NOAA Technical Memorandum NMFS-AFSC-356

D. J. Csepp, D. C. Honeyfield, J. J. Vollenweider, and J. Womble

Estuarine Distribution, Nutritional 

and Thiaminase Content of Eulachon 

(Thaleichthys pacificus) in Southeast 

Alaska, With Implications for Steller 

Sea Lions

U.S. DEPARTMENT OF COMMERCE

National Oceanic and Atmospheric Administration

National Marine Fisheries Service

Alaska Fisheries Science Center

June 2017

doi:10.7289/V5/TM-AFSC-356
NOAA Technical Memorandum NMFS

The National Marine Fisheries Service's Alaska Fisheries Science Center uses 

the NOAA Technical Memorandum series to issue informal scientific and 

technical publications when complete formal review and editorial processing 

are not appropriate or feasible. Documents within this series reflect sound 

professional work and may be referenced in the formal scientific and technical 

literature.

The NMFS-AFSC Technical Memorandum series of the Alaska Fisheries 

Science Center continues the NMFS-F/NWC series established in 1970 by the 

Northwest Fisheries Center. The NMFS-NWFSC series is currently used by 

the Northwest Fisheries Science Center. 

This document should be cited as follows:

Csepp, D. J., D. C. Honeyfield, J. J. Vollenweider, and J. Womble. 

2017. Estuarine distribution, nutritional and thiaminase content of

eulachon (Thaleichthys pacificus) in Southeast Alaska, with implications

for Steller sea lions. U.S. Dep. Commer., NOAA Tech. Memo. NMFSAFSC-356, 56 p.

Document available: https://www.afsc.noaa.gov/Publications/AFSC-TM/NOAA-TM-AFSC-356.pdf

Reference in this document to trade names does not imply endorsement by 

the National Marine Fisheries Service, NOAA.
June 2017

NOAA Technical Memorandum NMFS-AFSC-356

by

D. J. Csepp1, D. C. Honeyfield2, J. J. Vollenweider1, and J. Womble3

1

Auke Bay Laboratories 

Alaska Fisheries Science Center

17109 Pt Lena Loop Rd 

Juneau, AK 99801-8626 

2

United States Geological Survey

Northern Appalachian Research Laboratory 

176 Straight Run Road

Wellsboro, PA 16901

3

National Park Service 

Glacier Bay Field Station 

3100 National Park Road 

Juneau, AK 99801 

U.S. DEPARTMENT OF COMMERCE

Wilbur L. Ross Jr., Secretary

National Oceanic and Atmospheric Administration

 Benjamin Friedman, Acting Under Secretary and Administrator

National Marine Fisheries Service

Samuel D. Rauch III, Acting Assistant Administrator for Fisheries 

doi:10.7289/V5/TM-AFSC-356

Estuarine Distribution, Nutritional 

and Thiaminase Content of Eulachon 

(Thaleichthys pacificus) in Southeast 

Alaska, With Implications for 

Steller Sea Lions
This document is available to the public through: 

National Technical Information Service 

U.S. Department of Commerce 

5285 Port Royal Road 

Springfield, VA 22161 

www.ntis.gov 
iii

ABSTRACT

Eulachon (Thaleichthys pacificus) are small, pelagic fish whose spawning habits and 

marine distribution are not well understood. Eulachon are a nutrient-rich, seasonally important 

source of food for predators, including Steller sea lions (Eumetopias jubatus) in southeast 

Alaska. Echo integrated-trawl surveys were conducted from 3 April to 6 May 2006 to estimate 

eulachon population structure and biomass, identify fish movement, location, and acoustic 

targets. The presence of Steller sea lions and other marine predators attracted to pre-spawning 

aggregations of eulachon were used to fine-tune the timing and location of our survey sites. We 

identified the distribution of pre-spawning adults, sub-adult, and juvenile eulachon in five

estuaries of northern southeast Alaska during the 2006 spring spawning season and analyzed 

their nutritional and thiaminase content. Mean eulachon weight and nutritional energy varied 

between sites, from a low of 10.68 g body weight ± 2.93 g with a total energy of 94.4 kJ/fish in 

Berners Bay, to a high of 33.22 g body weight ± 5.99 g with a total energy of 291.9 kJ/fish in

Lutak Inlet. Of the five estuaries surveyed, juvenile and sub-adult eulachon were found only in 

Taku Inlet, Berners Bay, and Chilkat Inlet and were concentrated at a distinct depth of 50-80 m 

throughout the estuaries. Adult eulachon were found in three of the five estuaries: Lutak Inlet, 

Taku Inlet, and Berners Bay with no fish identified with our fishing gear or acoustics in Taiya 

Inlet. Eulachon school biomass and the duration these schools spend in the estuaries correlated

with sea lion abundance. Sea lion numbers were directly proportional to eulachon biomass. 

Spawning eulachon move quickly into their freshwater spawning river, with estuary size directly 

proportional to the time spent in the estuary. Thiaminase, a potentially harmful enzyme, was 

found in eulachon at all five sites, with a mean activity range of 5.0-7.0 umols·g-1

·min-1. The 

ingestion of thiaminase laced eulachon by Steller sea lions does not appear to affect the health of 
iv

sea lions in our study area because they were not ingested long enough for the thiaminase to take 

effect. The role that thiaminase plays in the health of marine predators is not well understood and 

warrants further study and could play a role in the junk food theory that was used to explain 

Steller sea lion declines in other areas especially in populations with low dietary diversity.
v

CONTENTS

ABSTRACT ................................................................................................................................... iii

CONTENTS .....................................................................................................................................v 

INTRODUCTION ...........................................................................................................................1 

METHODS ......................................................................................................................................4 

Field Operations - Study Area .............................................................................................4 

Field Operations - Hydroacoustic Methods .........................................................................5 

Field Operations - Fishing Methods ....................................................................................8 

Field Operations – Steller Sea Lion Enumeration ...............................................................9 

Laboratory Operations - Eulachon Physical and Chemical Analyses ...............................11 

Laboratory Operations - Thiaminase I Analysis ................................................................12 

RESULTS ......................................................................................................................................13 

Eulachon Abundance and Distribution ..............................................................................13 

Length Frequency ..............................................................................................................15 

Eulachon Nutritional Content ............................................................................................15 

Thiaminase Content ...........................................................................................................16 

Steller Sea Lion Abundance and Activity ..........................................................................16 

DISCUSSION................................................................................................18 

Eulachon Distribution ........................................................................................................19 

Spawning............................................................................................................................20 

Steller Sea Lion Abundance...............................................................................................22 

Eulachon Energetics and Nutrition ....................................................................................23 

Thiaminase Content ...........................................................................................................25 

Steller Sea Lion Nutrition ..................................................................................................26 

CONCLUSIONS............................................................................................................................28 

ACKNOWLEDGMENTS .............................................................................................................31 

CITATIONS ..................................................................................................................................33 

INTRODUCTION

Eulachon Thaleichthys pacificus (Richardson 1836), are a small, anadromous, energydense and nutritious forage species that are widespread in southeast Alaska (Carlson et al.1

, 

Csepp et al. 2011). Adult eulachon display little size variation throughout their broad latitudinal 

range and relatively little genetic diversity among populations (McLean et al. 1999, McLean and 

Taylor 2001). There appears to be two distinct geographical populations in the Gulf of Alaska: a 

northern one from Yakutat to Cook Inlet and a southern one that encompasses all of southeast 

Alaska inside waters (Flannery et al. 2009). Eulachon are planktivorous, feeding primarily on 

copepods and euphausids in deeper nearshore water when not spawning (Hay and McCarter 

2000). 

