Mortality of Coho Salmon (Oncorhynchus kisutch)
Associated with Burdens of Multiple Parasite Species
International Journal for Parasitology
2011
Ferguson, Jayde*
*Corresponding Author
jayde.ferguson@alaska.gov
Alaska Department of Fish and Game, Commercial Fisheries Division,
Fish Pathology Laboratory, Anchorage, Alaska
Koketsu, Wataru
Ecology and Civil Engineering Research Institute, Fukushima pref. Japan
Ninomiya, Ikuo
Laboratory of Forest Resource Biology, Ehime pref. Japan
Rossignol, Philippe A.
Department of Fisheries and Wildlive, Oregon State University
Jacobson, Kym C.
NOAA Fisheries, Northwest Fisheries Science Center, Newport, Oregon
Kent, Michael L.
Department of Microbiology, Oregon State University
This is the authors’ post-peer review version of the final article. The final published version is
copyrighted by Elsevier and can be found at:
http://www.elsevier.com/wps/find/journaldescription.cws_home/353/description#description
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Mortality of coho salmon (Oncorhynchus kisutch) associated with burdens of multiple parasite
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species
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Jayde A. Fergusona.1,*, Wataru Koketsub, Ikuo Ninomiyac, Philippe A. Rossignold, Kym C. Jacobsone,
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Michael L. Kenta
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a
Department of Microbiology, Oregon State University, 220 Nash Hall, Corvallis, Oregon 97331 USA
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b
Ecology and Civil Engineering Research Institute, Ishibatake275, Miharu-cho, Fukushima pref. 963-
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7722 Japan
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c
Laboratory of Forest Resource Biology, Faculty of Agriculture, Ehime University, Tarumi 3-5-7,
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Matsuyama, Ehime pref. 790-8566 Japan
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d
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USA
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e
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Marine Science Drive, Newport, Oregon 97365 USA
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333 Raspberry Rd., Anchorage, Alaska 99518 USA.
Department of Fisheries and Wildlife, Oregon State University, Nash Hall, Corvallis, Oregon 97331
NOAA Fisheries, Northwest Fisheries Science Center, Hatfield Marine Science Center, 2030 South
Alaska Department of Fish and Game, Commercial Fisheries Division, Fish Pathology Laboratory,
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*
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Pathology Laboratory, 333 Raspberry Rd., Anchorage, Alaska 99518 USA.
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Tel.: +1 907 267 2364; fax: +1 907 267 2194.
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E-mail address: jayde.ferguson@alaska.gov (J.A. Ferguson).
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Note: Supplementary data associated with this article.
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Corresponding author. Alaska Department of Fish and Game, Commercial Fisheries Division, Fish
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ABSTRACT
Multiple analytical techniques were used to evaluate the impact of multiple parasite species on
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the mortality of threatened juvenile coho salmon (Oncorhynchus kisutch) from the West Fork Smith
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River, Oregon, USA. We also proposed a novel parsimonious mathematical representation of
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macroparasite distribution, congestion rate, which i) is easier to use than traditional models, and ii) is
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based on Malthusian parameters rather than probability theory. Heavy infections of Myxobolus
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insidiosus (Myxozoa) and metacercariae of Nanophyetus salmincola and Apophallus sp. occurred in
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parr (subyearlings) from the lower mainstem of this river collected in 2007 and 2008. Smolts
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(yearlings) collected in 2006 - 2009 always harbored fewer Apophallus sp. with host mortality
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recognized as a function of intensity for this parasite. Mean intensity of Apophallus sp. in lower
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mainstem parr was 753 per fish in 2007 and 856 per fish in 2008, while parr from the tributaries had a
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mean of only 37 or 13 parasites per fish, respectively. Mean intensity of this parasite in smolts ranged
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between 47 - 251 parasites per fish. Over-dispersion (variance to mean ratios) of Apophallus sp. was
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always lower in smolts compared with all parr combined or lower mainstem parr. Retrospective
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analysis based on smolt data using both the traditional negative binomial truncation technique and our
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proposed congestion rate model showed identical results. The estimated threshold level for mortality
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involving Apophallus sp. was at 400 - 500 parasites per fish using both analytical methods. Unique to
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this study, we documented the actual existence of these heavy infections prior to the predicted
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mortality. Most of the lower mainstem parr (approximately 75%) had infections above this level.
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Heavy infections of Apophallus sp. metacercariae may be an important contributing factor to the high
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over-wintering mortality previously reported for these fish that grow and develop in this section of the
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river. Analyses using the same methods for M. insidiosus and N. salmincola generally pointed to
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minimal parasite-associated mortality.
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Keywords: Multispecies parasitism; Negative Binomial distribution; Truncation; Digenea; Myxozoa
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1. Introduction
Parasites may be a significant source of mortality in wild fish populations (Dobson and May,
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1987; Sindermann, 1987; Adlard and Lester, 1994; Bakke and Harris, 1998). Assessing the impact of
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parasitism on wild populations presents several significant challenges. Specifically for macroparasites,
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impacts are a function of parasite load rather than prevalence alone (Brass, 1958; Crofton, 1971; May
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and Anderson, 1979; Dobson, 1988; Burgett et al., 1990; Scott and Smith, 1994; Shaw and Dobson,
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1995; Galvani, 2003; Holt et al., 2003). Furthermore, estimates of effects are complicated by the
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aggregated distribution of parasites, as often most hosts harbor few or no parasites (Smith, 1994;
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Galvani 2003). A corollary is that heavy infections occur in few hosts, many of which may have died
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and cannot be sampled. Consequently, prevalence of infection yields at best only a weak assessment of
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macroparasite impact (Smith, 1994) and may be misleading (Dobson and Hudson, 1986).
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Lester (1984) reviewed the common methods used for estimating parasite-associated mortality
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in wild fishes, many of which require temporal observations of the same host populations. There are
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practical limitations involved in the study of hosts in an aquatic environment. For example, fish are
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often inaccessible and the most impacted fish are likely to die without detection (Bakke and Harris,
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1998). Nevertheless, there have been several studies reporting that wild fish with higher intensities of
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trematode metacercariae have a higher mortality rate (Gordon and Rau, 1982; Lemly and Esch, 1984;
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Lafferty and Morris, 1996; Jacobson et al., 2008).
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Coho salmon (Oncorhynchus kisutch) from coastal Oregon, USA are listed as threatened under
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the Endangered Species Act (US National Research Council, 1996). We previously reported on high
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loads of the digeneans Apophallus sp. (Heterophyidae) and Nanophyetus salmincola (Nanophyetidae),
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and the myxozoan Myxobolus insidiosus in parr (resident stage subyearlings) from the lower reaches of
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the West Fork Smith River, Oregon, USA (Rodnick et al., 2008). However, the older smolts (out-
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migrating yearlings) collected downstream in this river had low burdens of these same parasites
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(Ferguson et al., in press a). Parr from the lower reaches of the river also have greater than expected
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over-wintering mortality based on fisheries prediction models (Ebersole et al., 2006, 2009). Therefore,
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we hypothesized that parasites may have a role in over-wintering survival of the threatened coho
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salmon from this river.
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Studying host-parasite systems in wild salmon presents two specific challenges: i) many
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populations are listed as threatened, making it difficult to obtain large samples, and ii) parr grow and
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develop typically as separate, multiple, sub-populations and migrate to the ocean as a randomly mixed
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population of smolts, making temporal observations of the same cohort problematic. Hence, while
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numerous parasites have been described from Pacific salmon species, (Love and Moser, 1983;
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McDonald and Margolis, 1995; Hoffman, 1999), few studies have evaluated parasite-associated
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mortality involving these infections in these fish in the wild (e.g., Henricson, 1977; Halvorsen and
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Andersen, 1984; Vincent, 1996; Kocan et al., 2004; Krkosek et al., 2006; Jacobson et al., 2008).
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An alternative technique to tracking infections in cohorts over time is to conduct a retrospective
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analysis by predicting the parasite distribution in host populations based on observed data from lightly
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infected fish, as originally proposed by Crofton (1971). He demonstrated how analyzing the negative
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binomial distribution can estimate mortality associated with macroparasitism. Regarding macroparasite
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infections in wild animals, there are usually fewer heavily infected hosts than would be predicted. An
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explanation for this phenomenon is that heavily infected hosts are more predisposed to mortality.
