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JOURNAL OF EXPERIMENTAL ZOOLOGY 307A:568-577 (2007)

Prey Envenomation Does Not Improve Digestive


Performance in Western Diamondback Rattlesnakes
(Crotalus atrox)
MARSHALL D. MCCUE"

Department ofBiological Sciences, University ofArkansas, Fayetteville, Arkansas

ABSTRACT

Allhough the toxic properties of snake venoms have been recognized throughout
history, very little is known about the adaptive significance of these powerful mixtures. Thill study
examined the popular hypothesis that prey envenomation enhances digestion by influencing the
energetic costs of digestion and assimilation, gut passage time, and apparent assimilation efficiency
(ASSlM) in western diamondback rattlesnakes (Crotalus otrox), a species whose venom is recognized
for its comparatively high proteolytic activities. A complete randomized block design allowed
repeated measures of specific dynamic action and gut passage time to be measured in eight snakes
ingesting four feeding treatments (i.e. artificially envenomated live mice, artificially envenomated.
prekilled mice, saline injected live mice, and saline injeeted prekilled mice). A second experiment
measured ASSTM in eight snakes ingesting a series of six artificially envenomated or six saline
injected mice meals over an 8-week period. Contrary to expectations, the results of both these
experiments revealed that envenomation had no significant influence on any of the measured
digestive performance variables. Gut passage time averaged 6 days and ASSIM averaged 79.1%.
Twenty-one hours following ingestion, postprandial metabolic rates exhibited. factorial increases that
averaged 3.9-fold greater lhan resting metabolic rate. Specific dynamic action lasted on average 88 hr
and accounted for 26% of the total ingested. energy. The results of this study reinforce the need to
systematically examine the potential adaptive advantages that venoms confer on the snakes that
2007 Wiley-Liss, Inc.
produce them. J. Exp. 7..001. 307A-568-577. 2007.
How to cite this article: McCue MD. 2007. Prey envenomation does not improve digestive
performance in western diamondback rattlesnakes (Crotalus atrox). J_ Exp. Zool.
307A:568-577.

For decades scientists have speculated about the


various adaptive functions of snake venoms
(Zeller, '48; Gans and Elliott, '68; Pough and
Groves, '83; Hayes et aI., '95; Daltry et al., '96;
Kardong, '96). The most popular theories suggest
that snake venoms serve chiefly predatory,
defensive, and/or digestive functions. Although
each of these hypotheses are supported by a long
history of anecdotal evidence, because of the
obvious logistical difficulties in dealing with
venomous snakes, very few studies have
attempted to investigate systematically the specific advantages that venoms concede to the relative
fitness or life histories (sensu Dunham et al . '89;
Boggs, '92; Zera and Harshman, 2001) of
venomous snakes.
The "defensive hypothesis" suggests that venom
functions to release snakes from predation
pressures (Bogert, '43; Ruben, '76; Saint-Girons,

> 2007 WILEYLISS. INC.

'97), but no studies have formally examined


whether venomous and nonvenomous species are
subjected to differential predation pressures.
Moreover, this hypothesis does not address how
snake predators may be able to "learn" to identify
venomous from nonvenomous snake species, a
lesson that is likely to be lethal to potential
predators. The "predatory hypothesis" suggests
that the primary function of snake venoms is to
kill or otherwise incapacitate prey items that
could somehow injure the snake (Kardong, '75;

Grant sponsor: NSFGRF and Walton Distinguished Doctoral


Fellowship.
Correspondence to: Man.hall D. McCue, Department of Biological
Sciences. 601 Science Engineering. Univel1lily of Arkansas.
Fayetteville. AR 72701. E-mail: mmccue@uark.edu
Received 10 April 2007; Revi8ed 16 May 2007; Accepted 2 July 200;
Published online I AUg'U5t 2007 in Wiley InterScience (~.
interacience.wiley.oom). 001: IO.IOO2fj@zAll

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InrerScience'