Eulachon are found from northern California to Norton Sound in southwestern Alaska

(Wilson et al. 2006). They spawn in the lower reaches of the mainland and a few island rivers

(Blackburn et al. 1981, Hay et al. 1997). Little is known about their marine distribution (Willson 

et al. 2006) except that adults concentrate outside their spawning rivers in shallow water 

estuaries (Marston et al. 2002) just prior to spawning. In southeast Alaska they loosely aggregate 

in nearby waterways near the seafloor during the remainder of the year (Csepp et al. 2011). Even 

less is known of their offshore distribution with some eulachon showing up in areas with the 

right oceanographic conditions (Emmet and Brodeur 2000). Concentrations of eulachon are 

1

 Carlson, H. R., R. E. Haight, and K. J. Krieger. unpubl rep. Species composition and

relative abundance of demersal marine life in waters of southeastern Alaska, 1969 ̶ 77. Alaska Fisheries Science 

Center, Auke Bay Laboratories, 17109 Point Lena Loop Rd., Juneau, Alaska 99801.
2

found around Vancouver Island (Hay et al. 1997, Hay and McCarter 2000), and inconstant

abundance have been found in the western Gulf of Alaska (Anderson and Piatt 1999).

Eulachon spawn in early spring, and are lipid-rich (Kuhnlein 2000, Iverson et al. 2002),

making them a valuable energy source for marine predators at a time of year when there are few 

food sources. Seasonally abundant spawning aggregations of energy-rich forage fish are critical

resources for the survival and reproductive success of many marine predators including Steller 

sea lions (Eumetopias jubatus) (Iverson et al. 2002). Variation in prey consumption indicates that 

Steller sea lions forage on seasonally abundant and densely aggregated prey (Gende et al. 2001,

Sinclair and Zeppelin 2002, Marston et al. 2002, Womble and Sigler 2006, Sigler et al. 2009), 

especially those that aggregate during spawning or seasonal migrations. A study of Steller sea 

lion diets from the summer months found no eulachon present, which indicates eulachon are a 

seasonally important prey during eulachon spawning season in spring (Sigler et al. 2004, Sigler 

et al. 2009).

In a study of 18 fish species in the Gulf of Alaska, eulachon had the highest lipid and 

greatest energy content, ranging from 12% - 28% lipid and 9 - 13 kJ/g, wet mass (Payne et al. 

1999, Anthony et al. 2000, Vollenweider et al. 2011). Smaller, younger eulachon as well as

adults with depleted energy stores in spawning condition had lower lipid and energy content,

similar to two species of myctophids at 14% - 22% lipid, and 10 - 10 kJ/g, and sablefish 

(Anoplopoma fimbria) at 18% - 20% lipid, and 10 - 11 kJ/g. The remaining 14 fish species were 

significantly lower in lipid, and energy content compared to eulachon, including forage fish such 

as Pacific herring (Clupea pallasii) at 6 - 20% lipid and 7 - 8 kJ/g, Pacific sand lance 
3

(Ammodytes hexapterus) at 3 - 6% lipid and 4 - 6 kJ/g, and capelin (Mallotus villosus) at 2 - 12% 

lipid and 4 - 7 kJ/g (Payne et al. 1999, Anthony et al. 2000, Vollenweider et al. 2011). Of the 18 

fish species studied in the Gulf of Alaska, eulachon was one of the species with relatively low 

protein content at 12% - 14% than other forage species like capelin at 13% - 15% and sand lance

at 16% - 18% (Payne et al. 1999, Vollenweider et al. 2011). Eulachon have also been reported to 

contain high levels of vitamin A and E, calcium, iron, and zinc (Kuhnlein et al. 1996).

Eulachon and rainbow smelt (Osmerus mordax) are members of the Osmeridae family; a 

family known to contain thiaminase (Tillitt et al. 2005, Honeyfield et al. 2012). Thiaminase has 

not been previously reported in eulachon. Thiaminase is an anti-nutrient that destroys thiamine, 

also known as vitamin B1. The enzymatic degradation of thiamine by thiaminase I (enzyme 

number 2.5.1.2; Webb 1992) deactivates thiamine by acting as a catalyst for a base substitution 

reaction where the thiazole portion of a thiamine molecule is exchanged for one of several 

potential nucleophiles resulting in a non-functional molecule (Fujita 1954, Lienhard 1970, 

Honeyfield et al. 2012).

Thiamine is a water-soluble vitamin required by transketolase for the conversion of 

glucose to important end products and for enzymes in the Krebs cycle that converts glucose to 

adenosine triphosphate (ATP) for metabolic energy. Low levels of thiamine have a variety of 

secondary effects, which include immune dysfunction, reduced growth, reduced predator 

avoidance, reduced vision, alterations in genes and gene expression (Brown et al. 2005a, Brown 

et al. 2005b, Carvalho et al. 2009, Fitzsimons et al. 2009, Ottinger et al. 2012). Thiamine 

deficiency has been diagnosed in captive gray seals (Halichoerus grypus), California sea lions 
4

(Zalophus californianus), an Atlantic bottlenose dolphin (Tursiops truncatus), and has been

induced in harp seals (Pagophilus groenlandicus) (Fowler 1978, Dierauf 1990). Harp seals 

showed signs of altered behavior within 40 - 60 days; refusing to eat, becoming inactive, 

unresponsive to touch, noise, or light and were breathing irregularly. Within 2 - 3 days of the 

onset of these preliminary signs severe tremors, fore-flipper spasms, head shaking, muscle 

quivering occurred followed by death (Geraci 1970). Therefore, documenting the presence of 

thiaminase in eulachon and the length of time and the exclusivity Steller sea lions feed on 

eulachon is important to their health. 

Our study goals were to track the estuarine distribution of eulachon and to measure the 

energy, lipid, protein, ash, vitamins A and E content, and thiaminase activity in eulachon from 

five estuaries in southeast Alaska. Our specific objectives were to characterize eulachon 

estuarine aggregations by 1) estimating the biomass, timing, and location of aggregations, 2) 

characterizing the population age structure and distribution within each estuary, 3) characterizing 

pre-spawning distribution within a large geographic area with numerous pre-spawning locations, 

4) measuring the nutritional content of eulachon, 5) determining the presence or absence of 

thiaminase, and 6) characterize Steller sea lion activity during eulachon runs within a large 

geographic area.

METHODS

Field Operations – Study Area

We chose five estuaries to study within northern southeast Alaska that have historically 

supported year-round populations of Steller sea lions and seasonal spawning runs of eulachon. 
5

The study area spanned a 200-km section from Taku Inlet in Stephens Passage to Taiya Inlet in 

Lynn Canal which included four inlets and one bay (Fig. 1). Our five study locations, from south 

to north were Taku Inlet (58°11.303 ́N, 134° 05.891 ́W), Berners Bay (58°44.554 ́N, 

134°58.959 ́W), Chilkat Inlet (59°06.178 ́N, 135°22.048 ́W), Lutak Inlet (59°17.190 ́N, 

135°26.368 ́W), and Taiya Inlet (59°26.718 ́N, 135°21.051 ́W) (Fig. 1). Surveys were initially 

conducted from south to north between 3 April and 6 May 2006 in an effort to follow the 

eulachon spawning season.

Field Operations – Hydroacoustic Methods

Hydroacoustic data were collected in whole estuary standard box surveys and smaller 

school specific focal box surveys that were classified into five categories by location (Fig. 2).

