Archaeological data provide alternative hypotheses on Pacific herring (Clupea pallasii) distribution, abundance, and variability
- Proceedings of the National Academy of Sciences of the United States of America
- Published over 4 years ago
Pacific herring (Clupea pallasii), a foundation of coastal social-ecological systems, is in decline throughout much of its range. We assembled data on fish bones from 171 archaeological sites from Alaska, British Columbia, and Washington to provide proxy measures of past herring distribution and abundance. The dataset represents 435,777 fish bones, dating throughout the Holocene, but primarily to the last 2,500 y. Herring is the single-most ubiquitous fish taxon (99% ubiquity) and among the two most abundant taxa in 80% of individual assemblages. Herring bones are archaeologically abundant in all regions, but are superabundant in the northern Salish Sea and southwestern Vancouver Island areas. Analyses of temporal variability in 50 well-sampled sites reveals that herring exhibits consistently high abundance (>20% of fish bones) and consistently low variance (<10%) within the majority of sites (88% and 96%, respectively). We pose three alternative hypotheses to account for the disjunction between modern and archaeological herring populations. We reject the first hypothesis that the archaeological data overestimate past abundance and underestimate past variability. We are unable to distinguish between the second two hypotheses, which both assert that the archaeological data reflect a higher mean abundance of herring in the past, but differ in whether variability was similar to or less than that observed recently. In either case, sufficient herring was consistently available to meet the needs of harvesters, even if variability is damped in the archaeological record. These results provide baseline information prior to herring depletion and can inform modern management.
Microplastic is considered a potential threat to marine life as it is ingested by a wide variety of species. Most studies on microplastic ingestion are short-term investigations and little is currently known about how this potential threat has developed over the last decades where global plastic production has increased exponentially. Here we present the first long-term study on microplastic in the marine environment, covering three decades from 1987 to 2015, based on a unique sample set originally collected and conserved for food web studies. We investigated the microplastic concentration in plankton samples and in digestive tracts of two economically and ecologically important planktivorous forage fish species, Atlantic herring (Clupea harengus) and European sprat (Sprattus sprattus), in the Baltic Sea, an ecosystem which is under high anthropogenic pressure and has undergone considerable changes over the past decades. Surprisingly, neither the concentration of microplastic in the plankton samples nor in the digestive tracts changed significantly over the investigated time period. Average microplastic concentration in the plankton samples was 0.21±0.15particlesm(-3). Of 814 fish examined, 20% contained plastic particles, of which 95% were characterized as microplastic (<5mm) and of these 93% were fibres. There were no significant differences in the plastic content between species, locations, or time of day the fish were caught. However, fish size and microplastic in the digestive tracts were positively correlated, and the fish contained more plastic during summer than during spring, which may be explained by increased food uptake with size and seasonal differences in feeding activity. This study highlights that even though microplastic has been present in the Baltic environment and the digestive tracts of fishes for decades, the levels have not changed in this period. This underscores the need for greater understanding of how plastic is cycled through marine ecosystems. The stability of plastic concentration and contamination over time observed here indicates that the type and level of microplastic pollution may be more closely correlated to specific human activities in a region than to global plastic production and utilization as such.
During the last 50 years human anisakiasis has been rising while parasites have increased their prevalence at determined fisheries becoming an emergent major public health problem. Although artificial enzymatic digestion procedure by CODEX (STAN 244-2004: standard for salted Atlantic herring and salted sprat) is the recommended protocol for anisakids inspection, no international agreement has been achieved in veterinary and scientific digestion protocols to regulate this growing source of biological hazard in fish products. The aim of this work was to optimize the current artificial digestion protocol by CODEX with the purpose of offering a faster, more useful and safer procedure for factories workers, than the current one for anisakids detection. To achieve these objectives, the existing pepsin chemicals and the conditions of the digestion method were evaluated and assayed in fresh and frozen samples, both in lean and fatty fish species. Results showed that the new digestion procedure considerably reduces the assay time, and it is more handy and efficient (the quantity of the resulting residue was considerably lower after less time) than the widely used CODEX procedure. In conclusion, the new digestion method herein proposed based on liquid pepsin format is an accurate reproducible and user-friendly off-site tool, that can be useful in the implementation of screening programs for the prevention of human anisakiasis (and associated gastroallergic disorders) due to the consumption of raw or undercooked contaminated seafood products.