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PREY ENVENOMATION AND DIGESTIVE PERFORMANCE

Kardong, '86; Hirabayashi et al., '91; Daltry et al.,


'96; Andrade and Abe, '99). Although the temporal
connection between prey envenomation and
3ubsequent ingestion is clear to anyone who
watches a captive venomous snake at "feeding
time," this hypothesis does not address the fact
that constriction, which is the ancestral mode of
prey immobilization (Greene and Brughardt, '78;
Kardong, '80; Savitzsky, '80; Greene, '83), is still
employed by a variety of extant species (Gans, '61;
Franz, '77; Shine and Schwaner, '85; Rochelle and
Kardong, '93; Moon and Mehta, 2007). Moreover,
no studies have examined the fitness of venomous
snakes that have been deprived of their ability to
subdue their prey using envenomation. The
"digestive hypothesis" suggests that the proteolytic activities of snake venoms function to increase
digestive performance among venomous snakes
(Gans, '61; Pough and Groves, '83; Andrade and
Abe, '99; Kini and Chan, '99; Sass, '99), but
remains unable to explain why the venoms of
different species vary so widely with regard to
their proteolytic activity (Zeller, '48; Deutsch and
Diniz, '55; Oshima and Iwanaga, '69; Passey, '69;
Mebs, '70; Kocholaty et al., '71; Geiger and
Kortmann, '77). Given the dearth of studies that
have attempted to examine the potential function
of snake venoms, this study was designed to
investigate the digestive hypothesis in a snake
species (i.e., Crotalus atrox), whose venom is
recognized for its high proteolytic activity.
Early morphological and histological observations revealed that the venom glands of snakes
were structurally homologous to mammalian
parotid glands (Kellaway, '37). This discovery,
combined with observations that many snake
venoms are rich in proteolytic activity (see Zeller,
'48), most likely led to the first speculations that
snake venom served a functional role in prey
digestion. Interestingly, the only contemporary
observations that support the "digestion hypothesis" were not examined systematically, but
rather were based on informal observations or
were communicated anecdotally. For example,
Reichert ('36) stated that pitvipers consuming live
prey items required only 4-5 days to digest meals
compared with the 12-14 days they required to
process prekilled meals (cited in Thomas and
Pough, '79). A second observation was provided
by C. Stimmler-Morath who apparently noticed
that the duration of digestion increased from 3
days after envenomating a meal to 5-8 days when
vipers were force-fed prekilled meals (unpublished
observation cited in Zeller, '48). A limited number

569

of recent studies has examined the digestion


hypothesis <Thomas and Pough, '79; RodriguezRobles and Thomas, '92; McCue, 2002) but
employed snakes belonging to the family Colubridae, which are either nonvenomous or produce
comparatively small amounts of toxic secretions
that lack the proteolytic activities characteristic of
true-vipers and pitvipers (Weinstein and Kardong.
'94; Mackessy, 2002; Vidal, 2002; Fry and \Vuster:
2004).
The only modern study to employ venomous
snakes to examine the effect of prey envenomation
on digestive performance consists of an abstract
published by Mendes and Abe (99). The researchers
examined the metabolic costs of digestion, [Le.,
specific dynamic action (SDA)j in a South American
rattlesnake ingesting mice that were either artificially envenomated or freshly killed via cervical
dislocation. Although they concluded that envenomation had little, if any, effect on SDA, they did not
examine the possibility that prey envenomation
might influence the gut passage rate or assimilation
efficiency in snakes. Given the working hypotheses
that envenomation increases digestive performance
in C. atrox (e.g., by increasing the gut passage rate,
reducing costs of digestion, or increasing assimilation efficiency), the goal of this study was to Quantify
the influence of prey envenomation on several
digestive performance traits. The two experiments
described in this study measured physiological
performance variables that have clear connections
to the life histories of venomous snakes.
The first experiment measures metabolic
expenditure during digestion and gut passage time
in C. atrox subjected to four feeding treatment
levels. An understanding of the degree to which
prey envenomation influences the costs associated
with digestion has significant ecological importance because the costs of meal processing can
account for approximately one-third of the annual
energy expenditure of some pitvipers (McCue and
Lillywhite, 2002). The fitness consequences of the
passage rate are also ecologically important
because increased gut passage rates would allow
snakes to process an increased number of prey
items during a limited feeding season.
The second experiment investigates the effects of
assimilation efficiency in two groups of snakes
consuming prekilled mice injected with either
venom or saline. Although the apparent assimilation efficiency (ASSIM) of snakes is comparatively
high ranging from 80 to 95% (Smith, '76;
Greenwald and Kanter, '79; Reichenbach and
Dalrymple, '86; Bedford and Christian, 2000;
J. Exp. Zool. DOl 1O.1002fjez

570

M.D.MCCUE

Canjani et aI., 2003). any improvement in assimilation efficiency should translate to increased
mass and energy gains from a given meal. The
ultimate effects of increased passage rate,
increased assimilation efficiency, and reduced
costs of meal processing could provide important
insight into the adaptive role that venom plays
among snakes.

