Regulation of Gut Function Varies with Life‐History Traits in Chuckwallas (Sauromalus obesus:...

Regulation of Gut Function Varies with Life‐History Traits in Chuckwallas ( Sauromalusobesus : Iguanidae)Author(s): Christopher R. Tracy and Jared DiamondSource: Physiological and Biochemical Zoology, Vol. 78, No. 4 (July/August 2005), pp. 469-481Published by: The University of Chicago PressStable URL: http://www.jstor.org/stable/10.1086/430232 .

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469

Regulation of Gut Function Varies with Life-History Traits in

Chuckwallas (Sauromalus obesus: Iguanidae)

Christopher R. Tracy1

Jared Diamond2

1Department of Zoology, University of Wisconsin, Madison,Wisconsin 53706-1708; 2Department of Physiology, School ofMedicine, University of California, Los Angeles, California90095-1751

Accepted 2/8/2005; Electronically Published 5/24/2005

ABSTRACT

We examined the effects of hibernation and fasting on intestinalglucose and proline uptake rates of chuckwallas (Sauromalusobesus) and on the size of organs directly or indirectly relatedto digestion. These lizards show geographic variation in bodysize and growth rate that parallels an elevational gradient inour study area. At low elevation, food is available only for ashort time during the spring; at high elevation, food may alsobe available during summer and autumn, depending on rainfallconditions in a given year. We hypothesized that low-elevationlizards with a short season of food availability would show morepronounced regulation of gut size and function than high-elevation lizards with prolonged or bimodal food availability.Hibernating lizards from both elevations had significantly loweruptake rates per milligram intestine for both nutrients, andlower small intestine mass, than active lizards. The combinationof these two effects resulted in significantly lower total nutrientuptake in hibernating animals compared to active ones. Thestomach, large intestine, and cecum showed lower masses inhibernators, but these results were not statistically significant.The heart, kidney, and liver showed no difference in mass be-tween hibernating and nonhibernating animals. Lizards fromlow elevations with a short growing season also showed a greaterincrease in both uptake rates and small intestine mass from thehibernating to the active state, compared to those from highelevations with longer growing seasons. Thus, compared tothose from long growing season areas, lizards from short grow-ing season areas have equal uptake capacity during hibernationbut much higher uptake capacity while active and feeding. Thispattern of regulation of gut function may or may not be anadaptive response, but it is consistent with variation in life-

Physiological and Biochemical Zoology 78(4):469–481. 2005. � 2005 by TheUniversity of Chicago. All rights reserved. 1522-2152/2005/7804-4123$15.00

history characteristics among populations. In areas with a shortseason, those lizards that can extract nutrients quickly and thenreduce the gut will be favored; in areas where food may beavailable later in the year, those lizards that maintain an activegut would be favored. While other researchers have found muchgreater magnitudes of gut regulation when making comparisonsamong species, we find the different patterns of change in gutfunction between different populations of chuckwallas partic-ularly intriguing because they occur within a single species.

Introduction

The regulation of intestinal size and function is a well-knownresponse to variation in its use (Karasov and Diamond 1983a;Toloza et al. 1991; Secor and Diamond 1998, 2000; Starck 1999).Many animals increase intestinal size and/or function duringperiods of feeding and reduce them when not feeding. Hiber-nating mammals show a change of intestinal transporter activityduring hibernation (Carey and Sills 1992, 1996; Carey and Mar-tin 1996), birds show a reduced mass of intestines and otherorgans during migration (Piersma and Lindstrom 1997;Piersma and Gill 1998), and snakes show both reduced intestinemass and transporter activity when not digesting (Secor andDiamond 1995, 2000). Changes in the transport activity of theintestine appear to be a response to the presence of nutrientsin the intestinal lumen (Kotler et al. 1980, 1981; Diamond andKarasov 1984; Carey and Cooke 1991; Secor et al. 2002). Directinfusions of glucose into the intestinal lumen of rats showedthat transporter activity only increased at the location of theinfusion and immediately downstream (Kotler et al. 1980,1981), suggesting that increased transporter activity is the resultof an increase in use of the intestine. In snakes, infusions ofproteins and, to a lesser extent, amino acids resulted in elevatedtransport rates (Secor et al. 2002).