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Crofton’s technique has become widely accepted and is used extensively in theoretical and empirical
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models (e.g., May and Anderson, 1979; Lanciani and Boyett, 1980; Anderson and May, 1982; Dobson,
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1988; Royce and Rossignol, 1990; Scott and Smith, 1994; Galvani, 2003). Crofton’s techniques rely on
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approximating the distribution. Although the statistical assay has proven reliable as a theory (Dobson
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and Carper, 1992), it is descriptive, having at best indirect biological interpretation and it is also
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somewhat arduous to perform.
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Here, we evaluated the impacts of parasites on coho salmon from parr to smolt stage from the
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West Fork Smith river by comparing parasite burdens of different age classes (parr and smolt) using
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four analytical techniques: i) comparison of parasite prevalence and intensity between life stages, ii)
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comparison of parasite over-dispersion (variance to mean ratios) between life stages, iii) a
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retrospective analysis of smolt data using the negative binomial truncation technique developed by
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Crofton (1971), and iv) our new parsimonious mathematical representation of macroparasite
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distribution, which was first reported by one of the current authors (Koketsu, 2004 M.Sc. thesis,
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Environmental correlates of parasitism in introduced threespine stickleback (Gasterosteus aculeatus)
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in the Upper Deschutes River Basin, Oregon, Oregon State University, USA). This model is based on
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the standard growth model that applies to all life rather than probability theory that is used in current
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models. No such model has been proposed since the probability-based negative binomial model of
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Crofton (1971). Based on all four analytical techniques, we conclude that parasites, especially
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Apophallus sp., have an impact on coho salmon freshwater over-winter survival.
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2. Materials and methods
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2.1. Sampling fish
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Coho salmon parr were collected by electrofishing in September, 2007 and October, 2008 from
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two general locations of the West Fork Smith River: the lower mainstem and the tributaries (see Fig. 1
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for sample sizes and exact locations). These two sections were chosen as they represent distinctly
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different habitats. The lower mainstem has been subjected to extensive logging practices that have
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simplified substrate and removed riparian vegetation, which has caused increased winter flow rates and
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high summer temperatures (Ebersole et al., 2006). In contrast, the tributaries of this system are much
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cooler during the summer and flow more slowly during the winter. An additional difference between
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these two sections of the river is parasite burden in the coho salmon, as lower mainstem parr harbor
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much higher infections than those from the tributaries (Rodnick et al., 2006; Ferguson et al., 2010).
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Wild coho salmon smolts were captured in April 2007 - 2010 (corresponding to brood years 2006 -
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2009, respectively) in a rotary screw trap downstream from the parr collecting sites (Fig. 1) and killed
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immediately for parasite evaluation. Data from many of these sampled fish have been previously used
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in our earlier studies involving different types of analyses (see Supplementary Table S1). Formal
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animal ethics approval was given by Oregon State University’s (OSU’s) Institutional Animal Care and
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Use Committee (IACUC) for the work with all animals in the present and past studies.
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2.2. Parasite evaluation
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We were particularly interested in muscle parasites due to heavy infections reported in previous
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studies in coho salmon parr from this river (Rodnick et al., 2008; Ferguson et al., 2010). One fillet was
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evaluated for each fish. Tissue squashes were prepared by squashing fillets between two 15- x 30 cm
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plexiglass plates and parasites were identified and enumerated, which were then multiplied by two in
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order to represent the number of parasites per fish. The posterior half of the kidney was similarly
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evaluated for metacercariae of N. salmincola, but counts were not multiplied to estimate the entire
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kidney because this parasite targets the posterior kidney via the renal portal system (Baldwin et al.,
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1967). Methods for identification of the metacercariae and myxozoans are described in detail in
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Ferguson et al. (2010), which included excystation of metacercariae. Adult worms of Apophallus sp.
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were also obtained from chicks that were fed metacercariae from coho salmon from this river. Chicks
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were cared for and maintained at OSU’s Laboratory Animal Resources Center and formal animal
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ethics approval for this work was given by OSU’s IACUC. These worms were consistent with
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Apophallus but did not correspond with any described species (J.A. Ferguson, unpublished data).
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Hence, we denote this worm as Apophallus sp. Prevalence (number of infected animals per total
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animals examined), mean intensity (average number of parasites per infected animal examined), and
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mean abundance (average number of parasites per animal examined, including uninfected animals) of
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infections are reported in accordance with the definitions provided by Bush et al. (1997).
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2.3. Inferring parasite-associated mortality
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2.3.1. Comparison of parasite burden
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Mean intensities of parasites in parr were compared with those of smolts with a non-parametric
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bootstrap t-test with 100,000 replications, as data were not normally distributed. Fisher’s exact tests
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were used to test differences in prevalence of parasites between parr and smolts. Data from parr from
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both river locations were pooled to represent total parr of the river to compare with out-migrating
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smolts. Samples of parr and smolts for fish from brood years 2007 and 2008 were matched for this
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analysis. Data from separate parr sub-populations were also compared with smolt data to determine
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whether the conclusions would change using this approach. All statistical procedures were performed
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with Quantitative Parasitology (Rózsa et al., 2000), significance was set at P < 0.05 and P-values are
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two-tailed.
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2.3.2. Comparison of parasite overdispersion
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Over-dispersion (variance to mean abundance ratios) of each parasite species was calculated for
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comparison between the parr (data pooled from both river locations) and smolt coho salmon life stages.
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Samples of parr and smolts for fish from brood years 2007 and 2008 were matched for this
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comparison.
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2.3.3. Crofton’s truncation model of the negative binomial distribution
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Crofton’s model has been widely accepted, so only a brief overview of this technique is
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provided (see Scott and Smith, 1994). The truncation technique estimates an overall expected host
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distribution from the low frequency classes, where lethal effects are less significant. The truncated
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curve will fit the negative binomial distribution better than the observed curve because the observed
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data will be missing hosts from the high parasite load class owing to parasite-induced mortality, and
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the difference in fitness is considered to be the parasite-induced host mortality (see Royce and
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Rossignol, 1990). The analysis of Crofton’s truncation of the negative binomial distribution was
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performed using the DOS-based software, BASICA (Ludwig, 1988). Briefly, the observed number of
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hosts was entered for each frequency class of zero to up to 10, which corresponded to different
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categorized infections (see below). An estimate of k, which is a measure of aggregation, was obtained
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through an iterative process of balancing both sides of an equation in the BASICA program, then the
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probability of finding a given number of individuals (i.e., parasites) in a sampling unit (i.e., host) was
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computed using the probability-based negative binomial equation. Instructions for using the BASICA
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program, including all equations and DOS codes, can be found in Ludwig (1988). A +1 transformation
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on all raw data was performed so that categories did not contain zero hosts. Data from smolts of brood
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years 2006-2009 were used in this analysis, except for data of N. salmincola in smolts from brood year
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2006 because kidney data were not available. Infections were categorized into groups of 100
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metacercariae per fish for Apophallus sp., 75 metacercariae per fish for N. salmincola and 200
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pseudocysts per fish for M. insidiosus to best fit the negative binomial distribution. This resulted in
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approximately 10 groups (categories of intensities), which was consistent with other studies using this
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analysis that have high intensity data (Halvorsen and Andersen, 1984; Lemly and Esch, 1984; Kang et
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al., 1985). The size of categories was chosen for two reasons: i) groups with a smaller range resulted in
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too few, and often no, data in most of the individual categories, and ii) groups with too large a range
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resulted in too few categories to properly conduct the analysis. The effects of using differently sized
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categories with each parasite were evaluated and no real difference was found (data not shown).
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The algorithm used to truncate the negative binomial distribution first estimates the maximum
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likelihood value of k (aggregation coefficient of the negative binomial distribution). Then, the expected
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distribution from zero to one of the frequency classes is estimated and compared with the observed
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distribution using a Chi-square test. If there is density-dependent mortality associated with parasitism,
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a sudden change in fit will likely occur at some point. The equations for this algorithm are standard
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and may be found in the literature (see Box 1 in Royce and Rossignol, 1990).
