Aquaculture Nutrition 2000 6;153^158
..............................................................................................
Acceptability of various microparticulate diets
to ®rst-feeding walleye Stizostedion vitreum larvae
K.M. GUTHRIE & M.B. RUST Northwest Fisheries Science Centre, Resource Enhancement and Utilization
Technologies Division, Seattle, USA
C.J. LANGDON Oregon State University, Hat®eld Marine Science Center, Newport, OR, USA
F.T. BARROWS US Fish and Wildlife Service, Bozeman Fish Technology Center, Bozeman, MT, USA
Abstract
The acceptability of eight diets made by a wide variety of
microparticulate manufacturing processes was studied using
®rst-feeding walleye Stizostedion vitreum larvae. Diets were
formulated using a common dietary mix but di€ered in
manufacture technique. The microparticulate diets fed were
(1) carrageenan bound, (2) alginate bound, (3) starch/
1 konjack bound, (4) microextruded/maurmurized (MEM),
(5) zein bound, (6) carboxymethyl cellulose bound (CMC),
(7) particle-assisted rotationally agglomerated (PARA) and
(8) a commercial microparticulate diet (Fry Feed Kyowa B-
700, FFK). Controls were groups fed live Artemia nauplii
and unfed. Gut fullness was measured as the cross-sectional
optical area of the bolus visible through the transparent body
of the larvae using computer-aided image analysis. Feeding
2 incidence on MEM particles (71 ‹ 8%, mean ‹ standard
error), zein-bound particles (69 ‹ 7%), alginate-bound par-
ticles (68 ‹ 2%) and PARA particles (65 ‹ 6%) were not
signi®cantly di€erent (P 0.05) from the feeding incidence for
Artemia (71 ‹ 6%). FFK (49 ‹ 14%) and particles bound
with carboxymethyl cellulose (27 ‹ 0.07%), starch
(21 ‹ 10%) or carrageenan (20 ‹ 0.8%) had signi®cantly
(P < 0.05) lower feeding incidence. Larvae that did initiate
feeding did not di€er signi®cantly (P > 0.05) in the amount
of each microparticulate diet or Artemia consumed. This data
indicates that once ®rst-feeding walleye start on a diet, they
will consume that diet to a similar ®xed level of satiation.
Given the di€erences in the amounts of water and nutrients
in the various diets, more nutrients were delivered to the gut
of walleye larvae feeding on microparticulate diets than on
the Artemia control.
KEY WORDS: Artemia, feeding, larval, nutrition, start-feeding
3 Received 14 October 1997, accepted 25 January 1999
..............................................................................................
Ó 2000 Blackwell Science Ltd
Correspondence: Michael B. Rust, Northwest Fisheries Science Center,
Resource Enhancement and Utilization Technologies Division, 2725
Montlake Boulevard East, Seattle, WA 98112±2097, USA. E-mail: mike.
rust@noaa.gov
Introduction
Walleye Stizostedion vitreum are an important sport and
commercial ®shery in North America, with a large geograph-
ical range (Hubbs & Lagler 1949; Trautman 1957; Becker
1983). In the USA, the value based on angler expenditures
was US $2.2 billion in 1991 (Summerfelt 1996) and in
Canada, walleye represented 16.3% of the total freshwater
®shes caught by anglers (Fenton et al. 1996). From 1990 to
1995, Canadian harvest of walleye ranged from 3.0 to 4.9
million kg annually. In 1992, ®shers in Canada received an
average of US $2.60 kg±1 for walleye netted from remote
natural lakes (Summerfelt 1996). High prices for walleye
resulted in interest in production of food-size walleye from
aquaculture (Summerfelt 1996). Most walleye aquaculture is
currently conducted by public agencies who culture fry and
®ngerlings in ponds for restocking purposes (Conover 1986;
FWS 1992; Heidinger et al. 1987). Nearly all commercial
walleye aquaculture is also targeted for sport ®sh enhance-
ment (FWS 1992).