Changes in size and function of the intestine may be favoredby natural selection under some circumstances to reduce met-abolic costs of maintaining an unused organ. Although lizardsand snakes do not appear to have the same costly turnover ofintestinal cells that birds and mammals do (Starck 1996; Starckand Beese 2001, 2002; Overgaard et al. 2002), maintenance ofa metabolically active organ like the intestine, which accountsfor up to 20%–30% of basal metabolism (Cant et al. 1996),when it is not in use may divert energy that could otherwise



470 C. R. Tracy and J. Diamond

be used for growth, storage, or reproduction (Secor and Dia-mond 1998).

Species with different patterns in the timing of feeding showdifferences in their pattern of intestinal regulation (Secor andDiamond 1995, 1998, 2000; Secor 2001). In particular, speciesthat undergo extended periods without feeding (e.g., ambush-hunting snakes such as Burmese pythons that can go withoutfood for many months) show much greater upregulation ofintestinal size and function than do species that feed morefrequently (e.g., actively foraging snakes or most endothermicanimals; Secor and Diamond 1998, 2000). However, withinsome species the feeding regime varies geographically becauseof geographic variation in environmental conditions. To date,no studies comparing digestive responses among different pop-ulations within a species have been published, nor have therebeen any single studies that have compared intestinal perfor-mance among digesting, fasting, and hibernating individuals ofone species.

Here, we report on a comparison of digestive performanceand regulation of digestive performance among populations ofchuckwallas (Sauromalus obesus: Iguanidae), an herbivorous liz-ard species that experiences geographic variation in environ-mental conditions that may affect strategies of digestive systemregulation (Tracy 1999). In some areas within the geographicrange of chuckwallas, rainfall (and thus the growing season)occurs only once per year for a short time and may occur inas few as 50% of years; these sites are typically at low elevations.Other areas (typically higher elevations) have longer growingseasons because they receive more rainfall more regularly andmay also experience a second bout of rainfall later in the year,creating a short second growing season.

This geographic variation in food availability allows thechuckwalla to be an ideal species with which to study popu-lation differences in the regulation of digestive performance.All chuckwallas experience highly seasonal variations in foodavailability with long periods when food is absent. Therefore,we predicted that all chuckwallas would show a pattern ofenergy conservation by reducing organ size and gut functionduring hibernation, when food was unavailable. Under con-ditions experienced at low elevations, however, a strategy thatincludes a very reduced gut during extended fasts and a verylarge, active gut when food is available would be the mostenergetically efficient over the years. Therefore, we predictedthat chuckwallas from low elevations would show a greaterfactorial increase in organ size and gut function than thosefrom populations that experience longer growing seasons andoften see a second period of food availability. We use measuresof gut size and function of chuckwallas from different popu-lations to show that chuckwallas regulate intestinal size andfunction depending on whether they are active, feeding, orhibernating, and that chuckwallas from areas experiencing dif-ferent environmental conditions show different patterns of in-testinal regulation.

Material and Methods

Study Species

Chuckwallas (Sauromalus obesus) are relatively large lizards inthe family Iguanidae and are found throughout the Mojave andSonoran deserts of North America. They are strictly herbivo-rous and live almost exclusively on isolated rock outcrops(Johnson 1965; Abts 1987; but see Feldner and Feldner 1991),which allows for genetic isolation of populations (Lamb et al.1992) and local adaptation (Tracy 1999, 2004). Chuckwallasare usually active from March to October, although there isregional and seasonal variability in their activity season (e.g.,Nagy 1973; Berry 1974; C. R. Tracy, personal observation).

The desert habitats inhabited by chuckwallas vary consid-erably in environmental conditions. The region shows patternsof environmental variation at three different scales. At the finestscale, rainfall events can be highly localized, particularly duringsummer monsoonal rainfalls. A single storm event may doublethe average annual amount of rainfall on a particular outcrop,while leaving an outcrop less than a kilometer away completelyuntouched. At a broader scale, parts of the region experienceprimarily winter rainfall and subsequent spring blooms of an-nuals, while some areas receive primarily summer monsoonalrainfall and subsequent autumn blooms. For instance, winterrainfall generally occurs in the northern and western parts ofthe Mojave Desert; southern Baja California, at the southernedge of the geographic range of chuckwallas, receives only sum-mer rainfall and subsequent autumn blooms; and parts of theSonoran Desert receive both winter rainfall and summer mon-soonal rains, creating two growing seasons. Finally, across theentire desert region, there is an environmental gradient thatfollows elevation. Low elevations tend to be more extreme, withhigher average temperatures, lower average rainfall, and morefrequent years in which there is too little rainfall for annualplants to bloom. The combination of these three patterns resultsin highly localized climates and much geographic variability inenvironmental conditions.