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2.3.4. Congestion rate model
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Koketsu (2004 M.Sc. thesis, Environmental correlates of parasitism in introduced threespine
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stickleback (Gasterosteus aculeatus) in the Upper Deschutes River Basin, Oregon, Oregon State
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University, USA) developed and validated an alternative model that may be more biologically
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meaningful because it is analogous to a population growth model. The relationship between parasite
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load and host frequency is expressed with the exponential function:
Y = ae - bx
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(1)
Where, Y = frequency of hosts (observed plots), x = number of parasites per host, a = constant
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parameter, b = constant parameter (named congestion rate), e = Euler’s constant. The congestion rate
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b, (the slope of the linearized equation, which is negative) is analogous to the intrinsic rate of growth
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of a population.
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Equation (1) was transformed into a differential equation,
dY
= −bY
dx
then divided on both sides by dt and solved for b.
(2)
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1 dY
−
Y dt
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dx
=b
dt
(3)
Equation (3) represents the per capita rate of change in parasitized hosts, − 1 dY over the rate of
Y dt
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change in parasite load class, dx . Given that b is a constant, if dx increases, then − 1 dY decreases,
dt
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Y dt
and vice versa. Furthermore, when both sides are multiplied by x:
−
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dt
1 dY
Y dt
1 dx
= bx
x dt
(4)
Equation (4) represents the ratio of − 1 dY to 1 dx in proportion to x, that is, the negative per
Y dt
x dt
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capita rate of host frequency change over the per capita rate of parasite load class change. In other
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words, when x is large, the influence or regulation of the parasite load class on both − 1 dY and 1 dx
Y dt
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x dt
becomes strong.
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The congestion rate formalizes the relationship between parasite load and host distribution in an
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equation that is analogous to one found in population dynamics. Congestion rate is itself analogous to
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the intrinsic rate of growth (frequently represented as r) of that equation. We suggest that congestion
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may be a useful index of regulation between host and macroparasite. The standard index used in
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studies of macroparasitism has been the aggregation parameter of the discrete negative binomial
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distribution, k, which is a statistical descriptor difficult to relate to population dynamics. In addition to
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a greater ease of use, our alternative interpretation can be related to standard life table equations (see
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Carey, 1993). Macroparasitism involves the interdependence of multiple hosts and different parasite
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stages, resulting in great complexity and is often counterintuitive. The interpretation of the constant b
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is therefore more complex than found in a single species population but does provide insight into the
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dynamics of macroparasitism.
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Fitting of this model to observed data and comparison of differences from predicted values were
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performed in Excel (Microsoft Office Corp., 2003) and used data on sampled smolts from brood years
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2006-2009. Categories of parasites were used as above for Crofton’s method. The basic
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methodology for this model is to graph the observed data and add an exponential trendline (and
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displayed equation), using the Excel chart wizard. The exponential equation (analogous to equation
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(1)) can then be used to generate the predicted values by substituting the number of parasites per host
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(category) into the x variable and then solving for Y (see equation (1)).
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3. Results
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3.1. Prevalence
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Although prevalence may be an incomplete metric of infection for macroparasites, we
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compared prevalences to provide additional information on parasite burden in host populations. All
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parr originating from the lower mainstem were infected with metacercariae of Apophallus sp., whereas
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prevalence was less than 40% in parr from the tributaries in both 2007 and 2008 (Table 1). Almost all
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smolts were infected with this parasite each year of the study (Table 1). Prevalence was approximately
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60% when samples from parr from the lower mainstem and tributaries were pooled. Using these
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pooled data, prevalence in the parr was significantly less (P < 0.01; Fisher’s exact test) than in smolts
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(Table 1). For N. salmincola, essentially all parr and smolts were infected (Table 1). The prevalence of
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M. insidiosus ranged from 47% to 97% with no significant differences between fish life stages, except
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between lower mainstem and tributary parr from brood year 2008 (Table 1).
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3.2. Mean intensity
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Mean intensities of infection in our samples were compared to evaluate differences in burden.
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The mean intensity of Apophallus sp. in parr was always higher in fish originating from the lower
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mainstem (Table 1). For each year that combined parr to smolt data were compared, the mean intensity
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of Apophallus sp. in smolts was approximately three to seven times lower than that of parr (P < 0.01;
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bootstrap t-test). Although we observed some overlap in the range of infection between smolt and
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parr samples, the few heavy infections in smolts did not even closely approximate those of heavily
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infected lower mainstem parr (Fig. 2). The mean intensity of N. salmincola differed (P < 0.01;
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bootstrap t-test) in parr from the lower mainstem and tributaries for brood year 2007, but not 2008
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(Table 1). Smolts had a higher mean intensity of N. salmincola than parr, which was statistically
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significant only for brood year 2007 (P < 0.02; bootstrap t-test). The mean intensity of M. insidiosus
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was higher in parr from the lower mainstem than parr from the tributaries, which was significant only
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for brood year 2008 (P < 0.03; bootstrap t-test). Smolts had the same infection level as combined parr
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for both years (Table 1). Overall, the most prominent difference in parasite burden was with
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Apophallus sp., as smolts always had a lower mean intensity compared with parr, with lower mainstem
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fish harboring the most metacercariae.
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3.3. Variance to mean ratio
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Over-dispersion (variance to mean abundance ratio) was evaluated as another indicator of
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parasite-associated mortality. The variance to mean abundance ratio of Apophallus sp. in parr was
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approximately three times higher than that of smolts of the same brood year for both years (Table 1).
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The over-dispersion was influenced by infections in the lower mainstem parr because they had high
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mean intensities compared with parr from the tributaries (Table 1), which increased the variance of the
268
data set. Thus the higher over-dispersion of Apophallus sp. in the lower mainstem parr subset
269
compared with smolts was less pronounced. For the second year, the tributary parr had such a low
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prevalence and intensity of Apophallus sp. infections that it resulted in a low variance to mean
271
abundance ratio. With N. salmincola, the variance to mean abundance ratio was lower in parr
272
compared with smolts. Lastly, the variance to mean abundance ratio of M. insidiosus was similar
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between parr and smolts (Table 1). Of all three parasites, the most dramatic difference between parr
274
and smolts was with Apophallus sp.
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3.4. Truncation of negative binomial model
276
A retrospective technique to was applied to compare observed and expected parasite distributions
277
and thus estimate a ‘threshold’ of parasite-associated mortality. For this analysis, data was included for
278
all available smolts (i.e., from brood years 2006-2009), which increased our sample size and was
279
permissible because we were not making direct comparisons with parr of the same year classes.
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Analysis of data from all three parasites predicted that the parasite distribution in smolts was truncated
281
(Table 2; Fig. 3). The truncation was calculated to occur within the first few infection categories (Table
282
2; Fig. 3A, C, E), particularly for N. salmincola and M. insidiosus. However the truncation point was
283
actually more towards the tail end of the distributions in that the majority of fish had an abundance of
284
infection below the truncation point (i.e., to the left; see Fig. 3A, C, E). Regarding parasite
285
aggregation, N. salmincola was much less aggregated (k value above 1.0) than Apophallus sp. and M.
286
insidiosus (k values of approximately 0.2) (Table 2).
287
Analysis of our data fitted to the negative binomial distribution indicated that the threshold for
288
parasite-associated mortality began at approximately 400 and 150 parasites per fish for metacercariae
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of Apophallus sp. and N. salmincola (Fig. 3A, C), respectively, and 200 parasites per fish for
290
pseudocysts of M. insidiosus (Fig. 3E). Using these threshold data, we determined the percentage of
291
infected fish above this threshold. For Apophallus sp., approximately 10% of smolts had burdens
292
above this level. Data for parr were available, which represented hosts sampled prior to any potential
293
parasite-associated mortality in general. This allowed us to assign estimates to the proportion of
294
heavily infected fish linked to mortality by parasitism. Approximately 75% of lower mainstem parr
295
and only 1% of parr from the tributaries had infections of Apophallus sp. greater than this value. In
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296
contrast, approximately 31% of smolts had N. salmincola above this threshold, whereas only 14%
297
and 6% of lower mainstem and tributary parr, respectively, were above this value. With M. insidiosus,
298
approximately 18% of smolts were above the threshold and 22% and 10% of lower mainstem and
299
tributary parr, respectively, were above this level. Based on these analyses, Apophallus sp. was the
300
parasite most closely associated with host over-winter mortality, as essentially all of the lower
301
mainstem parr had infection levels above the predicted threshold and those high infections were
302
consistently not detected in smolt samples over a 4 year period.
