Kym C. Jacobson

Integrating fish and parasite data as a holistic solution for identifying the elusive stock structure of Pacific sardines (Sardinops sagax)

There is an urgent need to clarify how different stocks, or subpopulations of fish species, are vulnerable to fishing pressure and unfavorable ocean conditions because of the increasing demand on fisheries for human consumption. For marine fishes, the potential for high gene flow increases the difficulty in determining the number of subpopulations managed in a specific fishery. Although the use of molecular data has become a common method in the past 15xa0years to identify fish subpopulations, no single technique or suite of techniques has been established for fish stock structure studies. We review the use of fish morphometrics, artificial tags, fish genetics, parasite genetics, and parasites as biological tags to identify subpopulations of marine fishes with a focus on the Pacific sardine (Sardinops sagax) fishery off the west coast of North America. We suggest an integration of fish- and parasite-based techniques for future stock structure studies, particularly for pelagic fish species whose stock structure can be elusive. An integration of techniques may also resolve fish stock structure over small geographic areas by increasing the number of spatial and temporal scales studied simultaneously leading to methods for successful management of marine fish species.

Mortality of coho salmon (Oncorhynchus kisutch) associated with burdens of multiple parasite species

Multiple analytical techniques were used to evaluate the impact of multiple parasite species on the mortality of threatened juvenile coho salmon (Oncorhynchus kisutch) from the West Fork Smith River, Oregon, USA. We also proposed a novel parsimonious mathematical representation of macroparasite distribution, congestion rate, which (i) is easier to use than traditional models, and (ii) is based on Malthusian parameters rather than probability theory. Heavy infections of Myxobolus insidiosus (Myxozoa) and metacercariae of Nanophyetus salmincola and Apophallus sp. occurred in parr (subyearlings) from the lower mainstem of this river collected in 2007 and 2008. Smolts (yearlings) collected in 2007-2010 always harboured fewer Apophallus sp. with host mortality recognised as a function of intensity for this parasite. Mean intensity of Apophallus sp. in lower mainstem parr was 753 per fish in 2007 and 856 per fish in 2008, while parr from the tributaries had a mean of only 37 or 13 parasites per fish, respectively. Mean intensity of this parasite in smolts ranged between 47 and 251 parasites per fish. Over-dispersion (variance to mean ratios) of Apophallus sp. was always lower in smolts compared with all parr combined or lower mainstem parr. Retrospective analysis based on smolt data using both the traditional negative binomial truncation technique and our proposed congestion rate model showed identical results. The estimated threshold level for mortality involving Apophallus sp. was at 400-500 parasites per fish using both analytical methods. Unique to this study, we documented the actual existence of these heavy infections prior to the predicted mortality. Most of the lower mainstem parr (approximately 75%) had infections above this level. Heavy infections of Apophallus sp. metacercariae may be an important contributing factor to the high over-wintering mortality previously reported for these fish that grow and develop in this section of the river. Analyses using the same methods for M.insidiosus and N. salmincola generally pointed to minimal parasite-associated mortality.

Population Structure of Three Species of Anisakis Nematodes Recovered From Pacific Sardines (Sardinops sagax) Distributed Throughout the California Current System