METHODS
Metabolic and passage experiments
Eight subadult, western diamondback rattle
snakes (C. atrox) were employed in the SDA and
gut passage experiments. Before experimentation,
the snakes were housed individually and allowed
to acclimate to laboratory conditions of 27-30"C
and 12L: 120 photoperiod for a minimum of 3
months and 8 maximum of 6 months. During the
acclimation period, snakes were fed prekilled
young adult mice every 10-14 days and provided
water ad libitum.
A randomized block design with four treatment
levels was used so that each of the eight snakes
could serve as its own control. The four treatment
levels li.e., live venom, (LV), dead venom (DV), live
no-venom (LNV), and dead no-venom (DNV
involved feeding snakes similar-sized mice derived
from the same feeder colony. These experimental
mouse meals were offered. to snakes at 14-day
intervals ensuring that snakes were fully postabsorptive at the start of each feeding trial
(Stevenson et al., '85; Overgaard et al., 2002;
Holmberg et aI., 2003; Zaidan and Beaupre, 2003;
Dorcas et al., 2004).
In the LV treatment level, a 26-g needle was
used to inject 20 mg of lyophilized C. atrox venom
(Kentucky Reptile Zoo) reconstituted by dissolving
it in 0.2 mL of 0.9% saline warmed to 37C into the
tail vein of a live adult mouse (Bolyn, '40; Russell
and Eventov, '64; Tu et aI., '69; Ownby and
Colbeg, '88). Lyophilized venom, obtained during
the year before beginning these experiments, was
used because it could be conveniently reconstituted when needed and because it has been shown
to retain its pharmacological properties for over 50
years (Russell and Eventov, '64). The amount
of venom used in these experiments was similar to
that expended during normal predatory strikes
in rattlesnakes (Hayes, '92), but less than the total
venom stores found in similar-sized rattlesnakes
(Minton, '57; Jimenez-Porras, '61; McCue, 2oo6a).
Approximately 2 min after the venom injection,
each mouse was also labeled with a fluorescent
J. Exp. Zool. DOl 1O.1002Jjez

tracer (Scientific Marking Materials Inc., Seattle,


WA), which allowed to track the gut passage rates
of each meal. To accomplish this, a 1.0 mL saline
suspension containing 50 mg of the indigestible,
fluorescent tracer in one of four colors, specific to
each treatment group, was injected. intraperif.o..
nealy (lP) using a 16-g needle into each mouse.
The labeled mice were then placed near each
snake in a manner such that the snakes did not
strike at the meals, but were able to locate and
consume them. In most cases snakes consumed
the experimental meal within ca. 30 min.
The LNV treatment level was similar to the LV
treatment except that no venom was added to the
0.2 mL intravenous (IV) saline injections. The
mice were then euthanized via cervical dislocation,
and injected IP with a unique color of the
fluorescent tracer suspension described above.
Approximately 20-30 min before ingestion, snakes
in the LNV treatment level were anesthetized
using isofturane (IsoFlo, Abbot Laboratories,
North Chicago, Il). A previous study demonstrated.
that metabolic rates are not altered significantly in
rattlesnakes that have recently recovered from
IsoFlo-induced anesthesia (McCue, 2006a). The
anesthetized snakes were then placed into clear
acrylic tubes appropriate for their size, and 18inch forceps were used to gently force feed the
experimental meals to snakes, thus ensuring that
venom was not inadvertently introduced into the
meals during the normal ingestion process.
The DV treatment level utilized mice that were
previously euthanized via cervical dislocation.
These mice were warmed to ca. 37C and IV
injected with 0.2 mL of the reconstituted venom
solution and 1.0 mLLLof the fluorescent tracer IP.
The DV mice were then placed near snakes for
them to consume. The DNV treatment level
consisted of a frozen mouse that was warmed as
described above, and injected IV with saline
solution and IP with the tracer suspension. Like
the LNV treatment, the DNV mice were gently
force fed to anesthetized snakes.
Upon ingesting the experimental meals, snakes
were placed individually into ca. 2-L metabolic
chambers where their rates of oxygen consumption were recorded hourly for 120 hr using a
multiplexing flow-through respirometry system
contained within an environmental chamber set
to 30~C. All metabolic trials began and ended at
1200 2 h to minimize any effects of diel variation
in metabolic rate on the SDA measurements
(Beck, '95; Beaupre and Duvall, '98; Hopkins
et al., '99; Beaupre and Zaidan, 2001). Carbon

