AN ABSTRACT OF THE THESIS OF
James P. Losee for the degree of Master of Science in Fisheries Science presented on May 29,
2012.
Title: Trophically Transmitted Parasites as Ecosystem Indicators: Relationships Among Parasite
Community Structure, Juvenile Salmon Diet Composition, and Ocean Conditions.
Abstract approved:_______________________________________________________________
Jessica A. Miller
Recent research conducted throughout the Northern California Current (NCC) on the
ecology of Pacific salmon (Oncorhynchus spp.) indicates that variable ocean conditions affect the
community composition of zooplankton in the nearshore environment which, in turn, can affect
the quality of prey for fish, sea birds and mammals. Interannual variability in the quality and
composition of the copepod community in the NCC during early marine residency of some
Pacific salmon populations is related to survival to adulthood. However, copepods make up a
small portion of the diet of coho and Chinook salmon, and the mechanistic linkages between
ocean climate, zooplankton composition and salmon prey remain unclear. Parasite analysis
provides a supplement to traditional diet analysis that can describe the foraging history of a host
species. Coho salmon (O. kisutch) and Chinook salmon (O. tshawytscha) serve as hosts to an
array of marine parasites acquired through consumption of infected intermediate hosts such as
copepods, euphausiids, and planktivorous fishes. Causing little or no harm to their salmon host,
the presence of trophically transmitted parasites provides information on the dietary history of
their salmonid host beyond the 24 hours associated with traditional diet analysis.
This study (1) examined differences in feeding behavior of coho and Chinook salmon
during their early marine residency using both stomach and parasite community analyses and (2)
tested the hypothesis that variability in ocean circulation patterns (measured through the Pacific
Decadal Oscillation, sea surface temperature (SST) and Bakun’s upwelling index) and copepod
species composition are related to variability in the community structure of trophically
transmitted marine parasites found in juvenile salmon. I compared the abundance and species
composition of parasites recovered from juvenile Columbia River coho and upper Columbia
River summer and fall Chinook salmon captured off the coast of Washington from 2002 to 2009.
I also compared interannual variability in parasite assemblages to physical and biological indices
of ocean conditions.
Coho and Chinook salmon consumed similar prey taxa; however, the species richness
and abundance of trophically transmitted parasites indicated that Chinook salmon consumed a
greater diversity and abundance of infected prey. In addition, differences in the abundance of fish
in the diet and Anisakis simplex, a parasitic nematode known to infect salmon through fish
consumption, suggest that Chinook salmon consistently consumed more fish prey than coho. In
contrast, coho appeared to consume more euphausiids as indicated by stomach content analysis
and increased abundance of the euphausiid parasite, Rhadinorhynchus trachuri. Shifts in the
parasite community composition of both coho and Chinook salmon were related to interannual
variability in SST and the biomass of southern-origin copepods (r > 0.7, P < 0.05). The
acanthocephalan R. trachuri and a tetraphyllid cestode were associated with “warm” SSTs and
greater biomass of lipid-poor, subtropical copepods while the nematode A. simplex was more
abundant in years of “cold” SST and a relatively low biomass of subtropical copepods. These
results provide novel insight into differences in the diet of Columbia River coho and Chinook
salmon and illustrate linkages between ocean climate, zooplankton community composition and
salmon diet during early marine residency.
©Copyright by James P. Losee
May 29, 2012
All Rights Reserved
Trophically Transmitted Parasites as Ecosystem Indicators: Relationships Among Parasite
Community Structure, Juvenile Salmon Diet Composition, and Ocean Conditions
by
James P. Losee
A THESIS
Submitted to
Oregon State University
in partial fulfillment of
the requirements for the
degree of
Master of Science
Presented May 29, 2012
Commencement June 2012
Master of Science thesis of James P. Losee presented on May 29, 2012.
APPROVED:
______________________________________________________________________________
Major Professor, representing Fisheries Science
______________________________________________________________________________
Head of the Department of Fisheries and Wildlife
______________________________________________________________________________
Dean of the Graduate School
I understand that my thesis will become part of the permanent collection of Oregon State
University libraries. My signature below authorizes release of my thesis to any reader upon
request.
______________________________________________________________________________
James P. Losee, Author
ACKNOWLEDGEMENTS
The author wishes to thank:
Advisors: Dr. Kym Jacobson, Dr. Jessica Miller and Dr. William Peterson
Past and present Jacobson, Miller and Peterson lab members: Dr. Rebecca Baldwin, Andrew
Claxton, Mary Beth Rew, Andrew Claiborne, Jose Marin Jarrin, Londi Tomaro, Cheryl Morgan,
Jessi Lamb, Dr. Jay Peterson and Dr. Jennifer Fisher.
Researchers at NOAA and crew of the F/V Frosti who assisted in collecting fish and tissue
samples used in this study.
Center for Coastal Margin Observation and Prediction researchers for providing Columbia River
plume data, lab space and valuable input regarding this project: Antonio Baptista, Joe Needoba,
Tawnya Peterson.
Statistical assistance: Brian Burke and Dr. Bruce McCune.
Funding Agencies: Bonneville Power Administration, National Marine Fisheries Service, Mamie
Markham Research Award, Neil Armantrout Scholarship, American Society of Parasitologists
and Hatfield Marine Science Center Student Organization.
Past mentors: Steve Wolthausen, Dr. Ann Knowlton and Nicki Kamimoto.
Family and Friends: My parents Sherman and Chris Losee for always allowing me to choose my
own path. My son Finnegan and daughter Juniper for keeping me young. My father-in-law, Dave
Flitcraft for teaching me what’s most important in life. Most of all, thanks to the love of my life,
Kate Losee for providing an unending supply of support as well as valuable insight into the study
of parasites, salmon and ocean processes.
CONTRIBUTION OF AUTHORS
Dr. Jessica Miller served as major advisor and contributed to the experimental design and writing
in Chapter 2 and 3. Dr. Kym Jacobson contributed to experimental design, provided assistance in
parasite data collection, analysis and writing in Chapter 2 and 3. David Teel provided genetic
stock assignments used in Chapter 2 and 3. Elizabeth Daly processed stomach contents for diet
and contributed to data analysis of Chapter 3. Dr. Bill Peterson contributed to experimental
design, developed copepod community indices and contributed to data analysis in Chapter 3.
TABLE OF CONTENTS
Page
CHAPTER 1: Introduction…………………………………………………...
1
Literature Cited……………………………………………...
5
CHAPTER 2: Parasites and Diet Indicate Interspecific Differences in Feeding
Of Coho and Chinook Salmon in the Nearshore Marine Environment…........
7
INTRODUCTION……………………………………………………..
8
METHODS…………………………………………………………….
11
Fish Collections………………………………………………….
11
Genetic Stock Identification……………………………………..
12
Parasite Analysis…………………………………………………
13
Diet Analysis…………………………………………………….
13
RESULTS………………………………………………………………
17
DISCUSSION………………………………………………………….
20
LITERATURE CITED…………………………………………………
26
Chapter 3: Influence of Ocean Ecosystem Variability on Trophic Interactions
and Survival of Juvenile Coho and Chinook Salmon……………..
44
INTRODUCTION………………………………………………………
45
METHODS……………………………………………………………...
47
Fish Collections……………………………………………………
47
Collection of Parasites and Analysis………………………………
48
Genetic Stock Identification……………………………………….
48
Physical and Biological Environmental Indices…………………...
48
RESULTS……………………………………………………………….
53
DISCUSSION…………………………………………………………...
55
LITERATURE CITED………………………………………………….
60
Chapter 4: CONCLUSION…………………………………………………….
72
LIST OF FIGURES
Figure
Page
2.1 Sampling area and collection locations……………………………………… 36
2.2 Number of hatchery releases and estuary catch……………………………... 37
2.3 Relationship between parasite abundance and species richness to FL………. 38
2.4 Mean parasite species richness and abundance…………………………….... 39
2.5 Mean prey species richness and abundance…………………………………. 40
2.6 Numerical prey and parasite species composition…...………………………. 41
2.7 Prey composition by weight………………………………………………….. 42
2.8 Nonmetric multidimensional scaling of stomach contents and parasites……. 43
3.1 Sampling area and collection locations………………………………………. 68
3.2 Nonmetric multidimensional scaling of coho and Chinook salmon parasites. 69
3.3 Annual anomalies of SST, southern copepod biomass and parasites………... 70
3.4 Relationship between coho and Chinook salmon parasites to survival……… 71
LIST OF TABLES
Table
Page
2.1 Sample size and mean size (FL, mm) for coho and Chinook salmon………
30
2.2 ANOVA results for FL between coho and Chinook salmon across years….
31
2.3 Parasite prevalence (%) for coho and Chinook salmon……………………..
32
2.4 Parasite mean abundance for coho and Chinook salmon…………………… 33
2.5 Prey mean abundance for coho and Chinook salmon……………………….
34
2.6 Indicator species for coho and Chinook salmon parasites and prey………… 35
3.1 Sample size and mean size (FL, mm) for coho and Chinook salmon………. 65
3.2 Intermediate hosts of parasites recovered from coho and Chinook salmon… 66
3.3 Correlation coefficients between environmental variables and parasites
species on axis 1 and axis 2 ordination scores…………………………………… 67
CHAPTER1: INTRODUCTION
Numerous studies have identified early marine residency as a period of high mortality for
Pacific salmon (Beamish and Mahnken, 2001; Beamish et al., 2004; Pearcy, 1992). Over the last
decade, dynamic ocean conditions in the Northern California Current (NCC) have been coupled
with variable returns of adult Pacific salmon (Logerwell et al., 2003; Scheuerell and Williams,
2005) and abundances of other species of pelagic nekton (Brodeur et al., 2005; Phillips et al.,
2007; Zeidberg and Robison, 2007). While factors that contribute directly to variability in marine
survival rates of Pacific salmon and other commercially important species are not fully
understood, some physical and biological components in the marine ecosystem correlate
significantly with salmon survival (Mackas et al., 2007; Mantua et al., 1997; Peterson and
Schwing, 2003; Scheuerell and Williams, 2005).
In the NCC, basin and local scale indices such as the Pacific Decadal Oscillation (PDO)
and Bakun’s upwelling index have shown potential in describing ocean conditions that are
favorable for Pacific salmon (Rupp et al., 2011). The Pacific Decadal Oscillation (PDO) is a
climate oscillation based on monthly sea-surface temperature variability in the Northeast Pacific
(NEP). Negative values of the PDO indicate anomalously cool waters in the NEP and have been
shown to signal relatively high salmon survival while positive values are associated with “poor”
salmon survival and warm surface waters (Mantua et al., 1997). On a local scale, coastal
upwelling events are dominant physical processes and their strength and frequency can have a
dramatic effect on water mass characteristics in the ocean and food web structure on the
continental shelf. For instance, bi-weekly sampling of marine zooplankton in the NCC revealed
onshore/offshore variation in species composition (Morgan et al. 2003) that coincides with
physical transport mechanisms and sea surface temperature (Keister et al., 2011). Warm water on
the shelf has been associated with zooplankton species of southern or offshore origin, including
euphausiids, copepods, and chaetognaths (Hoof and Peterson 2006, Keister et al., 2005). Results
from these surveys have shown that two distinct copepod communities exist in the NCC (Morgan
et al., 2003; Peterson and Keister, 2003). In years of strong upwelling and negative PDO the
copepod communities in the NCC were dominated by lipid-rich, sub-arctic boreal fauna (Peterson
and Keister, 2003) and salmon survival was relatively high (Mackas et al., 2007). In contrast,
years associated with positive values of the PDO index and weak upwelling have resulted in
lipid-poor, subtropical oceanic zooplankton species on the shelf (Hinch et al., 1995; Mackas et
al., 2007; Peterson and Schwing, 2003) and relatively poor salmon survival. The positive
2
relationship between the biomass of “cold water”, lipid-rich zooplankton species and salmon
productivity suggests bottom-up processes are important in determining salmon survival. It has
been hypothesized that interannual variability in the ocean circulation patterns that determine
species composition and biomass of zooplankton present in early summer may affect the quality
of salmon prey, and in turn influence salmon survival (Keister et al., 2011; Mackas et al., 2007).
However, copepods make up a small contribution of coho and Chinook salmon diet (Brodeur and
Pearcy, 1990; Peterson et al., 1982); therefore the direct linkages between ocean conditions,
copepod community structure and salmon survival are unclear.
Direct measurements of salmon prey composition and quality are available through
traditional diet analysis (Brodeur and Pearcy, 1990, Peterson et al. 1982). Analyses of stomach
contents have increased our understanding of salmon ecology and bioenergetics. In addition,
recent multivariate approaches of analyzing stomach contents may provide evidence for
differences in species composition of fish consumed by salmon in years of high vs. low salmon
survival (E. Daly pers. comm, OSU, CIMRS). While increasing evidence suggests that bottomup processes regulate salmon abundance (Mackas et al., 2007), current research to-date has not
identified a relationship between the quality or composition of prey items found in the stomach of
salmon and year-class strength, suggesting that variability at lower levels of the food web may
alter the relative abundance or composition of prey for salmon.
Analysis of trophically transmitted parasites can supplement analyses of stomach
contents and has been shown to clarify trophic interactions between and among species. The
abundance of trophically transmitted parasites in a host is dependent on the abundance and
species composition of free living fauna in the ecosystem and host diet (Marcogliese, 2005).
While copepods may not contribute substantially to the diet of piscivorous salmon (e.g. coho and
Chinook), they are considered an important organism in marine food webs in terms of biomass
and are the chief prey item for those fishes upon which piscivorous salmon feed. For these
reasons copepods act as a reliable intermediate host for marine parasites to become distributed
through the food web (Rhode et al. 1984). However, the short lifespan of copepods has resulted
in the development of transport or second intermediate hosts as part of the [parasite] lifecycle in
order to maintain their presence in the food web (Marcogliese, 2002; Petric et al., 2011). Longer
lived, predatory invertebrates (i.e. euphausiids, amphipods and chaetognaths) and planktivorous
fishes that serve as common prey items of juvenile salmon bridge the gap between copepods and
the required, predatory vertebrate final host of the parasites (i.e. teleost, elasmobranch, marine
3
mammal etc.). Differences in species composition and abundance of trophically transmitted
parasites can then reflect variability of a suite of invertebrates both in the environment and the
food web (Zander et al., 2000).
