1 - Berens and Murie - 2008

Journal of Fish Biology (2008) 72, 1406–1426
doi:10.1111/j.1095-8649.2008.01806.x, available online at http://www.blackwell-synergy.com
Differential digestion and evacuation rates of prey in

a warm-temperate grouper, gag Mycteroperca microlepis
(Goode & Bean)
E. J. B ERENS * AND D. J. M URIE
Department of Fisheries and Aquatic Sciences, University of Florida,
7922 N.W. 71st Street, Gainesville, FL 32653, U.S.A.
(Received 9 January 2007, Accepted 27 December 2007)
Prey-specific gastric evacuation rates and digestion state indices were modelled for gag
Mycteroperca microlepis, a large warm-temperate grouper, consuming meals of either baitfish
(scaled sardine Harengula jaguana) or crab (purple swimmer crab Portunus gibbesii). Power
exponential models best fit the wet and dry mass gastric evacuation data and the average
digestion indices over post-prandial time (PPT), regardless of prey type or gag size (Adjusted
R2 079). Gag mass (M) or total length (LT) incorporated into an expanded power exponential
model, along with exponential scalars, resulted in highly predictive (R2 087) gastric
evacuation and average digestion state models. The expanded power exponential models fit
to the baitfish and crab wet mass gastric evacuation data differed significantly (Kimura’s
likelihood ratio test (LRT), both P < 0001). Gag consuming crab showed a digestive lag period
of at least 4 h (wet mass) and took a longer time to complete digestion relative to gag consuming
baitfish. Gag, as well as many other warm-temperate and tropical groupers, consume a mixture
of fish and crab prey and they will therefore require the development of a consumption model
that incorporates mixed-prey gastric evacuation models. # 2008 The Authors
Journal compilation # 2008 The Fisheries Society of the British Isles
Key words: bioenergetics; consumption; digestion indices; gastric evacuation.
INTRODUCTION
In warm-temperate and tropical ecosystems, groupers (Serranidae) typically
function as large-bodied macrocarnivores by consuming fishes, crustaceans
and cephalopods (Polovina & Ralston, 1987). Gag Mycteroperca microlepis
(Goode & Bean), a large, reef-associated grouper in the south-eastern U.S.A.,
not only supports valuable recreational and commercial fisheries throughout
its range (Turner et al., 2001), but it is also important in reef ecosystems
where it is known to have a structuring affect on fish assemblages (Hart, 2002;
Lindberg et al., 2006). Within the past two decades, several studies have examined
*Author to whom correspondence should be addressed. Tel.: þ1 352 3929617 ext. 245; fax: þ1 941
3884223; email: [email protected]
1406
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Journal compilation # 2008 The Fisheries Society of the British Isles
DIGESTION AND EVACUATION IN A LARGE GROUPER 1407
various aspects of gag biology, including age and growth, diet, reproduction,
and the effect of fishing and habitat on gag populations (Collins et al., 1987,
1998; Hood & Schlieder, 1992; Coleman et al., 1996; Mullaney & Gale,
1996; Weaver, 1996; McGovern et al., 1998; Lindberg et al., 2002, 2006). To
date, estimates of prey consumption rates of gag, as well as other groupers,
have been unavailable due to the lack of models for gastric evacuation rate,
or the rate at which food passes from the gut. Gastric evacuation has been
modelled in mostly cold-temperate fish species, commonly using linear, expo-
nential, square root, logistic or power exponential models (Swenson & Smith,
1973; Jobling & Davies, 1979; Jobling, 1980a, 1981; Elashoff et al., 1982;
Brodeur, 1984; Hopkins & Larson, 1990; dos Santos & Jobling, 1992; Temming &
Andersen, 1994). Gastric evacuation model coefficients are then either put
directly into, or used to meet the assumptions of, a consumption model. Addi-
tionally, some consumption models require estimates of the original prey mass
at time of capture (Elliott & Persson, 1978; Adams & Breck, 1990), and models
for digestion rates are therefore also necessary. This paucity of information is not
restricted to gag alone, since there is a general lack of any published gastric evac-
uation rate models or digestion rate estimates for grouper or other large warm-
temperate or tropical macrocarnivorous fishes. Therefore, gastric evacuation
models and estimates of original prey mass must be calculated for gag before
their prey consumption can be estimated.
Important factors influencing gastric evacuation processes include tempera-
ture, prey type and composition, ration size and predator size. Groupers, like
most fishes, are ectotherms and therefore their metabolic rates and the corre-
sponding physical and chemical processes, such as enzyme production and
kinetics (Hochachka & Somero, 2002; Diana, 2004), and consumption rates
and evacuation rates (Brett & Higgs, 1970; Jobling, 1980a; He & Wurtsbaugh,
1993), increase with increasing water temperatures. This is an important con-
sideration for tropical and warm-temperate groupers since water temperatures
may reach >30° C in the summer, with concomitant increases in metabolic rate
(Kline, 2004). Prey type can also be influential in gastric evacuation rates in
that the least digestible hard skeletal elements of prey are generally low in
energy and are often the last part of a meal to be emptied from the stomach
(Flowerdew & Grove, 1979; Hopkins & Larson, 1990). Crustacean exoskele-
tons, in particular, have been shown to remain in the stomach for longer peri-
ods of time compared to food with fewer indigestible hard parts, such as fish
prey (Hopkins & Larson, 1990). Predator size is another factor that can affect
consumption and evacuation models (Adams & Breck, 1990). Absolute gastric
evacuation rates (grams of food leaving the stomach per hour) tend to increase
with increasing predator body size, but relative rates (per unit body mass)
either decrease with increasing predator size or stay the same (Flowerdew &
Grove, 1979; Jobling, 1980a; Bromley, 1994).
Like gastric evacuation estimates, calculating the original time of prey inges-
tion by a wild predator and incorporating this required variable into a con-
sumption model has been difficult. One method involves estimating the
percentage of the prey in the stomach contents relative to the original prey
masses obtained by backcalculation, and then back-casting the time of prey in-
gestion (Adams et al., 1982; Murie & Lavigne, 1986, 1991; Murie, 1987; Lindberg
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Journal compilation # 2008 The Fisheries Society of the British Isles, Journal of Fish Biology 2008, 72, 1406–1426
1408 E. J. BERENS AND D. J. MURIE
et al., 2002). Another method involves creating a semi-quantitative visual in-