Viral hemorrhagic septicemia virus (VHSV) genotype IVa causes mass mortality in wild Pacific herring, a species of economic value, in the Northeast Pacific Ocean. Young of the year herring are particularly susceptible and can be carriers of the virus. To understand its pathogenesis, tissue and cellular tropisms of VHSV in larval and juvenile Pacific herring were investigated with immunohistochemistry, transmission electron microscopy, and viral tissue titer. In larval herring, early viral tropism for epithelial tissues (6d post-exposure) was indicated by foci of epidermal thickening that contained heavy concentrations of virus. This was followed by a cellular tropism for fibroblasts within the fin bases and the dermis, but expanded to cells of the kidney, liver, pancreas, gastrointestinal tract and meninges in the brain. Among wild juvenile herring that underwent a VHS epizootic in the laboratory, the disease was characterized by acute and chronic phases of death. Fish that died during the acute phase had systemic infections in tissues including the submucosa of the gastrointestinal tract, spleen, kidney, liver, and meninges. The disease then transitioned into a chronic phase that was characterized by the appearance of neurological signs including erratic and corkscrew swimming and darkening of the dorsal skin. During the chronic phase viral persistence occurred in nervous tissues including meninges and brain parenchymal cells and in one case in peripheral nerves, while virus was mostly cleared from the other tissues. The results demonstrate the varying VHSV tropisms dependent on the timing of infection and the importance of neural tissues for the persistence and perpetuation of chronic infections in Pacific herring.
A new method is presented to estimate individuals' (1) age at maturation, (2) energy acquisition rate, (3) energy expenditure for body maintenance, and (4) reproductive investment, and the multivariate distribution of these traits in a population. The method relies on adjusting a conceptual energy allocation model to individual growth curves using nonlinear mixed-effects modelling. The method’s performance was tested using simulated growth curves for a range of life-history types. Individual age at maturation, energy acquisition rate and the sum of maintenance and reproductive investment rates, and their multivariate distribution, were accurately estimated. For the estimation of maintenance and reproductive investment rates separately, biases were observed for life-histories with a large imbalance between these traits. For low reproductive investment rates and high maintenance rates, reproductive investment rate estimates were strongly biased whereas maintenance rate estimates were not, the reverse holding in the opposite situation. The method was applied to individual growth curves back-calculated from otoliths of North Sea plaice (Pleuronectes platessa) and from scales of Norwegian spring spawning herring (Clupea harengus). For plaice, maturity ogives derived from our individual estimates of age at maturation were almost identical to the maturity ogives based on gonad observation in catch samples. For herring, we observed 51.5 % of agreement between our individual estimates and those directly obtained from scale reading, with a difference lower than 1 year in 97 % of cases. We conclude that the method is a powerful tool to estimate the distribution of correlated life-history traits for any species for which individual growth curves are available.
The Pacific herring (Clupea pallasii) population in Prince William Sound, Alaska crashed in 1993 and has yet to recover, affecting food web dynamics in the Sound and impacting Alaskan communities. To help researchers design and implement the most effective monitoring, management, and recovery programs, a Bayesian assessment of Prince William Sound herring was developed by reformulating the current model used by the Alaska Department of Fish and Game. The Bayesian model estimated pre-fishery spawning biomass of herring age-3 and older in 2013 to be a median of 19,410 mt (95% credibility interval 12,150-31,740 mt), with a 54% probability that biomass in 2013 was below the management limit used to regulate fisheries in Prince William Sound. The main advantages of the Bayesian model are that it can more objectively weight different datasets and provide estimates of uncertainty for model parameters and outputs, unlike the weighted sum-of-squares used in the original model. In addition, the revised model could be used to manage herring stocks with a decision rule that considers both stock status and the uncertainty in stock status.
In the coming decades, environmental change like warming and acidification will affect life in the ocean. While data on single stressor effects on fish are accumulating rapidly, we still know relatively little about interactive effects of multiple drivers. Of particular concern in this context are the early life stages of fish, for which direct effects of increased CO2 on growth and development have been observed. Whether these effects are further modified by elevated temperature was investigated here for the larvae of Atlantic herring (Clupea harengus), a commercially important fish species. Over a period of 32 days, larval survival, growth in size and weight, and instantaneous growth rate were assessed in a crossed experimental design of two temperatures (10°C and 12°C) with two CO2 levels (400 μatm and 900 μatm CO2) at food levels mimicking natural levels using natural prey. Elevated temperature alone led to increased swimming activity, as well as decreased survival and instantaneous growth rate (Gi). The comparatively high sensitivity to elevated temperature in this study may have been influenced by low food levels offered to the larvae. Larval size, Gi and swimming activity were not affected by CO2, indicating tolerance of this species to projected “end of the century” CO2 levels. A synergistic effect of elevated temperature and CO2 was found for larval weight, where no effect of elevated CO2 concentrations was detected in the 12°C treatment, but a negative CO2 effect was found in the 10°C treatment. Contrasting CO2 effects were found for survival between the two temperatures. Under ambient CO2 conditions survival was increased at 12°C compared to 10°C. In general, CO2 effects were minor and considered negligible compared to the effect of temperature under these mimicked natural food conditions. These findings emphasize the need to include biotic factors such as energy supply via prey availability in future studies on interactive effects of multiple stressors.