PREY ENVENOMATION AND DIGESTIVE PERFORMANCE

dioxide-free atmospheric gas was passed through


metabolic chambers at constant flow rates that
were monitored daily using a mass flow meter.
The oxygen concentrations of excurrent gas from
each chamber were measured using a Sable
Systems FC-l (Las Vegas, NY) oxygen analyzer
connected to a computer-controlled multiplexer
that serially subsampled the excurrent gas from
eight chambers each hour. During each trial, at
least one respirometry chamber was left empty to
monitor the baseline incurrent oxygen concentration. Flow rates through respirometry chambers
averaged approximately 150 mLlmin, and oxygen
concentrations in the chambers never fell below
20%. At the end of each trial, rates of oxygen
consumption were calculated at hourly intervals
using the following equation modified from Withers (1977),

[0, - O,IE
Ooonsumption

1 - rOd

where Ocon~umption is the aerobic metabolic rate


(0 2 mL!hr), E is the mass flow of gas stream
passing through respirometry chambers, and 0 is
the fractional concentration of oxygen in incurrent
(i) and excurrent (e) gas streams.
Body masses and baseline resting metabolic
rates (RMRs) were determined on postabsorptive
snakes over a 48-hr period to get starting values,
and SDA was calculated using each snake's
respective RMR. For example, the metabolic scope
of SDA (Le., SCOPE) was calculated as the highest
measured metabolic rate for each postprandial
snake in each treatment level divided by its mean
RMR (Machida, '81; Andrade et al., '97; Overgaard
et a1., '99; Secor and Diamond, 2000; McCue,
200Gb). The time for peak SDA (Le., PTIME) was
determined as the length of time required for each
snake to reach its highest postprandial metabolic
rate. The duration of SDA (Le., DURAT) was
calculated as the time following a meal at which
the postprandial metabolic rate of an individual
returned to within the two standard deviations
(Le., ca. 95% confidence interval) of its mean RMR
(Dorcas et aI., 2004; McCue et al., 2005). The
energetic cost of SDA (Le., SDA-KJ) was quantified as the summation of differences between
measured postprandial metabolic rates and mean
postabsorptive metabolic rates each hour for
120 hr according to the following equation,
120

~ (SDA" - RMR) E.

571

where SDA is defined as the postprandial metabolic rate at hour n, RMR is the mean postabsorptive metabolic rate, and E is an energy conversion
factor (20.13kJIL0 2 ; Jobling, '81). It should be
noted that the initialism SDA is used throughout
this paper to refer generally to the phenomenon of
SDA, whereas the term SDA-KJ refers specifically
to the energetic costs associated with SDA. The
coefficient of SDA (Le., COEFF) was calculated by
dividing the SDA-KJ by the energetic content of
each mouse meal assuming 7.02 kJ/g wet mass
(McCue et al., 2005), and multiplying the resultant
by 100 to convert it to percentage (Guinea and
Fernandez, '97; Secor and Diamond, 2000; Roe
et a1., 2004; McCue, 200Gb).
Metabolic chambers were examined twice daily
under black light to determine the gut passage
time (i.e., PASS). If a snake defecated in its
metabolic chamber during respirometric measurements, the chamber was cleaned and the snake
was replaced into the chamber for the remainder
of the measurement period. After 120 hr, the
snakes were returned to their respective cages
that were then checked under a black light every
24 hr over the subsequent 4 days. Response
variables (i.e., SDAKJ, COEFF, SCOPE, PTIME,
DURAT, and PASS) were compared among the
four treatment levels using repeated measures
analysis of variance (ANOVA) ; P-values ::;0.05
were considered significant. All statistical tests
were conducted using [StatView<E (SAS), Cary,
NC]. Repeated measures responses are presented
in the text as mean standard error and the
results pooled among treatments are presented
as mean standard deviation.