dex of digestion stages based on prey descriptions (MacDonald et al., 1982;
Lindberg et al., 2002). An index of digestion may be a faster method due to
the fact that a general time of prey ingestion can be estimated based on the
prey’s appearance without having to backcalculate its size through regression
analysis, but it may not be as accurate a method since it can only provide
a range in digestion time, rather than a specific time after feeding.
Currently, for macrocarnivores such as the groupers, gastric evacuation rates
have only been estimated preliminarily from field sampling of gag consuming
primarily small pelagic fishes (baitfishes) off the west coast of Florida during
the warm summer months (Lindberg et al., 2002). Gag, however, can also have
a significant proportion of crabs in their diet (13–17%) during some years
(Weaver, 1996; Lindberg et al., 2002). While crustacean prey found in the stom-
ach contents of groupers is variable among species, it can constitute the major-
ity of prey in the stomachs of some common tropical and warm-temperate
epinepheline groupers, such as red grouper Epinephelus morio (Valenciennes)
and goliath grouper Epinephelus itajara (Lichtenstein) (Longley & Hildebrand,
1941; Randall, 1967; Bullock & Smith, 1991; Weaver, 1996).
The goals of the present study were therefore to: (1) determine experimen-
tally gastric evacuation rates for gag as a function of prey type, either baitfish
or crab prey, in relation to gag size, (2) create semi-quantitative indices of prey
digestive states in order to estimate consumption times of prey sampled from
the stomach contents of wild gag and (3) model and compare evacuation rates
and prey digestive states of gag as a function of prey type and gag size. This
research therefore represents one of the first studies of prey-specific, experimentally-
derived gastric evacuation rates and digestion in a warm-temperate and sub-
tropical marine fish.
MATERIALS AND METHODS
G A G C O LL E C TI O N S A N D M A I N T E N A N C E
Gag were trapped or caught with hook-and-line by scuba divers on artificial reefs off
the west coast of Florida at a depth of 12 m. Fish were transported to an aquaculture
facility at the University of Florida’s Department of Fisheries and Aquatic Sciences
using aerated coolers with 100% diffused oxygen. A re-circulating saltwater system with
378–473 l (870–1470 mm diameter) fibreglass tanks held one to three gag each. Water
changes with fresh sea water kept ammonia, nitrite, nitrate and pH within acceptable
limits (Stickney & Kohler, 1990) and salinity was maintained between 30 and 35. Light
regimes averaged 135 h of light and 105 h of darkness per day, following the photo-
period of the eastern Gulf of Mexico during the summer. In addition, gag were accli-
mated and maintained at a mean S.E. water temperature of 280 10° C. This
temperature corresponded to the mean water temperature at 12 m depth during the
summer at gag collection sites (Bledsoe & Phlips, 2000). Gag were fed on maintenance
rations of thawed, whole baitfish or crab prey at 30% of their body mass every other
day. This feeding rate was based on preliminary field estimates of average daily con-
sumption of gag during the warmer summer months of 12–18% body mass per day
(Lindberg et al., 2002). When two or more gag were maintained in a single tank, the
consumption of maintenance rations was confirmed visually, as fish would eat immedi-
ately on most days. Only fish feeding voluntarily on the maintenance diet were used in
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the experimental feeding trials. All gag were anaesthetized with 150 mg l–1 tricaine
methanosulphate (MS-222) for measurement of total length (LT), fork length (LF)
and mass (M).
EXPERIMENTAL FEEDING TRIALS FOR GASTRIC

EVACUATION RATES
Scaled sardines Harengula jaguana Poey and purple swimmer crabs Portunus gibbesii
(Stimpson), two common prey species of gag (Lindberg et al., 2002), were used in the
experimental feeding trials to represent pelagic baitfish v. crab prey types. Scaled sar-
dines were caught with 36 m cast nets towed by scuba divers over reef areas occupied
by gag during September to November. Purple swimmer crabs were collected at night
with trawls in the eastern Gulf of Mexico with the help of commercial bait-shrimp fish-
ermen. After capture, the baitfish and crabs were immediately placed on ice for trans-
port to the laboratory, then vacuum-sealed in bags and frozen until used in the feeding
trials. A sub-sample of whole scaled sardines (n ¼ 25) collected from the field were indi-
vidually measured for LT, LF and vertebral column length (LVC; measured from the
atlas or axis to the hypural plate), and weighed to the nearest 1 mg after damp-
blotting to remove excess water. Swimmer crabs were measured for carapace length
(LC) and carapace width (WC), and then weighed (n ¼ 24). Individual prey samples were
then macerated and freeze-dried to constant mass to determine per cent moisture.
Energy densities (kJ g–1 dry mass) of each individual prey item were determined using
an isoperibol bomb calorimeter, using standard operating procedures, including correc-
tions for fuse wire burn and acid production (Parr 1261; Moline, IL, U.S.A.).
Gag were acclimated for a minimum of 2 weeks or until they voluntarily accepted
baitfish or crab prey when offered (i.e. they were not force fed). Food was withheld
for 1–2 days before baitfish feeding trials and for 2 days before crab trials to insure that
all maintenance rations had been evacuated from the stomach. Meals of whole scaled
sardines or crabs weighing c. 15% of the grouper’s wet mass were fed voluntarily to
individual small (300–449 mm LT), medium (450–599 mm LT) and large (600–750
mm LT) gag. Stomach contents were recovered from euthanized gag (via overdose of
MS-222) after pre-determined time intervals spanning the range between 018 h (5 min)
and 24 h post-prandial time (PPT). Stomach contents were recovered from the oesopha-
geal opening to the pylorus, immediately damp-blotted to remove excess water, and
then weighed to the nearest 01 mg. After digestion state analysis, the stomach contents
were freeze-dried to constant mass and re-weighed to the nearest 01 mg to determine
dry mass.
I N D I C E S O F DI G E S T I V E S T A T E S
Stomach contents recovered from gag were immediately analysed for their state of
digestion using the presence, absence and appearance of the skin or carapace, eyes,
muscle and bones or exoskeleton of prey (Berens, 2005). Based on the approximate per-
centage of digestion, each prey item was assigned an index of digestion, ranging from
0 (<5% digested) to 6 (>90% digested) (Berens, 2005). The mean digestion index per
gag meal was determined and regressed as a function of PPT to create quantitative indi-
ces of prey digestive states over time.
G A S TR I C E V A C U A TI O N A N D A V E R A G E D I G E ST I O N
I N D E X MO D E L S
Linear, exponential, square root, logistic and power exponential evacuation models
(MacDonald et al., 1982; Hopkins & Larson, 1990) were fitted to the wet and dry mass
gastric evacuation data and the average digestion index data separately, for each prey
type by gag size. Proportions were used to fit the power exponential model (Hopkins &
# 2008 The Authors

