 4.2 kPa PO2 ); and (4) the mean oxygen tension (12.4 kPa PO2 ) experienced by the diel cycled fish. Some responses were similar in diel O2 cycled and mean PO2 -treated fish, but overall, exposure to ecologically representative diel hypoxia cycles improved hypoxia tolerance. Diel hypoxia-induced protective responses included increased inducible HSP70 concentration and mean corpuscular hemoglobin concentration, as well as reduced plasma cortisol. Acclimation to diel hypoxia allowed metabolic rates to decline during hypoxia, reduced oxygen debt following subsequent exposures, and allowed fish to return to an anabolic phenotype. The data demonstrate that acute diel cycling hypoxia improves hypoxia tolerance in previously intolerant fish through the activation of cellular protective mechanisms and a reduction in metabolic O2 requirements.

High thermal tolerance of a rainbow trout population near its southern range limit suggests local thermal adjustment.

Transformation of earth's ecosystems by anthropogenic climate change is predicted for the 21st century. In many regions, the associated increase in environmental temperatures and reduced precipitation will have direct effects on the physiological performance of terrestrial and aquatic ectotherms and have already threatened fish biodiversity and important fisheries. The threat of elevated environmental temperatures is particularly salient for members of the Oncorhynchus genus living in California, which is the southern limit of their range. Here, we report the first assessments of the aerobic capacity of a Californian population of wild Oncorhynchus mykiss Walbaum in relationship to water temperature. Our field measurements revealed that wild O. mykiss from the lower Tuolumne River, California maintained 95% of their peak aerobic scope across an impressive temperature range (17.8-24.6°C). The thermal range for peak performance corresponds to local high river temperatures, but represents an unusually high temperature tolerance compared with conspecifics and congeneric species from northern latitudes. This high thermal tolerance suggests that O. mykiss at the southern limit of their indigenous distribution may be locally adjusted relative to more northern populations. From fisheries management and conservation perspectives, these findings challenge the use of a single thermal criterion to regulate the habitat of the O. mykiss species along the entirety of its distribution range.

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.

Effects of feed restriction on the upper temperature tolerance and heat shock response in juvenile green and white sturgeon.

The objective of the current study was to investigate the effects of feed restriction on whole-organism upper thermal tolerance and the heat shock response of green and white sturgeon to determine how changes in food amount might influence physiological performance of each species when faced with temperature stress. Two parallel feed restriction trials were carried out for juvenile green (202g; 222-day post hatch: dph) and white sturgeon (205g; 197-dph) to manipulate nutritional status at 12.5%, 25%, 50%, or 100% of optimum feeding rate (100% OFR were 1.6% and 1.8% body weight/day, respectively) for four weeks. Following the trials, the critical thermal maximum (CTMax, 0.3°C/min) of sturgeon (N=12/treatment/species) was assessed as an indicator of whole-organism upper thermal tolerance. To assess temperature sensitivity, sturgeon (N=9/treatment/species) were acutely transferred to two temperature treatments (28°C and 18°C as a handling control) for 2h followed by 2h of recovery at 18°C before being sacrificed, and gill, brain, and mucus sampled for measurements of 70-kDa heat shock protein levels (Hsc/Hsp70). Feeding rate had species-specific effects on CTMax in green and white sturgeon such that CTMax of green sturgeon decreased as the magnitude of feed restriction increased; whereas, CTMax of white sturgeon did not change with feed restriction. Elevated temperature (28°C) and feed restriction increased Hsc/Hsp70 levels in the gill tissue of green sturgeon, while heat shock increased Hsc/Hsp70 levels in the mucus of white sturgeon. Our results suggest that green sturgeon may be more susceptible to temperature stress under food-limited conditions.

Effects of feed restriction on salinity tolerance in white sturgeon (Acipenser transmontanus).

A multistressor study was conducted to investigate interactive effects of nutritional status and salinity on osmoregulation of juvenile white sturgeon. Our hypothesis was that lower nutritional status would decrease the salinity tolerance of juvenile white sturgeon. A four-week feed restriction (12.5%, 25%, 50%, 100% of optimum feeding rate: OFR defined as the rate (% body weight per day) at which growth is maximal) trial was performed, and relevant indices of nutritional status were measured. Following the trial, sturgeon were acutely exposed to various salinities (0, 8, 16, 24 ppt) for 120 h, and relevant osmoregulatory measurements were made at 12, 72, and 120 h post-salinity exposures. The feed-restriction trial resulted in a graded nutritional response with the most feed-restricted group (12.5% OFR) showing the lowest nutritional status. The salinity exposure trial showed clear evidence that lower nutritional status decreased the salinity tolerance of juvenile white sturgeon. Increasing salinities resulted in significant alterations in osmoregulatory indices of all feeding groups; however, a significantly slower acclimatory response to 24 ppt was detected in the most feed-restricted group compared to the non-feed-restricted group (100% OFR). Furthermore, evaluation of the effect of nutritional status on the relationship between osmoregulatory measurements and body size showed that there was a significant negative relationship between osmoregulatory performance and body size within the most feed-restricted group. This suggests that there is a certain body size range (200-300 g based on our finding) where juvenile white sturgeon can maximize osmoregulatory capacity at a salinity of 24 ppt.

Larval green and white sturgeon swimming performance in relation to water-diversion flows.

Little is known of the swimming capacities of larval sturgeons, despite global population declines in many species due in part to fragmentation of their spawning and rearing habitats by man-made water-diversion structures. Larval green (Acipenser medirostris) and white sturgeon (Acipenser transmontanus) inhabit the highly altered Sacramento-San Joaquin watershed, making them logical species to examine vulnerability to entrainment by altered water flows. The risk of larval sturgeon entrainment is influenced by the ontogeny of swimming capacity and dispersal timing and their interactions with water-diversion structure operations. Therefore, the aim of this study was to describe and compare the ontogeny and allometry of larval green and white sturgeon swimming capacities until completion of metamorphosis into juveniles. Despite the faster growth rates and eventual larger size of larval white sturgeon, green sturgeon critical swimming velocities remained consistently, though modestly, greater than those of white sturgeon throughout the larval life stage. Although behavioural interactions with water-diversion structures are also important considerations, regarding swimming capacity, Sacramento-San Joaquin sturgeons are most vulnerable to entrainment in February-May, when white sturgeon early larvae are in the middle Sacramento River, and April-May, when green sturgeon early larvae are in the upper river. Green sturgeon migrating downstream to the estuary and bays in October-November are also susceptible to entrainment due to their movements combined with seasonal declines in their swimming capacity. An additional inter-species comparison of the allometric relationship between critical swimming velocities and total length with several sturgeon species found throughout the world suggests a similar ontogeny of swimming capacity with growth. Therefore, although dispersal and behaviour differ among river systems and sturgeon species, similar recommendations are applicable for managers seeking to balance water demands with restoration and conservation of sturgeons worldwide.