The five categories were Taku Inlet, the largest estuary surveyed at 96 km long with a total area 

of 49.04 km2 and two school-specific, smaller focal surveys of 10.75 and 20.2 km long (n = 15

separate surveys). Chilkat Inlet survey was 87.8 km long with a total area of 35.6 km2 (n = 2

surveys). Berners Bay survey was 76 km long with a total area of 26.8 km2 and two overlapping 

school-specific smaller focal surveys of 18 and 16.5 km long (n = 7 surveys). Lutak Inlet survey 

was 60.2 km long with a total area of 15.8 km2 (n = 4 surveys), plus a periodically used sea lion 

haulout at Low Point (n = 2 surveys) just outside Lutak Inlet in Chilkoot Inlet. Taiya Inlet survey 

was 27.8 km long with a total area of 7.4 km2 (n = 2) (Fig. 2). Eulachon biomass at each location 

was calculated by multiplying total surface area (km2

) by eulachon density (weight per area). 

Hydroacoustic data were collected using a Kongsberg Simrad Fisheries EK 60 split-beam 

system with two frequencies: 120 kHz 7o and 38 kHz 12o transducers set in a tow body. The tow 
6

body was towed at roughly 12 - 16.7 km·hr-1 at a depth of 2 m. Both transducers were calibrated 

using a multi-frequency tungsten carbide calibration sphere and conductivity, temperature, and

depth (CTD) data for environmental parameters were collected just prior to and at the same 

location of the calibration. A standard parallel box survey was laid out for each of the five 

locations with survey replicates conducted at each location. Aerial surveys and opportunistic 

observations by survey and fishing vessels of foraging sea lions were used to coordinate acoustic

surveys on schools of pre-spawning eulachon. Smaller focal hydroacoustic surveys were 

conducted when acoustic data showed schooling fish sign during the larger acoustic surveys.

Midwater trawling or gillnetting were used to collect aquatic fauna for species identification, to 

verify acoustic data, obtain length, and weight data for relative biomass estimates, and to collect 

samples for nutritional analysis. Dipnets and fish traps were also used to obtain additional

samples for nutritional analyses. 

RAW acoustic data were collected as nautical area backscatter coefficient (NASC), 

which was monitored and saved in real-time with Kongsberg Simrad software on a laptop, 

copied to an external hard drive, and entered into Echoview® Software Pty. Ltd. analytical 

software to delineate the seafloor, erroneous data, to identify species and schools of interest, and 

to export NASC values. Two frequencies were chosen to better identify species with 120 kHz 

frequency used for weak less reflective (Rayleigh) backscatters like eulachon without gas 

bladders and 38 kHz for strong more reflective (Geometric) backscatters like walleye pollock

(Gadus chalcogrammus) with gas bladders. A Kongsberg Simrad general purpose transceiver 

(GPT) actively produced an echo and then integrated and summed the returning echoes from 

fauna caught within the acoustic beams during surveys. Acoustic data were categorized by 
7

species on an echogram, integrated for 0.183-km length and 10-m depth intervals, and corrected 

for transducer calibration using Echoview® software. Frequency threshold was lowered to 

-76 dB from its standard -70 dB in Echoview® to better identify eulachon, which are less 

acoustically reflective because they do not have swim bladders (Gauthier and Horne 2004), 

without introducing extra noise. According to Simmonds and MacLennan 2005, the output of 

acoustic scattering or NASC is proportional to species and size. To convert NASC to fish density

in numbers, acoustic reflectivity, quantified as target strength (TS) for single fish, was needed. 

Target strength for single fish depends on length in centimeters. The equation used in this study 

to determine TS was

TS = 20log LF + b,

where LF equals fork length and the constant (b) used for eulachon in brackish estuarine water b 

is -81 (Sigler et al. 2004). The b constant was adjusted between saltwater and freshwater values 

to best match published TS values for 120 kHz (Gauthier and Horne 2004). Target strength (TS)

was then transformed to backscattering cross-section (σbs) where

σbs = 4π10TS/10.

Eulachon density in numbers was computed by dividing NASC by σbs. Eulachon density in 

weight equals density in number multiplied by average weight (Simmonds and MacLennan 

2005). Eulachon biomass was then calculated for each location by multiplying the surface area of 

each location (km2

) by eulachon density in weight.

NASC values attributed to eulachon were used to show when and where eulachon moved 

into an area, and showed when numbers peaked and dropped. After species were identified on 

the echogram we used acoustic data as an ethological tool to follow the movement of eulachon 
8

within an estuary and thus determine the pre-spawning behavior and the juvenile and sub-adult 

distribution. We determined distribution by live viewing acoustic data, and followed the survey 

on NobeltecTM navigational software, which provided real-time global positioning system 

reference. We marked the edges of the schools seen throughout each survey on the navigational 

software map and labeled edge marks by species. Related marks were connected to construct 

polygons around the school to plot the school’s location, shape, and size in real time per day for 

each estuary. This allowed us to document GPS data in real time on a map of the surveyed 

location, enabling us to track daily and weekly movements of eulachon and other species 

throughout and between estuaries on maps of their specific locations during the time of each 

survey.

Field Operations – Fishing Methods

Fish samples were collected for nutritional analysis, to identify species with acoustic 

sign, and to obtain biological information (e.g., length, weight, age and sex) to estimate biomass.

At the two southern most sites (Taku Inlet and Berners Bay), we used the NOAA ship John N. 

Cobb to fish with a 164 Nordic rope trawl with a 7 m-high and 17 m-wide net opening and a 

32-mm mesh codend liner. In Berners Bay, we also collected riverine eulachon samples from

fish traps operated by the U. S. Forest Service. In the northern estuaries of Chilkat, Lutak, and 

Taiya inlets, we sampled fish using gillnet and local recreational dipnet catches. The demersal 

gillnet was deployed from the FV Nanasse to sample from the sea floor up into the water 

column. The gillnet was 27.5 m-long and 2.4 m-deep with five 5.5 m panels (13, 19, 25, 38, and 

51 mm of stretched mesh) oriented vertically along its length. We used standard recreational 

dipnets, which have a 31-cm deep bag made of 5 mm mesh with a 31-cm diameter mouth
9

attached to a telescoping pole. In Lutak Inlet, we also had the opportunity to collect dipnet 

samples and visual observations from the bridge over the Chilkoot River (< 100 m upstream

from Lutak Inlet) when fish density was very high. Fish used for thiamine analysis were 

collected in the Ferebee, Chilkat, Chilkoot, and Taiya rivers using recreational fishing methods 

by the Southeast Alaska Watershed Coalition and ADF&G, Haines, Alaska, throughout May

2015. Fish were collected and frozen whole in the field. Lengths and weights were recorded for

whole fish in the laboratory prior to thiaminase analyses, gender identification, and for 

determination of maturity stage.

Field Operations – Steller Sea Lion Enumeration

Steller sea lions were located, counted, and special attention given to identifying feeding 

behavior in order to locate schooling eulachon. Sea lion activity was noted during all fishing and 

acoustic sampling surveys and recorded using marine mammal sampling forms. Data recorded 

included count, behavior (e.g., feeding, transiting, and milling), orientation (bearing), and 

distance to boat. Sea lion counts from the acoustic survey vessel were made by photographing 

larger (>10) aggregations with a Canon D5 digital single-lens reflex (DSLR) camera with a 

28 - 300 mm image stabilizing (IS) lens. Sea lions were marked on images in Adobe Photoshop

software and animals in the image were enumerated; counts were made twice for accuracy. 

When sea lion aggregations were small (< 10), enumeration was done by two observers using

Pentax 10 × 42 binoculars, with two to three counts collected per aggregation and averaged. 