Commercial production of walleye is limited to varying
degrees by diculties in rearing the larval stages (Nickum
1986). At ®rst-feeding, walleye are small, possess a very
limited yolk reserve, start feeding with an incompletely
developed digestive system and have a comparatively short
4 lecithrotrophic stage (Balon 1975, 1984). Digestive function
changes during larval development, becoming more ecient
as the larvae approach metamorphosis (Rust 1995). Before
metamorphosis, feed must be readily consumed and be
highly digestible to support good larval growth and
survival.
153

154 K.M. Guthrie et al.
One of the impediments to intensive rearing of walleye
5 larvae is the lack of high quality microparticulate diets that
are acceptable, digestible, and which meet the nutritional
needs of the larvae. Microparticulate diets that are uniform
both in size and nutritional quality have been shown to
dramatically increase the rearing success of species such as
white®sh Coregonus clupeaformis (Zitzow & Millard 1988),
carp Cyprinus carpio (Lubzens et al. 1984), smallmouth bass
Micropterus dolomieui (Ehrlich et al. 1989) and muskellunge
Esox masquinongy (Zitzow 1986). Larval walleye have been
cultured wholly on formulated dry feeds; however, survival
and growth are generally low (Krise & Meade 1986; Nickum
1986; Loadman et al. 1989).
E€ective microparticulate diets should: (1) eciently retain 8,9 1000 lm nitex screen (Aquatic Ecosystems Inc., Apopka, FL,
nutrients despite large surface area to volume ratios that are
conducive to rapid nutrient leaching after particles are
suspended in water; (2) possess physical and chemical
characteristics that result in their ingestion by ®sh larvae;
(3) be readily digested and assimilated by larvae; and
(4) consist of an optimal nutrient composition for maximum
larval survival, development and growth. This study address-
es the second requirement by comparing the acceptability of
eight types of microparticulate diets fed to ®rst-feeding
walleye larvae.
Materials and methods
Dietary treatments
Ten dietary treatments were applied to duplicate tanks of
®rst-feeding walleye. The treatments consisted of eight
preparations using a common dietary mash and two controls
(live Artemia and unfed treatments). Speci®c treatments
6 were: (1) carrageenan bound (particle size: 250±425 lm),
(2) alginate bound (250±425 lm), (3) starch/konjack bound
(250±425 lm), (4) microextruded/maurmurized (MEM,
250±425 lm), (5) zein bound (250±425 lm), (6) carboxy-
methyl cellulose bound (CMC, 250±425 lm), (7) particle-
assisted rotationally agglomerated particles (PARA, 250±
425 lm), (8) fry feed Kyowa B-700 (FFK, 400±700 lm,
Biokyowa Inc., Chester®eld MO, USA), (9) live newly
hatched Artemia nauplii (430 lm, San Francisco Bay strain,
Bayou Brine Shrimp and Aquatic Foods, Onterio, CA,
7 USA), and (10) unfed. Microparticulate diets were dispensed
every 15 min for 28 h by automatic feeders controlled by
timers. Each tank was fed a total of 12 g (as fed at 10%
moisture) of each microparticulate diet.
Artemia cysts were hatched in aerated sea water (30 g L±1) 10 Biomedical Inc., Costa Mesa, CA, USA) dissolved in 90%
at 28°C. The nauplii were decanted after 24 h and rinsed
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prior to being fed to the walleye larvae. Feeding was (10 g
each tank, wet weight basis) over a 28-h period.
Fish and rearing
Larval walleye at their ®rst-feeding stage (4 days post hatch
at 19°C) were obtained from Garrison Dam National Fish
Hatchery (Riverdale, ND, USA). Larvae were held in one
tank supplied by a recirculation system for 2 days prior to
the start of the study. Random groups of 100 larvae were
stocked into 20 (10 treatments ´ 2 replicates) 30 L circular
tanks (radius 30 cm, depth 33 cm) from a batch of 30 000
larvae. All tanks were screened with nylon stockings over a
USA) to retain feed in the tanks and supplied with
recirculated water maintained at 19.0 ‹ 1.0°C by a
heat pump (Model #AHP6, Aquanetics, San Diego, CA,
USA). Recirculated water was pumped through a bio-®lter
(Model #BBF-2, Water Garden Gems, Borne, TX, USA) and
UV ®lter (Model #DZ401, Rainbow Lifeguard, El Monte,
CA, USA) prior to returning to the tanks. Lighting was
controlled by a timer to provide a photoperiod of 12 h dim
light/12 h dark. The 28 h trial began and ended during the
light phases.