The analysis of trophically transmitted parasites can offer supplemental information on
specific aspects of salmon diet and has proven reliable in detecting ontogenetic, geographic, and
temporal variation in feeding behavior in a variety of marine fish (Blaylock et al., 1998;
Campbell et al., 1980; Pascual et al., 1996b; Petric et al., 2011). With infection rates of marine
invertebrates estimated to be less than 1% (Marcogliese, 2005), the recovery of few trophically
transmitted parasites in salmon may reflect the consumption of many prey items. For example,
the parasite species composition of coho and Chinook salmon recovered in 2000 and 2002
suggested that juveniles consumed more fish and euphausiids during early marine residency than
estimated through stomach contents analysis (Baldwin et al., 2008). The accumulation of
parasites obtained through the diet have been shown to be a useful and comprehensive indicator
of diet over a much longer time period than assessments of diet based solely on gut content
analyses (Baldwin et al., 2008; Bertrand et al., 2008; Valtonen et al., 2010).
The primary objective of my research was to determine if variability in the physical and
biological characteristics of the marine environment are related to the species composition and
abundance of parasites found in juvenile coho and Chinook salmon during early marine
residency. However, to understand how ocean climate may affect coho and Chinook salmon
differently I first sought to gain a better understanding of how the feeding behavior of coho and
Chinook salmon differ from one another within years.
In Chapter 2, I compared the species composition and abundance of trophically
transmitted parasites encountered through marine trophic interactions of yearling Columbia River
coho salmon and Upper Columbia River summer and fall (UCR Su/F) Chinook salmon. These
salmon were captured during an 8-year period of variable ocean conditions (2002-2009) and
exhibited overlap in their distribution and timing of outmigration from the Columbia River.
Therefore we were able to control for variability that may be associated with distribution, timing
of outmigration and stock specific feeding behavior. While numerous studies have documented
the food habits of juvenile coho and Chinook salmon in the marine environment, interspecific
comparisons of prey composition or dietary overlap are not consistent across or within studies
(Baldwin et al., 2008; Schabetsberger et al., 2003). For this reason, differences in feeding
behavior of juvenile coho and Chinook salmon and the potential for interspecific competition are
4
unclear. Analysis of trophically transmitted parasites suggested that Chinook salmon consistently
consumed a greater abundance of infected prey. In addition, analysis of parasites and prey
revealed that Chinook salmon fed on a greater number of higher energetically valuable prey, per
gram (fish, Davis et al. 2005) during early marine residency while coho ate more euphausiids. By
incorporating both stomach content analysis (indicators of recent foraging) and parasite
community composition (indicators of prior foraging) the current study provides a more
comprehensive comparison of the diet of coho and Chinook salmon than previous studies that
relied only on traditional diet analysis and highlights the accuracy to which parasite analysis can
identify variation in feeding habits.
With a better understanding of interspecific differences in feeding habits we determined
if marine, trophically transmitted parasite communities of juvenile coho and Chinook salmon
relate to variability in ocean conditions during early marine residency. In Chapter 3, we first
describe interannual differences in the trophically transmitted parasites of yearling coho and
Chinook salmon using non-metric multidimensional scaling (NMS). Patterns of parasite
abundance and species composition were then compared to a variety of physical (i.e. PDO, SST,
upwelling strength) and biological indicators (i.e. copepod biomass) of ocean conditions shown to
be related to salmon productivity. We then examined the relationship between variability in
parasite species composition and subsequent adult returns to test the hypothesis that the
composition and/or quality of prey are related to interannual variation in salmon abundance.
While results from Chapter 2 provide evidence that coho and Chinook salmon from the
Columbia River exhibit differences in feeding during early marine residency, the parasite
abundance and species composition of both fish species were related to variability in ocean
conditions across years. Trophic interactions of juvenile salmon, as inferred from parasite species
composition, are related to variation in ocean climate in the NCC. In general, trophic interactions
associated with successful recruitment occurred when SST was low, the biomass of southernorigin, lipid-poor copepods was low, and the volume of the Columbia River plume was large in
early summer. Results from this study demonstrated consistent differences in feeding behavior
between coho and Chinook salmon originating from the Columbia River and provided evidence
for a link between variability in copepods and salmon prey. Further investigation is needed to
test whether differences in parasite composition are the result of variation in salmon prey or
variability in species composition of invertebrates consumed by salmon prey and how these
interannual and interspecific differences in feeding directly affect salmon growth and survival.
5
LITERATURE CITED
Baldwin R.E., Miller T.W., Brodeur R.D., Jacobson K.C. (2008) Expanding the foraging history
of juvenile Pacific salmon: combining stomach-content and macroparasite-community
analyses for studying marine diets. Journal of Fish Biology 72:1268-1294. DOI:
10.1111/j.1095-8649.2007.01792.x.
Beamish R.J., Mahnken C. (2001) A critical size and period hypothesis to explain natural
regulation of salmon abundance and the linkage to climate and climate change. Progress
in Oceanography 49:423-437. DOI: 10.1016/s0079-6611(01)00034-9.
Beamish R.J., Mahnken C., Neville C.M. (2004) Evidence that reduced early marine growth is
associated with lower marine survival of coho salmon. Transactions of the American
Fisheries Society 133:26-33. DOI: 10.1577/t03-028.
Bertrand M., Marcogliese D.J., Magnan P. (2008) Trophic polymorphism in brook charr revealed
by diet, parasites and morphometrics. Journal of Fish Biology 72:555-572. DOI:
10.1111/j.1095-8649.2007.01720.x.
Blaylock R.B., Margolis L., Holmes J.C. (1998) Zoogeography of the parasites of Pacific halibut
(Hippoglossus stenolepis) in the northeast Pacific. Canadian Journal of Zoology-Revue
Canadienne De Zoologie 76:2262-2273. DOI: 10.1139/cjz-76-12-2262.
Brodeur R.D., Fisher J.P., Emmett R.L., Morgan C.A., Casillas E. (2005) Species composition
and community structure of pelagic nekton off Oregon and Washington under variable
oceanographic conditions. Marine Ecology-Progress Series 298:41-57.
Brodeur R.D., Pearcy W.G. (1990) Trophic relations of juvenile Pacific salmon off the Oregon
and Washington coast. Fishery Bulletin 88:617-636.
Campbell R.A., Haedrich R.L., Munroe T.A. (1980) Parasitism and ecological relationships
among deep-sea benthic fishes. Marine Biology 57:301-313. DOI: 10.1007/bf00387573.
Davis N.D., Fukuwaka M.A., Armstrong J.L., Myers K.W. (2005) Salmon food habits studies in
the Bering Sea, 1960 to present, NPAFC Tech. Rep 6: pp. 24-28.
Hinch S.G., Healey M.C., Diewert R.E., Henderson M.A. (1995) Climate change and ocean
energetics of Fraser River sockeye (Oncorhynchus nerka). Canadian Special Publication
of Fisheries and Aquatic Sciences 121:439-445.
Hooff R.C., Peterson W.T. (2006) Copepod biodiversity as an indicator of changes in ocean and
climate conditions of the northern California current ecosystem. Limnology and
Oceanography 51:2607-2620.
Keister J.E., Di Lorenzo E., Morgan C.A., Combes V., Peterson W.T. (2011) Zooplankton
species composition is linked to ocean transport in the Northern California Current.
Global Change Biology 17:2498-2511. DOI: 10.1111/j.1365-2486.2010.02383.x.
Keister J.E., Johnson T.B., Morgan C.A., Peterson W.T. (2005) Biological indicators of the
timing and direction of warm-water advection during the 1997/1998 El Nino off the
central Oregon coast, USA. Marine Ecology-Progress Series 295:43-48.
Logerwell E.A., Mantua N., Lawson P.W., Francis R.C., Agostini V.N. (2003) Tracking
environmental processes in the coastal zone for understanding and predicting Oregon
coho (Oncorhynchus kisutch) marine survival. Fisheries Oceanography 12:554-568.
Mackas D.L., Batten S., Trudel M. (2007) Effects on zooplankton of a warmer ocean: Recent
evidence from the Northeast Pacific. Progress in Oceanography 75:223-252. DOI:
10.1016/j.pocean.2007.08.010.
Mantua N.J., Hare S.R., Zhang Y., Wallace J.M., Francis R.C. (1997) A Pacific interdecadal
climate oscillation with impacts on salmon production. Bulletin of the American
Meteorological Society 78:1069-1079. DOI: 10.1175/1520-0477(1997)078<1069
6
Marcogliese D.J. (2002) Food webs and the transmission of parasites to marine fish. Parasitology
124:S83-S99. DOI: 10.1017/s003118200200149x.
Marcogliese D.J. (2005) Parasites of the superorganism: Are they indicators of ecosystem health?
International Journal for Parasitology 35:705-716. DOI: 10.1016/j.ijpara.2005.01.015.
Morgan C.A., Peterson W.T., Emmett R.L. (2003) Onshore-offshore variations in copepod
community structure off the Oregon coast during the summer upwelling season. Marine
Ecology-Progress Series 249:223-236. DOI: 10.3354/meps249223.
Pascual S., Gonzales A., Arias C., Guierra A. (1996) Biotic relationships of Illex condetii and
Todaraposis eblana (Cephalopoda, Ommastrephidae) in the Northeast Atlantic: evidence
from parasites. Sarsia 81:265-274.
Pearcy W.G. (1992) Ocean ecology of North Pacific salmonids Washington Sea Grant Program,
University of Washinton Press, Seattle, WA.
Peterson W.T., Brodeur R.D., Pearcy W.G. (1982) Food Habits of juvenile salmon in the Oregon
coastal zone, June 1979. Fishery Bulletin 80:841-851.
Peterson W.T., Keister J.E. (2003) Interannual variability in copepod community composition at
a coastal station in the northern California Current: a multivariate approach. Deep-Sea
Res, Part II 50:2499-2517. DOI: 10.1016/s0967-0645(03)00130-9.
Peterson W.T., Schwing F.B. (2003) A new climate regime in northeast pacific ecosystems.
Geophysical Research Letters 30. DOI: 1896: 10.1029/2003gl017528.
Petric M., Mladineo I., Sifner S.K. (2011) Insight into the short-finned squid Illex coindetii
(Cephalopoda:Ommastrephidae) feeding ecology: is there a link between helminth
parasites and food composition? Journal of Parasitology 97:55-62.
Phillips A.J., Ralston S., Brodeur R.D., Auth T.D., Emmett R.L., Johnson C., Wespestad V.G.
(2007) Recent pre-recruit Pacific hake (Merluccius productus) occurrences in the
northern California Current suggest a northward expansion of their spawning area.
California Cooperative Oceanic Fisheries Investigations Reports 48:215-229.
Rhode K. (1984) Ecology of Marine Parasites. Helgoland marine research 37:5-33.
Rupp D.E., Wainwright T.C., Lawson P.W., Peterson W.T. (2011) Marine environment-based
forecasting of coho salmon (Oncorhynchus kisutch) adult recruitment. Fisheries
Oceanography 21(1):1-19.
Schabetsberger R., Morgan C.A., Brodeur R.D., Potts C.L., Peterson W.T., Emmett R.L. (2003)
Prey selectivity and diel feeding chronology of juvenile Chinook (Oncorhynchus
tshawytscha) and coho (O. kisutch) salmon in the Columbia River plume. Fisheries
Oceanography 12:523-540.
Scheuerell M.D., Williams J.G. (2005) Forecasting climate-induced changes in the survival of
Snake River spring/summer Chinook salmon (Oncorhynchus tshawytscha). Fisheries
Oceanography 14:448-457. DOI: 10.1111/j.1365-2419.2005.00346.x.
Valtonen E.T., Marcogliese D.J., Julkunen M. (2010) Vertebrate diets derived from trophically
transmitted fish parasites in the Bothnian Bay. Oecologia 162:139-152. DOI:
10.1007/s00442-009-1451-5.
Zander C.D., Reimer L.W., Barz K., Dietel G., Strohbach U. (2000) Parasite communities of the
Salzhaff (Northwest Mecklenburg, Baltic Sea) II. Guild communities, with special regard
to snails, benthic crustaceans, and small-sized fish. Parasitology Research 86:359-372.
Zeidberg L.D., Robison B.H. (2007) Invasive range expansion by the Humboldt squid, Dosidicus
gigas, in the eastern North Pacific. Proceedings of the National Academy of Sciences of
the United States of America 104:12946-12948. DOI: 10.1073/pnas.0702043104
7
CHAPTER 2:
PARASITES AND DIET INDICATE INTERSPECIFIC DIFFERENCES IN
FEEDING OF COHO AND CHINOOK SALMON IN THE
NEARSHORE MARINE ENVIRONMENT
James P. Losee
ABSTRACT
Recent diet studies have shed light on many aspects of the trophic ecology of coho salmon
Oncorhynchus kisutch and Chinook salmon O. tshawytscha. Comparison of stomach content
analysis over a variety of temporal and spatial scales may have contributed to the inconsistent
conclusions reported in prior studies of comparing the feeding habits of coho and Chinook
salmon. We used genetic stock identification to select juvenile coho and Chinook salmon stock
groups with similar spatial and temporal distributions in the nearshore marine environment. We
compared the diets of Columbia River coho salmon and Upper Columbia River summer and fall
Chinook salmon captured off the coast of Washington in June of 2002-2009 using stomach
content analysis (indicators of recent foraging) and parasite community composition (indicators
of past foraging,>1 month). We examined interspecific variation in stomach fullness and parasite
abundance as well as prey richness, estimated using prey species richness and parasite species
richness. While stomach contents did not reveal consistent differences in stomach fullness or
prey species richness across years, parasite abundance and parasite species richness was higher
for Chinook salmon. We used nonmetric multidimensional scaling to further examine
interspecific differences in abundance and species composition of the parasite and prey
community of coho and Chinook salmon. Stomach contents and parasite community composition
revealed that coho and Chinook salmon consistently consumed similar prey taxa but in different
proportions. Chinook salmon consumed more fish and amphipods while coho salmon ate more
euphausiids. Results from this study illustrated consistent differences in the feeding behavior of
8
coho and Chinook salmon originating from the Columbia River basin. Whether these differences
in diet are attributed to food preference, competitive interaction or are the result of small-scale
differences in feeding location is still unknown.