Aerial surveys were conducted at approximately 5 - 7-day intervals between 1,000 and 

1,400 hours using a fixed-wing single engine Cessna 206 aircraft, flown at an altitude of 316 m 
10

and a speed of 183 - 210 km·h-1

. Aerial surveys were conducted in Taku Inlet from 2 April to 

27 April 2006, and in Berners Bay and Lutak Inlet from 2 April to 12 May 2006. Transects were 

flown perpendicular to the shoreline, but when sea lions were present, we deviated from this 

pattern to better enumerate the sea lions. Sea lions throughout the bay were enumerated and 

locations were relayed to the acoustic survey vessel. Digital photographic images of sea lions 

were taken from the aircraft using a Nikon D1X digital camera with an 80 - 300 mm telephoto 

lens. Small aggregations of sea lions (< 10) were counted by the observer while larger 

aggregations were photographed. The majority of photos were taken when sea lion groups were 

at the surface; however, when aggregations were active (e.g., diving and transiting), the plane

circled until all members of the group were at the surface and could be photographed. Counts 

from aerial surveys represent the observed number of sea lions in the study area, with an 

unknown proportion of sea lions not at the surface and thus unavailable to be counted or 

photographed.

Date, time, GPS location, frame numbers, and estimated numbers were recorded for all 

sea lions that were encountered at all locations. Digital photographic images were stored on 

compact flash media cards and then downloaded to a computer. The clearest digital image was 

imported into the geographic information system software ArcView®, and each sea lion was 

marked on the image and counted. Marks were checked and counted twice by an experienced 

counter. The variability of the total sea lion counts for each estuary was not measured, as only 

one survey was flown each day.
11

Laboratory Operations – Eulachon Physical and Chemical Analyses

Fish length (fork length) was recorded when collected and immediately frozen whole at 

-20 °C, held for 10 - 20 days, and then transferred to -80 °C. In the laboratory, fish were 

weighted prior to analysis for nutritional content. We classified juveniles as those from 4.6 -

8.9 cm long, sub-adults as 9.0 - 15.0 cm, and pre-spawning adults > 15.1 cm (fork length). Adult 

lengths < 16 cm came from fish that were collected, measured, and dissected for chemical 

analysis and verified as pre-spawning adults.

Individual fish were homogenized while frozen and aliquots of the total body 

homogenate were randomly selected for the analysis with every seventeenth fish sampled was

analyzed twice. A 0.5 - 1.0 g aliquot of homogenate was used for lipid analysis. Lipid was 

extracted using a solution of 2:1 v:v chloroform:methonal in an accelerated solvent extractor 

with two cycles on a temperature/pressure regime of 120 °C and 8.27 million Pa. The resultant 

filtrate was washed twice with a 0.5% KCl solution and 1:1 v:v methonal:deionized water to 

remove the co-extractables. Percent lipid was calculated gravimetrically.

Moisture content was determined gravimetrically by drying ~ 4 g of sample homogenate 

in a 75 °C oven until a constant weight was attained. After percent moisture was calculated, dried 

samples were ground to a fine powder and nitrogen content was analyzed using a nitrogen 

analyzer. Percent protein was calculated from the nitrogen content using a conversion factor of 

6.25 (Craig et al. 1978). Total-body lipid and protein contents were converted from relative 

percentages to masses on a wet-weight basis and then multiplied by their corresponding 

conversion factors to calculate total-body energy content.
12

Energy content in thermochemical kJ was calculated as the sum of caloric contribution by 

total body lipid and protein, using the accepted conversion factors of 9.50 kcal·g-1 for lipid and 

5.65 kcal·g-1 for protein (Watt and Merrill 1963):

(1) 9.50 kcal/g x % lipid + 5.65 kcal/g x % protein

(2) 1 kcal = 4.1840 thermochemical kJ.

Vitamin analysis was conducted according to methods at the University of Connecticut’s 

Department of Nutritional Sciences. Whole body fish homogenates were stored frozen at –70°C 

until analyzed. Subsamples of homogenate were weighed, homogenized in phosphate buffer and 

hexane-extracted. Vitamin A1 (retinol) and vitamin E (α-tocopherol) were determined by 

reversed-phase isocratic high-performance liquid chromatography (HPLC). Vitamins were 

separated on a Waters C18 Resolve Column (15 cm × 3.9 mm; Millipore, Milford, MA) 

protected with an Upchurch C18 guard column (Upchurch Scientific, Oak Harbor, WA). A 

mobile phase of methanol/water (98/2) at 1 mL/min was used to elute the vitamins. Quantitation 

for both vitamins were at 300 nm (Catignani 1986).

Laboratory Operations – Thiaminase I Analysis

Thiaminase activity was measured using the colorimetric thiaminase I assay of 

Honeyfield et al. (2010). Reaction volumes were scaled down to quantify changes in optical 

density of 4NTP on a microplate spectrophotometer (BioTek®, PowerWave 340) rather than a 

standard UV-vis spectrophotometer. Samples of approximately 0.3 g from ground, whole, frozen 
13

fish were first homogenized in five volumes of chilled buffer. The sample was then vortexed, 

centrifuged, and the supernatants transferred into 2-ml Pierce centrifuge columns 

(~30 μm pore size, Thermo Fisher Scientific Inc.) to remove any residual particulate matter.

Then 6 μl of processed, filtered supernatant was placed in each of four replicate wells of the 

microplate (NUNC, 96 well, Thermo Fisher Scientific Inc.) containing 194 μl of cocktail A (with 

thiamine) and 4 wells containing 194 μl cocktail B (no thiamine). The wells without thiamine 

served as assay controls for each sample. Plates were placed into a pre-heated (37o

C) plate 

reader, the microplate was shaken at medium speed for 10 s, and absorbance was read at 411 nm.

After initial absorbance was recorded, absorbance was measured at 1̶ min intervals over 1 hour.

Rate of 4NTP degradation was calculated and reported as μmol of thiamine inactivated per gram 

of tissue per minute. All buffers and reagents were prepared immediately prior to use.

RESULTS

Eulachon Abundance and Distribution

We estimated the biomass of pre-spawning eulachon in Berners Bay at 332 metric tons (t)

during 2006 which could be one of the lowest in recent years (pers. comm. with USFS and 

ADF&G, Juneau, AK). We did not identify any pre-spawning eulachon acoustic sign in Chilkat 

or Taiya inlets, but found what could be a relatively high run of 3,180 (t) in Lutak Inlet and a 

relatively average run in Taku Inlet of 1,785 (t) (Table 1). 

Pre-spawning eulachon did not spend much time lingering in the estuary, with time spent 

proportional to estuary size. Taku Inlet was the only study site where we observed adult eulachon 

schools lingering in the estuary, in this case it was a few dense schools in the middle and inner 
14

parts of the inlet for a few days. Pre-spawning runs varied in duration with Lutak Inlet having 

one of the shortest with a rapid increase to a maximum biomass day then a rapid 3-day decrease

in biomass. Taku Inlet had the longest lasting pre-spawn run with a less rapid increase than 

Lutak increase to a mid-level biomass plateau lasting days then a doubling of biomass in a day to 

a high level plateau lasting 3 days before a rapid one day decrease (Fig. 3). Since we had only 

one boat to survey five estuaries in a large geographic area we were unable to spend the time at 

each estuary to determine the precise beginning and end of each run. 