Highly localized environmental conditions, combined withthe relative isolation of chuckwalla populations, have led tosignificant geographic variation in chuckwalla phenotype. Inparticular, chuckwallas vary in color pattern (usually to matchsubstrate) and in body size and composition (Case 1976; Tracy1999, 2004). At low elevations, lizards generally experience ashort, but unpredictably wet, growing season and subsequentlong dormancy period, part of which is usually extremely hot.Furthermore, there is a high probability that the next year willhave too little rainfall to produce significant production of food.The chuckwallas in these low-elevation sites tend to be smalland to have large fat stores (Case 1976; Tracy 1999). At higherelevations, the environmental conditions are cooler and wetter,with fewer years in which rainfall is too scant to produce abloom of annuals. Chuckwallas at higher elevations tend to belarger and leaner. Furthermore, when the annual plants senesce



Digestive Regulation in Chuckwallas 471

at low elevations, there is usually no more food available to aforaging chuckwalla. In contrast, small patches of green plantsare often present the entire year at higher elevations (C. R.Tracy, personal observation).

Experimental Animals

Adult chuckwallas were collected from four sites encompassingtwo elevations. Two sites at each elevation were chosen becauseof concern that any significant differences found between onlyone site per elevation might simply be the result of falselyinflated P values, as cautioned by Garland and Adolph (1994).In the spring of 1998, lizards were collected from the VirginMountains (high elevation [1,100 m], ,n p 14 mass p

g) and the Newberry Mountains (low elevation235.4 � 15.1[350 m], , g) in Nevada, repre-n p 12 mass p 192.1 � 15.8senting high and low elevations, respectively. In the spring of1999, lizards were collected from Colorock Quarry, Nevada(high elevation [890 m], , g), andn p 5 mass p 183.7 � 35.8Amboy, California (low elevation [210 m], ,n p 6 mass p

g). After collection, all animals were maintained in164.0 � 8.3the laboratory to acclimate them to similar recent physiologicalconditions.

In the laboratory, we separated lizards from the Virgin andNewberry Mountains into three treatment groups: active andfeeding (hereafter “feeding”), active and fasting (hereafter “fast-ing”), and hibernating and fasting (hereafter “hibernating”).Lizards from the Colorock Quarry and Amboy sites were eachdivided into feeding and hibernating groups. We distributedanimals among treatment groups such that, for each popula-tion, all treatment groups had similar size distributions andmeans. However, because the populations at different elevationsdiffered significantly in body size, we were unable to matchbody sizes between elevations. We corrected for this statisticallyin our analyses by using body mass as a covariate.

The lizards were maintained in cages that included baskingrocks, refugia, and incandescent (150 W) and full-spectrumfluorescent lamps that allowed lizards to reach preferred bodytemperatures of 36�–38�C and provided them with UV expo-sure for vitamin D production. We kept lizards under a14L : 10D photoperiod and provided them with food and waterad lib. During winter months, all lizards were induced intohibernation by moving them to a controlled-temperature roomset at 8�C with a 10L : 14D photoperiod. We fasted lizards for2 wk before hibernation to allow their guts to clear. Duringhibernation, water was available, but the lizards were neverobserved to drink. Lizards in the hibernating treatment groupwere allowed to hibernate for at least 2 mo. They were thenkilled by decapitation, followed by pithing, while still hiber-nating (i.e., they were never awakened), and intestinal uptakerates were measured. Lizards of the other two treatment groups(feeding and fasting) were aroused from hibernation after atleast 3 mo by increasing the photoperiod to 14L : 10D, and

increasing ambient temperature to 30�C. These lizards wereagain provided with food and water and were either maintain-ing or increasing their body mass within 3 wk. Lizards of thefeeding group were fed ad lib. until the day they were killedfor intestinal uptake rate measurements. Lizards of the fastinggroup were fasted until they stopped producing fecal pellets(6–12 d) and were then killed for intestinal uptake rate mea-surements. Chuckwallas in the wild could experience fasts ofmuch longer than this; however, it is unlikely that they wouldfast for long durations without undergoing some sort of dor-mancy (estivation, brumation; C. R. Tracy, personal observa-tion). Additionally, chuckwalla metabolic rate returns to pre-feeding levels within 3 d of being fed a single meal (C. R. Tracyand J. Diamond, unpublished data), so we expected that evenrelatively short fasts of 6–12 d would elicit a full digestive organresponse. During the fast, water was offered ad lib.