abstract:u2003 Members of the Anisakidae are known to infect over 200 pelagic fish species and have been frequently used as biological tags to identify fish populations. Despite information on the global distribution of Anisakis species, there is little information on the genetic diversity and population structure of this genus, which could be useful in assessing the stock structure of their fish hosts. From 2005 through 2008, 148 larval anisakids were recovered from Pacific sardine (Sardinops sagax) in the California Current upwelling zone and were genetically sequenced. Sardines were captured off Vancouver Island, British Columbia in the north to San Diego, California in the south. Three species, Anisakis pegreffii, Anisakis simplex ‘C’, and Anisakis simplex s.s., were identified with the use of sequences from the internal transcribed spacers (ITS1 and ITS2) and the 5.8s subunit of the nuclear ribosomal DNA. The degree of nematode population structure was assessed with the use of the cytochrome c oxidase 2 (cox2) mitochondrial DNA gene. All 3 Anisakis species were distributed throughout the study region from 32°N to 50°N latitude. There was no association between sardine length and either nematode infection intensity or Anisakis species recovered. Larval Anisakis species and mitochondrial haplotype distributions from both parsimony networks and analyses of molecular variance revealed a panmictic distribution of these parasites, which infect sardines throughout the California Current ecosystem. Panmictic distribution of the larval Anisakis spp. populations may be a result of the presumed migratory pathways of the intermediate host (the Pacific sardine), moving into the northern portion of the California Current in summer and returning to the southern portion to overwinter and spawn in spring. However, the wider geographic range of paratenic (large piscine predators), and final hosts (cetaceans) can also explain the observed distribution pattern. As a result, the recovery of 3 Anisakis species and a panmictic distribution of their haplotypes could not be used to confirm or deny the presence of population subdivision of Pacific sardines in the California Current system.

Infections by Renibacterium salmoninarum and Nanophyetus salmincola Chapin are associated with reduced growth of juvenile Chinook salmon, Oncorhynchus tshawytscha (Walbaum), in the Northeast Pacific Ocean

We examined 1454 juvenile Chinook salmon, Oncorhynchus tshawytscha (Walbaum), captured in nearshore waters off the coasts of Washington and Oregon (USA) from 1999 to 2004 for infection by Renibacterium salmoninarum, Nanophyetus salmincola Chapin and skin metacercariae. The prevalence and intensities for each of these infections were established for both yearling and subyearling Chinook salmon. Two metrics of salmon growth, weight residuals and plasma levels of insulin-like growth factor-1, were determined for salmon infected with these pathogens/parasites, both individually and in combination, with uninfected fish used for comparison. Yearling Chinook salmon infected with R.xa0salmoninarum had significantly reduced weight residuals. Chinook salmon infected with skin metacercariae alone did not have significantly reduced growth metrics. Dual infections were not associated with significantly more severe effects on the growth metrics than single infections; the number of triple infections was very low and precluded statistical comparison. Overall, these data suggest that infections by these organisms can be associated with reduced juvenile Chinook salmon growth. Because growth in the first year at sea has been linked to survival for some stocks of Chinook salmon, the infections may therefore play a role in regulating these populations in the Northeast Pacific Ocean.

Parasites in subyearling Chinook salmon (Oncorhynchus tshawytscha) suggest increased habitat use in wetlands compared to sandy beach habitats in the Columbia River estuary

Many estuaries in the Pacific Northwest have been severely altered reducing wetlands habitat and resulting in an interest in their importance as rearing areas for juvenile salmon. To examine differences in habitat use during residency in the Columbia River estuary, we examined parasite communities acquired through food web interactions in subyearling Chinook salmon (Oncorhynchus tshawytscha) collected from four different habitat types in May and July of 2004 and 2005. Collections were made from two sandy bottom habitat types in the tidal freshwater and marine mixing areas of the estuary. These were compared to two wetlands types: one composed of scrub and shrub vegetation and another with emergent vegetation. Parasite assemblages differed among habitats suggesting differences in salmon feeding opportunities and rearing behaviors. In both years, the nematode, Hysterothylacium aduncum and the acanthocephalan, Echinorhynchus lageniformis, which use intermediate hosts found in the estuary, were more prevalent in lower wetlands suggesting increased feeding by salmon in these habitats. The differences in parasite assemblages among habitats suggests a variety of rearing and migration patterns through the Columbia River estuary and the increased prevalences of some parasites in the wetlands show that these habitats can be important feeding grounds for salmon.