INTRODUCTION
Chinook salmon, Oncorhynchus tshawytscha, and coho salmon, O. kisutch, are the most
important species of Pacific salmon inhabiting marine waters off Washington and Oregon in
terms of biomass and economic value with annual commercial harvest totaling over five million
fish (Lichatowich, 1999; Shaul et al., 2007). Hatcheries on the Columbia River and its tributaries
are responsible for over 200 million coho and Chinook salmon smolts produced annually
(Mahnken et al. 1998, www.cbr.washington.edu/dart/dart.html, 1995-present). Historically,
juvenile salmon leaving the Columbia River expressed substantial variation in the timing of their
migration to the marine environment (Gilbert, 1912; Lichatowich, 1999; Miller, 2011; Williams
et al., 2005). Emigration of wild juvenile salmon leaving the Columbia River is thought to have
evolved over the last 100,000 years (Waples et al., 2004) possibly as a means to reduce spatial
overlap and competition among populations of salmon. In the last 30 years, however, the timing
of outmigration for juvenile coho and Chinook salmon has been, in large part, a product of fixed
timing of hatchery releases (Lichatowich, 1999).
Currently a large proportion of coho and Chinook salmon leaving the Columbia River
originate from hatcheries and are released in April/May without consideration of the carrying
capacity of the Columbia River or marine environment (Williams et al., 1999). For example, in
2011 over 90% of the approximately 125 million coho and Chinook salmon produced by
hatcheries were released into the Columbia River during a four-month period (March-June)
(www.cbr.washington.edu, 1995-present). By increasing the temporal and spatial overlap of
coho and Chinook salmon, fish hatcheries may enhance the potential for out migrating juvenile
9
salmon to compete for resources (Beamish and Mahnken, 2001). Evidence for inter- and intraspecific competition in the marine environment has been reported for various populations of
salmonids (Bigler et al., 1996; King and Beamish, 2000; Martinson et al., 2008; Ruggerone et al.,
2003), but not for coho or Chinook salmon, and indicates that hatchery releases of some salmon
species may lead to increased competitive interaction and/or density-dependent mortality (Bigler
et al. 1996).
Numerous studies have shown that coho and Chinook salmon consume similar prey
including larval and juvenile fish, crustaceans and other planktonic invertebrates (Brodeur et al.,
1992; Brodeur and Pearcy, 1990; Weitkamp and Sturdevant, 2008). However, it is not clear if
there are consistent differences in the relative contribution of these prey categories to coho and
Chinook salmon. Juvenile Chinook salmon, for example, have been shown to switch from a diet
comprised primarily of invertebrates to a diet comprised of primarily fish at a smaller body size
than juvenile coho salmon (80-100 mm vs. 121-140 mm, respectively, Daly et al., 2009) and will
consume larger prey for their size (Schabetsberger et al., 2003; Weitkamp and Sturdevant, 2008).
In contrast, others have found that coho salmon consume larger prey for their size (Brodeur 1991)
and appear to be more piscivorous than Chinook salmon at times (Baldwin et al., 2008; Brodeur
et al. 2007; Emmett et al., 1986). In addition to prey species composition, stomach fullness, prey
diversity, and dietary overlap also vary substantially for juvenile coho and Chinook salmon by
month, year and location. For instance, some comparative studies off the Oregon and
Washington coast report significant dietary overlap between juvenile coho and Chinook salmon
(Emmett et al., 1986; Peterson et al., 1982) while Brodeur and Pearcy (1990) reported dietary
overlap to be low in most years. These inconsistent reports suggest that the trophic relations of
juvenile coho and Chinook salmon vary among regions, seasons and potentially populations,
which indicate that these factors should be considered when comparing feeding behavior.
10
The overwhelming majority of studies that compare the trophic interactions of fishes do
so by examining stomach contents. While traditional stomach content analysis offers an accurate
picture of recent feeding, it is unable to detect foraging events that occurred beyond the 24 hours
prior to capture (Benkwitt et al., 2009; Brodeur and Pearcy, 1987). Methods that incorporate
long-term variability in diet may allow researchers to better identify patterns of diet similarity,
feeding intensity and prey diversity among juvenile salmon species during early marine
residency.
The analysis of trophically transmitted parasites has been used to compare trophic
interactions for a wide range of marine fish hosts (Poulin, 1998; Gonzalez and Poulin, 2005;
Valtonen et al., 2010). The presence of trophically transmitted parasites, which cause little or no
harm to their host (Paperna and Dzikowski, 2006), can serve as a proxy for salmon trophic
interactions that took place several months prior to the time of capture. The types and quantity of
trophically transmitted parasites present are determined by the diet and habits of the host (Rhode,
1984). For example, a fish host exhibiting a high consumption rate and feeding on a diversity of
prey from a range of trophic levels typically has a higher abundance and greater species richness
of parasites compared to a host consuming fewer prey from a less diverse prey assemblage
(Luque et al., 2004; Marcogliese, 1995; Poulin, 1998). In this way, a comparison of the species
richness and abundance of parasites between juvenile coho and Chinook salmon, captured at the
same place and time can offer insight into differences in feeding behavior. In addition, when
combined with diet data, parasite analysis can improve understanding of food web linkages
(Campbell et al., 1980; Scott and Bray, 1989) and provide additional information beyond
observed diet (Valtonen, 2010). For example, Baldwin et al. (2008) recognized that parasites
recovered from juvenile salmon with empty stomachs offered diet information on fish that
otherwise could not have been included in a diet study. Based on parasite species composition
11
and abundance, they concluded that the specificity of traditional diet analysis combined with the
long-lived nature of parasites allowed for a more comprehensive picture of the trophic
interactions of juvenile salmon in the marine environment and suggested that salmon may
consume more zooplankton and fish than estimated by stomach contents (Baldwin et al., 2008).
However, when comparing the diet of juvenile coho and Chinook salmon, Baldwin et al. (2008)
and others (Brodeur, 1991; Brodeur, 1992; Weitkamp and Sturdevant, 2008) did not observe
consistent differences in species composition or stomach fullness between species across months,
years and salmon stocks.
The current study determined if the diets of juvenile coho and Chinook salmon differed
across years of variable ocean conditions while controlling for factors known to influence
variation in diet. We sampled genetic stock groups with overlapping catch distribution that
originated from a common source (the Columbia River) with similar dates of outmigration to
evaluate the potential for diet overlap and competition. We used the stomach contents and the
trophically transmitted parasites of juvenile coho and Chinook salmon to: (1) compare the
stomach fullness, parasite abundance and prey diversity estimated by each approach; (2) evaluate
interannual variation in diet overlap as determined by the parasite compared with the prey
community and; (3) to identify differences in the abundance of specific prey items and parasite
species between fish species and across years (2002-2009).
METHODS
Fish collections
Juvenile salmon were collected during 10 days in the second half of June in eight cruises
2002-2009. Sampling stations were located on five transects (Fig. 2.1) ranging from the
Columbia River (46º53’N) to La Push, Washington (47 º 55’N). Stations on each transect ranged
from 3 to 50 km offshore. Juvenile salmon were collected during daytime using a Nordic 264-
12
rope trawl towed at the surface. The mouth opening of the trawl was approximately 20 m deep
and 30 m wide when towed. Tows lasted for 15-30 min at an approximate speed of 6.5 km h-1.
In the lab fish were thawed, measured (FL, mm) and weighed (g). Yearling coho and Chinook
salmon were distinguished from subyearling, subadult or adult fish by fork length (FL, mm)
(Fisher et al. 2007) and immediately frozen. We inspected normal probability plots and
conducted Levene’s test to assess normality and homogeneity of variance for FL data of coho and
Chinook salmon. Data were transformed if necessary to meet parametric assumptions. A twofactor Analysis of Variance (ANOVA) was used to evaluate variance in FL between coho and
Chinook salmon across years. We conducted multiple comparisons using post-hoc Fisher’s Least
Significant Difference (Fisher’s LSD) procedure.
Genetic stock identification
The relative probability of stock origin was estimated for each fish using the likelihood
model of Rannala and Mountain (1997), as implemented in the genetic stock identification
software ONCOR (Kalinowski et al. 2007). A microsatellite DNA baseline data from Van
Doornik et al. (2007) was used to assign coho salmon and the standardized database described by
Seeb et al. (2007) was used for Chinook salmon. Coho salmon were genotyped at 11
microsatellite DNA loci (Van Doornik et al. 2007) and Chinook salmon were genotyped at 13
loci (Teel et al. 2009). Only coho salmon from the Columbia River genetic stock group and
Chinook salmon from the Upper Columbia River Summer and Fall (UCR Su/F) genetic stock
group were included in this study (mean probability: 92.6% ±5.2% SE). These genetic stock
groups have similar marine distributions (Figure 2.1, Fisher et al., 2007) and emigrate from the
Columbia River at similar times (Fig. 2.2, Fish Passage Center Hatchery Database, Laurie
Weitkamp, National Ocean and Atmospheric Administration, Newport, OR,pers. comm). In
addition, using observed adipose fin clips and known rates of fin clipping at hatcheries obtained
13
from the Regional Mark Information System database (RMIS), we estimated that greater than
90% of fish included in this study were of hatchery origin.
Parasite analysis
The exterior of all internal organs (heart, liver, spleen, gall bladder, digestive tract,
gonads, kidney, urinary bladder and gas bladder) were macroscopically examined for free or
attached parasites. The entire gastrointestinal (GI) tract (stomach, pyloric caeca and intestine)
was removed for microscopic inspection. The length of the caeca and intestine was measured
(1.0 mm) and divided into five segments of equal length. Each segment was separated and
examined for parasites using a dissecting microscope. All portions of the GI tract were opened
longitudinally and rinsed into glass plates using de-ionized water. Parasites were then recovered
from settled solution and removed manually from the walls of the stomach, caeca and segments
of intestine. Parasites were separated by phylum (Acanthocephala, Nematoda and
Platyhelminthes) and then identified to lowest taxonomic level possible using a compound
microscope. For long-term storage, specimens were either slide-mounted using balsam medium
or transferred to 95% ethanol (R. Overstreet, from, pers. comm.). To confirm the identity of
some species, individual parasites were compared to specimens from the reference parasite
collection of R. Olson at the Hatfield Marine Science Center and to type specimens from the U.S.
National Parasite Collection (Beltsville, MD, U.S.A.). We only used parasites known to infect
fish in the marine environment in subsequent analyses. To assess the proportion of juvenile coho
and Chinook salmon infected with any particular parasite we calculated the prevalence, defined as
the number of hosts infected by a particular parasite species divided by the number of hosts
examined (Bush et al., 1997).
Diet analysis
14
The majority of the fish used in this study were processed for both diet (N = 554) and
parasite (N = 607) analysis. Stomach contents were identified by E. Daly (OSU, Cooperative
Institute for Marine Resource Studies) to the lowest possible taxonomic category and life history
stage using a dissecting microscope.Prey were enumerated and weighed (0.001 g). For the
majority of analyses, prey species were grouped into 7 categories (Osteichthyes, Copepoda,
Euphausiacea, Insecta, Decapoda, Amphipoda and other) which is similar to those of other
studies comparing the diet of coho and Chinook salmon (Schabetsberger et al., 2003; Weitkamp
and Sturdevant, 2008). These groupings provide a robust comparison of diet by not
ovemphasizing rare and unidentifiable diet items and provides a similar level of specificity as
parasite analysis. For analyses of species richness, we expanded our groupings to 22 categories:
fish (unidentified fish and other fish that made up < 5% of diet), Cottidae, Pleuronectidae,
rockfishes (Sebastes spp.), Ronquilus sp., Pacific sand lance (Ammodytes hexapterus), Osmeridae,
Cancer spp. larvae, copepods, other decapod larvae (non-Cancer spp. decapods), Euphausiidae,
Amphipoda, and "other" (pteropods, mysids, polychaetes, gelatinous zooplankton, cephalopods,
insects, and cirripede larvae).
Feeding habits
Parasite species richness is defined as the number of parasite species occurring in a
sample (individual fish)(Bush et al., 1997). We calculated parasite species richness for individual
coho and Chinook salmon and then determined the average per fish species for each year of the
study. We used parasite species richness as a proxy for foraging diversity (Gonzalez and Poulin,
2005; Rhode, 1984). Prey species richness was calculated as the number of taxa represented in
the stomach contents of juvenile salmon. For this analysis prey were grouped into the 22 prey
categories described above. Prey species richness was calculated for individual coho and
Chinook salmon and then averaged by species for each year of the study.
15
We calculated the mean parasite abundance and mean stomach fullness for coho and
Chinook salmon in each year of the study. Parasite abundance is defined as the total number of
parasites in a sample divided by the total number of hosts examined (Bush et al., 1997). The
abundance of trophically transmitted parasites in a host is dependent on the consumption of
infected intermediate hosts (Marcogliese, 1995). Therefore, hosts with a high abundance of
parasites are assumed to have consumed a greater number of infected prey or prey that have
acquired more parasites, compared to hosts with a low parasite abundance captured at a similar
time and place. Stomach fullness was expressed as total prey wet weight relative to predator
body wet weight (% BW) for individual coho and Chinook salmon. Differences in parasite
abundance, stomach fullness and parasite and prey species richness of coho and Chinook salmon
were compared within years using the non-parametric Mann-Whitney test as data did not meet the
assumption of homogenous variance. In all Mann-Whitney tests, a Bonferroni correction was
used, resulting in an adjusted level of 0.006 to achieve a P-value of 0.05 (i.e. α = 0.05/8 = 0.006)
across multiple comparisons presented as realized experiment-wide error rate.
Parasite/prey composition
We calculated the percent numerical composition (%N) for both parasite and diet data for
each year. For parasites, %N was calculated as the numerical count of parasite species divided by
the total count of all parasites within a year. Similarly, for stomach contents, %N was calculated
as the count of prey items from the seven major prey categories divided by the total count of all
prey items within each year. Additionally, we calculated the percent biomass (%W) of stomach
contents from seven major prey categories. %W was calculated as the wet weight of each type of
prey divided by the total wet weight of all prey. For parasite and diet data, proportions were
multiplied by 100 in order to express values as percentages.
Community analysis
16
Communities of both parasite and prey were characterized using nonmetric
multidimensional scaling (NMS) ordination techniques (Mather, 1976). The abundance of each
parasite species and major prey group recovered from coho and Chinook salmon within a year
were used as the values for the sample units (year) in two matrices. The first matrix contained
mean parasite abundance for coho and Chinook salmon and consisted of 16 sample units (8 years
for 2 salmon species) by 10 parasite species. The second matrix contained mean prey abundance
for coho and Chinook salmon and consisted of 16 sample units by 7 prey groups. Outlier analysis
and summary statistics of matrices indicated that no sample units in any matrix fell beyond two
standard deviations of the mean parasite abundance; therefore no transformations were used (PCORD version 6.05 software: McCune and Mefford, 2009).