303
3.5. Truncation of congestion rate model
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A similar retrospective technique has been included to augment current results and to provide a
305
simpler analysis that may be more biologically meaningful. The newly proposed congestion rate model
306
provided identical results to the negative binomial method regarding the location of the predicated
307
location for truncation (Table 2; Fig. 3).
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4. Discussion
309
Studying the impacts of parasites in wild populations is difficult due to the nature of chronic
310
infections being sublethal (McCallum and Dobson, 1995). Such studies involving fish populations are
311
often further complicated due to their inaccessibility, especially for migratory species such as salmon
312
(Bakke and Harris, 1998). Prior knowledge of the West Fork Smith River being separated into areas
313
with heavily and lightly infected rearing parr (Rodnick et al., 2008; Ferguson et al., 2010) was a
314
benefit to the current study. Multiple analytical techniques were used to evaluate parasite-associated
315
mortality and results from all of the different analyses indicated that parasites were associated with
316
over-winter mortality of juvenile coho salmon in this river. This was particularly evident with
317
Apophallus sp. infections in lower mainstem fish. The dramatic difference in intensity and over-
16
318
dispersion of Apophallus sp. between parr and smolts indicated that the heavily infected lower
319
mainstem fish did not survive to the smolt stage in either year.
320
The use of a retrospective analytical technique with migratory species, such as salmon, is
321
particularly useful. This technique requires only one sampling time point and thus avoids the inherent
322
difficulties with sampling the same population of salmon throughout different life stages. However, to
323
our knowledge there are few available reports using this approach with salmonid fishes i.e., Arctic
324
char (Salvelinus alpinus) infected with Diphyllobothrium spp. (Henricson, 1977; Halvorsen and
325
Andersen, 1984). The predicted threshold of parasite-associated mortality for Apophallus sp. was
326
approximately 400 metacercariae per fish using Crofton’s method (Crofton, 1971). It was remarkable
327
that our new congestion model provided identical results. These findings, together with our previous
328
comparison using the same data set from Crofton (1971) (Koketsu, 2004 M.Sc. thesis, Environmental
329
correlates of parasitism in introduced threespine stickleback (Gasterosteus aculeatus) in the Upper
330
Deschutes River Basin, Oregon, Oregon State University, USA), further indicate that similar results
331
were obtained with both models.
332
Most studies using retrospective analyses, such as Crofton’s technique, only provide a
333
prediction of the number of heavily infected animals that should have theoretically existed before death
334
(Lanciani and Boyett, 1980; Burgett et al., 1990; Royce and Rossignol, 1990). Thus a unique aspect of
335
our study is that by sampling lower mainstem parr, we actually documented the existence of heavily
336
infected hosts above the threshold predicted with smolt data. Natural, presumably sustainable, wild
337
populations typically have only a small percentage of hosts that occur above the truncation point and
338
hence parasite-associated mortality seldom threatens an entire population. Most of the lower mainstem
339
fish, however, were above this threshold level. Indeed, some mortality may have even occurred earlier
340
for these fish, based on their relatively low variance to mean abundance ratios of Apophallus sp., and it
17
341
would be interesting to evaluate fry (early summer) fish compared with parr (late summer/autumn)
342
fish from this system.
343
The threshold for parasite-associated mortality indicates the level of infection where mortality
344
begins to occur, but due to the dynamic nature of the process not every fish will die from infection at
345
the tested time point. Typically this occurs towards the tail end of the distribution, which was not the
346
case with our analysis using categorized data. However, Kang et al. (1985) obtained similar results
347
using categories of 50 metacercariae per fish. Nevertheless, with almost 75% of the lower mainstem
348
parr having heavy Apophallus sp. infections above this level, we can conclude that most of these fish
349
die during the late fall or winter before smoltification. This is reflected by the absence of heavy
350
infections in smolt stage fish. In comparison, there were very few parr from the tributaries with
351
infections above this level (only one fish from 176 sampled), suggesting that fish surviving to the
352
smolt stage are over-represented by parr originating from the tributaries. Admittedly, combining data
353
from two separate parr subpopulations has an inherent problem i.e. assuming this population provides
354
the actual representation of parr to compare with the mixed smolt population. However, we emphasize
355
that this is a general limitation of evaluating parasite-related mortality in salmonids, which is
356
particularly problematic for endangered or threatened species for which scientific samples are very
357
limited.
358
Myxobolus insidiosus was also indicated to be associated with over-winter mortality but much
359
less so than Apophallus sp. Anderson and May (1979) defined microparasites as organisms that
360
reproduce directly in the invaded individual host, usually induce long lasting immunity to reinfection
361
and typically cause transient infections (e.g., bacteria and viruses). In contrast, macroparasites do not
362
multiply within a host (the load is thus determined by invasion events), generally elicit a short-term
363
immune response and cause chronic infections associated with a long life expectancy of the parasite
364
(e.g., helminths). Myxobolus insidiosus is a metazoan parasite but it has features of a microparasite in
18
365
that asexual reproduction occurs in the fish host. However, this species is also similar to a
366
macroparasite in that plasmodial pseudocysts, which grow in size due to the proliferation of a single
367
progenitor cell, do not increase in number within the host. Also, with histozoic species such as M.
368
insidiosus, infection persists throughout the juvenile life stages of the fish host (Ferguson et al., 2010).
369
Therefore, the models used to observe a decrease in parasite burden over time to infer parasite-
370
associated mortality were appropriate for the current study. Mean intensity decreased significantly
371
between parr and smolts and over-dispersion was lower in the latter. Truncation models indicated that
372
parasite-associated mortality occurred and approximately 20% of parr were above the predicted
373
threshold level. To our knowledge, this is the first study to evaluate myxozoans with these
374
macroparasite techniques. Nanophyetus salmincola infection was the least linked to parasite-associated
375
mortality, as mean intensity and over-dispersion of this parasite actually increased from parr to smolt
376
stage, and the percentage of parr above the predicted threshold level was low. Jacobson et al. (2008)
377
used the former two techniques and showed that N. salmincola was associated with mortality in coho
378
salmon during early ocean residency.
379
Ebersole et al. (2006) reported poor survival (ca. 2%) for fish from the lower mainstem of this
380
river but concluded this was due to abiotic factors such as poor habitat. However, this could in turn be
381
related to the heavy infection levels associated with mortality in our study, as the production of
382
digenean trematodes and their intermediate hosts increases with elevated temperature (Poulin, 2006).
383
The extensively logged lower mainstem of this river often exceeds 20° C during summer (Ebersole et
384
al., 2006) and Cairns et al. (2005) found a positive correlation between temperature and neascus
385
metacercariae in the skin (black spot) of coho salmon at the same location. The intermediate snail hosts
386
of Apophallus spp. in Oregon are Fluminicola spp. (Niemi and Macy, 1974; Villeneuve et al., 2005)
387
and Apophallus sp. from the West Fork Smith River can utilize snails from the genera Fluminicola and
388
Juga (Ferguson et al., in press b). Perhaps the increased temperature in the lower mainstem of this
19
389
system enhances these snail populations, which would in turn increase parasite transmission to fish
390
at this location.
391
Apophallus sp.-associated mortality is most likely indirect. In support of this, Ferguson et al.