Larson, 1990), so the percentage of meal remaining was divided by 100 and the diges-
tion indices were divided by 6 (maximum digestion index). Therefore, to facilitate com-
parison with the outputs of other models, all gastric evacuation y-intercepts for the
power exponential model had to be multiplied by 100, while digestion index y-intercepts
were multiplied by 6 (Elashoff et al., 1982; Hopkins & Larson, 1990). Only initial zeros
(i.e. the first feeding trial resulting in 0% stomach contents remaining at PPT) were
included in the data to prevent biases associated with including zeros past endpoints,
as well as biases from excluding all zeros, thereby increasing the proportion of faster
digesting fish that are eliminated from the distribution (Olson & Mullen, 1986). The
fit of a model was considered acceptable if it: (1) was significant at the a ¼ 005 level,
(2) showed homoscedasticity of variances, (3) had gastric evacuation y-intercept values
between 95 and 105% prey remaining or digestion index y-intercepts between –05 and
05 and (4) had lower asymptotes showing <5% prey remaining or upper asymptotes
showing >825% prey digested (index ¼ 55) for the gastric evacuation and digestion
index data, respectively (Hopkins & Larson, 1990; Zar, 1999). For models that fit these
initial selection criteria, adjusted R2 values were compared to determine which model
best explained the data (Healy, 1984; SAS, 1999).
Kimura’s likelihood ratio test (LRT) was used to test for differences among models
(Kimura, 1980; Haddon, 2001). For curves that differed significantly among gag size
groups, data were pooled by prey type and modelled with either an M or LT scaling
exponent to create prey-specific models of gastric evacuation and average digestion
indices that account for differences in gag size as: Y ¼ function (Mc) and
Y ¼ function ðLT c Þ; where Y ¼ % prey remaining in the stomach or average digestion
index, function ¼ model and C ¼ M or LT scaling exponent. Non-linear R2 values were
calculated according to Elashoff et al. (1982). All tests of significance were at a 005.
RESULTS
GAG AND PREY COLLECTIONS

A total of 66 gag were collected for gastric evacuation experiments; 22 small
gag (314–441 mm LT, 371–977 g), 30 medium gag (452–598 mm LT, 988–2295 g)
and 19 large gag (600–733 mm LT, 2204–4703 g). The relationship between gag
M and LT was: M ¼ 2E 05ðLT 28865 Þ (R2 ¼ 098 n ¼ 71). Baitfish fed to gag in
the experimental feeding trials were greater in LT than crabs were in LC but
with a lack of exoskeleton they had less mass (Table I). Baitfish were also
almost twice the energy density of crabs, and their energy density was not as
variable as that for crabs. During the experimental feeding trials, individual
gag consumed meals of whole baitfish mean S.D. 151 002% or whole crab
meals mean S.D. 145 002% of their wet body mass.
G A S T R I C E V A C U A T I O N MO D E L S F O R G A G C O N S U M I N G
B A I T FI S H P R E Y
Baitfish feeding trials were completed on 44 gag (14 small, 19 medium and 11
large). Initial zero points from gag with faster digestion were included in the wet
and dry mass analyses while all zero points following this (n ¼ 3) were dropped
to prevent model bias, as well as one outlying data point that was >2 S.D. from
the mean, resulting in usable data from 40 gag. The linear and power exponen-
tial models both met the selection criteria for each gag size class, however, only
the power exponential model met the criteria on both a wet and dry mass basis
(Table II). There was no apparent lag phase in baitfish evacuation on a wet
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TABLE I. Total length (LT) and carapace length (LC), mass (M) and energy density of
baitfish prey (scaled sardines) and crab prey (purple swimmer crab) fed to gag in the
experimental feeding trials
Prey type Measurement Mean S.E. Range n
Baitfish LT (mm) 786 03 640–930 231

M (g) 508 006 296–850 231
Energy density 1775 008 1700–1886 25
(kJ g–1dry mass)
Crab LC (mm) 194 02 150–235 111
M (g) 593 016 277–1168 111
Energy density 929 025 603–1172 24
(kJ g–1dry mass)
mass basis [Fig. 1(a)] as 5–30 min trials showed between 999 and 985% of
prey remaining, with 925% remaining just 15 h after feeding. On a dry mass
basis [Fig. 1(b)], small and large gag evacuation rates showed a lag of up to
25 h PPT. Estimated times to 5% remaining, on a wet mass basis for small,
medium and large gag were 147, 195 and 174 h PPT and on a dry mass basis
were 94, 165 and 125 h PPT, respectively.
GA S TR IC E V A C UA TI O N MO DE L S F O R G A G C O N SU M ING
CRAB PREY
Crab feeding trials were completed on 27 gag (eight small, 11 medium and
eight large). Fewer gag were used in crab trials due to the availability of crab
and because it took gag longer to feed reliably on crab when offered. One zero
datum was eliminated to prevent model bias. As with gag consuming baitfish,
the power exponential model met all selection criteria for all three size classes
of gag and for both wet and dry mass measurement (Table II). The logistic
model also met all selection criteria but only for evacuation measured as wet
mass. No other models met selection criteria in each gag size class. Evacuation
of crab prey modelled using a power exponential equation showed long lag
phases in evacuation, with noticeable breakdown starting after 4 h PPT on
a wet mass basis [Fig. 2(a)] and 1–4 h PPT on a dry mass basis [Fig. 2(b)].
Times to 5% prey remaining on a wet and dry mass basis for each gag size
class were determined to be 210, 196 and 245 h PPT and 201, 172 and
262 h PPT, respectively.
COMPARATIVE GASTRIC EVACUATION MODELS –