In addition to pre-spawning eulachon, we observed other life stages of eulachon and 

aquatic fauna in our study estuaries. One of our more interesting observations was a dense 

consistent layer of osmerids between 50 m and 80 m found throughout three of the five estuaries

(Fig. 4) based on our acoustic sampling. This “osmerid layer” was approximately 80% juvenile 

and sub-adult eulachon with some capelin mixed in, with the remaining percentage comprised of 

crustaceans (mainly euphausids) based on our physical sampling. When this layer was present, it 

was seen throughout the estuary at a consistent depth at each estuary. The presence, size, and

density of this layer appears to be related to the size and shape of the estuary. Taku Inlet had the 

largest and densest layer, Chilkat Inlet next, Berners Bay a close third, with Lutak and Taiya 

showing no osmerid layer. Lutak and Taiya inlets are both fed by small river systems into small,

fairly shallow inlets with simple straight landscapes. Our trawl data shows a variety of species 

like capelin, euphausids (Euphausiacea), Pacific herring, walleye pollock, northern lampfish 

(Stenobrachius leucopsarus) and Pacific glass shrimp (Pasiphaea pacifica) inhabiting most 

estuaries and are also found in specific layers. Capelin were found in the osmerid layer in low 

numbers, with most adults found tightly aggregated along the shoreline near the river mouth. 
15

Juvenile walleye pollock were found at all locations, from 80 m to the bottom and were mainly 

located in the outer portions of the estuary where it was ≥ 80 m which was below the osmerid 

layer and outside the estuary where the osmerid layer was found.

Length Frequency

Length frequency of pre-spawning eulachon in Taku and Lutak inlets and Berners Bay 

were variable showing distinct life stage patterns of juveniles, sub-adults, and adults (Fig. 5).

Berners Bay had an average length of 11.5 cm (Table 1) with a range of 7.9 - 15.7 cm (Fig. 5). 

The average fish length in Taku Inlet was 11.9 cm (Table 1) with a range of 4.6 - 20.5 cm

(Fig. 5). Lutak Inlet had the largest average size of 17.4 cm (Table 1) with a range of 15.5 -

19.3 cm, which were all adults (Fig. 5). The average adult size in all locations was 17.4 cm 

(Fig. 6), SD = 1.1, n = 249 with 8.8 % of the adult fish < 16.0 cm (Fig. 6). The smallest adult fish

in our study was found in Taku Inlet at 14.6 cm, we also found a 15.5 cm gravid female in Lutak 

Inlet, which falls below the normal size range (≥ 16 cm) (Clark et al. 2007) for an adult. All fish 

< 16 cm were determined as gravid adults though dissection prior to chemical analysis of 

collected specimens.

Eulachon Nutritional Content

There were little significant differences in total nutrition between locations. Eulachon 

from all estuaries combined had an average of 11.96% protein, 15.04% lipid content (wet mass

oil), 72.51% moisture, 1.57% ash, 184.58 μg/100g vitamin A and 7267.54 μg/100g vitamin E 

(Fig. 7). Mean weight and total energy available per fish from Berners Bay were, 10.68g ± 2.93 g 

and 94.4 kJ, Taku Inlet 16.55g ± 1.16 g and 145.4 kJ, and from Lutak Inlet 33.22g ± 5.99 g and
16

291.9 kJ (Table 1). Nutritional content of eulachon varied to some extent among and within 

estuaries with a lipid content range of 10.04% - 19.76% and an average of 15.04%, with 

considerable overlap among estuaries (Fig. 7). Protein content varied less than lipid with a range

of 10.21 - 13.90% and an average of 11.96%. Combining these data with trawl and acoustic 

analysis we get total energies available by location of 2.9 billion kJ for Berners Bay, 

15.7 billion kJ for Taku Inlet and 27.9 billion kJ for Lutak Inlet (Table 1).

The mean vitamin A content of eulachon was 195.3±11.1 μg/100 g and vitamin E content 

was 7,249 ± 213 μg/100 g. Neither vitamin varied by collection month or maturation status (prespawner vs. spawner, mature vs. spent) (ANOVA, P > 0.05). Nor did vitamin content vary with 

fish length R2 < 0.01% or lipid content R2 < 9.5% (regression), both vitamins are lipid-soluble.

Thiaminase Content

Eulachon thiaminase activity was highly variable for all fish sampled from the four sites,

with a range of 1.05 - 17.92 umols·g-1·min-1. Mean thiaminase activity (umols·g-1·min-1),

however, was not significantly different (ANOVA, P = 0.81) among eulachon from Ferebee 

River (5.67), Chilkat River (6.48), Chilkoot River (5.54), or Taiya River (7.04) (Figs. 1 and 2)

with an overall mean activity range of 5.0 - 7.0 umols·g-1·min-1.

Steller Sea Lion Abundance and Activity

Taku Inlet sea lion aerial counts started on 2 April 2006 with < 10 animals, growing to 40 

on 10 April, then increased rapidly to 160 animals by 14 April (Fig. 3). By 15 April, sea lion 

numbers had rapidly decreased to 55 on 19 April and stayed consistent until 24 April, when 
17

numbers started to slowly decline to a low of < 10 by the end of April. Berners Bay aerial counts 

started on 2 April 2006 with 15 sea lions counted with a gradual increase to a maximum of 40 

animals counted on 13 April followed by a few decreases to 0 and increases to 10 to 30 between

1 May and the end of the aerial survey on 15 May (Fig. 3). On 24 April we enumerated only 10 

sea lions but on April 26 we counted the peak number of 158 with a drop to 70 on 27 April and 

to < 10 by 30 April (Fig. 3). Lutak Inlet sea lion counts started on 7 April 2006 with no animals 

found until 28 April when the numbers increased precipitously to 400 on 3 May followed by an

equally steep decrease to 50 animals counted on 7 May and decreased to 0 on 15 May. Vessel 

counts for Berners Bay were from 6 to 30 April 2006 with counts varying up and down from 15 

to 40 animals between 6 and 21April. The sea lion counts from vessels from 3 to 15 April, 2006 

counted < 10 animals until 10 April when 20 animals were counted with a maximum of 50 sea 

lions on 14 April and numbers declining to < 10 on 15 April (Fig. 3).

In general it took a day or few for sea lion numbers to catch up to eulachon biomass in all 

locations. Comparing sea lion numbers to pre-spawning eulachon biomass in Lutak Inlet, on 

28 April the eulachon biomass was at its peak but < 10 sea lions were counted. Then on 1 May

the count was up to 300 sea lions but the eulachon numbers were dropping fast and on 3 May the 

sea lion count reached its maximum of more than 800 animals but the eulachon numbers were

falling fast until both bottomed out on 5 May (Fig. 3).

In summary, Steller sea lion numbers were relatively low in Berners Bay and Chilkat and 

Taiya Inlets, average in Taku Inlet, and unusually high in Lutak Inlet (Fig. 3). Acoustic tracking 

of eulachon demonstrated that sea lions move into the inlets soon after the eulachon start 
18

congregating, but do not arrive en masse until after eulachon numbers have peaked (Fig. 3). Taku 

Inlet had a more gradual increase and decrease in eulachon biomass then peaked and leveled off

for a few days, providing sea lions more time to forage. We also observed a few dense schools of 

pre-spawning (adult) eulachon lingering within Taku Inlet, which also enabled sea lions more 

time to forage. 

DISCUSSION

We examined three ecologically connected variables: location and movement of 

eulachon, their nutritional composition, and movement of Steller sea lions with respect to 

eulachon spawning in four Lynn Canal and one Stephens Passage estuaries. Because eulachon

spawn in bays and inlets earlier than most other fish species in southeast Alaska and have a high 

energy content, eulachon can be an ecologically important species for southeast Alaska’s marine 

predators by providing much needed energy at a crucial time of the year. Our study provided 

additional data on eulachon for Berners Bay, and new data for four additional estuaries. From 

these data, we can infer some much needed information about the marine distribution and life 

history of eulachon. Eulachon ethology and morphology make this forage species hard to study 

in the marine environment. They are hard to catch by net because of their dispersed marine 

shoaling behavior associated with the seafloor when not in their pre-spawning inlets or bays

(Csepp et al. 2011). They are also hard to detect using hydroacoustics because they are weak 

acoustic reflectors that are in association with the sea floor in a heterogeneous species layer

(Csepp et al. 2011) of equally weak acoustic reflectors (Gauthier and Horne 2004).
19

We used length frequencies to determine life stage of fish that were not dissected for 

nutritional analysis. With the length frequencies we observed and an age at maturity of 3 to 

4 years (Clark et al. 2007), we were able to estimate the marine distribution of juvenile and subadult eulachon in the estuaries within our study area. According to Clark et al. 2007, 16.0 cm is 

the minimum size for spawning eulachon with size increasing with latitude, although, we found 

8.8% of our adults were < 16.0 cm, with our smallest adult at 14.6 cm. We can say with certainty 

that both length and weight increase with age (Spangler 2002) and that size differs between 

rivers and years (Barraclough 1964, Spangler 2002).