392
(2010) held coho salmon from the lower and upper mainstem of this river in laboratory tanks and only
393
four of approximately 50 lower mainstem fish died early in the study. However, during winter high
394
flow rates occur in the lower mainstem of this river due to simplified substrate, which may displace
395
fish and account for high over-winter mortality of coho salmon from this section of this river (Ebersole
396
et al., 2006, 2009). Certain parasites may decrease the swimming performance of heavily infected fish,
397
which would exacerbate this phenomenon. Apophallus brevis is associated with reduced growth of
398
yellow perch (Perca flavescens) (Johnson and Dick, 2001) and we have found a similar association
399
with Apophallus infections in coho salmon from the West Fork Smith River (Ferguson et al., in press
400
b). Consequently, smaller salmonids have reduced swimming performance (Taylor and McPhail,
401
1985; Ojanguren and Brana, 2003), which in turn may also decrease predator avoidance (Taylor and
402
McPhail, 1985). Heavily Apophallus-infected lower mainstem coho salmon from this river were
403
associated not only with reduced growth but also decreased swimming performance and
404
osmocompetence (Ferguson et al., in press b), both of which could severely impact survival of
405
outmigrating smolts in the estuarine environment. An Apophallus sp. identified as Apophallus donicus
406
experimentally develops in both avain and mammalian hosts (Niemi and Macy, 1974) and naturally
407
infects gulls (Shaw, 1947). West Fork Smith River resides near a national wildlife refuge that could
408
provide a source of various piscivorous birds to prey upon heavily parasitized fish in this river
409
(Ferguson et al., in press b). When taken together, coho salmon from the lower mainstem of this river
410
are subjected to warmer summer temperatures, higher winter flow rates and higher levels of parasitism
411
than fish from the upstream tributaries, all of which may contribute to a poorer over-winter survival of
412
these fish compared with those from the tributaries.
20
413
The ‘source-sink’ is a well recognized paradigm in population ecology, where a certain
414
species may persist in a deficient habitat due to immigration from nearby rich ‘source’ habitats (Holt
415
and Hochberg, 2002). Holt and Hochberg (2002) present theoretical models on how pathogens could
416
drive this relationship. In our coho salmon system, the sink is the lower mainstem, which is driven by
417
heavy parasite burdens, and new fish are derived mostly from brood fish that originally grew as parr in
418
the tributaries of the same river, i.e., the source. Some salmon have developed genetic strains that are
419
resistant or resilient to other parasite infections when those occur in endemic watersheds
420
(Bartholomew, 1998; Gilbey et al., 2006), and this has even been reported with N. salmincola infecting
421
different strains of cutthroat trout (Oncorhynchus clarkii clarkii) (Baldwin et al., 1967). As very few of
422
the coho salmon from the lower mainstem survive to the smolt stage or even to sexual maturity, these
423
fish contribute very little to the genetic structure of this coho salmon population. This would negate the
424
possibility for genetic pressure for the development of resilience to the parasites in this river, which is
425
consistent with the theory that there are constraints to adaptive evolution to sink conditions (Holt and
426
Hochberg, 2002). Most Pacific salmon populations do not have genetic separation between nearby
427
rivers, let alone within a river (Johnson and Bank, 2008). We conclude that the parents of the lower
428
mainstem parr are almost always derived from regions of the river with little genetic pressure to
429
develop resilience to parasitism, thus resulting in a constant pool of susceptible fish in the lower
430
mainstem.
431
In conclusion, we have shown that metazoan parasites, especially Apophallus sp., are
432
associated with over-winter mortality of juvenile coho salmon. Fish from the lower mainstem were
433
heavily parasitized and the level of mortality associated with parasitism indicated in our analysis
434
approximates previous reports of estimated mortality of these fish in this section of the West Fork
435
Smith River. Our results stress the importance of examining parasitism as a potential limiting factor for
436
threatened populations. Several other coastal rivers in the Pacific Northwest also contain Endangered
21
437
Species Act listed coho salmon and our analytical techniques could be applied to these systems.
438
Understanding why certain salmon populations are heavily infected with these parasites, likely due to
439
landscape characteristics, would provide useful data for management or recovery planning. Lastly, our
440
newly proposed model for inferring parasite-associated mortality may be applied to many host-parasite
441
systems and is a significant contribution to the field of parasitology because a biological basis of
442
macroparasitism is more parsimonious and intuitive than a statistical one.
443
Acknowledgements
444
This research was funded, in most part, by an Oregon Department of Fish and Wildlife
445
(ODFW), USA, Fish Health Graduate Research fellowship (agency grant 010-7032-IAA-FISH) to
446
J.A.F. We would also like to thank J. Sanders, C. Ferguson and the research personnel at ODFW for
447
assistance in gathering field samples. The concept of congestion rate was originally developed by I.
448
Ninomiya, Ehime University, Japan. Thanks to K. Lafferty and E. Casillas for manuscript review and
449
comments.
450
22
451
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585
Figure legends
586
587
Fig. 1. Map of West Fork Smith River, Oregon, USA showing sampling sites for coho salmon
588
(Oncorhynchus kisutch) parr (indicated by boxes) from brood year (BY) 2007 and 2008 from the
589
tributaries and lower mainstem,and outmigrating smolts (Smolt Trap). Sample sizes of all parr and
590
smolt samples are also shown.
591
592
Fig. 2. Frequency distributions of Apophallus sp. infections in coho salmon (Oncorhynchus kisutch)
593
smolts, lower mainstem parr and tributary parr from West Fork Smith River, Oregon, USA. Data from
594
all years of the study were pooled for each group. Triangle = smolts, square = lower mainstem parr,
595
diamond = tributary parr.
596
597
Fig. 3. Categorized frequency distributions of parasites infecting coho salmon (Oncorhynchus kisutch)
598
smolts from West Fork Smith River, Oregon, USA fitted to either the negative binomial distribution or
599
the congestion rate. Apophallus sp. metacercariae (A, B), Nanophyetus salmincola metacercariae (C,
600
D) and Myxobolus insidiosus pseudocysts (E, F) using the negative binomial distribution truncation
601
technique (A, C, E) compared with the congestion rate model (B, D, F). Triangle = observed, square =
602
predicted, arrow = threshold where parasite-associated mortality is predicted to initially occur as
603
indicated by comparing predicted and truncated observed distributions. Note the different scales for
604
each type of parasite.
1
Table 1. Prevalence (%), mean intensity and over-dispersion (variance to mean abundance ratio; S2/x) of Apophallus sp. in muscle,
Nanophyetus salmincola in muscle and kidney, and Myxobolus insidiosus in muscle from coho salmon parr (subyearlings) from the Lower
mainstem and Tributary groups, and outmigrant smolts (yearlings) of West Fork Smith River, Oregon, USA.
Apophallus sp.
Groups
N. salmincola
M. insidiosus
n
%
Mean intensity
(95% CI)
S2/x
%
Mean intensity
(95% CI)
S2/x
%
Mean intensity
(95% CI)
S2/x
Smolts
20
95
47 (24-123)
171
100
43 (29-61)d
32
75
18 (11-30)
24
Brood Year 2007
Lower mainstem Parr
Tributary Parr
58
76
100a
37b
753 (656-870)a
37 (6-110)b
237
380
100a
100a
123 (105-146)a
52 (46-58)b
50
14
84a
86a
487 (320-824)a
300 (217-424)a
1481
643
134
29
64c
100a
520 (423-636)c
77 (42-138)b
647
208
100a
97a
83 (73-95)c
158 (110-220)a
52
143
85a
79a
380 (291-535)a
409 (210-753)a
1113
1096
70
100
100a
30b
856 (695-1,107)a
13 (6-25)b
881
54
100a
99a
103 (89-121)a
124 (106-142)a,b
45
70
97a
47b
313 (215-494)a
136 (72-287)b
998
878
170
30
59c
93a
603 (465-786)a
191 (115-329)c
1367
415
99a
100a
113 (102-126)a,b
161 (125-210)b
61
88
68c
63b,c
241 (176-366)a,b
221 (108-422)a,b
1049
575
31
100
251 (153-393)
467
97
190 (141-255)
141
81
482 (311-774)
777
Brood Year 2006
Combined Parr
(Lower mainstem + Tributary)
Smolts
Brood Year 2008
Lower mainstem Parr
Tributary Parr
Combined Parr
(Lower mainstem + Tributary)
Smolts
Brood Year 2009
Smolts
The prevalence and mean intensity of infection (95% confidence intervals, (95% CI)) were tested among parr (Lower mainstem, Tributary,
and Combined) and smolt groups for brood year 2007 and 2008. a-c = different letters represent significant differences (P < 0.05), if any parr
group or the smolts from a given brood year share the same letter, then there was no significant difference between those groups. d = only
muscle data were available.