B A I T F I S H V E R SU S C R A B P R E Y
The power exponential evacuation models differed among gag size classes on
both a wet and dry mass basis when fit to the baitfish evacuation data (LRT,
n ¼ 40, P < 0001 and n ¼ 40, P < 001, for wet and dry mass, respectively), or
crab evacuation data (LRT, n ¼ 26, P < 005 and n ¼ 26, P < 005, for wet
and dry mass, respectively), and therefore size-specific models were retained.
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1412
TABLE II. Gastric evacuation coefficients of gag fitted to each model that met selection criteria for baitfish prey (scaled sardines) and crab prey
(purple swimmer crab). All models were significant at P 0001
Prey Measurement
Journal compilation
type type Model* n Gag size A B C y-intercept Adjusted R2
#
Baitfish Wet mass Linear 13 Small 9550 632 9550 094
Linear 16 Medium 9985 603 9985 094
Linear 11 Large 10319 618 10319 092
Wet mass Power exponential 13 Small 616 168 10000 098
Power exponential 16 Medium 744 152 10000 095
Power exponential 11 Large 801 189 10000 095
Dry mass Power exponential 13 Small 626 364 10000 079
Crab Wet mass Logistic 8 Small 8776 –049 –1142 9969 094
Logistic 10 Medium 10130 –037 –1231 9896 098
Logistic 8 Large 12990 –019 –1623 9470 094
Wet mass Power exponential 8 Small 1249 285 10000 095
E. J. BERENS AND D. J. MURIE

Dry mass Power exponential 8 Small 892 180 10000 089
*t ¼ post-prandial time (h) for all models; linear model, y ¼ A – Bt, where A ¼ y-intercept and B ¼ gastric evacuation rate; power exponential model,
1 B
y ¼ 2 ðtA Þ ; where A ¼ half-life of decaying prey and B ¼ shape coefficient, model was fitted using proportional data and due to model specifications the
y-intercept of the power exponential model is fixed at y ¼ 1 (100%) and not uniquely estimated; logistic model, y ¼ 100 – (A{1þe[B(t þ C)]}–1), where A ¼ estimated
coefficient, B ¼ scale coefficient and C ¼ x-ordinate of the point of inflection of the curve.
2008 The Fisheries Society of the British Isles, Journal of Fish Biology 2008, 72, 1406–1426
# 2008 The Authors
120 (a)
100
80
60
40
Food remaining in stomach
20
120 (b)
100
80
60
40
20
0 5 10 15 20 25
Post-prandial time (h)
FIG. 1. Power exponential model describing the per cent food remaining in the stomach of small ( ),
medium ( ) and large ( ) gag consuming baitfish prey (scaled sardines) as a function of post-
prandial time on a (a) wet and (b) dry mass basis. Model coefficients are given in Table II.
When exponential scaling factors for gag M or LT coefficients were incorpo-

rated into the wet and dry mass power exponential models, each met selection
criteria and was highly predictive (P < 0001, R2 087; Table III). Gag evac-
uated baitfish more quickly than crabs on both a wet and dry mass basis
(Table III and Fig. 3), with the comparable half-life (A) of decaying prey
always less for baitfish than crab prey. Of particular relevance to food habit
studies, the expanded power exponential models scaled to M fit to the baitfish
and crab wet mass data, pooled across all gag size classes by prey type, differed
significantly from one another (LRT, n ¼ 66, P < 0001). Again, these models
indicated that gag completed gastric evacuation earlier when fed baitfish, on
a wet mass basis, and lags in prey digestion of c. 4 h PPT were only evident
when gag consumed crabs (Fig. 3).
I N D I C E S O F DI G E S T I O N F O R P R E Y C O N S U M E D B Y GA G
All gag consumed the baitfish and crab prey whole with very minimal, if any,
loss of scales and skin of fish prey, or the cracking of carapaces and limb
removal of crab prey. Digestion was observed to be most rapid in the pyloric
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120 (a)
100
80
60
40
20
120 (b)
100
80
60
40
20
0 5 10 15 20 25
FIG. 2. Power exponential model describing the per cent food remaining in the stomach of small ( ),
medium ( ) and large ( ) gag consuming crab prey (purple swimmer crabs) as a function of
post-prandial time on (a) wet and (b) dry mass basis. Model coefficients are given in Table II.
TABLE III. Gastric evacuation coefficients of the expanded power exponential models
incorporating gag total length (LT) or mass (M). The curves were fitted by
1 B 1 B
y ¼ 2 ðtA Þ M C or y ¼ 2 ðtA Þ LTC ; where t ¼ post-prandial time (h), A ¼ half-life of
decaying prey, B ¼ shape coefficient and C ¼ scaling exponent. All models were
significant at P < 0001, with n ¼ 40 for gag consuming scaled sardines (baitfish) and
n ¼ 26 for gag consuming purple swimmer crabs (crab)
Prey type Measurement type Scalar A B C Adjusted R2
Baitfish Wet mass M 712 164 000134 096

LT 716 165 000081 096
Dry mass M 640 185 –000240 087
LT 646 188 –000444 087
Crab Wet mass M 1247 265 000084 097
LT 1246 264 000123 097
Dry mass M 930 188 –000370 094
LT 926 186 –000371 094
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120