Other studies have found that eulachon spawning locations are inconsistent and spawning 

occurs in some locations during some years but not others, making regular appearances in some 

areas but rarely seen in others (Minckley et al. 1986, Hinrichsen 1998, Willson et al. 2006).

Berners Bay is a classic example of this with its fairly regular pre-spawning aggregations and 

variable fluctuations in biomass with a high year seen in 2002 and low in 2003 (Sigler et al. 

2004) and during our study in 2006. The low biomass seen in Chilkat Inlet, Berners Bay, and 

Taiya Inlet, and a very high biomass in Lutak indicate a correlation between these four northern 

estuaries and the possible sharing of a spawning stock. On the other hand, Taku Inlet with its

typical biomass could suggest a separate breeding stock from the four northern estuaries or just 

another example of the erratic spawning nature of eulachon.

Eulachon Distribution

Through eulachon length frequencies (Fig. 5), life stage structure, and the presence of a 

distinct osmerid (and euphausid) layer (Fig. 4) found in Berners Bay, Chilkat, and Taku Inlets,
20

we were able to describe eulachon estuarine distribution by life history stage. Surveys of other 

similar inlets south of our study area within southeast Alaska’s inside waters also show a similar 

layer throughout the year (Csepp et al. 2011). We propose from these data that estuaries that 

have the right size, shape, and bathymetry can create the right conditions where immature 

eulachon could stay for the first 1 to 2 years, using these estuaries as nursery grounds. This is in 

agreement with Hay and McCarter (2000), who found that larvae are immediately carried into 

the estuary and may use it as a nursery area. Smaller Inlets could offer less area for outgoing 

juveniles to aggregate in and have more tidal and river currents pushing small fish out of the 

estuary more rapidly. Note in Figure 2 the small size and linear shape of Taiya and Lutak inlets,

which have no osmerid layer to the larger size and more serpentine or bottleneck shape of 

Chilkat and Taku Inlets and Berners Bay which harbor an osmerid layer. We do not know how 

long eulachon stay in their natal estuary, where they go or how far they travel when they leave or 

weather they return to it to spawn. We have, however, regularly found adults outside their 

spawning bays and inlets in the main waterways of southeast Alaska in a heterogeneous, biotic 

layer associated with the sea floor (Csepp et al. 2011).

Spawning

Eulachon are known to spawn unpredictably, by how many fish show up (biomass), by 

where they choose to spawn (location) and by when they chose to spawn (timing). For example, 

eulachon usually spawn once in a lifetime making them semelparous (monocyclic) (Clarke et al. 

2007) but some are known to spawn twice, making a select few iteroparous (polycyclic). The 

frequency of iteroparity and the variability among and between populations is still unresolved 

(Hart and McHugh 1944, Barraclough 1964, Blackburn et al. 1981, Hay and McCarter 2000,).
21

Most eulachon spawning rivers have only one spawn per year but some have two (Langer et al. 

1977, Bishop et al. 1989, Betts 1994). There are several examples of this with one found in our 

study area; Chilkat River has its regular run in May, and a sporadic one in February (Bishop 

et al. 1989, Betts 1994). The timing when eulachon spawn does not show a latitudinal 

relationship, early in the south to later in the north (Hay and McCarter, 2000), making attempts 

at timing a run difficult. For example, Chilkat River run can begin late April and peak by early 

May, but in other years it peaks around 23 May (Bishop et al. 1989). On Twentymile River the 

run can start from 17 April to 4 May (Spangler 2002), and in Berners Bay it can start from early 

April to early May (Marston et al. 2002, Sigler et al. 2004). Eulachon not only change their run 

timing, they even fail to show up in their regular spawning rivers in some years like the Cowlitz 

(Hinrichsen, 1998) and the Sacramento (Minckley et al. 1986). We observed in the fish traps in 

the Lace and Antler Rivers that the runs into Berners Bay and the recreational fishery in Chilkat 

River that runs into Chilkat Inlet showed up but in such low numbers they could not be caught or 

seen with our acoustics in the estuary and apparently moved over to nearby Lutak Inlet as per the

unusually high biomass seen in 2006. Hay and McCarter (2000) also noted this straying 

behavior. Berners Bay spawning runs were usually very reliable from year to year (Marston et al. 

2002). Berners Bay, however, appears to have regular fluctuations in run biomass as seen by us 

and Sigler et al. 2004. The Sigler et al. (2004) study resembles ours in that eulachon runs in 

Berners Bay cycled between high and low years, which could be indicative of good and bad 

brood years or just verify the erratic nature of eulachon spawning locations. Our study combined 

with Sigler’s et al. (2004) clearly shows the unpredictable nature of eulachon spawning in 

Berners Bay. For future studies, high and low spawning years could help identify brood stock if 

the spawning population returns to the same river to spawn. In addition, when studying a larger 
22

geographic area with many spawning locations attention is needed in determining separate 

spawning populations.

Steller Sea Lion Abundance

Factors that appear to influence sea lion presence and numerical response are eulachon 

biomass, estuary schooling density, duration, and location in the water column, average fish size, 

and fish behavior. In our study, sea lion numbers are directly proportional to eulachon biomass, 

and schooling duration. Sea lion numbers grew from a few to several hundred in 2 - 3 days, soon 

after eulachon biomass increased. This suggests that sea lions may be using some form of

communication regarding the presence of eulachon to animals across a larger area. We know that 

sea lions use haulouts throughout the area with a large, centrally located haulout at Benjamin 

Island in Lynn Canal. Even though sea lion numbers are directly proportional to eulachon 

biomass, sea lion arrival is a bit off sync from eulachon peak biomass, with sea lions showing up 

en masse 2 - 3 days after eulachon biomass has peaked (Fig. 3). In other words, there is a 

2 - 3 day delay for sea lions throughout an area to react to a forage species schooling event;

Lutak Inlet was a typical example of this. With the small size of Lutak Inlet the eulachon prespawning event had a shorter duration compared to larger inlets. Taku Inlet had a smoother 

biomass increase, building up to a plateau that lasted 5 to 6 days, with sea lion numbers slowly 

and steadily increasing to a peak of 160 animals at the end of the biomass plateau (Fig. 3). One 

thing similar between large and small inlets is that once the eulachon pre-spawning biomass 

starts declining it declines quickly as do the sea lion numbers (Fig. 3). During a previous study 

Berners Bay sea lions peaked at 949 in 2003, but the peak count in 2002 was only 120 (Sigler 

et al. 2004), suggesting that there may have been a reduced abundance of eulachon in 2002 when 
23

using the sea lion count alone. Sea lion activity in Berners Bay in 2006 was also a low year with 

a maximum of only 156 animals.