Ordinations of sample units (years) in parasite species space and prey taxa space were
performed separately using NMS ordination techniques (Mather, 1976) to examine differences in
the parasite and prey community composition between coho and Chinook salmon. Sorensen
distances were used for all ordinations. Due to the frequency of zeros in the community matrices
(>40%) and few sample units (<20), it was not possible to generate P-values using Monte Carlo
simulations for NMS. The non-parametric blocked multi-response permutation procedure
(MRPP) was used to test for differences in the parasite community and prey community between
salmon species (coho and Chinook salmon) within years. This method calculates the average
multivariate distance within each group (coho vs. Chinook salmon) and compares whether the
observed average within-group distance is significantly smaller than average within-group
distances generated by random assignment of sample units to groups. For both the MRPP of the
parasite ordination and the stomach contents ordination, we used “salmon species” i.e. coho vs.
Chinook salmon, as the grouping variable blocked by “year.” Ordinations and MRPP statistical
tests were conducted using PC-ORD version 6.91, (McCune and Mefford, 2009).
17
A blocked Indicator Species Analysis (ISA) (Dufrene and Legendre, 1997) was used to
identify parasite and prey taxa that were responsible for significant differences between salmon
species identified from MRPP. The importance of an indicator in distinguishing groups (indicator
value) is based on the relative abundance and frequency of occurrence of a parasite species or
prey taxa in a group (coho vs. Chinook salmon). Statistical significance was determined and Pvalues obtained using a Monte Carlo randomization (N=4999 simulations).
RESULTS
Yearling salmon were captured between June 19th and June 30th from 5 transects sampled
in years 2002-2009. Size at capture ranged from 137 to 236 mm FL for 234 UCR Su/F Chinook
salmon and 108 to 304 mm FL for 373 Columbia River coho (Table 2.1). There was a significant
difference in ln-transformed FL between salmon species and among years as well as a “year x
species” interaction (P<0.05, ANOVA, Table 2.2). Chinook salmon were significantly longer
than coho salmon in 2006 and 2009 (P<0.05, Fisher’s LSD). However, there was no relationship
between ln-transformed FL and parasite abundance or species richness for coho and Chinook
salmon (r<0.3, P> 0.05, Figure 2.3).
Feeding habits
In general, UCR Su/F Chinook salmon displayed a greater parasite abundance and higher
parasite species richness than Columbia River coho (Fig. 2.4). Chinook salmon parasite
abundance was significantly greater in four of the eight years (P < 0.05, Mann-Whitney test) and
parasite species richness was significantly higher than coho salmon in three of the years (P <
0.05, Fig. 2.4).
Prey diversity and stomach fullness were not significantly different between coho and
Chinook salmon in most years. Prey species richness was significantly higher (P<0.05, Mann-
18
Whitney test) in Chinook salmon in 2006 while stomach fullness (% BW) was not significantly
different in any of the years sampled (P>0.05, Fig. 2.5).
Parasite species composition
Parasite prevalence and abundance revealed that coho and Chinook salmon are infected
with similar parasite species during early marine residency (Table 2.3 & 2.4). The parasite
species composition of both coho and Chinook salmon was dominated by the trematode
Lecithaster gibbosus (Fig. 2.6), which accounted for an average of 30.4% (range: 6.3-56.4%) and
of 27.8% (range: 15.4-46.6%) of the parasites recovered from coho and Chinook salmon,
respectively. In coho salmon, the acanthocephalan Rhadinorhynchus trachuri was the second
most abundant parasite encountered in (mean = 20.6%, range: 0-50%). In Chinook salmon,
Anisakis simplex was the second most common parasite (mean = 24.6%, range: 4.2-31.8%).
Furthermore, coho salmon harbored two parasite species that were not encountered in Chinook
salmon: Lecithophylum sp. and Tubulovesicula sp. (Table 2.3 & 2.4). Both of these species were
rare (<1% of samples), and this study represents the first known record of Lecithophylum sp. in
coho salmon.
Diet composition
Yearling coho and Chinook salmon consumed similar types of prey in each year of the
study period (Table 2.5). Decapods accounted for the greatest numerical proportion of prey in the
diet of both coho (55.8%) and Chinook salmon (36.3%) although the proportion was highly
variable across years (coho range:17.6-76.5%, Chinook salmon range: 5.8-66.1%, Fig. 2.6).
Euphausiids were a larger portion of the coho diet, on average, than the Chinook salmon diet
(mean: 14.1% vs. 9.0%). In contrast, fish contributed a smaller proportion of the diet for coho
salmon compared to Chinook salmon (15.2 vs. 33.3%). Amphipods were also an important
component of the diet in terms of numerical composition of coho and Chinook salmon in some
19
years (Table 2.5). By mass, fish accounted for the greatest proportion of prey in the diet of both
coho (83.1%) and Chinook salmon (93.1%) although Chinook salmon consumed a greater
proportion of fish overall (Fig. 2.7) .
Ordination of parasite and prey communities
NMS ordination techniques and MRPP revealed that juvenile coho and Chinook salmon
exhibited distinct differences in recent feeding (stomach contents) and past feeding (parasite
analysis) in the marine environment. An NMS of the marine parasite community showed
separation between coho and Chinook salmon in parasite species space (Fig. 2.8a). In addition,
blocked MRPP revealed that the parasite community of coho and Chinook salmon was
significantly different within all years of the study (Blocked MRPP, P<0.005). Community
analysis of the stomach contents showed similar results to that of the parasite community. Coho
and Chinook salmon occupied different places in prey taxa space (Fig. 2.8b), demonstrating
distinct differences in their prey community. Statistically, these differences between coho and
Chinook salmon were significant across all years (Blocked MRPP, P<0.05)
The MRPP analysis also provides an A (agreement) statistic as an indicator of withingroup similarity. When all items within a group are identical, A=1 (McCune and Mefford, 2009).
A-statistic values less than 0.1 are common in community data even with significant separation of
groups. The A statistic for the MDS of the parasite community of coho and Chinook salmon
groups was 0.254 compared to 0.129 for the NMS of stomach contents. These results suggest
that the differences between coho and Chinook salmon were more clearly defined using the
parasites than the stomach contents.
Indicator Species Analysis
ISA identified three parasite species which were important in distinguishing between the
parasite community of coho and Chinook salmon (Table 2.6). The nematodes A. simplex and H.
20
aduncum were identified as indicators of the Chinook salmon parasite community. Chinook
salmon had a higher abundance of A. simplex in every year of the study. Similarly H. aduncum
was more abundant in Chinook salmon than in coho in all years except 2008 (Table 2.4). In
contrast, R. trachuri was identified as an indicator of the parasite community of coho salmon. R.
trachuri was more abundant in coho salmon than Chinook salmon in all years of this study except
for 2002 when R. trachuri was not recovered from either coho or Chinook salmon.
Similarly, ISA of stomach contents identified three prey items responsible for differences
in stomach contents of coho and Chinook salmon. Fish prey (Osteichthyes) and amphipods were
more abundant in Chinook salmon (P<0.05) while euphausiids were more abundant in the diet of
coho (P<0.05, Table 2.6).
DISCUSSION
In this study we accounted for many of the factors that can influence the marine diets of
juvenile salmon in order to increase our ability to detect interspecific differences in feeding. We
focused our analysis on coho and Chinook salmon from a common origin with similar migration
patterns. Thus, our results provided a robust comparison of feeding habits during early marine
residency for coho and Chinook salmon originating from the Columbia River. Unlike previous
studies which included fish from multiple genetic stocks and sampled across a relatively short
time frame, results from our analysis highlight consistent differences in feeding and prey diversity
between juvenile coho and Chinook salmon. Due to the nature of our sampling design we can
attribute variation in feeding to differences in feeding behavior such as prey handling, capture,
preference etc. rather than differences in feeding location, size or stock (Baldwin et al., 2008;
Weitkamp and Sturdevant, 2008).
We further improved our ability to detect differences in foraging between coho and
Chinook salmon by examining both stomach contents and parasites. Stomach content analysis
21
revealed few clear or consistent differences in stomach fullness or prey diversity between coho
and Chinook salmon across years. These results reflect the variable nature of recent foraging and
corroborate previous studies that report inconsistent differences in stomach fullness for these two
salmon species. Due to the dynamic nature of the marine environment and the rapid digestion
rate for coho and Chinook salmon (Benkwitt et al., 2009; Brodeur and Pearcy, 1987), it is not
surprising that stomach fullness or prey diversity did not reveal clear differences in feeding in this
or prior studies (Brodeur et al., 1992; Emmett et al., 1986). In contrast, patterns of parasite
species richness and parasite abundance, which take into account trophic interactions from the
past several months, suggested that Chinook salmon consumed a greater diversity and a greater
number of infected prey compared to coho salmon. A high feeding rate and diverse diet are
thought to be important to juvenile salmon during early marine residency to maintain high growth
rates (Brodeur et al., 1992; Fisher and Pearcy, 1988). Therefore, interspecific differences in these
metrics may relate to differences in rates of growth between coho and Chinook salmon exiting the
Columbia River and/or represent the ability of juvenile Chinook salmon to outcompete juvenile
coho for resources. A comparison of salmon feeding and growth across years of variable salmon
density would provide a better understanding of the potential for competitive interactions between
coho and Chinook salmon.
While the parasite data suggested a clearer picture of differences in the feeding habits of
coho and Chinook salmon compared to analysis of stomach contents, separate community
analysis using the two approaches revealed important similarities. The nematodes A. simplex and
H. aduncum were identified as significant indicators of the parasite community of Chinook
salmon across the study period while R. trachuri was consistently more abundant in coho salmon.
Differences in species composition and abundance of these parasites in coho and Chinook salmon
can be attributed to differences in host feeding habits. For example, the nematode A. simplex has
22
been recovered from a diversity of invertebrate intermediate hosts, however, it has been
associated with the consumption of fish and has proven reliable in detecting piscivory in a variety
of marine fish species (Blaylock et al., 1998; Campbell et al., 1980; Pascual et al., 1996b; Petric
et al., 2011). The relationship between A. simplex and host piscivory is due to the parasites’
ability to be transferred from one fish to another and accumulate via predation (Koie, 1993). In
addition, the relatively high abundance of another nematode, H. aduncum, in Chinook salmon
compared to coho is probably the result of an increased consumption of infected hyperiid
amphipods for Chinook salmon. While H. aduncum has been shown to use various
marine/brackish water invertebrates as intermediate hosts to infect fish, field studies have
concluded that amphipods may be especially important for transmission of H. aduncum (Klimpel
and Ruckert, 2005; Moravec and Nagasawa, 1986). Similarly, fish and amphipods were
identified as indicators in separating the stomach contents of Chinook salmon from coho.
Together, both parasite and stomach content analysis provide complimentary evidence that fish
and amphipods were consistently more important in the diets of Chinook salmon than coho
during early marine residency.
While some previous studies have suggested reduced stomach fullness, on average, for
coho salmon compared to Chinook salmon (Baldwin et al., 2008; Schabetsberger et al., 2003),
few have identified specific prey items that are consumed more by coho vs. Chinook salmon. In
the current study ISA revealed increased abundance and frequency of euphausiids and the
acanthocephalan R. trachuri in coho vs. Chinook salmon. The lifecycle of R. trachuri is not
completely understood, however, other parasites in the same phylum as R. trachuri are known to
use a variety of zooplankton taxa as intermediate hosts such as amphipods and euphausiids
(Rhode 1984). More specific information regarding transmission routes can be inferred from
other known host records. Prior studies reveal that R. trachuri is a parasite commonly recovered
23
from the gut of jack mackerel (Trachurus symmetricus) and Pacific saury (Cololabis saira)
(Hughes, 1973; Jacobson et al., 2012) which have a diet dominated by euphausiids (Brodeur et
al., 2008; Emmett and Krutzikowsky, 2008; Johnson et al., 2008; Sugisaki and Kurita, 2004).
The evidence indicates that euphausiids are the most likely prey responsible for the increased
abundance of R. trachuri in juvenile coho salmon. Studies that analyze the parasites of salmon
prey would be needed to further clarify the lifecycle of R. trachuri and other parasites, increasing
the precision of trophically transmitted parasites in detecting differences in diet.
Based on both stomach contents and analysis of trophically transmitted parasites, coho
and Chinook salmon originating from the Columbia River consumed similar prey, however,
Chinook salmon consistently consumed more fish and amphipods while coho ate more
euphausiids. It has been suggested that resource partitioning and a lack of similarity in the diet,
as we observed in this study, may indicate that the potential for interspecific competition is low
(Brodeur and Pearcy, 1990). Alternatively, recent studies suggest low niche overlap may be the
result of competitive interaction (Herder and Freyhof, 2006; Ruggerone and Nielsen, 2004).
Under this hypothesis, the less dominant species will be forced to switch to alternative less
preferred prey. While this pattern has not been observed previously between coho and Chinook
salmon, interspecific competition has been demonstrated in other salmonid populations
(Ruggerone and Nielsen, 2004). For example, in the Bering Sea, Ruggerone et al. (2003)
documented an alternating cycle of prey composition for sockeye salmon O. nerka. They
observed reduced consumption of higher energetic value prey per gram (fish, Davis et al. 2005)
by sockeye salmon in years when competitively dominant pink salmon were present in the
Bering Sea (even years) compared to years when pink salmon were absent from the system. In
the current study, Chinook salmon exhibited greater parasite abundance, higher parasite species
richness and increased piscivory compared to coho. These differences in feeding could be the
24
result of a competitive advantage by Chinook salmon resulting in prey-switching by coho to less
energetically valuable zooplankton prey. Lab studies could clarify interspecific differences in
prey choice in response to variations in population density, prey quality and/or prey availability.
The vast majority of the fish in this study were likely of hatchery origin (>90%) and were
released into the Columbia River during a one month period (April 1st to May 1st, L. Weitkamp
pers. comm., Fig. 1.2). Historically, coho and Chinook salmon from the Columbia River
migrated through the Columbia River throughout the year (Lichatowich, 1999; Williams et al.,
2005). Reducing temporal and spatial overlap through well-planned hatchery releases may, in
turn, reduce potential competitive interactions between coho and Chinook salmon and make prey
of higher caloric value (i.e. fish) more available to coho. A combined effort of researchers and
those conducting large scale hatchery releases could provide a better understanding of the
interaction between various populations of Columbia River salmon.
Given that we sampled stock groups from the same basin, that entered the ocean at
similar times and with similar early ocean distributions, it is likely that the observed differences
between parasite and prey communities are an accurate reflection of variation in marine feeding
habits. While parasites offered insight into long-term patterns of feeding that were not detected
through stomach content analysis, traditional diet analysis revealed fine-scale variability in prey
that could not be detected using parasites alone. For instance, diet analysis suggested a high
consumption of euphausiids by coho and Chinook salmon in 2002 compared to other years.