Recent Increase in Nybelinia surmenicola Prevalence and Intensity in Pacific Hake (Merluccius productus) Off the United States West Coast

abstract:u2003 A larval marine cestode was found in 82.0% of 834 Pacific hake (Merluccius productus) stomachs collected from 341 trawl stations along the United States west coast during the summers of 2008 and 2009. Morphology and DNA sequencing was used to identify the cestode as Nybelinia surmenicola. In an examination of 131 Pacific hake stomachs collected from the same region in 1999, N. surmenicola prevalence was 35.1%. The results from a general linear model suggested that their prevalence is influenced by year and latitude, Pacific hake size, and sex. Mean intensity of N. surmenicola in 2008–2009 was 20.22 (±1.13 SE) and was positively related to Pacific hake length and the latitude of collection. Year-1 Pacific hake (<27 cm length) had significantly lower prevalence and intensity of N. surmenicola compared to older and larger fish. Pacific hake collected south of Point Conception, California (32.5 to 35°N) had lower prevalence and intensity of N. surmenicola compared to those collected in northern latitudes (35.1 to 48.4°N). Higher N. surmenicola prevalence in Pacific hake in recent years suggests food-web fluctuations in the northern California current ecosystem caused by changes in ocean transport of zooplankton or pelagic fish distributions and warrants future monitoring as a metric for ecosystem change.

Prevalence of the Nematode Hysterothylacium aduncum in the Amphipod Americorophium salmonis Consumed by Juvenile Chinook Salmon (Oncorhynchus tshawytscha) in the Columbia River Estuary

Abstract Parasites transmitted through the consumption of infected prey items are commonly used to examine patterns of host feeding. However, an estimate of the prevalence of larval parasites in consumed prey items is often lacking restricting the ability to translate the number of parasites observed into the number of prey consumed. This study examined the prevalence of the nematode parasite Hysterothylacium aduncum in the benthic amphipod Americorophium salmonis recovered from the stomachs of juvenile Chinook salmon (Oncorhynchus tshawytscha) collected near the mouth of the Columbia River estuary (USA) in May, June, and July of 2011. This study represents the first estimate of the prevalence of H. aduncum in A. salmonis from this locality. The stomachs of 118 subyearling Chinook salmon were examined for prey items. We recovered 472 undigested A. salmonis from stomachs that were then examined for juvenile H. aduncum. Six of the 472 A. salmonis were infected with H. aduncum (1.3%). However, prevalence and mean intensity of H. aduncum was 74.6% and 12.9 ± 15.0 S.D. respectively in the gastrointestinal tracts of those salmon. The low prevalence of the parasite in the ingested A. salmonis and the high recovery of adult parasites in subyearling salmon suggest salmon fed on perhaps hundreds of this prey item to acquire the observed numbers of H. aduncum as opposed to the 4.0 ± 6.2 S.D. A. salmonis found on average during stomach content examination. This reemphasizes the importance of A. salmonis as a prey item for subyearling Chinook salmon within the estuary.

Morphological and molecular characterisation of Aporocotyle margolisi Smith, 1967 (Digenea: Aporocotylidae) from the North Pacific hake Merluccius productus (Ayres) (Gadiformes: Merlucciidae) off Oregon, USA

AbstractnAporocotylid blood flukes conspecific with Aporocotyle margolisi Smith, 1967 were collected from the bulbus arteriosus of the North Pacific hake Merluccius productus (Ayres). This study revisits the morphology of A. margolisi, including drawings, measurements and scanning electron microscopy images, and provides for the first time molecular data for the large subunit of the ribosomal RNA (28S rDNA) and the mitochondrial cytochrome c oxidase subunit 1 (cox1) genes for this species. A 28S rDNA phylogenetic study of A. margolisi, and all available Aporocotyle spp., was also performed. The distribution range of A. margolisi is extended to the Pacific coast of the USA. We provide a morphological comparison of Aporocotyle spp. from the Pacific coast in North America as well as other Aporocotyle spp. infecting hake. Comparisons with the original description revealed that the new specimens of A. margolisi were considerably larger with respect to all morphological features, except for shorter spines. Molecular results showed a close relationship between A. margolisi and A. argentinensis Smith, 1969 from the Argentine hake Merluccius hubbsi Marini. The phylogenetic relationships of Aporocotyle spp. point to a possible co-speciation of hakes species and these blood fluke parasites.