100
80
60
40
20
0 5 10 15 20 25
FIG. 3. Expanded power exponential models, incorporating total length as an exponential scaling factor,
describing the per cent food remaining in the stomachs of all gag consuming either baitfish ( ,
scaled sardines) or crab ( , purple swimmer crab) prey, on a wet mass basis, as a function of post-
prandial time. Model coefficients are given in Table III.
region of the stomach. Baitfish prey were digested fairly continuously from
their initial consumption up to c. 5 h PPT [Table IV and Fig. 4(a)]. At c. 8 h
PPT, incomplete baitfish vertebral columns began to appear, and skulls, oto-
liths, guts, skin and fin rays were often absent (digestion index ¼ 4). By 10
h PPT, most baitfish were unrecognizable with only incomplete vertebral col-
umns and very small bits of muscle present (digestion index 5). With PPT
> 15 h, digesta consisted only of chyme and small bits of loose bones and indi-
vidual baitfish were indistinguishable (stomach contents 90% digested; diges-
tion index ¼ 6).
After a lag phase of at least 4 h PPT, crab prey recovered from stomach con-
tents commonly had several legs detached from the carapace, especially those
TABLE IV. Mean S.E. and range of post-prandial times (PPT) in relation to the
digestion index and the per cent digestion for gag consuming scaled sardines (baitfish)
(n ¼ 40) and purple swimmer crab (crab) (n ¼ 26)
PPT (h)
Baitfish prey Crab prey

Digestion Per cent
index digestion Mean S.E. Range Mean S.E. Range
0 <5 020 009 008–050 360 108 080–800

1 5–10 236 053 050–450 730 075 650–800
2 10–25 450 150 300–600 1000 000 1000
3 25–50 400 050 300–450 1100 100 900–1200
4 50–75 800 067 600–1200 1500 173 1200–1800
5 75–90 1050 203 750–1650 1600 000 1600
6 >90 1480 071 900–1800 2090 084 1600–2400
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6
(a)
5
1
Average digestion index
6
(b)
5
0 5 10 15 20 25
FIG. 4. Power exponential models describing the average meal digestion indices of small ( ), medium
( ) and large ( ) gag consuming (a) baitfish (scaled sardines) and (b) crab (purple swimmer crab)
as a function of post-prandial time. The model coefficients are given in Table V.
located toward the pyloric end of the stomach [Table IV and Fig. 4(b)]. The
exoskeleton, however, was not yet softened nor had it been noticeably digested.
Subsequently, the carapace began to soften and collapse while the carapace
spines began to erode and appendages began to detach. At around 11 h PPT
(digestion index ¼ 3), the carapace was softened, folded and eroded, with holes
forming in the carapace and exposing the internal body cavity. This pattern
continued until c. 15 h PPT when the crab prey was recognizable only by scat-
tered and pigmented carapace pieces, void of any muscle, gut or appendages.
After 16 h PPT, the crabs were 90% digested and only small bits of carapace
were present in the digesta (digestion index ¼ 6).
A V E R A G E D I G E ST I O N I N D E X M O D E L S
The power exponential models met selection criteria and best described
the relationship between the average digestion indices and PPT for small,
medium and large gag consuming either baitfish or crab prey (all P 0001,
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adj. R2 090) (Table V). While initial data with digestion indices of 6 were
included in the analyses, subsequent data with indices of 6 were excluded to
prevent model bias (three baitfish and one crab). There were slight lag phases
detected in the baitfish data, as 25 h feeding trials resulted in average digestion
indices 112, and large lags in the onset of digestion of crabs, as indices were
still <10 at 60 h PPT (Fig. 4). For each size of gag, the models’ upper asymp-
totes equalled or exceeded an average digestion index of 55, which equates to
c. 825% digestion, at 180 and 240 h PPT for baitfish and crab prey, respec-
tively. The square root and logistic models also met selection criteria for all sizes
of gag (all P 0001, adj. R2 ¼ 083–090 and 093–098, respectively), when
fitted to the crab digestion indices. The square root model, however, slightly
overestimated the digestion indices at the earliest time intervals (y-intercepts ¼
012–041 h PPT) and the logistic model could not adequately estimate the
upper asymptote of large gag consuming baitfish.
The power exponential models fit to the average digestion indices of either
baitfish or crab meals differed significantly between the three different gag size
classes (LRT, n ¼ 40, P < 005; n ¼ 26, P < 001, respectively). Because pred-
ator size had a significant effect, the data were pooled across gag sizes by prey-
type and fit to expanded power exponential models with M or LT scaling
factors incorporated. The resulting models met selection criteria and were
TABLE V. Average digestion index model coefficients for gag consuming baitfish (scaled
sardines) or crab (purple swimmer crab) that met selection criteria. All models were
significant at P 0001
Prey type Model* n Gag size A B C y-intercept Adjusted R2
Baitfish Logistic 13 Small 602 –046 –532 047 092

Logistic 16 Medium 562 –057 –477 034 092
Power exponential 13 Small 418 –166 000 090
Power exponential 16 Medium 456 –184 000 092
Power exponential 11 Large 579 –197 000 091
Crab Linear 8 Large –043 030 –043 094
Logistic 8 Small 601 –056 –1172 001 095
Logistic 11 Medium 622 –037 –1255 006 098
Logistic 8 Large 561 –036 –999 015 093
Power exponential 8 Small 1118 –480 000 096
Power exponential 11 Medium 1129 –347 000 095
Power exponential 8 Large 972 –238 000 094
Square root 8 Small 012 011 012 083
Square root 11 Medium 040 008 040 087
Square root 8 Large 041 009 041 090
*t ¼ post-prandial time (h) for all models; linear model, y ¼ A – Bt, where A ¼ y-intercept and B ¼
1 B
gastric evacuation rate; power exponential model, y ¼ 2 ðtA Þ ; where A ¼ half-life of decaying
prey and B ¼ shape coefficient, model was fit using proportional data and due to model
specifications the y-intercept is fixed at y ¼ 0 (0%) and not uniquely estimated; logistic model,
y ¼ 100 – (A{1þe[B(t þ C)]}–1), where A ¼ estimated coefficient, B ¼ scale coefficient and C ¼ x-ordinate
of the point of inflection of the curve; square root model, Oy ¼A – Bt, where A ¼ y-intercept and
B ¼ gastric evacuation rate.
# 2008 The Authors