Because we were concerned about potential day-to-day var-iation in the measurement of nutrient uptake (Levey and Kara-sov 1992), we measured nutrient uptake of individuals fromtwo or three treatment groups on any given day wheneverpossible. Except for those in the feeding groups from Amboyand Colorock Quarry, all of the lizards were kept under lab-oratory conditions for 6–12 mo, long enough to undergo a fullcycle of hibernation followed by arousal. The feeding lizardsfrom Amboy and Colorock Quarry were housed in the labo-ratory for at least 1 mo to allow their digestive system to ac-climate to the lab diet and to bring them to feeding and activitylevels that were comparable to the rest of the active group.

Measurement of Intestinal Nutrient Uptake

We measured intestinal brush-border uptake rates of d-glucoseand l-proline using the everted sleeve technique, as describedin detail by Karasov and Diamond (1983b). Briefly summarized,lizards were killed and their small intestine removed and flushedof contents with ice-cold reptile Ringer solution. We measuredthe intestine’s wet mass and length, everted it so that its mucosalsurface faced outward, and divided it into equal-length prox-imal, middle, and distal segments. Each of these was sectionedinto 1-cm sleeves which were mounted on grooved glass rods.We first preincubated sleeves in reptile Ringer’s solution for 5min at 37�C, the preferred body temperature of chuckwallas,and then incubated the sleeves for 2 min at 37�C in a single-nutrient solution containing the radiolabeled nutrient and anadherent fluid marker labeled with a different radiolabel (seeKarasov and Diamond 1983b for details). We measured uptakerates of l-proline at 1 mM labeled with 3H, and d-glucose at10 mM labeled with 14C.

The transport mechanisms of d-glucose and l-proline havebeen well described (e.g., Stevens et al. 1982) and are repre-sentative of simple sugar and amino acid transport activity,respectively. d-glucose, but not l-glucose, is transported acrossthe intestinal brush-border membrane by a Na�-glucose co-




Figure 1. Light micrographs of sections of the distal portion of the small intestine at each stage in the everted-sleeve technique. A, Excision.B, Excision and eversion. C, Excision, eversion, and preincubation (2 min). D, Excision, eversion, preincubation, and incubation (5 min). E,Excision, eversion, preincubation, incubation, and rinse (2 min). Scale mm. Gross villus structure remained intact throughout allbar p 500stages, so we judged the technique to be an adequate index of intestinal function.

transporter, and l-proline also has a specific transporter. Weused 14C polyethylene glycol to correct estimates of l-prolinefor the amount of labeled nutrient in the fluid adherent to thetissues, and 3H l-glucose to correct estimates of d-glucose. Inaddition, 3H l-glucose corrects for passive diffusion of d-

glucose, providing a measure of carrier-mediated uptake of d-glucose. We quantified uptake rates as nanomoles per minuteper milligram of sleeve wet mass by averaging the values forthe three segments (proximal, middle, distal). We expressedtransporter activity rates in the small intestine in two ways, on




Figure 2. Mass-specific small intestinal uptake rates of d-glucose (A)and l-proline (B) for fed, fasted, and hibernating chuckwallas fromlow (open bars) and high (filled bars) elevations. Bars represent leastsquares means, and error bars represent 1 SE. Numbers above barsindicate statistically distinguishable groups using post hoc pairwisecomparisons. All variables were log transformed before the analysis,and least squares means were back-transformed (antilog) after theanalysis for ease of interpretation. For both nutrients, there were sta-tistically significant effects of both feeding/activity level and elevation(see also Table 1).

a mass-specific basis (per milligram of small intestine) and ona whole-organ basis by multiplying the mass-specific rates bythe mass of the intestine. Total uptake capacity of the entiresmall intestine was calculated by multiplying the mass-specificuptake rate of each segment by its wet mass and then summingthe products of the three segments.