However, the parasite most commonly associated with euphausiids, the acanthocephalan R.
trachuri, was absent in both coho and Chinook salmon during this year, which suggests an
increase in euphausiid abundance in the coastal ocean immediately prior to the 2002 sampling
event that was not detected through parasite analysis. The 24-hour “snapshot” provided by
traditional diet analysis allows for the accurate depiction of recent foraging events that may be
25
undetectable in parasite data but may not reflect broader patterns of foraging behavior. In
addition, the relative abundance of trophically transmitted parasites in salmon prey may not be
consistent across regions and years. Including both parasite and diet data from fish with similar
marine distributions provided a better understanding of feeding behavior overall and allowed for
an accurate comparison of coho and Chinook salmon feeding habits during early marine
residency.
Research aimed at understanding the diets of coho and Chinook salmon is extensive and
has revealed significant variability in prey composition by month, year and location. However,
these factors could obscure differences when comparing the feeding behavior of two species of
salmon. By accounting for trophic interactions from the time of ocean entry to capture for two
populations of salmon with overlapping spatial and temporal distribution, this study revealed that
while coho and Chinook salmon feed on similar types of prey, they exhibit significant variation in
their utilization of major prey taxa. While these results provide insight into the biology of
juvenile salmon they also raise important questions about hatchery production in the Columbia
River. Are the interspecific differences we observed in diet of coho and Chinook salmon the
result of competitive interaction? Should hatchery releases take into account historical run timing
and habitat carrying capacity to reduce competition between salmon species? Future
investigation should focus on these and other questions aimed at understanding the effects that
multispecies, large-scale hatchery releases have on growth and survival of this important
resource.
26
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30
Table2.2.
2.1.Sample
Sample
size,
mean
length
SEmean
and
Table
size,
mean
forkfork
length
(mm (mm
± SE)±and
mean
weight
(gram
±
SE)
of
Upper
Columbia
River
weight (gram ± SE) of Upper Columbia River summer andsummer
fall
and fallsalmon
Chinook
andRiver
Columbia
River coho
collected
Chinook
andsalmon
Columbia
coho collected
off the
coast of
off
the
coast
of
Washington.
Washington.
Chinook salmon
Coho salmon
Year
n Size (FL, mm) (Wt., g)
n Size (FL, mm) (Wt., g)
2002
32
177±4
73±5
68
175±4
66±5
2003
29
191±4
89±6
40
187±3
76±4
2004
37
190±5
92±7
44
185±4
78±5
2005
13
177±5
70±7
19
177±8
61±5
2006
35
189±4
92±6
47
169±4
59±5
2007
34
190±4
86±5
58
180±2
67±3
2008
23
207±8
126±13
48
186±3
82±4
2009
31
205±6
117±11
49
170±4
63±6
31
Table 2.2. ANOVA results for ln transformed fork length of
juvenile salmon between species (coho and Chinook salmon)
and years (2002-2009).
Source
ln(FL)
Year
Species
Year x Species
Error
Total
Sum of Squares df
0.637
0.591
0.491
11.38
13.25
7
1
7
592
607
Mean Square F-Ratio P-Value
0.091
0.591
0.070
0.019
4.73
30.72
3.65
<0.001
<0.001
<0.001
32
Table 2.3. Prevalence (% infected) of parasite species from the stomach, intestine and body
cavity of coho and Chinook salmon collected in June of 2002-2009 off the coast of
Washington, U.S. Empty cells indicate species not found.
Oncorhynchus sp. Parasite Species
Coho Salmon
Anisakis simplex
Bothriocephalus sp.
Hemiurus levinseni
Hysterothylacium aduncum
Lecithaster gibbosus
Lecithophylum sp.
Parahemiurus merus
Rhadinorhynchus trachuri
Tetraphyllidean sp.
Tubulovesicula sp.
Chinook Salmon
Anisakis simplex
Bothriocephalus sp.
Hemiurus levinseni
Hysterothylacium aduncum
Lecithaster gibbosus
Lecithophylum sp.
Parahemiurus merus
Rhadinorhynchus trachuri
Tetraphyllidean sp.
Tubulovesicula sp.
2002 2003 2004
7.4 12.5 6.7
1.5
1.5
1.0 13.3
8.8
5.0
5.9
5.0
6.7
2.2
1.5
2.5
2.2
7.5 53.3
1.5
24.4
1.5
2005 2006 2007 2008 2009
8.2
3.6
1.4 24.0
34.4
3.1
6.3
25.0
28.1
13.8
3.1
5.3
31.6
14.3
44.9
15.8
1.5
22.9
43.8
6.0
34.0
26.3
21.5
2.5
6.1
4.8
1.8
14.4
1.8
2.8
12.5
4.2
12.0
2.0
8.2
7.7
34.3
26.5
3.4
65.6
6.9
31.3
13.8
1.8
27.3
56.8
23.8
46.2
34.3
77.1
29.4
23.5
13.4
3.4
3.1
18.8
12.5
6.9
6.9
1.3
16.2
24.3
48.6
7.7
38.5
2.0
5.9
23.5
4.3
17.4
3.1
6.3
33
Table 2.4. Mean abundance (# of individuals/fish) of parasite species from the stomach,
intestine and body cavitiy of coho and Chinook salmon collected in June of 2002-2009 off the
coast of Washington, U.S. Empty cells indicate species not found.
Oncorhynchus sp. Parasite Species
Coho Salmon
Anisakis simplex
Bothriocephalus sp.
Hemiurus levinseni
Hysterothylacium aduncum
Lecithaster gibbosus
Lecithophylum sp.
Parahemiurus merus
Rhadinorhynchus trachuri
Tetraphyllidean sp.
Tubulovesicula sp.
Chinook Salmon
Anisakis simplex
Bothriocephalus sp.
Hemiurus levinseni
Hysterothylacium aduncum
Lecithaster gibbosus
Lecithophylum sp.
Parahemiurus merus
Rhadinorhynchus trachuri
Tetraphyllidean sp.
Tubulovesicula sp.
2002
0.07
0.03
0.01
0.13
0.10
2003 2004 2005 2006 2007 2008 2009
0.13 0.07
0.10 0.05 0.10 0.58
0.01
0.03
0.15
0.25
0.05
0.10
0.01
0.03
0.36
0.07
0.02
0.02
1.49
0.38
0.05
0.79
0.27
1.98
0.19
0.18
0.31
0.88
0.06
0.94
0.58
0.21
0.02
0.06
0.06
0.02
0.19
0.02
0.02
0.15
0.04
0.18
0.02
0.34
0.03
0.19
0.41
1.22
0.14
0.11
0.08
0.37
0.50
0.39
1.03
0.07
0.38
0.17
0.14
0.46
2.00
0.23
2.23
0.51
7.06
0.41
1.38
0.13
0.74
0.03
0.19
0.28
0.03
0.10
0.07
0.10
0.16
1.24
0.73
0.08
0.46
0.29
0.09
0.76
0.04
0.52
0.03
0.06
34
Table 2.5. Mean abundance (# of individuals/fish) of major prey from the
stomachs of coho and Chinook salmon collected in June of 2002-2009 off the
coast of Washington, U.S. Empty cells indicate taxa not found.
Oncorhynchus sp. Prey Category
Coho Salmon
Osteichthyes
Decapoda
Copepoda
Euphausiacea
Amphipoda
Insecta
Other
Chinook Salmon Osteichthyes
Decapoda
Copepoda
Euphausiacea
Amphipoda
Insecta
Other
2002 2003 2004 2005 2006 2007
2.79 1.59 1.67 1.43 1.36 0.70
19.18 6.05 5.48 3.24 0.86 10.56
0.57
0.04
5.79 3.54 0.07 4.33 0.52 0.18
0.95 1.79 0.26
1.76 1.20
0.30 0.28 0.36 0.05 0.10 0.08
0.04
2008 2009
2.27 0.96
7.66 6.19
0.21
0.76 0.06
0.02 0.71
0.00 0.00
2.65
3.39
2.89
2.47
1.32
1.42
0.16
0.21
0.26
1.29
7.84
0.52
2.32
4.36
0.04
0.24
0.56
3.88
0.30
1.03
1.27
4.45
0.09
0.09
1.00
0.27
2.12
7.58
0.03
0.52
0.76
1.84
1.91
1.34
0.13
0.69
35
Table 2.6. Indicator taxa (P<0.05) for stomach content analysis and parasite analysis
of coho and Chinook salmon collected in June of 2002-2009 off the coasts of
Washington, U.S.
Method
Indicator taxa
Oncorhynchus sp. Indicator value P value
Stomach contents Osteichthyes
Chinook salmon
52.1
0.015
Amphipoda
Chinook salmon
69.1
0.023
Euphausiacea
Coho salmon
67.2
0.036
Parasites
Anisakis simplex
Chinook salmon
Hysterothylacium aduncum Chinook salmon
Rhadinorhynchus trachuri Coho salmon
75.8
73.6
63.5
0.008
0.013
0.015
36
Figure 2.1. Percent of total Oncorhynchus kistuch (open triangles) and O. tshawytscha
(open circles) captured at stations (closed circles) off the coast of Washington, USA in
June of 2002 -2009. Size of open symbols represents the percent of fish captured at
corresponding station. Line indicates 200m depth contour.
37
Figure 2.2. Number of (a) Columbia River coho and (b)
upper Columbia River summer and fall Chinook salmon
released from hatcheries (left y-axis) into the Columbia
River (solid lines, 2002-2009) and captured by purse seine
(bi-weekly mean #/round haul, right y axis) in the
Columbia River estuary in 2006-2009 (dashed lines,
estuary catch data provided by Laurie Weitkamp, NOAA
fisheries). Vertical dotted line represents time of the
current study’s ocean sampling for juvenile salmon.
38
Figure 2.3. Mean natural log transformed fork length (± SE) vs. (a&b) mean parasite
species richness (± SE) and (c&d) mean parasite abundance (± SE) for coho and
Chinook salmon collected in June of 2002-2009 off the coast of Washington, U.S. Note
varying scales on axis.
39
Figure 2.4. (a) Parasite species richness (mean +/- SE) and (b) parasite abundance
(mean +/- SE) of juvenile coho (grey bars) and Chinook salmon (black bars)
collected in June of 2002-2009 off the coast of Washington, U.S. Asterisks denote
significant differences within years using Bonferroni corrected alpha-value
(P<0.006).
40
Figure 2.5. (a) Prey species richness (mean +/- SE) and (b) stomach fullness
(mean +/- SE) of juvenile coho and Chinook salmon collected in June of 20022009 off the coast of Washington, U.S. Asterisks denote significant differences
within years using Bonferroni corrected alpha-value (P<0.006). Data provided
by Elizabeth Daly, Cooperative Institute for Marine Resource Studies.
41
Figure 2.6. Numerical Percentage of major (a&b) prey categories and (c&d) parasite
species in the diet of (a&c) coho and (b&d) Chinook salmon collected in June of 20022009 off the coast of Washington, U.S.
42
Figure 2.7. Percentage by weight of major prey categories in the diet of (a) coho and (b)
Chinook salmon collected in June of 2002-2009 off the coast of Washington, U.S.
43
Figure 2.8. Nonmetric multidimensional scaling analysis of (a) stomach contents and (b)
parasites for Chinook salmon (closed circles) and coho salmon (open triangles) comparing
similarity in parasite and prey communities across years.
44
CHAPTER 3:
INFLUENCE OF OCEAN ECOSYSTEM VARIABILITY ON TROPHIC
INTERACTIONS AND SURVIVAL OF JUVENILE COHO AND CHINOOK SALMON
James P. Losee
ABSTRACT
Research conducted throughout the Northern California Current has identified linkages
among recruitment success of Pacific salmon and ocean conditions and the composition of the
copepod community on the shelf during the early marine residency of juveniles. Copepods do not
make up a large portion of the diet of coho and Chinook salmon; therefore it is hypothesized that
variability in near-shore marine processes such as coastal upwelling affects the quality (lipid
content) and/or species composition of zooplankton prey for planktivorous fish which may. in
turn. affect juvenile salmon growth and survival through bottom-up processes. Trophically
transmitted parasites of salmon use copepods and other zooplankton as intermediate hosts to
become distributed throughout the food web. Therefore,the abundance and species composition
of parasites can provide insight into the abundance and species composition of the salmon food
web at trophic levels not detected through traditional diet analysis. We examined the abundance
and composition of trophically transmitted marine parasites in juvenile coho and Chinook salmon
from the Columbia River, USA, during an eight year period (2002-2009) to test the hypothesis
that parasite community structure is related to variability in physical and biological variables in
the ocean. Furthermore, if variability in ocean conditions and prey composition during ocean
immigration is related to salmon abundance through bottom-up processes, we expected a
relationship between variability in parasite species composition and subsequent adult returns.
Correlation analysis was used to compare interannual variability in the parasite community
assemblage to indices of survival for Columbia River coho and Chinook salmon. Mean seasurface temperature and the biomass anomaly of sub-tropical, lipid-poor copepod species present
in coastal waters during early marine residency (April-June) explained > 50% of the variability in
the parasite community of juvenile coho and Chinook salmon. In addition, interannual variability
in the parasite community of juvenile salmon explained 89% of the variability in adult returns of
summer-run Chinook salmon 3 years later and 36% of the variability in survival of coho salmon 1
year later. These results indicate a linkage between variability in copepod community
45
composition during the summer and salmon prey and suggest that the quality and/or composition
of the prey directly affects Chinook salmon survival during the first few months in the ocean.