Assimilation experiment
Eight subadult wild-captured C. atrox were
employed in assimilation experiments. Like the
SDA and passage experiment, snakes were housed
individually and acclimated to the laboratory
conditions described above for a minimum of
3 months. After 14 days of fasting, the snakes
were considered postabsorptive. Individual snakes
were then assigned randomly to one of the two
feeding treatment groups (i.e., envenomated and
nonenvenomated) and were allowed to consume
one thawed feeder mouse every week over a 42-day
period. Snakes in the envenomated treatment
group ingested adult mice that had been killed
via CO2 asphyxiation and IV and IP injected with
0.5 mL of reconstituted C. atrox venom (I mg dry
venom perl mL 0.9% saline). Snakes in the noneJ. Exp. Zool. DOl 1O.IO02/jez

572

M. D. MCCUE

nvenomated treatment group ingested prekilled


mice that were injected with 0.5 mL of physiological saline. All the mice were presented to the
snakes in a manner such that they were unable to
strike the prey before locating and ingesting the
meals.
Egesta were periodically removed from each
cage during the 6-week trial and for an additional
14 days after each snake's final experimental
meal to ensure their guts were cleared. All
voided material was dried at BO"C in an oven
for approximately 72 hr (Golley, '61; Paine, '71).
Egested material from each snake was physically
pooled and ground to a fine powder using a mortar
and pestle. Six to twelve subsamples (ca. 60 mg) of
the homogenized egesta from each snake were
pelleted and combusted in a microbomb calorimeter (Gentry Instruments, Aiken, SC) calibrated
with benzoic acid pellets of known mass.
Ash content of voided material was determined
by weighing the uncombusted residue from each
calorimetry sample. ASSIM was calculated by
dividing the ingested energy by the energy content
of each diet assuming 7.02 kJ/g wet mass. ASSIM
and ash content of egesta (i.e., ASH) were
compared between the two treatment levels using
an unpaired t-test as well as an analysis of
covariance using "energy ingested" as the covariate to minimize the risk of spurious autocorrelation associated with measurements of ASSIM
efficiency (Packard and Boardman, '88; Raubenheimer, '95; Packard and Boardman, '99);
P-values ::;;0.05 were considered significant.
RESULTS
The C. atrox used in the SDA and gut passage
rate experiments had mean masses of 20047 g
and RMRs of 17.47.2mL Oz/h. Meal masses
averaged 20.3 0.3 g and did not differ significantly among the four treatment levels
(P ~ 0.557). The SDAKJ and the COEFF averaged 35.8 kJ and 26%, respectively, and did not
differ among treatment levels (Table 1). The
SCOPE and the PTIME averaged 3.9 and
21.9hr, respectively, and did not differ among
treatment levels (Fig. 1). The duration of the SDA
response was not statistically different among the
four treatments and averaged 88 hr (Table 1). The
PASS was not compared statistically among all
snakes at all treatment levels because two snakes
failed to defecate before the end of the 9day
observation period. One snake retained feces in
excess of 9 days following the LV, LNV, and DV
J. Exp. Zool. 001 1O.1002/jez

TABLE 1. Mean and standard errors of measurements made


in the SDA and gut passage experiments

LV
Meal (g)
SDA-KJ Ow)
COEFF (%)
SCOPE
PTIME (hr)
DURAT (hr)

19.7
35.5
26
3.9
22.6
77.8

(0.5)
(3.5)
(3)
(0.2)
(0.7)
(6.3)

LNY
20.7
35.1
24
3.9
22.1
81.5

<0.5)
(2.8)
(2)
(D.3}
(0.9)
(4.6)

DV
20.3
35.3
25
3.8
19.5
92.9

DNV

(0.5)
(3.1)
(2)
(0.3)
(0.7)
(7.5)

20.3
37.3
30
3.9
23.5
98.1

(0.6)
(5.0)
(4)
(0.3)
(2.5)
(6.6)

Repeated-measures analysis of variances revealed no significant


treatment effects.
SOA, specific dynamic action: LV, live venom: LNV. live no-venom;
OV, dead venom: ONV, dead no-venom; SOA-KJ, energetic cost of
SOA; COEFF, coefficient of SOA: SCOPE, metabolic scope of SOA;
PTIME, time for peak SOA; OURAT, duration ofSOA.