Water quality was monitored daily as follows: Alkalinity,
ammonia and nitrite were determined with commercial test
kits (Model 16900±01, DR/700 methods 8038 and 8507,
Hach Chemical Company, Loveland, CO, USA), pH,
temperature and dissolved oxygen were monitored with
meters (Hach pH meter, YSI models 30 and 55 oxygen
meters, Yellow Springs Instruments, Yellow Springs, OH,
USA).
Diet preparation
The particle types being tested for acceptability included
various microbound particles (alginate, carrageenan, CMC,
starch, and zein; Langdon 1989), microextruded/maurmuri-
zed (MEM) particles, and particles produced by a rotational
agglomeration technique (particle-assisted rotary agglomer-
ation, PARA; Barrows et al. 1993). All diets incorporated the
same mash. The formulation of the mash has produced good
growth and survival as a sole food for larval walleye
(Table 1, walleye starter #9501) in previous trials (Barrows
et al. 1993).
Zein particles were made with 20.0 g of the mash com-
bined with 30.0 mL of 100 g L±1 zein (corn zein, ICN
ethanol. The ethanol was removed by evaporation.
Ó 2000 Blackwell Science Ltd Aquaculture Nutrition 6; 153^158

Table 1 Formulation of mash used in all microparticulate diets
Ingredients g kg )1
Artemia meal 86
Egg solid 216
Fish meal 145
Fish oil 44
Krill meal 410
Liver meal 76
Yeast extract 23
Total 1000
Alginate particles were made with 30.0 mL of 1 M
Na2HPO4 added to 20.0 g of mash. After mixing, 30.0 mL
of 20 g L±1 sodium alginate (Protanol LF 120, Pronova
11 Biopolymer Portsmouth, NH, USA) solution was added with
vigorous mixing. Finally, 5.0 mL of 10 M calcium chloride
was added to gel the mixture.
CMC particles were made with 80.0 mL of 20 g L±1
carboxymethyl cellulose (F99±7HF, Hercules Inc. Wilming-
12 ton, DE, USA) solution mixed with 20.0 g of mash. Finally,
5.0 mL of 10.0 M calcium chloride solution was then added
to the gel mixture.
Starch/konjac particles were made with 20.0 g of mash
mixed with 30.0 mL of distilled water and 2.3 g of a
commercial mixture of starch and the gum konjac (Nutricol
13 GP 440; FMC Corporation, Philadelphia, PA, USA). The
mixture was heated to 80°C and 1.5 g of sodium carbonate
was added to help gel the mixture upon cooling.
Carrageenan particles were made with 20.0 g of mash
combined with 30.0 mL of 1 M Na2HPO4 and 30.0 g of
carrageenan (Gelcarin GPB 12, FMC Corporation). This
mixture was heated to 80°C to dissolve the carrageenan. The
mixture was gelled by addition of 7.0 mL of 2.5 M KCl and
then allowed to cool to room temperature.
All microbound diets were freeze-dried, ground with a
pestle and mortar, then separated through a series of sieves
14 agitated on a Rototap (Tyler Inc., Gastonia, NC, USA) to
produce particles of acceptable size.
Data collection and analysis
Data collections followed the method of Rust & Barrows
(1998). At the end of the feeding trial, tanks were cleaned of
uneaten feed and waste. All ®sh in each tank were collected in
15 a sieve (750 lm) and preserved in 100 g L±1 bu€ered forma-
lin. Feeding incidence was determined by observation of
larvae under a microscope and counting the number of full
and empty guts. Ten feeding larvae (i.e. only larvae that had
feed visible in the gut were used for gut fullness measure-
ments) from each tank were video-taped and digitized to
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Acceptability of various microparticulate diets 155
determine bolus cross-sectional optical area (an index of feed
consumption) using a Macintosh computer (Apple Computer
Inc., Cupertino, CA, USA) and NIH Image software (US
National Institutes of Health, http://rsb.info.nih.gov/nih-
image/).