INTRODUCTION
Large fluctuations in the abundance of Pacific salmon (Oncorhynchus spp.) were first
documented soon after the arrival of early settlers to the Columbia River in the early 1800s
(Lichatowich, 1999). However, studies in the Northern California Current (NCC) indicate that
salmon abundance fluctuated with shifts in ocean climate centuries prior to modern-day fishing
(Beamish et al., 1999; Mantua et al., 1997). While correlative studies suggest that interannual
variability in salmon abundance is linked to variability in local and basin-scale indices of ocean
conditions (Mackas et al., 2007), the processes that regulate salmon abundance in the NCC
remain poorly understood. Studies have demonstrated associations between juvenile salmon
survival during their first summer in the ocean and the Pacific Decadal Oscillation (PDO)(Mantua
et al., 1997; Rupp et al., 2011), the strength and timing of coastal upwelling (Scheuerell and
Williams, 2005) and sea-surface temperature (SST)(Mueter et al., 2002; Peterson and Schwing,
2003). It appears that a large proportion of the total lifetime mortality for Pacific salmon occurs
during the first few months of marine residency (Beamish and Mahnken, 2001; Beamish et al.,
2004). While factors that contribute directly to variability in marine survival rates of Pacific
salmon are multifaceted, rapid growth and increased salmon survival appear to occur when the
PDO is negative, coastal upwelling is strong and sustained, and SST is relatively cold (Mackas et
al., 2007). These observations have led researchers to hypothesize that ocean climate and salmon
abundance are linked through bottom-up processes, which regulate the quality (lipid content) and
species composition of their food supply. In addition, relationships between ocean conditions and
salmon abundance have proven useful in efforts to forecast adult returns of some Pacific salmon
populations (Nickelson, 1986; Logerwell et al., 2003; Rupp et al., 2011; Scheuerell and Williams,
2005). However, models that include ocean indices to predict recruitment of salmon and other
marine fish species often perform well for periods of time but become unreliable following a shift
in ocean climate. This phenomenon was described well by Beamish et al. in 1999 and, more
recently, by Rupp et al. (2011) and highlights the need for a better understanding of the
mechanisms that link variability in ocean climate to variability in adult salmon abundance.
In an effort to identify a mechanistic link between physical processes in the ocean and the
biological response of the marine ecosystem, consistent sampling of marine zooplankton in the
46
NCC has occurred since 1996. Bi-weekly sampling has highlighted fluctuations in abundance
and species composition of marine copepods that coincide with changes in SST and ocean
circulation (Hooff and Peterson, 2006, Kiester et al. 2011, Peterson and Schwing, 2003). It is
now known that two distinct copepod communities exist in the NCC (Morgan et al., 2003;
Peterson and Keister, 2003). In years of negative PDO the summer copepod community in the
NCC is typically dominated by large, lipid-rich, sub-arctic boreal fauna (Peterson and Keister,
2003) likely transported from the north. In contrast, years of positive PDO are associated with
smaller, subtropical zooplanktons which tend to be less lipid-rich (Hooff and Peterson, 2006; Lee
et al., 2006; Mackas et al., 2007) likely transported from the south or offshore. The relationship
between the biomass of “lipid-rich” vs. “lipid-poor” copepod species on the shelf during late
spring/early summer and the growth and survival of juvenile salmon during this time period
(Mackas et al., 2007) suggests that adult salmon abundance is linked, through bottom-up
processes, to variability in the ocean circulation patterns that determine species composition and
biomass of copepods (Bi et al., 2011; Keister et al., 2011). However, copepods make up a small
contribution of the diet of coho and Chinook salmon (Brodeur et al., 1992) which consume
primarily planktivorous fishes and large zooplankton (i.e. euphausiids).
The species composition and abundance of trophically transmitted parasites in marine
fishes is dependent on the abundance of free-living fauna in the marine environment and host diet
(Marcogliese, 2005). Trophically transmitted parasites rely on consumption of intermediate hosts
such as copepods, euphausiids, and planktivourous fishes prior to becoming mature in their
vertebrate final host (i.e. teleosts, elasmobranch, marine mammals etc.). While the majority of
trophically transmitted parasites use copepods as intermediate hosts, the short lifespan of
copepods has resulted in the development of transport, or second intermediate hosts as part of the
parasite lifecycle in order to maintain their presence in the food web (Marcogliese, 2002; Petric et
al., 2011). Longer lived, predatory invertebrates (i.e. euphausiids, amphipods and chaetognaths)
and planktivorous fishes serve as paratenic hosts and bridge the gap between copepods and the
preferred final host. Therefore, the absence of any one of a parasite’s required intermediate hosts
in the environment will result in the absence of that parasite in the food web (Choisy et al., 2003;
Rhode, 1984). In this way, local and basin scale oceanographic characteristics such as coastal
jets, temperature, and specific mass of water which influence zooplankton abundance and
distribution, have been shown to influence parasite assemblages in marine fishes (Gonzalez and
Poulin, 2005; Klimpel and Ruckert, 2005).
47
The ecological responses to variability in ocean climate are complex and not completely
understood. In the NCC, early and sustained upwelling, cold temperatures and high biomass of
lipid-rich “cold-water” copepods are associated with increased growth and survival of juvenile
salmon during early marine residency (Beamish et al., 2004; Peterson and Schwing, 2003; Trudel
et al., 2005). These findings suggest that prey quality and/or composition in early summer are
important in controlling interannual variability in the population size of Pacific salmon. While
recent efforts using multivariate approaches indicate a relationship between variability in marine
diets of juvenile Chinook salmon captured in May and salmon survival (pers. comm E. Daly), no
study to date has identified trophic interactions that relate significantly to favorable
oceanographic conditions or adult returns of Pacific salmon.
The primary objective of this study was to determine if the species composition and
abundance of the marine trophically transmitted parasites of juvenile coho and Chinook salmon,
relate to variability in physical and biological indices in the ocean during early marine residency.
We quantified interannual variation in the trophically transmitted parasites of yearling coho and
Chinook salmon during a period of variable ocean conditions (2002-2009) and related that
variation to a set of basin and local scale oceanographic variables previously shown to be
associated with salmon survival and/or abundance. In addition, parasite communities of juvenile
salmon were compared to variability in the near-shore zooplankton community. If interannual
variability in the copepod community affects the quality and/or the composition of salmon prey,
we expect a corresponding shift in those salmon parasites that use copepods as intermediate hosts.
Finally, variability in parasite assemblages across years was compared to fluctuations in salmon
survival to determine if variation in trophically transmitted parasite assemblage reflects variation
in recruitment success of juvenile salmon during early marine residency.
METHODS
Fish Collections
This study is one component of a multidisciplinary project designed to examine the early
ocean ecology of juvenile Pacific salmonids and the factors that affect their marine survival.
Samples for this project were collected during 10 days in the second half of June in 2002-2009.
Sampling stations were located on five transects (Fig. 3.1) ranging from La Push, Washington
(47º 55’N) to the Columbia River (46º53’N). Stations on each transect began as close to shore as
possible and ranged from 3 to 50 km offshore. Juvenile salmon were collected during daylight
hours using a Nordic 264-rope trawl towed at the surface. The mouth opening of the trawl was
48
20 m deep and 30 m wide when towed. Tows lasted for 15-30 min at an approximate speed of
6.5 km h-1. Yearling coho and Chinook salmon were distinguished from subyearling, subadult or
adult fish by fork length (Fisher et al., 2007) at-sea then immediately frozen.
Collection of parasites and analysis
A total of 373 yearling coho salmon and 234 yearling Chinook salmon were examined for
trophically transmitted parasites. Parasite recovery from stomachs, intestines, body cavities and
swim bladders was done according to standard necropsy procedures (Arthur and Albert, 1994).
The majority of parasites were identified to species. To confirm the identity of some species,
individual parasites were compared to specimens from the reference parasite collection of R.
Olson at the Hatfield Marine Science Center and to type specimens from the U.S. National
Parasite Collection (Beltsville, MD, U.S.A.).
Genetic stock identification
The relative probability of stock origin was estimated for each sample using the
likelihood model of Rannala and Mountain (1997), as implemented in the genetic stock
identification software ONCOR (Kalinowski et al. 2007). A microsatellite DNA baseline data
from Van Doornik et al. (2007) was used for coho salmon and from the standardized database
described by Seeb et al. (2007) for Chinook salmon. Coho salmon were genotyped at 11
microsatellite DNA loci (Van Doornik et al. 2007) and Chinook salmon were genotyped at 13
loci (Teel et al. 2009). Coho from the Columbia River Evolutionary Significant Unit (ESU) and
Chinook salmon from the Upper Columbia River Summer and Fall (UCR Su/F) ESU were
included in this study (mean probability: 92.6%)
Physical and biological environmental indices
The major focus of this study was to determine if variability in the parasite community of
juvenile salmon relates to variability in ocean conditions. Therefore, we selected ocean indices
previously shown to be related to survival and productivity of Pacific salmon. We hypothesized
that variability in these ocean indices are related to changes in the prey composition of juvenile
salmon, which ultimately affects their survival through bottom-up processes. If this hypothesis is
supported, abundance and/or species composition of trophically transmitted parasites should be
related to variability in physical and biological ocean indices.
Pacific Decadal Oscillation index
The Pacific Decadal Oscillation (PDO) index is the leading principal component of North
Pacific monthly sea surface temperature variability (northward of 20N) (Mantua et al., 1997).
49
Shifts in the sign of the PDO (+/-) have been correlated with variability in zooplankton species
composition (Peterson and Schwing, 2003) and catches of Pacific salmon (Mantua et al., 1997).
Negative values of the PDO are typically associated with increased upwelling, relatively cold
surface temperatures and lipid-rich copepod communities on the shelf (Keister et al., 2011;
Mackas et al., 2007), whereas positive values of the PDO have been associated with poleward
transport of warm surface water, southern origin, lipid-poor copepod species and anomalously
low catches of Pacific salmon. We calculated various 3-month running means of the PDO for the
6 months prior to capture of juvenile salmon for each year of the study as well as the mean of
January –June.
North Pacific Gyre Oscillation
The North Pacific Gyre Oscillation (NPGO) index is calculated from a principal
component (PC) analyses of sea surface height (SSHa) anomalies of the North Pacific. While
PDO represents the first PC of SST, the NPGO represents the second PC of SSHa and is
statistically independent of the PDO (Di Lorenzo et al., 2008). Variability in the NPGO has been
positively correlated with various measures of productivity (nutrients and chlorophyll) in the
North Pacific Ocean, which may have an effect on higher trophic levels (Di Lorenzo et al., 2008).
If fluctuations in the NPGO are related to variability in prey quality and/or composition for
salmon, we would expect interannual variability of the NPGO to relate to variability in the
species composition or abundance of trophically transmitted parasites. Similar to the PDO index,
we calculated 3-month running means as well as the 6-month average for the period prior to our
sampling (January-June).
Sea-surface temperature
SST has been used as a proxy for the type of water mass and copepod community present
on the shelf (Morgan et al., 2003). Furthermore, SST during early marine residency has been
shown to be negatively correlated with salmon survival (Rupp et al., 2011). The mean daily SST
was calculated during the period of outmigration for fish in our study (April-June) to determine if
variability in SST was related to variability in parasite assemblage during early marine residency.
Calculations were based on data from the NOAA Stonewall Banks Buoy (Buoy 46050,
www.ndbc.noaa.gov) located 20 NM west of Newport, Oregon (44.6 N 124.5 W).
Cumulative upwelling
In the NCC, coastal upwelling events are dominant physical processes and their strength
and frequency can have a dramatic effect on food web structure on the shelf. It has been shown
50
that cumulative cross-shelf transport in the NCC influences productivity in the nearshore marine
environment (Hickey et al., 2006; Pierce et al., 2006) and is important in determining the
distribution of zooplankton on the shelf (Keister et al., 2009) therefore we expected that
cumulative upwelling would be related to the trophically transmitted parasites which use
zooplankton to infect juvenile salmon and their prey (ie. planktivorous fish). We summed daily
values of Bakun’s coastal upwelling index for all months prior to our ocean sampling for salmon
(January-June) for each year in this study.
Columbia River plume volume
While direct impact of the Columbia River plume on the various salmon stocks leaving
the Columbia River is not fully understood, increased nutrient input and zooplankton biomass
associated with plume dynamics (fronts, eddies, trapped waves) may enhance food availability
and prey composition in the study area (Hickey and Banas, 2003; Kudela et al., 2010; Morgan et
al., 2005). Several factors alter the size and shape of the Columbia River plume (i.e. wind stress,
river discharge, tidal dynamics). We used daily SELFE (Semi-implicit Eulerian-Lagrangian
Finite Element) simulations of plume volume which have been shown to effectively describe its’
three dimensional size (Burla et al., 2010). If interannual variability in the plume size or
associated fronts alters zooplankton abundance or species composition (De Robertis et al., 2005),
we expect a corresponding shift in the parasite community of juvenile salmon foraging in areas
influenced by the plume. We calculated plume volume for the months of peak salmon
outmigration (April-June) prior to our cruises as described by Burla et al. (2010). Plume volume
data were obtained from the the Center for Coastal Margin Observation and Prediction (CMOP,
www.stccmop.org, 2012).
Northern and southern copepod indices
Relationships between adult returns of Pacific salmon and copepod community
composition have been well documented (Mackas et al., 2007; Peterson and Schwing, 2003).
While salmon do not typically consume copepods it is hypothesized that the variability in lipid
content of copepod species (arctic boreal vs. subtropical) can affect salmon indirectly by altering
the lipid content or species composition of their planktivorous prey. Differences in species
composition and abundance of trophically transmitted parasites can signal variability in presence
or abundance of certain invertebrates in the food web (Marcogliese, 1995; Zander et al., 2000).
Therefore, if changes in the copepod community composition (i.e. lipid-rich vs. lipid-poor
copepods) alter either the quality or composition of the prey of juvenile salmon we would expect
51
variability in the parasite community to be related to fluctuations in the copepod community.
Zooplankton were sampled bi-weekly at a hydrographic station five nautical miles off Newport,
OR. Calculation of the Northern Copepod Index is the log10-transformed biomass anomaly
(1998-2011) averaged during the period of peak outmigration of juvenile salmon in the study
(April-June) of three species of lipid-rich, boreal, cold–water copepods: Calanus marshallae,
Pseudocalanus mimus, and Acartia longiremis. The Southern Copepod Index is the log10transformed biomass anomaly (1998-2011) of a suite of sub-tropical species considered to be
lipid-poor: Acartia tonsa, Calanus pacificus, Calocalanus styliremis, Calocalanus tenuis,
Clausocalanus spp., Corycaeus anglicus, Ctenocalanus vanus, Mesocalanus tenuicornis, and
Paracalanus parvus (Hooff and Peterson, 2006).