70

60

-L-V
oL-NV

'0

aO-V
~O-NV

40
30

20
'0
0

...

80

70

0>

24

48

72

96

120

-L-V
oL-NV
aO-V

60

~D-NV

'0
40
30
20
10
24

46

72

96

120

Time (h)
Fig. 1. Postprandial metabolic responses measured in two
rattlesnakes ingesting four experimental mouse meals. The
horizontal line represents mean resting metabolic rate for
each snake and the gray region represents the 95% confidence
interval of postabsorptive metabolic rates.LV, live venom;
LNV, live no-venom; DV, dead venom; DNV, dead no-venom.

treatments, and another snake retained feces for


;;:: 9 days following the DV and the DNV treatments. When those trials were excluded from

573

PREY ENVENOMATION AND DIGESTIVE PERFORMANCE

analyses, the average passage time was 6 days


n = 27); analysis of variance revealed no significant difference in PASS among the four treatment
levels (P = 0.834).
The masses of the two C. atrox assimilation
groups did not differ significantly (P = 0.405) and
averaged 23317g (n = 8). Moreover, the total
energy ingested by each group did not differ
:5ignificantly (P = 0.234) and averaged 1098 kJ
Table 2). According to an unpaired t-test, neither
ASSIM nor ash content of egesta differed signifi
cantly
between
envenomation
treatments
,P = 0.814 and P = 0.646, respectively) averaging
79.14.8% and 16.82.5%, respectively. The
results of the analysis of covariance also revealed
that the ASSIM of the two envenomation treatments did not differ significantly (Ps/ope = 0.913,
Pintercept = 0.617).
I

DISCUSSION
The western diamondback rattlesnake (C. atrox)
was selected as a model organism in which to
investigate the influence of prey envenomation on
digestive performance because its venom is among
the best pharmaoologically characterized (Minton
and Weinstein, '86; Baramova et al., '91; Hirabayashi
et al., '91; Hung and Chiou, '94; Fox and Bjarnason,
'95) and possesses some of the greatest enzymatic
activities found among snake venoms (Oshima and
Iwanaga, '69; Passey, '69; Mebs, '70; Kocholaty et al.,
'71; Russell, '72; Geiger and Kortmann, '77). Given
the well-known proteolytic and necrotizing properties of rattlesnake venoms <Michaelis and Russell,
'63; Homma and Tu, '71; Pereira et al., '71; Huang
and Perez, '82; Nakada et aI., '84; Ownby and
eoH>eg, '88; Rodriguez-Acosta et aI., '99; Salvini
et al., 2001), the finding that envenomation did not
influence any of the measured digestive performance
variables was surprising, although not unprecedented (see Mendes and Abe, 1999).
Several factors might help explain the results of
the experiment examining the effect of envenomation on the cost of digestion and gut passage rates.
First, it is possible that the digestion temperature
of 30"C was too great to detect any significant
influence of envenomation on digestive performance. In their study examining qualitative rates
of digestion in artificially envenomated prey items
fed to nonvenomous snakes, Thomas and Pough
('79) found that the digestive advantages conceded
by prey envenomation were more dramatic at 15C
compared with 25"C. They subsequently specu
lated that prey envenomation might allow

TABLE 2. Mean ami sJandard deviation of responses mea


sured in snakes digesting envenomated arni nonenvelWmated
p"J'

Envenomated
Snake (g)
Ingest (kJ)

228 (20)
1048 (98)

ASSIM ('.II)
ASH ('.II)

80 (4)

15 (3)

Nonenvenomated
239 (14)

1148 11151
i9,51
1 i (3)

Envenomation had no significant effect on meal assimilation


efficiency.
ASSIM, apparent assimilation efficiency; ASH. alIh content or egesta.