In some bird species, the everted sleeve method causes severedamage to the mucosal surface of the intestine; thus it doesnot provide an accurate measure of uptake rates (Starck et al.2000; Stein and Williams 2003). Therefore, we checked to seewhether the everted sleeve method damages chuckwalla intes-tines by comparing intestinal samples at five stages of the pro-cedure: after the initial excision of the intestine, after eversion,after the 2-min preincubation, after incubation in the nutrientsolution, and after the final rinse. We set aside one to threesegments per animal, depending on the amount of excess in-testinal tissue after taking sleeves for uptake measurements, andall populations had several segments from each of the threesmall intestine regions at each stage of the eversion process.These segments were then stained with hematoxylin and eosin,embedded in paraffin, and sectioned in 5-mm segments. Weexamined the sections for gross damage to villi using an Axio-cam Zeiss microscope (Zeiss, Gottingen) attached to an Axio-cam Zeiss high-resolution digital camera and a computer withAxiovision image capture software. In examining the images,we found no gross damage to villus structure or to the overallintegrity of the mucosal layer in any of the chuckwalla intestinalsleeves (Fig. 1). The structural integrity of the chuckwalla in-testinal epithelium was maintained throughout the evertedsleeve process; therefore we concluded that the method providesan adequate index of intestinal transporter function for thechuckwalla.

To address any treatment effects on organ mass, we measuredwet mass of the heart, kidneys, liver, spleen, empty large in-testine, empty stomach, and empty cecum. All organs weredried at 60�C to constant mass and reweighed. Because muchof the small intestine was used for intestinal uptake experi-ments, we used a subsample to determine percentage dry massand then multiplied this percentage by the wet mass of thewhole small intestine.

Statistical Analyses

We used a two-factor ANOVA to determine the effects of el-evation and feeding treatment on nutrient uptake rates. Like-wise, we used a two-factor ANCOVA, with body mass as thecovariate (ln transformed), to assess the effect of elevation andfeeding treatment on total intestinal uptake capacity.

We compared organ size among treatments and betweenpopulations using two-factor ANCOVA to account for the var-iation in body size between and within treatment groups. Webegan with fully factorial designs for all analyses, but nonsig-nificant interaction terms that included the covariate (ln body

mass) were removed, and the analyses were rerun without them.All statistics were performed with SuperANOVA 1.11 for Mac-intosh (Abacus Concepts).

Results

Small Intestine Function

Mass-specific d-glucose transport rates were significantly af-fected by feeding/activity level ( , ) and byF p 4.44 P p 0.022, 31

elevation ( , ; Fig. 2). Mass-specific l-F p 4.87 P p 0.031, 31

proline uptake rates also were significantly affected by bothfeeding/activity level ( , ) and elevationF p 11.74 P p 0.00032, 25

( , ). Low-elevation fed lizards had mass-F p 5.44 P p 0.031, 25

specific uptake rates of 141% and 124% of high-elevation liz-ards for d-glucose and l-proline, respectively; while hibernat-ing, low-elevation lizards had mass-specific uptake rates of108% and 99% of high-elevation lizards for d-glucose and l-




Table 1: Results of pairwise comparisons of least squares means of uptake rate per milligram of intestinefor glucose (above diagonal) and proline (below diagonal) for all combinations of elevation and feeding/activity level

Low Elevation High Elevation

Fed (6) Fasted (6) Hibernating (6) Fed (5) Fasted (8) Hibernating (6)

Low elevation:Fed (6) … .333 .006* .035* .030* .002*Fasted (6) .517 … .054� .216 .230 .025*Hibernating (6) !.001* !.001* … .524 .368 .725

High elevation:Fed (5) .197 .062� .011* … .857 .333Fasted (5) .027* .006* .097� .337 … .205Hibernating (3) .002* .001* .986 .033* .170 …

Note. Numbers given are P values from t-tests on least squares means, using body mass as a covariate. Sample size for glucose is given

in parentheses across the top, sample size for proline is given in parentheses at left. See also Figure 1 for values of least squares means.� .0.1 ≥ P ≥ 0.05

* .P ! 0.05

proline, respectively. In general, hibernating lizards possessedlower l-proline uptake rates than active lizards from the samepopulation, although not all comparisons were statistically sig-nificant (Fig. 2; Table 1). d-glucose uptakes were similarlygreater in active lizards compared to hibernating lizards fromlow-elevation sites, but this was not the case for high-elevationpopulations (Fig. 2; Table 1).