Surveillance for pathogens of Atlantic herring, including viral hemorrhagic septicemia virus (VHSV), Ichthyophonus hoferi, and hepatic and intestinal coccidians, was conducted from 2012 to 2016 in the NW Atlantic Ocean, New Jersey, USA. Neither VHSV nor I. hoferi was detected in any sample. Goussia clupearum was found in the livers of 40 to 78% of adult herring in varying parasite loads; however, associated pathological changes were negligible. Phylogenetic analysis based on small subunit 18S rRNA gene sequences placed G. clupearum most closely with other extraintestinal liver coccidia from the genus Calyptospora, though the G. clupearum isolates had a unique nucleotide insertion between 604 and 729 bp that did not occur in any other coccidian species. G. clupearum oocysts from Atlantic and Pacific herring were morphologically similar, though differences occurred in oocyst dimensions. Comparison of G. clupearum genetic sequences from Atlantic and Pacific herring revealed 4 nucleotide substitutions and 2 gaps in a 1749 bp region, indicating some divergence in the geographically separate populations. Pacific G. clupearum oocysts were not directly infective, suggesting that a heteroxenous life cycle is likely. Intestinal coccidiosis was described for the first time from juvenile and adult Atlantic herring. A novel intestinal coccidian species was detected based on morphological characteristics of exogenously sporulated oocysts. A unique feature in these oocysts was the presence of 3 long (15.1 ± 5.1 µm, mean ±SD) spiny projections on both ends of the oocyst. The novel morphology of this coccidian led us to tentatively name this parasite G. echinata n. sp.
Parallel adaptive evolution of geographically distant herring populations on both sides of the North Atlantic Ocean
- Proceedings of the National Academy of Sciences of the United States of America
- Published over 1 year ago
Atlantic herring is an excellent species for studying the genetic basis of adaptation in geographically distant populations because of its characteristically large population sizes and low genetic drift. In this study we compared whole-genome resequencing data of Atlantic herring populations from both sides of the Atlantic Ocean. An important finding was the very low degree of genetic differentiation among geographically distant populations (fixation index = 0.026), suggesting lack of reproductive isolation across the ocean. This feature of the Atlantic herring facilitates the detection of genetic factors affecting adaptation because of the sharp contrast between loci showing genetic differentiation resulting from natural selection and the low background noise resulting from genetic drift. We show that genetic factors associated with timing of reproduction are shared between genetically distinct and geographically distant populations. The genes for thyroid-stimulating hormone receptor (TSHR), the SOX11 transcription factor (SOX11), calmodulin (CALM), and estrogen receptor 2 (ESR2A), all with a significant role in reproductive biology, were among the loci that showed the most consistent association with spawning time throughout the species range. In fact, the same two SNPs located at the 5' end of TSHR showed the most significant association with spawning time in both the east and west Atlantic. We also identified unexpected haplotype sharing between spring-spawning oceanic herring and autumn-spawning populations across the Atlantic Ocean and the Baltic Sea. The genomic regions showing this pattern are unlikely to control spawning time but may be involved in adaptation to ecological factor(s) shared among these populations.
Ecological adaptation is of major relevance to speciation and sustainable population management, but the underlying genetic factors are typically hard to study in natural populations due to genetic differentiation caused by natural selection being confounded with genetic drift in subdivided populations. Here, we use whole genome population sequencing of Atlantic and Baltic herring to reveal the underlying genetic architecture at an unprecedented detailed resolution for both adaptation to a new niche environment and timing of reproduction. We identify almost 500 independent loci associated with a recent niche expansion from marine (Atlantic Ocean) to brackish waters (Baltic Sea), and more than 100 independent loci showing genetic differentiation between spring- and autumn-spawning populations irrespective of geographic origin. Our results show that both coding and non-coding changes contribute to adaptation. Haplotype blocks, often spanning multiple genes and maintained by selection, are associated with genetic differentiation.