Mean consumption (10 ®sh per tank) and incidence (100
®sh per tank) values for each tank were considered units of
observation for statistical comparison (two observations per
treatment). One way analysis of variance was used to
determine signi®cantly di€erent dietary treatments
(P < 0.05) using a computer statistic software (STATVIEW,
Brain-Power, Calabasas, CA, USA). Means were separated
by the protected least-squares method. Per cent feeding data
was arcsine transformed prior to statistical analysis.
Results
Water quality
Alkalinity measurements averaged 113.0 ‹ 4.6 mg L±1
CaCO3 (mean ‹ standard error); the average pH was 7.51 ‹
0.12. Average ammonia nitrogen was 0.27 ‹ 0.26 mg L±1
(NH3-N), average nitrite was 0.16 ‹ 0.09 mg L±1 (NO2-N)
and the average temperature was 20.6 ‹ 0.11°C.
Feed
The percentage of larvae feeding on four of the micropar-
ticulate diets did not di€er signi®cantly (P > 0.05) from live
Artemia (71 ‹ 6%, Fig. 1). These diets were: (1) MEM
particles (71 ‹ 8%), (2) zein-bound particles (69 ‹ 7%),
(3) alginate-bound particles (68 ‹ 2%) and (4) PARA
particles (65 ‹ 6%). Feeding incidence for the commercial
control diet FFK (49 ‹ 14%) was intermediate. Particles
bound with carboxymethyl cellulose (27 ‹ 0.07%), starch
(21 ‹ 10%) and carrageenan (20 ‹ 0.84%) were accepted
at signi®cantly lower levels (P < 0.05).
The optical cross-sectional area of the bolus in feeding
larvae was similar (P > 0.03) for all dietary treatments
except in the unfed control (Fig. 2). This indicated that all
diets were consumed by feeding larvae to a similar degree,
although the within-treatment variability increased with less
acceptable diets. The mean cross-sectional areas for
each treatment were as follows: Artemia 1.11 ‹ 0.10 mm2;
PARA particles 1.05 ‹ 0.01 mm2; MEM particles 1.03 ‹
0.10 mm2; zein-bound particles 1.03 ‹ 0.02 mm2; alginate-
bound particles 0.98 ‹ 0.20 mm2; carboxymethyl cellulose
particles 0.95 ‹ 0.20 mm2; FFK 0.92 ‹ 0.20 mm2; starch
particles 0.89 ‹ 0.40 mm2 and carrageenan particles
0.72 ‹ 0.60 mm2.

156 K.M. Guthrie et al.
Nutrient delivery
The amount of binder and moisture can alter the e€ective
`payload' of mash or nutrients delivered to the gut of the
larval ®sh. Microparticulate diets varied in the ratio of binder
to mash. In addition, live Artemia have a much lower
nutrient density than microparticulate diets because of the
di€erence in moisture. Table 2 shows the percentage payload
for each diet, the consumption of each diet expressed as a
percentage relative to the treatment with the highest con-
sumption (in this case, live Artemia) and the product of the
two, which represents the relative dry matter payload of
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Figure 1 Feeding incidence of ®rst-
feeding larval walleye after 28 h expo-
sure to various microparticulate diets or
live Artemia. PARA is particle-assisted
rotationally agglomerated microparti-
cles; MEM is microextruded then ma-
urmurized; CMC is microbound with
carboxymethyl cellulose; FFK is Fry
Feed Kyowa, a commercial micropar-
ticulate diet. Error bars represent stan-
dard errors. Lower case letters indicate
signi®cant (P < 0.05) di€erences.
Figure 2 Feed consumption of ®rst-
feeding larval walleye after 28 h expo-
sure to various microparticulate diets or
live Artemia. Consumption was mea-
sured as the cross-sectional optical area
(mm2) of the bolus. Error bars represent
standard errors. Lower case letters indi-
cate signi®cant (P < 0.05) di€erences.
nutrients delivered to the larval gut. In terms of dry matter
nutrients delivered to the gut, all the microparticulate diets
were similar to, or higher than live Artemia, even though
more Artemia was consumed on an `as fed' basis.