Our survey vessel and aerial counts were comparable, in that they showed similar timing 

to the increases and decreases in sea lion numbers in association with eulachon biomass. Our 

vessel counts however, were greater than our aerial counts for all locations except Taku Inlet 

(Fig. 3). There may be several reasons for the different in vessel and aerial counts. First, vessel 

remain in the area over a much longer time period, thus providing a greater likelihood of 

observing and sea lions in a given area. In contrast, aerial surveys, occur over a short time period 

in a given study area. In addition, the size and shape of the bay and inlets, which are small 

enough and shaped so the acoustic survey vessel could see the entire waterway. Taku Inlet, on 

the other hand, was too large and serpentine in shape for viewing all sea lion activity from the 

vessel. 

Eulachon Energetics and Nutrition

Our data and previous studies demonstrate that eulachon are a lipid-rich forage species 

with an energy density higher than other forage species used by Steller sea lion such as herring, 

capelin, cod, pollock, or flounder (Perez 1994). The fish tested in this study represent data for 

estuary and river captured fish. Eulachon in our study and those previously collected from the 

Gulf of Alaska contained 18 - 20% lipid, which is higher than other fishes like sand lance at 3% -

6%, or capelin at 2% - 10% lipid (Payne et al. 1999). Similar to previous studies, protein content 

was slightly lower for eulachon at 12% - 13%, when compared with 13% - 15% for capelin and 

16% - 18% for sand lance (Payne et al. 1999). Fish energetics, particularly lipid and 
24

consequently energy content, are known to cycle seasonally in temperate environments in 

response to seasonal pulses in energy availability and reproductive cycles (Vollenweider et al. 

2011, Robards et al. 1999, Paul and Paul 1998).

Eulachon in our study tested within published values for protein, lipid, moisture, ash and 

energy content (Kuhnlein 2000, Clark et al. 2007); however, our numbers were just a bit low,

possibly due to our lower average sizes than previously sample fish. Our catches had a high 

percentage of juvenile and sub-adult fish, which were found in the pelagic, osmerid layer seen in 

three of the five surveyed locations (Fig. 4). The use of the 164 Nordic rope trawl in our study 

with its 32 mm mesh codend was better designed to catch smaller fish found throughout the 

water column than the standard commercial shrimp trawl used in other studies.

Eulachon also contain high levels of vitamins A and E (Fig. 7) (Kuhnlein et al. 1996)

compared to similar fish species. Data describing vitamin content of cold-water marine fish are

limited. Vitamin E content of eulachon whole-body homogenates (7,249) was found to be 

intermediate to vitamin content in muscle (1,700 - 2,100 μg/100 g) and lipid extract (11,800 -

14,700 μg/100 mg) of Atlantic herring (Clupea harengus harengus), a similarly oily fish 

(Engelhardt et al. 1975). Similarly, vitamin E content of eulachon was intermediate to walleye 

pollock fillets (490 μg/100 g) (USDA 2017) and carcass lipids (10,300 - 17,200 μg/100 g) (Wu 

and Bechtel 2009). In another gadid, Pacific cod (Gadus macrocephalus), vitamin E content (540 

μg/100 g) was 13 times less than eulachon (USDA 2017). Vitamin A content of eulachon was 

over 6 times greater than reported in Pacific herring (32 μg/100 g), Atlantic herring (28 μg/

100 g), and cisco fillets (Coregonus sp.) (30 μg/100 g) (USDA 2017). Unlike Atlantic herring in 
25

which vitamin E content was greater in ripe fish than undeveloped or spent fish, vitamins in 

eulachon were consistent between reproductive states.

Thiaminase Content

This is the first report showing that eulachon are thiaminase-positive and contain 

sufficient enzyme activity to result in thiamine deficiency under certain conditions. The mean 

eulachon thiaminase activity range was 5.0 - 7.0 umols·g-1

·min-1. Thiaminase activity greater 

than 2.5 umols·g-1·min-1 has been shown to reduce the thiamine status of the consumer (Fujita 

1954, Lienhard 1970, Honeyfield et al. 2012). Prey species with thiaminase activity 

< 1.5 umols·g-1·min-1 have not been associated with thiamine deficiency. The negative effects of 

thiaminase are directly proportional to the duration and exclusivity of its ingestion. For example,

harp seals fed prey fish high in thiaminase showed signs of altered behavior within 40 - 60 days:

refusing to eat; becoming inactive; unresponsive to touch, noise, or light, and were breathing 

irregularly. Within 2 - 3 days of the onset of these preliminary signs, severe tremors, foreflipper 

spasms, head-shaking, muscle quivering, and then death occurred (Geraci 1970). Eulachon,

however, are only available to sea lions for 7 - 14 days during pre-spawning, which is not long 

enough to affect their health even if they feed on them exclusively. Lake trout consumption of 

rainbow smelt has been linked to low egg thiamine in the Laurentian Great Lakes (Fitzsimons 

and Brown 1996). Low egg thiamine has been shown to cause fry mortality in lake trout and 

other salmonid species (Honeyfield et al. 2005, Wolgamood et al. 2005). 
26

Steller Sea Lion Nutrition

The benefits of eulachon as a prey item for sea lions are associated with the timing of the 

availability of the resource and their nutritional value. The time of year when eulachon spawn is 

a very energy demanding time for sea lions, with increased nutritional energy needed for the 

breeding season (Winship et al. 2002). During April and May, pregnant females are in their third 

trimester, when most of the fetal mass is accumulated (Frazer and Hugget 1974). According to 

Calkins and Pitcher (1982), 61% of female sea lions are still nursing a pup in May and lactating 

females require 70% more calories than lone females (Gittleman and Thompson 1988, Winship 

et al. 2002). Pregnant females will soon give birth, after which time they fast for 11- 14 days 

before foraging (Gentry 1970, Sandegreen 1970) and need to accumulate energy stores for both

gestation and lactation demands. The primary energetic demands for adult male sea lions is their 

extended period of fasting during breeding season, which can last up to 68 days (Gentry 1970, 

Sandegreen 1970, Gisiner 1985). During this time, breeding males focus on maintaining their 

breeding territory and breeding with females. Thus, adequate energy reserves prior to the 

breeding season are likely key to a male’s ability to maintain a territory and ultimately to 

breeding success. The demands put on sea lions at this time of year is why the timing of 

eulachon spawning is so critical for successful sea lion breeding and survival of pups and adults

(Sigler et al. 2009). 

The high energy density (Table 1) and percent lipid content of eulachon, in addition to its 

other nutritional values (Fig. 7), and the timing of spawning make eulachon an essential energy 

source for Steller sea lions at an energetically demanding time of year. Eulachon protein content 

is lower than other forage fish at 12% - 13%, but they contain high levels of vitamins A and E 
27

(Fig. 7), calcium, iron, and zinc (Kuhnlein et al. 1996) compared with other common forage fish 

species. Large eulachon contain 14.5% lipid, which is similar to northern lampfish, making 

eulachon and lampfish two of the most energy-dense fish tested (Anthony et al. 2000,

Vollenweider et al. 2011). However, lampfish are generally too deep and dispersed for sea lions 

to obtain in any quantity and regularity, as are eulachon when not pre-spawning. With the lack of 

eulachon in Berners Bay during our study, sea lions were likely feeding on other species present 

like capelin, herring, and walleye pollock.

Relating vitamin content of fish to requirements of marine mammals is difficult, as few 

studies have quantified this. Serum vitamin E and vitamin A have been measured in free-ranging 

gray seals (Halichoerus grypus) (Schweigert et al. 1987, 1990). In captivity, vitamin levels have 

been measured in northern fur seals (Callorhinus ursinus), California sea lions (Zalophus 

californianus), and gray (Halichoerus grypus) and harbor seals (Phoca vitulina) (Mazzaro 1994).