TABLE VI. Average digestion index model coefficients of the expanded power exponential
models incorporating gag total Blength (LT) or mass (M). The curves were fitted by
1 B 1
y ¼ 2 ðtA Þ M C or y ¼ 2 ðtA Þ LCT ; where t ¼ post-prandial time (h), A ¼ half-life of
decaying prey, B ¼ shape coefficient and C ¼ scaling exponent. All models met selection
criteria and were significant at P 0001, with n ¼ 40 for gag consuming scaled sardines
(baitfish) and n ¼ 26 for gag consuming purple swimmer crabs (crabs)
Prey type Scalar A B C Adjusted R2
Baitfish M 571 –130 00202 091

LT 633 –114 00355 091
Crab M 1197 –259 00188 095
LT 1219 –247 00258 095
significant and highly predictive (P < 0001, R2 ¼ 091), even though scaling
exponents were small (C ranged from 00188 to 00355) (Table VI and Fig. 5).
DISCUSSION
G A S T R I C E V A C U A T I O N MO D E L S
The power exponential model provided the best description of evacuated di-
gesta as a function of PPT for gag, regardless of prey type, gag size, or method
of measuring stomach contents (Table II and Figs 1 and 2). Gastric evacuation
rates of several other macrocarnivorous fishes have previously been described
using the power exponential model, including black-and-yellow rockfish Se-
bastes chrysomelas (Jordan & Gilbert) consuming whitebait smelt Allosmerus
elongatusus (Ayres) and purple shore crab Hemigrapsus nudus Dana (Hopkins
5
Average digestion index
0 5 10 15 20 25
FIG. 5. Expanded power exponential models, incorporating total length as an exponential scaling factor,
describing the average digestion index values of gag consuming baitfish ( , scaled sardines) or crab
( , purple swimmer crab) as a function of post-prandial time. Model coefficients are given in
Table VI.
# 2008 The Authors

& Larson, 1990), and Atlantic cod Gadus morhua L. consuming capelin Mallo-
tus villosus (Mueller) and Atlantic herring Clupea harengus L. (dos Santos &
Jobling, 1992). Other studies have also used an expanded power exponential
model incorporating two or more predictive variables, such as time after in-
gestion, temperature, meal size, prey size, prey energy density, predator M
and predator LT (dos Santos & Jobling, 1992; Temming & Andersen, 1994;
Andersen, 1999, 2001; Koed, 2001).
Effects of prey type

The power exponential models accounted for both the lack of a digestive lag
phase when gag consumed baitfish, based on wet mass, as well as the large lag
phases observed when gag evacuated crab prey (Figs 1, 2 and 3). While the
highly friable immature scaled sardines were quickly broken down by the gag’s
digestive enzymes, large lag phases in digestion of at least 4 h PPT occurred
when gag consumed crab. These lags were immediately followed by a rapid
increase in digestion for the next 12–15 h until residual hard parts persisted
in the stomach and slowed digestion once again. Digestion-resistant exoskeletal
material and other residual hard parts are known to cause lag phases in diges-
tion and cause evacuation curves to form lower asymptotes at the later time
periods (Battle, 1935; Windell, 1966; Hopkins & Larson, 1990; dos Santos &
Jobling, 1992). These lags in digestion have been attributed to impaired enzyme
secretion, force-feeding and starvation (Swenson & Smith, 1973; Jones, 1974;
MacDonald et al., 1982; Jackson et al., 1987). Considering that gag in this
study were not force fed or starved, these lag phases were probably due to
the exoskeleton initially acting as a barrier to enzymatic action, which would
be a combination of hydrochloric acid secretion necessary to decalcify the
exoskeleton’s calcium carbonate material, in addition to chitinase and chito-
biase secretion, as well as the mechanical peristalsis necessary to break up
the material in the softened exoskeleton (Pandian, 1967; MacDonald et al.,
1982; Lindsay, 1984; Hopkins & Larson, 1990; dos Santos & Jobling, 1992;
Bromley, 1994; Lovell, 1998). The pyloric sphincter may also limit the size
of items that pass into the intestine, thereby playing a role in the retention
of exoskeletal material and the formation of digestive lag phases. Basing the
power exponential models on the dry mass data tended to decrease the diges-
tive lag phases of crab prey to 1–4 h PPT. Similarly, Hopkins & Larson (1990)
found that the digestive lag phase was longer when black-and-yellow rockfish
consumed purple shore crab on a wet mass basis as compared to modelling
the data on a dry mass basis.
Previous work has shown that thawed prey, such as whole Cape anchovy
Engraulis capensis (Gilchrist), pieces of squid Loligo vulgaris reynaudii (comb.
nov.), pieces of hake Merluccius sp. and detached rock lobster Jasus lalandii
(Milne-Edwards) tails, used in in vitro digestion rate experiments digested faster
in pepsin than controls of fresh prey (Jackson et al., 1987). Field and labora-
tory experiments with black-and-yellow rockfish, however, indicated that labo-
ratory determined gastric evacuation rates using thawed purple shore crab gave
acceptable approximations of in situ evacuation rates using freshly killed indi-
viduals of the same species (Hopkins & Larson, 1990). Similarly, results from
the present laboratory study indicated that thawed baitfish prey were 95%
# 2008 The Authors

evacuated between 147 and 195 h PPT, which was comparable to preliminary
field estimates of gastric evacuation of wild gag that showed 90% evacuation at
c. 150 h PPT (Lindberg et al., 2002).
Evidence suggests that the extrapolation of single-meal and single-prey mod-
els, such as those in the present study, can yield reasonable estimates of total
daily ration (Persson, 1984; dos Santos & Jobling, 1992; Singh-Renton &
Bromley, 1996). Further research, however, will determine if the single-meal,
single-prey gastric evacuation rates determined in this study are biased when
applied to sequential-meal, mixed-meal, and sequential-meal and mixed-meal
situations, and whether or not their extrapolation will yield acceptable esti-
mates of total daily ration.
Effects of predator size