Table 2. Categorized frequency distribution of parasites infecting coho salmon (Oncorhynchus
kisutch) smolts from West Fork Smith River, Oregon, USA fitted to either the negative binomial
distribution or the congestion rate model.
No. Parasites
Observed
Crofton
Predicted
Congestion
Predicted
Apophallus sp.
0-100
79
79
13.12
101-200
10
13.99
10.53
201-300
7
7.48
8.45
301-400
7
4.89
6.78
5.44 a
401-500
1
3.49a
501-600
4
2.62
4.37
601-700
2
2.03
3.50
701-800
1
1.6
2.81
kb
NA
0.2256
NA
Nanophyetus salmincola
0-75
32
32
30.85
76-150
27
22.95
21.21
a
151-225
8
15.52
14.57 a
226-300
10
10.29
10.02
301-375
8
6.76
6.88
376-450
6
4.41
4.73
451-525
5
2.86
3.25
526-600
1
1.85
2.23
601-675
2
1.2
1.54
676-750
1
2.16
1.06
kb
NA
1.1275
NA
Myxobolus insidiosus
0-200
84
84
14.14
a
11.35 a
201-400
8
12.61
401-600
6
6.68
9.11
601-800
4
4.39
7.31
801-1000
3
3.16
5.87
1001-1200
4
2.4
4.71
1201-1400
3
1.88
3.78
1401-1600
3
1.51
3.03
1601-1800
2
1.23
2.43
1801-2000
2
1.01
1.95
kb
NA
0.1697
NA
a
Threshold where parasite associated mortality is predicted to initially occur as indicated by
comparing predicted and continually truncated observed distributions.
b
The k value is an inverse measure of aggregation for the negative binomial distribution.
NA, Not applicable. Supplementary Table S1. Raw data obtained from coho salmon (Oncorhynchus kisutch) from West Fork
Smith River, Oregon, USA used in this study. Parasite counts are shown for Apophallus sp.,
Nanophyetus salmincola and Myxobolus insidiosus for each fish. Fish are grouped according to brood
year (yr.), river site of residence and life stage.
Sample
No.
a
183
a
184
a
185
a
186
a
187
a
188
a
189
a
190
a
191
a
192
a
193
a
194
a
195
a
196
a
197
a
198
a
199
a
200
a
201
a
202
b
207
b
208
b
209
b
210
b
211
b
226
b
227
b
228
b
229
b
230
b
231
b
232
b
234
b
235
b
237
b
248
b
251
b
253
b
255
Fish group
(brood yr., river site, life stage)
2006, Migrant, Smolt
2006, Migrant, Smolt
2006, Migrant, Smolt
2006, Migrant, Smolt
2006, Migrant, Smolt
2006, Migrant, Smolt
2006, Migrant, Smolt
2006, Migrant, Smolt
2006, Migrant, Smolt
2006, Migrant, Smolt
2006, Migrant, Smolt
2006, Migrant, Smolt
2006, Migrant, Smolt
2006, Migrant, Smolt
2006, Migrant, Smolt
2006, Migrant, Smolt
2006, Migrant, Smolt
2006, Migrant, Smolt
2006, Migrant, Smolt
2006, Migrant, Smolt
Apophallus sp.
per fish
0
68
52
8
14
32
28
10
400
96
16
40
16
42
18
6
2
10
20
10
N. salmincola per
fish
4
114
16
12
20
30
36
6
118
56
44
84
20
112
48
26
8
32
60
14
M. insidiosus per
fish
14
0
0
16
2
0
18
0
60
26
8
0
24
6
8
2
14
4
58
4
2007, Lower mainstem, Parr
2007, Lower mainstem, Parr
2007, Lower mainstem, Parr
2007, Lower mainstem, Parr
2007, Lower mainstem, Parr
2007, Lower mainstem, Parr
2007, Lower mainstem, Parr
2007, Lower mainstem, Parr
2007, Lower mainstem, Parr
2007, Lower mainstem, Parr
2007, Lower mainstem, Parr
2007, Lower mainstem, Parr
2007, Lower mainstem, Parr
2007, Lower mainstem, Parr
2007, Lower mainstem, Parr
2007, Lower mainstem, Parr
2007, Lower mainstem, Parr
2007, Lower mainstem, Parr
2007, Lower mainstem, Parr
1412
912
1914
1022
1300
1178
692
960
2068
972
802
750
340
832
498
546
406
248
540
105
67
205
128
91
91
41
63
216
143
109
124
53
138
56
150
291
91
76
94
40
218
826
28
16
542
384
1012
258
334
0
2
60
0
97
1780
124
31
b
256
b
259
b
260
b
262
b
265
b
266
b
269
b
270
b
272
b
275
b
279
b
284
b
285
b
290
b
291
b
293
b
300
b
305
b
309
b
312
b
316
b
317
b
328
b
329
b
330
b
331
b
332
b
333
b
334
b
343
b
344
b
345
b
243
b
241
b
242
b
244
b
245
b
246
b
247
b
212
b
213
b
214
b
215
b
216
b
217
b
218
2007, Lower mainstem, Parr
2007, Lower mainstem, Parr
2007, Lower mainstem, Parr
2007, Lower mainstem, Parr
2007, Lower mainstem, Parr
2007, Lower mainstem, Parr
2007, Lower mainstem, Parr
2007, Lower mainstem, Parr
2007, Lower mainstem, Parr
2007, Lower mainstem, Parr
2007, Lower mainstem, Parr
2007, Lower mainstem, Parr
2007, Lower mainstem, Parr
2007, Lower mainstem, Parr
2007, Lower mainstem, Parr
2007, Lower mainstem, Parr
2007, Lower mainstem, Parr
2007, Lower mainstem, Parr
2007, Lower mainstem, Parr
2007, Lower mainstem, Parr
2007, Lower mainstem, Parr
2007, Lower mainstem, Parr
2007, Lower mainstem, Parr
2007, Lower mainstem, Parr
2007, Lower mainstem, Parr
2007, Lower mainstem, Parr
2007, Lower mainstem, Parr
2007, Lower mainstem, Parr
2007, Lower mainstem, Parr
2007, Lower mainstem, Parr
2007, Lower mainstem, Parr
2007, Lower mainstem, Parr
2007, Lower mainstem, Parr
2007, Lower mainstem, Parr
2007, Lower mainstem, Parr
2007, Lower mainstem, Parr
2007, Lower mainstem, Parr
2007, Lower mainstem, Parr
2007, Lower mainstem, Parr
797
302
558
304
1406
262
1005
354
352
1157
1814
940
1065
610
409
989
593
430
592
439
475
1010
806
1158
373
825
816
760
373
1027
343
490
942
168
803
430
432
200
474
83
220
352
175
113
59
79
128
131
101
274
212
81
61
137
41
51
75
75
86
44
69
88
335
323
53
121
61
104
237
189
93
118
194
120
90
30
39
57
409
0
0
724
113
0
19
48
70
630
60
1714
2479
1133
1392
0
391
21
7
188
341
88
0
51
100
0
331
572
4856
28
39
92
128
106
879
0
258
204
558
2007, Tributary, Parr
2007, Tributary, Parr
2007, Tributary, Parr
2007, Tributary, Parr
2007, Tributary, Parr
2007, Tributary, Parr
2007, Tributary, Parr
2
4
6
0
6
6
0
55
27
80
49
71
20
120
124
110
94
66
136
62
4
b
219
b
220
b
221
b
222
b
223
b
224
b
225
b
249
b
250
b
252
b
254
b
257
b
258
b
261
b
263
b
264
b
267
b
268
b
271
b
273
b
274
b
276
b
277
b
278
b
280
b
281
b
282
b
283
b
286
b
287
b
288
b
289
b
292
b
294
b
295
b
296
b
297
b
298
b
299
b
301
b
302
b
303
b
304
b
306
b
307
b
308
2007, Tributary, Parr
2007, Tributary, Parr
2007, Tributary, Parr
2007, Tributary, Parr
2007, Tributary, Parr
2007, Tributary, Parr
2007, Tributary, Parr
2007, Tributary, Parr
2007, Tributary, Parr