pitvipers to digest meals at cooler temperatures,


and thus inhabit more extreme elevations and
latitudes compared with most other snake taxa;
however, this hypothesis has yet to be examined
formally. Second, it is possible that increased.
digestive performance was not detected because
the meal sizes used in these experiments were too
small. Although the snakes in this study were
allowed to consume adult mice, pitvipers are
known to be able to ingest prey items in excess
of 50% of their own body mass (Beavers, '76;
Greene, '83; Pough and Groves, '83; Forsman and
Lindell, '93; Andrade et al., '97). It has been
suggested that venom may only confer digestive
advantages when exceptionally large meals are
consumed and the low ratio of surface area to
volume necessitates additional digestive surfaces
(Pough and Groves, 'S3), but again, this possibility
remains unexamined.
A third possibility is that the enzymatic and
proteolytic activities of C. atrox venom did function to break down prey items more rapidly,
congruent with the previous observations
of Thomas and Pough ('79). Although a trend
of reduced SOA duration was observed in
snakes consuming envenomated prey, this trend
remained statistically insignificant. Interestingly,
there was no apparent energetic cost reduction
associated with prey envenomation. A recent
study by McCue et aI. (2005) revealed that the
SDAKJ in pythons resulting from the digestion of
a whole mouse meal was not significantly reduced
when an equalsized meal was pureed and force
fed to snakes; in fact, the SOA-KJ was slightly
increased in the pythons digesting and assimilating the pureed meals. The same study concluded
that the majority of metabolic expenditure
associated with SOA resulted from the energetic
costs of protein synthesis; if this was also the case
with the rattlesnakes, the influence that prey
J. Exp. Zool.

Dor

1O.1002/jez

574

M. D. MCCUE

envenomation might have on net metabolic cost venoms facilitate digestion, by increasing metaof digestion would, therefore, be minimal.
bolic, assimilatory, and passage rates in a single
Even if SDA and assimilation efficiency were not pitviper species. Given this outcome, it may be
influenced by envenomation, it would still be prudent to further examine the generality of these
reasonable to expect to see an increase in gut findings by investigating the influence that prey
passage rate in snakes consuming envenomated envenomation may have on the digestive performeals; such a result was also not observed. mance of other venomous snakes that are disAlthough the fluorescent tracer was used to track tantly related to rattlesnakes (e.g., true-vipers and
the ingested food bolus, previous studies have members of the family Elapidae). A promising
reported that egestion events are not always species to conduct similar studies on is the king
predictably correlated with ingestion events. For cobra (Ophiophagus hannah), the venom of which
example, some snakes are noted for their tendency possesses the greatest enzyme activities found
to retain 8 large bolus of digested materials among elapid snakes (McCue, 2005). If forthin their distal large intestine for periods lasting coming studies confirm that venom concedes
as long as several months (Lillywhite et aI., 2002). limited or no digestive advantages to other snakes,
A previous study investigating the SDA in post- it could lead to an important paradigm shift
prandial pythons also reported that egestion regarding the adaptive significance of snake
events occurred irregularly despite a regular venoms. Such a shift would thus underscore the
feeding regime (Overgaard et a1., 2002). Although need for controlled studies that characterize
the fluorescent tracer proved to be an effective tool the defensive and predatory functions of snake
for identifying which egested bolus was associated venoms.
with which particular meal, it was less suited to
ACKNOWLEDGMENTS
interpret results of irregular egestion events. One
solution to this problem might be to label food
Experiments were conducted in accordance with
with a radioopaque tracer and conduct periodic
X-ray measurements on postprandial snakes to the University of Arkansas Institutional Animal
determine when undigested matter first enters the Care and Use Committee protocol 05011. Thanks
distal large intestine (Stevenson et al., '85; Dorcas also to J. Agugliaro, Dr. K.E. Cano-McCue, and
two anonymous reviewers for helpful comments
et a\., '971.
The inability to detect increased assimilation on this manuscript, as well as Prof. S. Beaupre for
efficiency in envenomated prey could be related to providing the laboratory space required for this
the fact that venom was administered to prekilled study.Funding was provided by a NSF-Graduate
mice, and was therefore unable to circulate, if only Research Fellowship and a Walton Distinguished
for a few seconds, throughout the bloodstream Doctoral Fellowship awarded to MDM.
of the prey items. Although necrosis is often
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