Diets low in vitamin E for 18 months have been found to cause electrolyte imbalance and 

abnormal molting patterns in phocid seals (Engelhardt and Geraci 1978). Vitamins A and E have 

many health benefits in mammals. Vitamin A is essential for reproduction, bone and muscle 

growth, cell maintenance, and vision (Ross 1999, Biswas et al. 2000). Vitamin E is known 

principally as an anti-oxidant (Azzi and Stocker 2000) and is essential for reproduction and 

lactation (Baldi et al 2000). Vitamin E deficiency can result in muscle degeneration, steatitis, 

liver necrosis, and anemia (Geraci 1981).
28

CONCLUSION

One of our observations during this study was the identification of a distinct juvenile and 

sub-adult eulachon layer in certain estuaries (Fig. 4), adding much needed data to eulachon 

estuarine distribution and life history. With a species composition of 80% juvenile and sub-adult 

eulachon in this layer, we propose that estuaries with the right characteristics with spawning 

rivers associated with them are possibly used as nursery grounds for eulachon. Our echointegrated trawl surveys also show a correlation between the location of juvenile pollock found at 

> 80 m and the osmerid layer found at < 80 m (Fig. 4), suggesting that depths of < 80 m could be 

protection from feeding pollock.

A second observation from our results was that sea lion abundance was correlated with 

prey biomass and schooling duration, and not with nutritional content of eulachon (Table 1, and 

Fig. 3). Even though individual pre-spawning eulachon were energy and lipid-rich, the sheer 

abundance of fish outweighs the differences in fish condition, attracting more sea lions where 

more fish are present.

Our results could also indicate (although a bit more uncertainly) the possibility of two 

separate eulachon spawning populations shared between our five sites: one being shared between 

the four northern estuaries and the other population spawning in Taku Inlet, the southernmost 

estuary.
29

Our study confirmed that eulachon are nutrient-rich and for the first time we showed that 

eulachon contain the anti-nutrient thiaminase, similar to other osmerids that have been tested. It 

is known that sea lions feed on dense schools of spawning forage species when available which 

could be detrimental to their survival if the forage species is fed on exclusively and long enough 

and has an anti-nutrient present. However, the short duration (7 - 14 days) that sea lions in our 

study area fed solely on eulachon would not be of sufficient duration (40 - 60 days) to lead to 

thiamine deficiency. Even species like Steller sea lions which have a varied diet could be 

susceptible considering the 50/50 chance of a forage species containing an anti-nutrient. The 

presence of an anti-nutrient in a forage species could shed some light onto why changes in prey 

species, which happen in regime shifts, affect predator population numbers, considering that 

51% of marine fish examined contained the anti-nutrient thiaminase (Deutsch and Hasler 1943, 

Neilands 1946, Ceh et al. 1964, Greig and Gnaedinger 1971, Fowler 1978, National Research 

Council 1982, National Research Council 1983, Dierauf 1990, Lichtenberger 2011). A simple 

change from one prey species (or genus) to another with any decrease in the dietary variety for 

an extended period of time could affect the survival of the predator. Such dietary changes could 

switch a predator’s diet from a nutritious species to a less nutritious species or one with antinutrient activity. Merrick et al. (1997) also found a strong correlation between diet diversity and 

sea lion decline; as diet diversity decreased, the sea lion population decreased no matter the 

nutritional value of the forage species. Special attention should be given to any nutritional study

of predatory species that does not have a variable diet, especially when the predatory species is 

in decline. Trites and Donnelly (2003), in their review of Steller sea lion decline in Alaska,

hypothesized that the decline was caused by nutritional stress from eating “junk food” species 

with poor nutritional value. Anti-nutrients like thiaminase should also be added to the junk food 
30

species nutritional content list in that seemingly nutritious species could be considered junk food

when they contain anti-nutrients and when such prey species are ingested too long and with too 

much exclusivity. Much more study needs to be done on anti-nutrients and their effects on

predators and how widespread they are in forage species.
31

ACKNOWLEDGMENTS

Thanks to the crew and captain of the NOAA ship John N. Cobb, FV Seaview, FV

Nanasse, and pilot Jacques Norvell of Tal Air for keeping everyone safe during some harsh 

conditions and allowing us to collect scientifically sound data. Special thanks to the AFSC’s

Auke Bay Laboratories (ABL) nutritional ecology lab personnel for working up the samples for 

energetics and to Robert Bradshaw, the database manager. A special thanks to the listed peers for 

reviewing an earlier version of this manuscript; Robert Stone, Phillip Rigby, Jon Heifetz, Chris 

Lunsford, Corey Fugate, and Cara Rodgveller. Thanks to ABL’s Corey Fugate for assisting with 

the thiaminase sample logistics. A thank you to Brad Ryan of the Southeast Alaska Watershed 

Coalition and Randy Bachman of Alaska Department of Fish and Game in Haines, Alaska, who 

helped collect eulachon for thiaminase sampling. Special thanks to Michele Masuda and Pete 

Hulson for their statistical help throughout the analysis. Mike Sigler and John Horne helped with 

acoustic analysis methodology and data verification. This project operated under Marine 

Mammal Laboratory (MML) permit # 782-1768-00. Additional funding was provided by MML

and the U. S. Forest Service.

33

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48

Table 1. -- Data from estuaries where biological values were collected to get average weight (g), 

fork length (cm), energy content/fish (with standard errors), and hydroacoustic NASC 

values were used to get total energy (kJ)/area, and biomass metric tons (t)/area.

Area

Average 

weight (g)

Average fork 

length (cm)

Energy

(kJ/fish)

Total 

energy 

(billion 

kJ/area) Biomass (t)

Taku 16.55 ± 1.16 11.9 ± 0.07 145.4 ± 3.10 15.7 1,785

Berners 10.68 ± 2.93 11.5 ± 0.08 94.4 ± 1.13 2.9 332

Lutak 33.22 ± 5.99 17.4 ± 0.42 291.9 ± 14.88 27.9 3,180
49

Figure 1. -- Map of southeast Alaska showing the five study sites surveyed for eulachon 

aggregations and associated foraging Steller sea lions.
50

Figure 2. -- Maps of the inlets and bay in our study, to compare size and shape of each estuary 

and to show the rivers that were sampled for thiaminase. The black lines within each 

map are the hydroacoustic survey track lines.
51

Figure 3. -- Aerial and vessel counts of Steller sea lions and nautical area scattering coefficient 

(NASC) values from pre-spawning adult eulachon by day and location.
52

Figure 4. -- Two hydroacoustic echograms visually showing RAW nautical area scattering 

coefficient (NASC) values of the same (spatially and temporally) osmerid layer 

collected with 120 kHz on the top and 38 kHz on the bottom as seen in Berners Bay, 

and Chilkat and Taku inlets. Note how the osmerid layer disappears when walleye 

pollock are present.

Osmerid layer in Bay

Pollock are seen as we leave estuary and move into deeper water
53

Figure 5. -- Length frequencies of all life stages of eulachon sampled in Berners Bay, Taku Inlet, 

and Lutak Inlet; juvenile = 4.6-8.9 cm, sub-adult = 9-15 cm, pre-spawning adults 

≥ 15.1 cm.

2

0

5

10

15

20

25

30

35

4 6 8 10 12 14 16 18 0

L

t necre P

engths (cm)

B

Locations

Taku Inlet

Lutak Inlet

erners Bay
54

Figure 6. -- Length frequencies for adult fish sampled, averaged for all five locations. 

14 15 16 17 18 19 20 21

40

30

20

10

0

Adult length (cm)

F

re

q

u

e

n

c

y
55

Figure 7. -- Nutritional (% lipid, protein, moisture and ash) and vitamins A and E (μg/100g) 

contents for eulachon by location, showing range with black bar, mean with red 

dotted line, and standard deviation with whiskers. 
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