Adult salmon returns
Adult salmon returns to Priest Rapids Dam were used as a proxy for survival of UCR
Su/F Chinook salmon. Priest Rapids Dam is located above the confluence of the Snake River,
therefore the number of adults counted at this dam include only adults returning to the upper
reaches of the Columbia River. Live-fish counting consisted of 16-hour, daily observation at fish
ladders during the period of returning summer-run adults (www.cbr.washington.edu/dart/
dart.html, 1995-present). Age-at-return of Chinook salmon from the UCR Su/F genetic stock
group ranges from 2-6 years (Myers, 1998); however, the majority mature as 3, 4 and 5 year olds
(Myers, 1998; Williams et al., 2005). The “yearling” life-history makes up a minority (<30%)of
the adult returnin the upper Columbia River (Myers, 1998); therefore counts of returning adults at
Priest Rapids Dam include other life histories (i.e. subyearlings). However, the yearling lifehistory is most commonly associated with earlier run timings compared to subyearlings (Myers,
1998). Therefore we calculated Chinook salmon survival as the number of adult Chinook salmon
crossing Priest Rapids Dam during the summer (June 14th-August 13th) using a 2, 3 and 4-year lag
from the year of capture in the ocean. In addition, this estimate of survival does not include
spawners below Priest Rapids Dam or in-river mortality occurring above the dam. Finally, stock
specific estimates of the number of smolts outmigrating compared to the number of adults
returning from the same cohort (SAR) may provide a more accurate estimate of survival, however
stock specific estimates of SARs are not available for this stock group.
We used the Oregon Production Index (OPIH) calculated from estimates of smolt-toadult survival for Washington, Oregon and California stocks as a proxy for coho salmon survival
(L. Weitkamp pers. comm). Coho migrate to the ocean as yearlings and the majority
52
(~90%)return to spawn in late spring 16 months later (Pearcy, 1992, Weitkamp, 1995); therefore
we used a one-year lag from the year of ocean capture to estimate survival of coho salmon.
Data structure and statistical analysis
For all analyses, trophically transmitted parasite abundance for juvenile coho and
Chinook salmon was averaged by year. The data were arranged into two parasite species
matrices (one for Chinook salmon and one for coho) and one environmental matrix. In these
three matrices, the parasite species or environmental variables formed the columns and years
formed the rows. Outlier analysis and summary statistics of matrices were conducted to reveal
the need for transformations using PC-ORD (v. 6.05) (McCune and Mefford, 2009). No sample
units in either species matrix fell beyond two standard deviations of the mean parasite abundance;
therefore, no transformations were used. No relativizations were used because of the interest in
patterns of abundance of dominant species.
Ordinations of sample units in parasite species space were performed using NMS
ordination techniques (Mather, 1976) to describe variability in the parasite community and relate
the parasite communities of coho and Chinook salmon to environmental variables. Sorensen
distances were used for all ordinations. Plots and output of instability and stress were examined
to identify the number of ordination axes at which the reduction in stress gained by adding
another axis was inconsequentially small (Mather 1976). Stress is a measure of the lack of fit of
the ordination, represented by a few dimensions (axes), to the original parasite data in
multidimensional species space; the lower the stress, the better the fit of the ordination. Due to
the frequency of zeros in the community matrix (>40%) and few sample units (<10), it was not
possible to generate P-values using Monte Carlo simulations for NMS.
To determine if parasite species composition and abundance differed across years, a
multi-response permutation procedure (MRPP) was used. This method calculated the average
multivariate distance within each year and compares whether the average within-group distance is
significantly smaller than average within-group distances generated by random assignment of
sample units to groups. A Sorensen distance measure was used for consistency with the NMS
ordinations. Correlation analysis was used to test whether variability in the parasite community,
described by Axis 1 of ordinations of juvenile salmon parasites, was related to variability in seven
environmental variables described above.
If variability in the trophic interactions of juvenile salmon, inferred from trophically
transmitted parasites, has an effect on salmon in a way that influences growth or condition during
53
early marine residency then we expect relative survival, as indicated by adult returns, to be
related to the parasite assemblage. Therefore, we regressed adult returns of coho and Chinook
salmon against Axis 1 scores from NMS ordinations of the parasite communities.
RESULTS
Yearling salmon were captured between June 19th and June 30th from 5 transects sampled
in years 2002-2009. Size at capture ranged from 137 to 236 mm for UCR Su/F Chinook salmon
and 108 to 304 (mm, FL) for Columbia River coho(Table 3.1). The number of parasite taxa
recovered differed for coho and Chinook salmon. A total of 8 taxa of marine-origin, trophically
transmitted parasites were recovered from 234 Chinook salmon while 10 parasite taxa were
collected from 373 coho. However, the additional two parasite species recovered in coho salmon,
Tubulovesicula sp. and Lecithophylum sp., were rare overall (<5% of samples). The parasites
recovered in this study represent a wide range of prey items and trophic levels utilized by their
salmonid host and or/ the prey of salmon including copepods, euphausiids and forage fish (Table
3.2).
We also observed a wide range of ocean conditions during the study period. For
example, annual spring (April-June) mean SST ranged from 11.0°C in 2008 to 13.5°C in 2005.
In addition, this study included a well-documented, anomalous subarctic intrusion of cold water
in 2002 leading to SST 0.5 degrees cooler than the historical average (Freeland et al., 2003) and
the warmest summer SST recorded off the Oregon coast since continuous observations began in
1961[2005] (Pierce et al., 2006). On a basin scale, the PDO index revealed that our sampling
period contained an equal number of “warm” ocean years as indicated by positive values (2003,
2004, 2005 & 2006) and “cold” ocean years as indicated by negative values (2002, 2007, 2008 &
2009).
The NMS ordinations of Chinook salmon (Fig. 3.2a; Stress=1.09 for 2-D solution) and
coho salmon (Fig. 3.2b; Stress=2.69 for 2D solution) revealed substantial interannual variability
in parasite assemblages during the study period. In addition, MRPP revealed that the parasite
abundance and species composition was significantly different across years (P<0.0001 MRPP).
Correlations between parasite community and environmental variables
Axis 1 of NMS ordinations accounted for >50% of the interannual variability in the
parasite community for both coho and Chinook salmon. Axis 2 described a smaller proportion of
the variance in juvenile salmon parasite communities (coho salmon: 33%, Chinook salmon: 18%)
compared to axis 1 (coho: 52%, Chinook salmon: 64%). We observed strong relationships
54
between interannual variability in the parasite community, i.e., Axis 1 scores, and the marine
environment. For coho and Chinook salmon, both mean spring SST (April-June) and the
southern copepod index (April-June) were positively correlated with variability in the parasite
community (P>0.05, Table 3.3). Warm SST and a high biomass of southern, lipid-poor copepods
were associated with positive scores on Axis 1 for both coho and Chinook salmon across years
(Figure 3.3). In addition, for Chinook salmon, Axis 1 scores were significantly correlated to two
basin-scale indices of ocean conditions (PDO and NPGO) so that years with positive scores on
Axis 1 were associated with positive values of the PDO index and negative NPGO values. The
volume of the Columbia River plume was negatively correlated to Axis 1 for coho salmon (Table
3.3). These findings suggest fluctuations in local and basin scale indices of ocean conditions in
late spring and early summer may influence the parasite community of juvenile salmon.
For coho and Chinook salmon, correlations between environmental variables and Axis 1
scores revealed associations between specific aspects of the parasite community and ocean
conditions. For both fish species the abundance of a Tetraphyllid cestode and an
acanthacephalan, Rhadinorhynchus trachuri, were highest during years when the SST was warm
and biomass of southern-origin copepods was high (P<0.05 on Axis 1, Table 3.3). In contrast,
cold SST and decreased biomass of southern copepods was associated with an increased
abundance of the nematode, Anisakis simplex, in Chinook salmon (P<0.05 on Axis 1) compared
to years of “warm” ocean conditions. In coho salmon, “cold” ocean conditions and high plume
volume was associated with an increased abundance of the nematode Hysterothylacium aduncum
(P<0.05 on Axis 1). Relationships between ocean conditions, zooplankton and trophically
transmitted parasites suggest that fluctuations in oceanographic climate (measured through the
PDO, NPGO, SST and plume volume), which influence copepod community composition on the
shelf, are also related to the abundance and species composition of marine parasites in coho and
Chinook salmon. While Axis 2 was less important in describing variability in the parasite
community there was a significant correlation between Axis 2 and one parasite species recovered
from coho and Chinook salmon, Lecithaster gibbosus. However, variability in abundance of this
trematode parasite was not significantly related with any of the environmental variables included
in this study.
Our analysis revealed linkages between ocean processes and marine parasite communities
found in juvenile coho and Chinook salmon after ~30 days of marine residency. Adult returns of
UCR Su/F Chinook salmon was related to the parasite community they harbored, with Axis 1
55
scores representing variability in the parasites community, explaining 89% of the variability in
adults returning to Priest Rapids dam when lagged by 3 years (r2=0.890, P<0.05; Figure 3.4a).
This relationship indicates that the parasite community could reflect favorable marine foraging
conditions. As mentioned above, the majority of adults returning to Priest Rapids Dam are made
up of a “subyearling” life-history type. Therefore, fluctuations in the number of returning adults
at Priest Rapids Dam three years from the time of capture are likely reflective of variability in
subyearling survival. No significant relationships were observed when comparing Axis 1 scores
to Chinook salmon adult returns when calculated with a 2 or 4 year lag (r2=0.179, 0.104, P>0.05).
It is possible that the variation in parasite communities in the yearlings is indicative of good
ocean survival conditions. Shifts in the species composition of the parasite community of coho
salmon (Axis 1 of NMS of coho parasites) were associated with ocean conditions during the
study period. However, the relationship between variability in the parasite community and coho
salmon survival across years was not significant (r2=0.360, P>0.05; Figure 3.4b).
DISCUSSION
In the current study, there were clear relationships between the species composition of
trophically transmitted parasites in juvenile coho and Chinook salmon and variability in ocean
climate in the NCC. Fluctuations in the assemblage of trophically transmitted parasites covaried
with the PDO, SST, and the Southern Copepod Index. Furthermore, variation in the parasite
assemblages in yearling Su/Fa Chinook salmon was related to summer-run adult returns three
years later. More specifically, when the biomass of lipid-poor, southern origin copepods was
high during juvenile salmon outmigration (April-June), coho and Chinook salmon contained
different parasite fauna and exhibited lower survival compared to years when the southern
copepod biomass was low. These findings support the hypothesis that changes in ocean climate
that alter copepod species composition may also regulate salmon production through bottom-up
processes. In the last decade, numerous studies have identified relationships between ocean
transport mechanisms, copepod community composition and salmon growth or abundance
(Mackas et al., 2007; Peterson and Schwing, 2003; Trudel et al., 2005). Past studies indicate that
variability in copepod composition, driven by ocean transport, may impact juvenile salmon
during early marine residency. However, since copepods do not make up a large proportion of
the diet of juvenile salmon, the mechanistic link between ocean climate and salmon diets can be
observed through the parasites that salmon obtain from the consumption of infected planktivorous
fish. Trophically transmitted parasites analyzed in this study rely on zooplankton hosts for
56
transmission (Marcogliese, 1995) and require that juvenile salmon consume infected hosts. The
significant relationships between parasite community composition, copepod assemblage, and
environmental conditions indicate that variability in copepod community composition during
marine residence may directly affect prey for salmon.
SST and the Southern Copepod index in late spring were the best predictors of variability
in the parasite community of coho and Chinook salmon. These results suggest that variability in
these physical and biological indices are also good indicators of variability in salmon trophic
interactions during the first month at sea. Specifically, the positive associations between SST, the
southern copepod index and the abundance of two parasite taxa, R trachuri and a tetraphyllid
cestode, likely represent changes in the food web at lower trophic levels (i.e. copepods). The fact
that many parasites require transmission through a variety of intermediate hosts via predator/prey
interactions suggests that differences in parasite assemblages reflect variability in species
composition of the hosts prey (Marcogliese, 2002; Zander et al., 2000). Our results support this
assumption and suggest that the prevalence of R. trachuri and a tetraphyllid cestode in juvenile
salmon may be determined, in large part, by the same ocean transport mechanisms that determine
copepod assemblage. In other words, parasites associated with “warm” water copepods may be
transferred to the prey of salmon (i.e. euphausiids and fish) in higher abundances than years of
“cold” ocean conditions, thus, bridging the gap between variability in the copepod community
composition and salmon trophic interactions.
Parasite analysis provided evidence that fluctuations in the copepod community
composition may alter the quality and/or composition of salmon prey prior to and during ocean
immigration. It is unknown whether variation in the parasite community is indicative of shifts in
salmon prey or variability at lower trophic levels (i.e. the prey of salmon prey). However, results
from this study provided supplemental information on some specific aspects of salmon diet. All
10 of the parasites recovered in the current study require a zooplankton host at some point in their
lifecycle and have been found in copepods. However one nematode, Anisakis simplex, has the
ability to move through an indeterminate number of fish hosts without maturing. This
nematode’s ability to be transferred from one intermediate host to another (fish to fish via
predation) explains why piscivorous fish are often found with many larval worms in the viscera
(Koie, 1993) as they inherit the parasite communities of the fish prey they consume (Bush et al.,
1997). This feature of the nematode lifecycle has enabled detection of piscivory in many species
of marine fish (Blaylock et al., 1998; Campbell et al., 1980; Pascual et al., 1996a; Petric et al.,
57
2011). Results from the current study suggest that increased abundance of A.simplex in years of
cold SSTs may have been the result of increased piscivory during the months prior to capture.
Fish prey, in general are known to be of significantly higher caloric value per gram than other
prey items commonly consumed by juvenile salmon (Davis et al., 2005). Therefore, increased
abundance of A. simplex in years of favorable ocean conditions provides additional support for a
bottom-up mechanism, where variability in the quality (energetic value) or species composition
of prey determines early marine survival.
Our results revealed that juvenile salmon carried a different assemblage of parasites in
years associated with high vs. low survival in Chinook salmon. It should be mentioned that we
do not consider the variability in observed adult salmon abundance to be the direct result of
variability in the parasite community. Rather, we suggest that variability in the parasite
community serves as a proxy for variability in the composition of salmon prey and/or variability
in the diet of planktivorous salmon prey. Ultimately we hypothesize, as others have, that
variability in growth rates (caused by variability in the quality of composition of prey in “cold”
vs. “warm” years) during early marine residency is the most likely cause of variability in survival
(Mackas et al., 2007). Food quality and consumption rate are important determinants of growth
and fast growing salmon are at lower risk of predation for a shorter time than those growing more
slowly (Duffy and Beauchamp, 2011; Pearcy, 1992). In addition, growth of juvenile salmon
during early marine residency may relate to ability to survive the first marine winter (Beamish
and Mahnken, 2001). While a variety of techniques have been implemented in assessments of
growth of juvenile salmon, including scales, otoliths and tagging (Beamish and Mahnken, 2001;
Fisher and Pearcy, 1988; McMichael et al., 2010; Tomaro et al., 2012) these techniques were not
used in this study. The current study provides an important link between variability in climate
and changes in salmon production and suggests that variability in the copepod community
composition during late spring affects the quality and/or composition of salmon prey. Additional
work focused on clarifying the linkage between variation in salmon trophic interactions, as we
observed, and salmon growth would provide a more complete mechanistic understanding of
bottom-up forces controlling juvenile salmon production off the Washington coast.