Discussion
Feeding incidence (% of larvae feeding) represents the
decision on the part of the larva to ingest a feed item for the
®rst time. A larva with only one particle in the gut counts
just as much as a satiated larva. Conversely, feed consump-
tion (gut fullness), measured as the cross-sectional optical
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Acceptability of various microparticulate diets 157

Table 2 Payload of dietary ingredients delivered to the gut of larval could explain why feeding incidence was similar. Conversely,
walleye. Per cent payload is the percentage of the diet that is not the freshwater zooplankton that make up the natural diet of
binder or moisture. Consumption of each diet is calculated as the
larval walleye are translucent. In addition, the ¯avour or the
percentage gut fullness relative to the treatment with the highest
consumption (live Artemia). Payload delivered represents the
lack of ¯avour of each diet, owing to the di€erent binders,
product of percentage payload and consumption (100% payload may also explain the results. Feeding may also have been
delivered would occur if the treatment with the highest consumption e€ected, to some extent, by odours circulated from one
also had no binder or moisture). See text for description of diets treatment to the others via the water recirculation system
Payload Consumption Payload used in this study. Further experiments using a single
Diet/Binder Type (%) (%) delivered (%) microparticulate diet type with di€erent colours or feed
Alginate Microbound 97 88 86 attractants using a ¯ow-through water supply could be used
Artemia Live 30 100 30 to address such possibilities.
Carrageenan Microbound 40 65 26 A high percentage of ®rst-feeding walleye accepted the
CMC Microbound 93 86 79
17 FFK Unknown NA1 83 NA
microparticulate feed without ®rst exposure to live feed, as in
MEM Microextruded 97 93 90 other experiments (Masterson & Garling 1986). Clearly, the
PARA Agglomerated 97 95 92 movement of a live prey item is not necessary to initiate
Starch Microbound 84 80 67
feeding in larval walleye.
Zein Microbound 87 93 81
The results of this study indicate that while walleye larvae
1
NA, not analysed.
will actively feed on several types of microparticulate diets,
they do show marked preferences for some types over others.
area of the bolus, represents a repeated decision to ingest feed. Particles that are highly acceptable to larval walleye, such as
Measuring consumption by determining the cross-sectional PARA, MEM, zein-bound and alginate-bound particles still
area of the bolus maybe more meaningful than by other need to be digestible and correctly formulated to support
methods, such as counting particles. Even if diets di€er in good growth and survival. Diets which are not highly
moisture content and particle size, or if gut passage times acceptable, such as those bound with CMC, carrageenan
di€er, the total size of the bolus will be an accurate re¯ection and starch, would only support survival and growth if high
of the volume of feed consumed (Rust & Barrows 1998). nutrient availability and density were possible.
In this study, feed incidence varied with diet type while Further studies are needed to determine optimal dietary
feed consumption did not. This indicates that once a diet is characteristics and environmental parameters for intensive
initially ingested, larval walleye will continue to ingest it to larval culture of walleye with microparticulate diets. Once
more-or-less the same degree. Once walleyes begin to accept methods are developed to produce high and consistent
diet, the positive reinforcement of odour, taste and satiation feeding incidence and maximal feed consumption, then work
may result in increased and continued consumption (Rottiers on improving formulation and digestibility can proceed.
& Lemm 1985).
It is not clear whether vision or olfaction are more
Acknowledgements
important in locating feed for larval walleye. Iwai (1980)
suggested that chemical senses may be e€ective in perception This study was supported in part by grant
of feed by larval and juvenile ®sh because their ®eld of vision NFFMP299600005 from the Saltonstall-Kennedy grant pro-
is limited, especially at night. Rottiers & Lemm (1985) gram. The authors wish to thank Jihye Kim and Ken Massee
suggested that when the larvae are relatively immobile, the for their help and support in the wet laboratory. The authors
sensory function of the exposed olfactory organ may be thank Rob Holms and Matt Bernard at Garrison Dam NFH
important in the imprinting of permanent behavioural for providing the larval walleye and Dr Conrad Mahaken,
responses to various olfactory sensations. The size or age Dr Robert Iwamato and two anonymous reviewers for
when the olfactory organ become functional in walleye is not critical review of the manuscript.
known. In our study, walleye larvae accepted a wide range of
particles types, including MEM and PARA particles, to the
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Ó 2000 Blackwell Science Ltd Aquaculture Nutrition 6; 153^158