2007, Tributary, Parr
2007, Tributary, Parr
2007, Tributary, Parr
2007, Tributary, Parr
2007, Tributary, Parr
2007, Tributary, Parr
2007, Tributary, Parr
2007, Tributary, Parr
2007, Tributary, Parr
2007, Tributary, Parr
2007, Tributary, Parr
2007, Tributary, Parr
2007, Tributary, Parr
2007, Tributary, Parr
2007, Tributary, Parr
2007, Tributary, Parr
2007, Tributary, Parr
2007, Tributary, Parr
2007, Tributary, Parr
2007, Tributary, Parr
2007, Tributary, Parr
2007, Tributary, Parr
2007, Tributary, Parr
2007, Tributary, Parr
2007, Tributary, Parr
2007, Tributary, Parr
2007, Tributary, Parr
2007, Tributary, Parr
2007, Tributary, Parr
2007, Tributary, Parr
2007, Tributary, Parr
2007, Tributary, Parr
2007, Tributary, Parr
2007, Tributary, Parr
2007, Tributary, Parr
2007, Tributary, Parr
2007, Tributary, Parr
0
2
4
0
342
0
2
0
0
19
19
0
0
0
0
0
529
0
0
0
0
0
0
0
0
4
0
0
0
6
0
5
0
0
0
2
0
2
10
4
2
3
0
7
0
4
105
82
62
79
52
72
52
49
34
68
100
29
77
56
85
58
46
70
53
80
15
28
16
41
43
18
28
21
44
39
39
61
36
56
23
104
43
77
55
89
23
21
18
56
99
96
268
44
6
46
464
4
104
894
80
728
0
1084
806
5
1043
130
172
462
305
0
6
383
495
0
0
0
0
284
349
0
138
1540
4
35
0
0
76
20
361
20
0
58
76
0
8
15
b
310
b
311
b
313
b
314
b
315
b
318
b
319
b
320
b
321
b
322
b
323
b
324
b
325
b
326
b
327
b
335
b
336
b
337
b
338
b
339
b
340
b
341
b
342
2007, Tributary, Parr
2007, Tributary, Parr
2007, Tributary, Parr
2007, Tributary, Parr
2007, Tributary, Parr
2007, Tributary, Parr
2007, Tributary, Parr
2007, Tributary, Parr
2007, Tributary, Parr
2007, Tributary, Parr
2007, Tributary, Parr
2007, Tributary, Parr
2007, Tributary, Parr
2007, Tributary, Parr
2007, Tributary, Parr
2007, Tributary, Parr
2007, Tributary, Parr
2007, Tributary, Parr
2007, Tributary, Parr
2007, Tributary, Parr
2007, Tributary, Parr
2007, Tributary, Parr
2007, Tributary, Parr
0
0
6
0
9
0
0
0
0
0
0
0
0
0
0
2
0
0
6
13
0
0
0
24
68
51
23
67
19
35
32
7
33
66
46
39
60
48
14
38
15
20
73
45
95
98
373
338
96
286
92
29
128
192
17
710
56
24
110
609
2046
150
15
159
64
1055
187
1602
28
346
347
348
349
350
351
352
353
354
355
356
357
358
359
360
361
362
363
364
365
366
367
368
369
2007, Migrant, Smolt
2007, Migrant, Smolt
2007, Migrant, Smolt
2007, Migrant, Smolt
2007, Migrant, Smolt
2007, Migrant, Smolt
2007, Migrant, Smolt
2007, Migrant, Smolt
2007, Migrant, Smolt
2007, Migrant, Smolt
2007, Migrant, Smolt
2007, Migrant, Smolt
2007, Migrant, Smolt
2007, Migrant, Smolt
2007, Migrant, Smolt
2007, Migrant, Smolt
2007, Migrant, Smolt
2007, Migrant, Smolt
2007, Migrant, Smolt
2007, Migrant, Smolt
2007, Migrant, Smolt
2007, Migrant, Smolt
2007, Migrant, Smolt
2007, Migrant, Smolt
54
16
10
6
140
4
298
510
12
196
14
62
4
10
352
266
52
20
12
14
8
14
24
20
117
35
19
4
367
128
302
381
224
406
15
388
60
70
86
252
59
23
0
38
36
23
497
281
0
30
24
0
1610
216
2414
1168
1358
56
28
2
0
772
90
162
0
8
4
30
324
4
334
12
370
371
372
373
374
c
418
c
420
c
421
c
422
c
427
c
430
c
431
c
432
c
433
c
434
c
435
c
436
c
437
c
439
c
446
c
447
c
448
c
449
c
450
c
451
c
452
c
453
c
454
c
455
c
456
c
457
c
458
c
460
c
462
c
463
c
464
c
465
c
466
c
467
c
468
c
469
c
470
c
471
c
472
c
473
c
474
2007, Migrant, Smolt
2007, Migrant, Smolt
2007, Migrant, Smolt
2007, Migrant, Smolt
2007, Migrant, Smolt
16
6
4
16
72
209
128
8
68
188
678
0
8
68
0
2008, Lower mainstem, Parr
2008, Lower mainstem, Parr
2008, Lower mainstem, Parr
2008, Lower mainstem, Parr
2008, Lower mainstem, Parr
2008, Lower mainstem, Parr
2008, Lower mainstem, Parr
2008, Lower mainstem, Parr
2008, Lower mainstem, Parr
2008, Lower mainstem, Parr
2008, Lower mainstem, Parr
2008, Lower mainstem, Parr
2008, Lower mainstem, Parr
2008, Lower mainstem, Parr
2008, Lower mainstem, Parr
2008, Lower mainstem, Parr
2008, Lower mainstem, Parr
2008, Lower mainstem, Parr
2008, Lower mainstem, Parr
2008, Lower mainstem, Parr
2008, Lower mainstem, Parr
2008, Lower mainstem, Parr
2008, Lower mainstem, Parr
2008, Lower mainstem, Parr
2008, Lower mainstem, Parr
2008, Lower mainstem, Parr
2008, Lower mainstem, Parr
2008, Lower mainstem, Parr
2008, Lower mainstem, Parr
2008, Lower mainstem, Parr
2008, Lower mainstem, Parr
2008, Lower mainstem, Parr
2008, Lower mainstem, Parr
2008, Lower mainstem, Parr
2008, Lower mainstem, Parr
2008, Lower mainstem, Parr
2008, Lower mainstem, Parr
2008, Lower mainstem, Parr
2008, Lower mainstem, Parr
2008, Lower mainstem, Parr
2008, Lower mainstem, Parr
4666
3984
1098
2868
2472
2004
2644
870
296
518
1918
724
204
1324
1322
78
434
420
1030
522
586
268
652
596
984
528
224
1542
1282
1394
248
1238
76
610
1858
372
208
540
792
182
208
25
75
96
46
48
236
147
83
223
74
111
117
115
212
69
40
206
88
119
85
74
76
53
65
121
66
28
81
95
133
163
283
118
278
72
117
64
37
69
37
62
46
106
334
98
16
30
54
958
232
72
32
42
40
188
390
52
98
66
0
58
654
210
56
162
1758
52
58
76
46
538
948
78
32
24
3454
1502
322
88
32
78
8
c
475
c
476
c
477
c
478
c
479
c
480
c
481
c
482
c
483
c
484
c
486
c
487
c
488
c
489
c
490
c
491
c
492
c
493
c
494
c
495
c
496
c
497
c
498
c
499
c
500
c
501
c
502
c
503
c
504
c
415
c
416
c
417
c
419
c
423
c
424
c
425
c
426
c
428
c
591
c
592
c
505
c
506
c
507
c
508
c
509
c
510
2008, Lower mainstem, Parr
2008, Lower mainstem, Parr
2008, Lower mainstem, Parr
2008, Lower mainstem, Parr
2008, Lower mainstem, Parr
2008, Lower mainstem, Parr
2008, Lower mainstem, Parr
2008, Lower mainstem, Parr
2008, Lower mainstem, Parr
2008, Lower mainstem, Parr
2008, Lower mainstem, Parr
2008, Lower mainstem, Parr
2008, Lower mainstem, Parr
2008, Lower mainstem, Parr
2008, Lower mainstem, Parr
2008, Lower mainstem, Parr
2008, Lower mainstem, Parr
2008, Lower mainstem, Parr
2008, Lower mainstem, Parr
2008, Lower mainstem, Parr
2008, Lower mainstem, Parr