Our results provide convincing evidence that both local (i.e. SST) and basin-scale (i.e.
PDO, NPGO) indicators of ocean conditions alter the quality or composition of salmon prey.
However the dominant physical forcing in the NCC, upwelling, was not significantly correlated
to the parasite community composition of coho or Chinook salmon. While metrics of coastal
58
upwelling strength provide good indicators of cross-shelf water transport (Austin and Lentz,
2002; Keister et al., 2011), the current study highlights the fact that upwelling strength alone may
not serve as a good predictor of water mass characteristics and ocean productivity. Underlying
basin scale processes such as the positioning of major ocean currents which alter source waters
may be of equal importance in shaping food web structure during late spring and early summer
(Hoof and Peterson, 2006; Peterson, 2009; Sydeman et al., 2011).
Results from this study suggested that the interaction between the fluvial and marine
environment at the mouth of the Columbia River may be important in shaping the prey
composition/abundance of salmon. During the period of peak ocean immigration for juvenile
salmon (April-June), the volume of the Columbia River plume was correlated with shifts in the
parasite community of juvenile coho salmon. In the last decade, attention has been focused on
the Columbia River Plume as a source of productivity and refuge for juvenile salmon leaving the
Columbia River. For example, Morgan et al. (2005) documented increased zooplankton
abundance in the Columbia River plume frontal region compared to surrounding marine and fresh
water and hypothesized that this region may serve as an important feeding opportunity for coho
and Chinook salmon. In addition, Kudela et al. (2010) documented a significant input of riverine
sourced nutrients into the marine environment that was associated with enhanced and sustained
nutrient concentration and increased abundance of zooplankton in and around the Columbia River
plume. In the current study, volume of the Columbia River plume was positively related to the
abundance of H. aduncum, which is known to infect salmon in the Columbia River estuary.
These results suggest that H. aduncum may serve as an indicator of variation in feeding rate
and/or prey composition, associated with the size of the Columbia River plume or associated
fronts. Furthermore, increased abundance of H. aduncum in amphipods and fish captured along
frontal regions compared to those captured in non-frontal areas provides support for the notion
that H. aduncum may represent feeding in the plume frontal regions (Klimpel and Ruckert, 2005).
Hickey and Banas (2003) demonstrated the role of the Columbia River plume in altering currents
and enhancing retentive mechanisms well beyond the shelf and as far north as the Straits of Juan
de Fuca. Therefore, relationships between plume volume and H. aduncum in salmon may also be
indicative of the effect that the Columbia River has on zooplankton distribution across the larger
marine ecosystem. In May of 2001 and 2002 De Robertis et al. (2005) documented substantial
differences in the use of the Columbia River plume frontal region by yearling coho and Chinook
salmon within and between years. A study similar to that of De Robertis et al. (2005), focused on
59
salmon foraging in and around the Columbia River plume across a greater time period that
includes years of variable river and ocean conditions would be helpful in better understanding the
importance of the Columbia River plume and associated frontal regions as an important feeding
opportunity for juvenile salmon.
Fluctuations in some aspects of the parasite community were not associated with
variability in physical or biological properties in the marine environment. These instances
indicate that some aspects of diet variation may be less variable and/or some parasites are less
sensitive to variability in ocean conditions. For example, the trematode L. gibbosus was
important in describing variability in the parasite community associated with Axis 2 of
ordinations of coho and Chinook salmon parasites but was not associated with any physical or
biological indices of ocean conditions. Like many parasites recovered in this study L. gibbosus
relies on the consumption of copepods by fish to complete its lifecycle. However, L. gibbosus
may exhibit a flexible life history with low intermediate host specificity allowing it to complete
its life cycle in a range of invertebrate species and environmental conditions.
We observed significant relationships between variability in the trophically transmitted
parasite community of salmon and ocean conditions in early summer. These findings are
consistent with the hypothesis that basin and local scale variability in ocean climate that alter
zooplankton community composition, also determine the quality and/or composition of prey for
juvenile salmon during early marine residency. Parasite communities of juvenile Chinook
salmon that are associated with successful recruitment occur when SST is low, the biomass of
sub-tropical copepods is low, and the plume volume is large in early summer. Similar, although
non-significant, trends were observed for coho salmon. Traditional diet analysis offers
quantitative information on recent foraging activity. However, it does not account for variability
in the trophic interactions occurring beyond the 24 hours prior to the time of capture or variability
in the food web at lower trophic levels. Trophically transmitted parasites can provide additional
insight into the relationships between lower trophic levels, i.e. copepod community composition,
and salmon prey. From the use of parasites this study provides a better understanding of the
mechanistic links between variability in ocean climate and salmon prey. Correlations between
lipid-poor copepods, trophically transmitted parasites and salmon survival suggest that prey
composition and/or quality may be important in regulating salmon abundance however knowing
whether variability in the parasite community represents differences in composition of salmon
prey or variability at lower trophic levels altering the quality of salmon prey remains to be tested.
60
Additional work comparing the parasite community of salmon prey across years of variable ocean
conditions would improve the precision of trophically transmitted parasite analysis and may
provide further evidence that variable ocean conditions in the NCC alter the quality of prey for
juvenile salmon during early marine residency.
ACKNOWLEDGEMENTS
I’d like to thank Dr. Bruce McCune for assistance in data analysis and I particularly thank the
crew of the F/V Frosti and scientists who assisted in collection of samples at-sea and in the lab.
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65
Table 3.1. Sample size, mean fork length (mm ± SE) and mean
weight (gram ± SE) of Upper Columbia River summer and fall
Chinook salmon and Columbia River coho collected off the
coast of Washington.
Year
2002
2003
2004
2005
2006
2007
2008
2009
n
32
29
37
13
35
34
23
31
Chinook salmon
Size (FL, mm) (Wt., g)
177±4
73±5
191±4
89±6
190±5
92±7
177±5
70±7
189±4
92±6
190±4
86±5
207±8
126±13
205±6
117±11
n
68
40
44
19
47
58
48
49
Coho salmon
Size (FL, mm) (Wt., g)
175±4
66±5
187±3
76±4
185±4
78±5
177±8
61±5
169±4
59±5
180±2
67±3
186±3
82±4
170±4
63±6
66
Table 3.2 Intermediate hosts of marine parasite species recovered from juvenile
Chinook and coho salmon collected off the coasts of Washington state.
Parasite species
Intermediate Host
Anisakis simplex
copepods, chaetognaths, euphausiids and
fish
cyclopoid and calanoid copepods
mollusc, copepods and chaetognaths
calanoid copepods, chaetognaths,
coelenteratres, crab larve, ctenophores,
euphausiids, hyperiid amphipods,
polychaetes, and fish
calanoid copepods
mollusc, copepods and chaetognaths
calanoid copepods and chaetognaths
amphipods and euphausiids
copepods, euphausiids
calanoid copepods and chaetognaths
Bothriocephalus sp.
Hemiurus levinseni
Hysterothylacium aduncum
Lecithaster gibbosus
Lecithophyllum sp.
Parahemiurus merus
Rhadinorhynchus trachuri
Tetraphyllid cestode
Tubulovesicula sp.
Reference
1,2 and 6
6
6
6
4
5
3
6
5
References: 1, Davey (1971); 2, Hays et al. (1998); 3, Hoffman (1999); 4, Klimpel et. Al.; 5, Koie (1989); 6,
Marcogliese (1995).
67
Table 3.3. Pearson correlation coefficients between environmental variables and parasite
species on axes scores of ordination of trophically transmitted parasites of coho and Chinook
salmon. Variance explained (%) by each axis included in column heading.
Environmental Variable
PDO
NPGO
SST
Cumulative Upwelling
Plume Volume
Northern Copepod Anomaly
Southern Copepod Anomaly
Parasite Species
Anisakis simplex
Hemiurus levinseni
Hysterothylacium aduncum
Lecithaster gibbosus
Parahemiurus merus
Rhadinorhynchus trachuri
Tetraphyllid Cestode
UCR Su/F Chinook Salmon
Axis 1 (64%)
Axis 2 (18%)
0.74
0.07
-0.71
-0.36
0.91
0.19
-0.60
0.20
-0.59
0.22
-0.51
-0.19
0.81
0.12
-0.86
0.24
0.41
0.60
0.48
0.67
0.94
Bold values are significant at the 95% confidence interval
-0.23
-0.46
0.09
-0.82
-0.34
-0.20
0.40
Columbia River Coho
Axis 1 (52%)
Axis 2 (33%)
0.48
-0.26
-0.60
-0.42
0.81
0.07
0.55
0.54
-0.63
0.40
-0.41
-0.31
0.76
0.08
-0.26
0.65
-0.61
-0.13
0.01
0.93
0.90
0.08
-0.45
0.27
0.87
-0.45
0.25
0.35
68
Figure 3.1 Station locations (●) along five transects in the northern
Pacific Ocean where juvenile coho and Chinook salmon were
collected.
69
Figure 3.2 Nonmetric multidimensional scaling analysis of (a) UCR Su/F Chinook salmon
and (b) Columbia River coho salmon comparing similarity in parasite communities across
years. Joint plots illustrate relationships between environmental variables and axis scores
(cutoff r2=0.50).
70
1.5
a
1.0
SST
0.5
0.0
-0.5
-1.0
Southern Copepods
-1.5
0.8
0.4
0.2
0.0
-0.2
-0.4
1.5
Parasite Community
b
0.6
c
1.0
0.5
0.0
-0.5
-1.0
-1.5
-2.0
2.0
Coho
Parasite Community
d
1.5
1.0
0.5
0.0
-0.5
09
20
08
20
07
20
06
20
05
20
04
20
03
20
20
02
-1.0
Figure 3.3 Time series of (a) annual anomalies of SST averaged over
April-June; (b) Southern Copepod Biomass anomalies from NH05
averaged over April-June; (c) MDS scores of parasite community
composition from UCR Su/F Chinook salmon and (d) Columbia
River coho salmon.
71
5.0
a
b
4.5
60000
Coho Surivival (OPIH)
Adult Returns to Priest Rapids Dam (3-year Lag)
70000
50000
40000
4.0
3.5
3.0
2.5
30000
2.0
20000
1.5
-2.0
-1.5
-1.0
-0.5
0.0
Axis 1 Score
0.5
1.0
1.5
-1.0
-0.5
0.0
0.5
1.0
1.5
Axis 1 Score
Figure 3.4 Relationship between (a) UCR Su/F Chinook salmon adult returns (r2=0.89) and (b)
Columbia R. coho survival (r2=0.36) with Axis 1 scores from NMS ordinations. Lines were fit
by least squares linear regression.
72
CHAPTER 4: CONCLUSION
Numerous studies have highlighted the importance of ocean conditions in determining
year class strength of Pacific salmon. Positive relationships among SST, marine copepod
community composition and salmon survival in the NCC suggest that bottom up processes may
be important in regulating salmon abundance. However, copepods make up a small contribution
of the diet of coho and Chinook salmon (Peterson et al. 1982; Brodeur et al., 1992) which
consume primarily planktivorous fishes and euphausiids. It has been hypothesized that variability
in the lipid content of copepods on the continental shelf may alter the quality and/or composition
of salmon prey higher in the food web (Peterson and Hoof, 2005; Hoof and Peterson, 2006).
Parasites that directly depend on the consumption of free-living fauna to transmit through
several hosts are a reliable tool to account for changes in the food web at trophic levels that are
undetectable through traditional diet analysis. In addition, when combined with diet data, parasite
analysis has been shown to improve understanding of salmon trophic interactions and provide
information on past foraging beyond the 24 hour period that traditional diet analysis allows.
The objectives of the current study was to identify interspecific differences in feeding of
coho and Chinook salmon and determine if variability in the physical and biological
characteristics of the marine environment relate to variability in the trophic interactions of
juvenile coho and Chinook salmon during early marine residency. In Chapter 2, we compared the
trophic interactions of Columbia River coho salmon, and UCR Su/F Chinook salmon captured off
the coast of Washington using stomach content analysis (indicators of recent foraging) and
parasite community composition (indicators of foraging over the previous month). In Chapter 3,
we tested the hypothesis that the trophically transmitted parasites of juvenile coho and Chinook
salmon are related to variability in physical and biological processes in the ocean during the study
period.
We found that coho and Chinook salmon consistently exhibit interspecific differences in
foraging. Chinook salmon harbored a greater diversity and higher abundance of parasites
suggesting that they consumed a greater number and diversity of infected prey compared to coho
salmon. In addition, the parasite data corroborated results from stomach content analysis of the
same fish and suggested that Chinook salmon consistently consumed a greater number of fish and
amphipods than coho salmon on average while coho consumed more euphausiids.
The results presented in Chapter 3 provide support for the hypothesis that variability in
ocean transport which determines species composition and biomass of copepods on the
73
continental shelf alter the prey quality and/or composition of juvenile salmon. Greater than 60%
of the variability in the parasite community of juvenile coho and Chinook salmon was explained
by mean sea-surface temperature from April-June and the biomass of sub-tropical, lipid-poor
copepod species present in coastal waters over the same time period from 2002-2009. In
addition, the parasite community of Chinook salmon explained 89% of the variability in adult
returns to Priest Rapids dam 3 years after they entered the ocean while the parasite community of
coho salmon explained 36% of the variability in salmon survival for coho. These results provide
evidence for a linkage between variability in copepod community composition during the summer
and salmon prey and suggest that variability in the food web during late spring alters the quality
and/or the composition of salmon prey.
The analysis of trophically transmitted parasites increased our understanding of the
feeding ecology of juvenile salmon. Our results demonstrated consistent differences in the
foraging habits of coho and Chinook salmon across years and provided evidence for linkages
between ocean conditions, copepod community composition, salmon trophic interactions and
salmon survival. While these results add to the growing body of evidence suggesting bottom-up
control of juvenile salmon in the marine environment, future work is needed to better understand
how interspecific and interannual variability in salmon feeding that we observed, directly affects
salmon growth and subsequent adult returns. Identifying the specific prey items associated with
variation of trophically transmitted parasites recovered from juvenile salmon would allow
researchers to determine whether the parasites reflect variation in the species composition of
salmon prey or variation in the diet of planktivorous prey consumed by salmon.