Gag size had a significant effect on gastric evacuation rates regardless of
prey type and the method of measuring stomach contents (wet v. dry). For
example, on a wet mass basis, small gag evacuated baitfish prey faster than
medium and large gag (Fig. 1). In contrast, all sizes of gag had similar lag
phases in evacuation of crab prey and initial evacuation, but then diverged
as digestion continued with large gag showing the slowest evacuation rates over
time (Fig. 2). Similarly, studies on haddock Melanogrammus aeglefinus L.,
Atlantic cod and whiting Merlangius merlangus L. fed saithe Pollachius virens L.
(Jones, 1974), turbot Scophthalmus maximus L. fed processed pellets (Flowerdew
& Grove, 1979), and Atlantic cod fed capelin, Atlantic herring, prawn Pandalus
borealis (Kroyer) or krill Meganyctiphanes norvegica (M. Sars) (dos Santos &
Jobling, 1995), found that predator size had a significant effect on rates of gas-
tric evacuation. In contrast, studies on Atlantic cod fed shrimp Pandalus mon-
tagui Leach (Tyler, 1970), dab Limanda limanda L. fed an artificial paste diet
(Jobling et al., 1977), and plaice Pleuronectes platessa L. fed fish-paste (Jobling,
1980b) did not observe size-specific evacuation rates. While previous work has
shown that feeding meals to a predator as a percentage of their body mass can
account for variability due to their size (Swenson & Smith, 1973), the present
study showed that this is not always the case. Gag size significantly affected
rates of gastric evacuation despite feeding meals relative to each gag’s body
mass. Scaling factors for gag M or LT were incorporated into the baitfish
and crab power exponential models to account for the significant differences
between gag sizes, based on the assumption of multiplicity (Andersen, 1999).
In the present study, M and LT raised to a power approaching 00 (C
00355) created multiplicative scaling factors that were very close to 10 (e.g.
M ¼ 10, LT ¼ 10) (Table III). These small but significant exponents are rea-
sonable considering that relative mass meals have been known to take out
much of the variation in meal mass recovered from different sized predators
(Bromley, 1994).
PREY COMPOSITION
Crustacean exoskeletons contain chitin, a carbohydrate (polysaccharide) that
most fishes break down to N-acetyl-D-glucosamine (NAG) and D-glucosamine
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(Jackson et al., 1992), however they are not known to assimilate NAG or D-
glucosamine directly (Battle, 1935; MacDonald et al., 1982; Lindsay & Gooday,
1985; Medved, 1985). Although many fishes secrete chitinase, the general
acceptance is that piscivorous fishes, especially marine fishes, cannot utilize chi-
tin as an energy source (Battle, 1935; MacDonald et al., 1982; Lindsay &
Gooday, 1985, Medved, 1985, Vollhardt & Schore, 1987). Lindsay (1984)
hypothesized that the primary function of chitinase in the gut of fishes may
be to chemically disrupt the outer chitinous material of prey. For fishes with
chitinase, one advantage of chitinolysis would be to decrease prey handling
time due to increased gastric evacuation rates associated with increased
mechanical breakdown of the exoskeleton, thereby allowing enzymes easier
access to more readily digestible tissues and cuticle proteins (Holling, 1959;
Jackson et al., 1992). Even so, digestion-resistant materials have been shown
to slow rates of gastric evacuation due to residual matter and ash that must
be passed from the body (Battle, 1935; Windell, 1966; Hopkins & Larson,
1990; dos Santos & Jobling, 1992). Therefore, prey with high amounts of diges-
tion-resistant materials, such as crabs with exoskeletal coverings, would be ex-
pected to have relatively slower rates of gastric evacuation (Flowerdew &
Grove, 1979; Jobling, 1980b). In fact, in the present study, times to 95% evac-
uation at 280° C for small, medium and large gag consuming crab prey on
a wet mass basis took 43 h longer than gag consuming baitfish (Fig. 3). In
a colder, north temperate environment, times to 95% evacuation for black-
and-yellow rockfish consuming whitebait smelt and purple shore crabs were
270 and 495 h, respectively, a difference of 225 h (Hopkins & Larson, 1990).
I N D I C E S O F DI G E S T I O N
Visual indices of prey digestive stages over PPT are one way that researchers
can estimate times of prey consumption in the field based on the average diges-
tion index assigned to recovered stomach contents. When each size class of gag
consumed either baitfish or crab prey the power exponential model best
described their average digestive indices over PPT (Table V and Fig. 4). Again,
little or no lag phase was seen when gag consumed baitfish prey, however, lag
phases of a minimum of 4 h PPT resulted when gag consumed crab (Figs 4 and
5). The visual index of baitfish and crab digestive states showed that prey con-
taining higher percentages of chitin remain recognizable for longer periods in
the gut (MacDonald et al., 1982). Previous evacuation studies on Atlantic
cod, ocean pout Macrozoarces americanus (Bloch and Schneider), winter floun-
der Pseudopleuronectes americanus (Walbaum) and American plaice Hippoglos-
soides platessoides (Fabricius) fed bivalves Yoldia sapotilla, amphipods Tmetonyx
cicada and polychaetes Nephtys incise have also found that visual indices of
prey digestion are correlated with quantitative differences in evacuation rates
between prey types (MacDonald et al., 1982). These digestion indices and mod-
els of average digestion indices over PPT will allow researchers to estimate con-
sumption times of wild gag. In addition, measurement effort and processing
time of wild gag stomach contents will be reduced, as only the average diges-
tion indices of prey will need to be estimated. Most importantly, these backcal-
culated times of prey consumption can help determine gag feeding frequency
# 2008 The Authors