2008, Lower mainstem, Parr
2008, Lower mainstem, Parr
2008, Lower mainstem, Parr
2008, Lower mainstem, Parr
2008, Lower mainstem, Parr
2008, Lower mainstem, Parr
2008, Lower mainstem, Parr
2008, Lower mainstem, Parr
412
322
456
1360
446
426
286
546
122
492
1736
456
284
468
784
304
1034
682
326
946
202
66
1462
158
526
476
184
558
632
80
85
63
120
56
22
93
41
45
54
208
113
274
59
125
24
90
43
146
41
66
327
89
47
87
167
42
164
118
46
956
0
114
734
466
502
40
210
64
94
16
116
1842
56
20
252
212
234
26
192
12
62
32
1060
152
76
398
202
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
6
0
0
0
0
0
14
20
6
42
82
0
2
0
0
0
0
230
116
204
0
76
148
88
14
82
94
118
154
54
44
107
69
70
0
400
166
152
0
112
134
458
0
98
204
1854
1356
0
0
4
0
c
511
c
512
c
513
c
514
c
515
c
516
c
517
c
518
c
519
c
520
c
521
c
522
c
523
c
524
c
525
c
526
c
528
c
529
c
530
c
531
c
532
c
533
c
534
c
536
c
537
c
538
c
539
c
540
c
541
c
542
c
543
c
544
c
545
c
546
c
547
c
548
c
549
c
550
c
551
c
552
c
553
c
554
c
555
c
556
c
557
c
558
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
0
4
0
0
0
0
0
0
0
0
0
2
0
0
0
0
0
2
0
0
0
6
0
0
0
0
0
2
2
2
2
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
93
20
31
62
170
201
41
98
76
81
433
141
66
282
78
36
129
179
108
35
95
146
129
67
470
42
49
60
158
117
157
9
16
261
37
146
76
66
152
84
55
584
40
48
50
82
22
0
2
12
0
0
14
0
4
0
0
20
0
0
0
0
0
24
0
0
2
0
0
6
12
12
8
12
122
90
2
0
0
0
0
0
0
0
0
4
0
0
30
0
8
0
c
559
c
560
c
561
c
562
c
563
c
564
c
565
c
566
c
567
c
568
c
569
c
570
c
571
c
572
c
573
c
574
c
575
c
576
c
577
c
578
c
579
c
580
c
581
c
582
c
583
c
584
c
585
c
586
c
587
c
588
c
589
c
590
c
441
c
442
c
443
c
444
c
445
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
2008, Tributary, Parr
0
0
0
0
2
2
0
2
0
0
0
2
2
0
0
2
0
0
4
0
0
0
0
0
0
2
0
0
2
0
4
0
6
62
4
96
2
204
168
85
170
114
210
44
128
226
110
90
99
187
123
117
134
143
36
151
156
164
128
25
111
30
135
135
136
93
123
81
56
114
133
58
321
143
0
0
0
0
290
0
0
70
2
0
38
0
22
0
2
0
0
20
62
0
0
22
6
0
70
0
68
0
68
58
0
0
6
0
0
258
4
620
621
622
623
624
625
626
627
628
2008, Migrant, Smolt
2008, Migrant, Smolt
2008, Migrant, Smolt
2008, Migrant, Smolt
2008, Migrant, Smolt
2008, Migrant, Smolt
2008, Migrant, Smolt
2008, Migrant, Smolt
2008, Migrant, Smolt
48
820
30
124
0
1150
0
62
76
61
186
261
146
95
320
465
43
135
0
412
1148
552
0
358
20
0
14
629
630
631
632
633
634
635
636
637
638
639
640
641
642
643
644
645
646
647
648
649
2008, Migrant, Smolt
2008, Migrant, Smolt
2008, Migrant, Smolt
2008, Migrant, Smolt
2008, Migrant, Smolt
2008, Migrant, Smolt
2008, Migrant, Smolt
2008, Migrant, Smolt
2008, Migrant, Smolt
2008, Migrant, Smolt
2008, Migrant, Smolt
2008, Migrant, Smolt
2008, Migrant, Smolt
2008, Migrant, Smolt
2008, Migrant, Smolt
2008, Migrant, Smolt
2008, Migrant, Smolt
2008, Migrant, Smolt
2008, Migrant, Smolt
2008, Migrant, Smolt
2008, Migrant, Smolt
74
214
626
282
34
22
344
350
16
100
8
40
6
50
80
16
42
522
16
64
144
22
82
389
146
61
142
374
114
93
121
3
370
61
85
122
90
231
135
89
136
259
4
0
0
4
34
0
44
80
0
6
4
296
80
0
0
0
46
44
0
120
940
818
819
820
821
822
823
824
825
826
827
828
829
830
831
832
833
834
835
836
837
838
839
840
841
842
843
844
845
2009, Migrant, Smolt
2009, Migrant, Smolt
2009, Migrant, Smolt
2009, Migrant, Smolt
2009, Migrant, Smolt
2009, Migrant, Smolt
2009, Migrant, Smolt
2009, Migrant, Smolt
2009, Migrant, Smolt
2009, Migrant, Smolt
2009, Migrant, Smolt
2009, Migrant, Smolt
2009, Migrant, Smolt
2009, Migrant, Smolt
2009, Migrant, Smolt
2009, Migrant, Smolt
2009, Migrant, Smolt
2009, Migrant, Smolt
2009, Migrant, Smolt
2009, Migrant, Smolt
2009, Migrant, Smolt
2009, Migrant, Smolt
2009, Migrant, Smolt
2009, Migrant, Smolt
2009, Migrant, Smolt
2009, Migrant, Smolt
2009, Migrant, Smolt
2009, Migrant, Smolt
314
72
8
1082
28
44
988
1004
102
4
130
502
8
80
146
50
40
80
872
40
100
302
52
134
290
110
14
24
52
0
53
291
111
276
378
185
62
227
91
647
216
461
367
149
150
33
147
53
40
370
26
509
110
172
58
71
84
38
538
1512
32
1972
522
0
152
16
0
1072
10
712
1360
542
178
32
1504
0
218
250
0
192
84
0
0
0
846
847
848
2009, Migrant, Smolt
2009, Migrant, Smolt
2009, Migrant, Smolt
232
2
922
263
56
77
832
130
60
For brood year 2006 migrant smolts, N. salmincola counts are derived from only skeletal muscle,
whereas counts of the parasite from all other fish groups include counts from both skeletal
muscle and posterior kidney.
a
Original data taken from Ferguson et al. (in press a).
Original data taken from Ferguson et al. (2010).
c
Original data taken from Ferguson et al. (in press b).
b
Ferguson, J.A., St-Hilaire, S., Peterson, T., Rodnick, K., Kent, M.L., in press a. Survey of
Parasites in Threatened Stocks of Coho Salmon (Oncorhynchus kisutch) in Oregon by
Examination of Wet Tissues and Histology. J. Parasitol.
Ferguson, J.A., Schreck, C.B., Chitwood, R., Kent, M.L., 2010. Persistence of infection by
metacercariae of Apophallus sp., Neascus sp., and Nanophyetus salmincola plus two myxozoans
(Myxobolus insidiosus and Myxobolus fryeri) in coho salmon Oncorhynchus kisutch. J. Parasitol.
96, 340-347.
Ferguson, J.A., Romer, J., Sifneos, J.C., Madsen, L., Schreck, C.B., Glynn, M., Kent, M.L., in
press b. Impacts of Multispecies Parasitism on Juvenile Coho Salmon (Oncorhynchus kisutch) in
Oregon. Aquaculture.
Highlights
f Parasite-associated mortality of threatened coho salmon is reported to occur.
f Parasite infection, overdispersion and distribution are compared among three
species.
f Apophallus sp. (Digenea) was most commonly associated with coho salmon
mortality.
f A new alternative to Crofton’s (1971) distribution truncation technique is
proposed.
f Our Malthusian based congestion rate model does not require statistical inference.