and chronology, both of which affect the type of consumption model most
appropriate for the species (Adams & Breck, 1990).
CONSUMPTION
One of the most important factors influencing growth, either individual
growth or growth at the population level, is the consumption of prey. On an
ecosystem scale, consumption relative to biomass (Q:B) is one of the most
important variables required for trophic ecosystem modelling (Palomares &
Pauly, 1998). While there are several ways to estimate consumption, using
a bioenergetics modelling approach requires the use of gastric evacuation rates,
either directly in the model or to meet the model’s assumptions. To date, the
lack of gastric evacuation-rate data on large warm-temperate or tropical mac-
rocarnivorous fishes has prevented the use of bioenergetics modelling as
a means of estimating consumption in these fishes. An ability to estimate con-
sumption rates for these fishes may ultimately allow an ecosystem-based
approach to their management and conservation.
Based on results from this study, gag as well as other large warm-temperate
and tropical macrocarnivorous fishes will probably require a multiplicative con-
sumption model, such as that of Atlantic cod feeding on Atlantic herring in the
Barents Sea (Johansen et al., 2004) or an additive model, with a delay for gag
consuming crab. The multiplicative or additive model chosen must incorporate
gastric evacuation models specific to the prey types consumed, i.e. both fish and
crustacean prey, among others, as well as their species-specific influences on
gastric evacuation due to seasonality of prey quality and quantity. Gag con-
suming low-energy prey that contain large amounts of indigestible materials,
such as crab prey, presumably would need to consume more crab prey to grow
at rates similar to gag consuming baitfish. Results from the present study
clearly show that crab prey require more handling time (at a minimum, more
gastric evacuation time) than baitfish prey, therefore consumption rates and
energy uptake by individual gag should be limited to the time needed to digest
the crab meals (Holling, 1959). Prey consumption by gag may also be a function
of differing prey vulnerabilities (Sih & Christensen, 2001) and density-dependent
effects that may reduce the number of successful foraging episodes, thereby
causing an increase in the gag’s optimal diet breadth to include lower energy
prey, such as crabs (Emlen, 1966; MacArthur & Pianka, 1966).
In conclusion, the power exponential model best fitted both the wet and dry
mass gastric evacuation data and the average digestion index data irrespective
of prey type (baitfish v. crabs) and gag size. Gag gastric evacuation rates as
a function of PPT were significantly affected by prey type, in terms of the
curve’s shape and total prey retention times; most notably, crabs were associ-
ated with a lag in digestion of at least 4 h PPT. Gag size (300–750 mm LT) sig-
nificantly affected both the baitfish and crab gastric evacuation models when
using either the wet or dry mass data. The size of gag used in this study was
within the size range of pre-reproductive individuals normally encountered
on coastal reefs in the eastern Gulf of Mexico (Lindberg et al., 2006). Addi-
tional work on quantifying the gastric evacuation rates of gag <300 mm LT
and >750 mm LT, at temperatures <28° C and >28° C, with different relative
# 2008 The Authors

meal sizes, mixed-meals, sequential-meals and differing prey types will improve
the ability of the evacuation models to predict the percentages of prey remain-
ing over PPT and the average digestion indices over PPT. The power exponen-
tial gastric evacuation models for gag determined in the present study have
shown that prey type and gag size are not only significant variables when deter-
mining rates of gastric evacuation but they, along with backcalculated times of
prey consumption by wild gag, are variables that must be included in any
future consumption model for gag or other large marine, macrocarnivorous
fishes.
We especially thank D. Parkyn and W. Lindberg, University of Florida, Department
of Fisheries and Aquatic Sciences, and K. Bjorndal, University of Florida, Department
of Zoology, for their advice and review of a previous draft. Many thanks to M. Butler,
J. Debicella, R. Kline, S. Larsen, E. Leonard, D. Marcinek, D. Colle and L. Tolbert for
help with specimen collection and assistance in the aquatic facility. In particular, we
thank fishermen D. Cherry and D.J. White for allowing us to collect crabs from their
trawls. Financial and logistical support was provided by Florida Sea Grant, the Fish-
eries and Aquatic Sciences Department of the University of Florida, and through
a scholarship awarded to E. Berens from the Florida Chapter of the American Fisheries
Society.
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Journal of Fish Biology (2008) 72, 1406–1426

doi:10.1111/j.1095-8649.2008.01806.x, available online at http://www.blackwell-synergy.com

Differential digestion and evacuation rates of prey in

(Received 9 January 2007, Accepted 27 December 2007)

Journal compilation # 2008 The Fisheries Society of the British Isles

Key words: bioenergetics; consumption; digestion indices; gastric evacuation.

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et al., 2002). Another method involves creating a semi-quantitative visual in-

MATERIALS AND METHODS

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EXPERIMENTAL FEEDING TRIALS FOR GASTRIC

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GAG AND PREY COLLECTIONS

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Prey type Measurement Mean S.E. Range n

Baitﬁsh LT (mm) 786 03 640–930 231

COMPARATIVE GASTRIC EVACUATION MODELS –

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Power exponential 8 Large 1291 228 10000 095

When exponential scaling factors for gag M or LT coefﬁcients were incorpo-

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Prey type Measurement type Scalar A B C Adjusted R2

Baitﬁsh Wet mass M 712 164 000134 096

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Food remaining in stomach

Baitﬁsh prey Crab prey

0 <5 020 009 008–050 360 108 080–800

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Prey type Model* n Gag size A B C y-intercept Adjusted R2

Baitﬁsh Logistic 13 Small 602 –046 –532 047 092

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Prey type Scalar A B C Adjusted R2

Baitﬁsh M 571 –130 00202 091

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Effects of prey type

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Effects of predator size

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consequences of ﬁshing spawning aggregations. Environmental Biology of Fishes

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approach to estimating consumption in piscivorous ﬁsh. Canadian Journal of

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Palomares, M. L. D. & Pauly, D. (1998). Predicting food consumption of ﬁsh populations

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