Total intestinal uptake capacity of d-glucose was significantlyinfluenced by elevation ( , ; Fig. 3) and byF p 5.91 P p 0.021, 29

feeding/activity level ( , ). We found aF p 16.11 P ! 0.00012, 29

significant interaction between elevation and log body mass( , ), suggesting that glucose uptake capac-F p 6.42 P p 0.021, 29

ities scale with different exponents for lizards from differentelevation. Total intestinal uptake capacity of l-proline likewisewas significantly affected by elevation ( , )F p 6.01 P p 0.021, 24

and feeding/activity level ( , ). For eachF p 20.34 P ! 0.00012, 24

nutrient, and each feeding/fasting level, low-elevation lizardshad higher uptake capacities than high-elevation lizards (Fig.3; Table 2). Uptake capacities were typically higher for fedlizards compared to fasted lizards, which themselves tended topossess higher uptake capacities than hibernating lizards, al-though not all of these comparisons were statistically significant(Fig. 3; Table 2).

Organ Size (Gut Size, Viscera)

Since organ response was similar for wet and dry masses, wedescribe here only the response of organ dry mass (Tables 3,4). Small intestinal mass differed significantly with respect toelevation and feeding level ( , ; ,F p 7.7 P ! 0.01 F p 23.61, 29 2, 29

, respectively). In addition, there were significant in-P ! 0.001teractions between elevation and feeding level ( ,F p 4.12, 29

) and between elevation and body mass ( ,P p 0.03 F p 8.11, 29

). These results follow our predictions that low-P ! 0.01

elevation lizards would have proportionally larger digestive or-gans and that they would show a greater response to feeding/activity level than high-elevation lizards.

The rest of the digestive tract (stomach, cecum, and largeintestine) also showed a response to feeding/activity level, withthe feeding group generally having larger organs than the fastingor hibernating group (Table 3). Further, several parts of thedigestive tract showed a significant effect of elevation, generallywith the low-elevation lizards having proportionally larger organswhen fed and smaller organs when hibernating compared tohigh-elevation lizards (Table 3). Taken together, the organs ofthe digestive tract suggest a pattern of regulation consistent withour hypotheses. There appears to be a relatively strong effect offeeding/activity level; digestive organs are larger when the lizardsare active and/or feeding than when hibernating. There may bea moderate effect of elevation on digestive tract mass, althoughstatistical support for this is weak; low-elevation lizards mayincrease gut size more while feeding than high-elevation lizards.

Discussion

We hypothesized that chuckwallas regulate intestinal perfor-mance in order to maximize energy assimilation during theiractivity season and reduce energy expenditures during dormantperiods. Our results support this hypothesis by demonstratingthat chuckwallas regulate digestive performance depending ondigestive demand. When fasting, chuckwallas had smaller stom-achs, ceca, and small intestines and lower rates of intestinalnutrient uptake compared to when they were feeding. Duringhibernation, we found small intestine size and nutrient uptakerate to be further reduced. In contrast, organs involved in as-similation and excretion (e.g., liver, kidney) appeared unaf-fected by the lizards’ activity or feeding levels. We will discuss(1) how these results are similar to those for carnivorous reptiles




Figure 3. Total uptake capacity of the small intestine for d-glucose (A)and l-proline (B). Bars represent least squares means, and error barsrepresent 1 SE, calculated as described in Figure 2. Open bars are forlow-elevation chuckwallas, and filled bars are for high-elevation chuck-wallas. Numbers above bars indicate statistically distinguishable groupsusing post hoc pairwise contrasts. Both nutrients showed significanteffects of feeding/activity level and elevation (see text and Table 2 forstatistical tests, interactions, and pairwise comparisons).

during fasting but differ from those for fasting and migratingbirds and hibernating mammals and (2) the adaptive and evo-lutionary implications of gut regulation in chuckwallas.

Patterns of Regulation of Intestinal Function

Feeding, fasting, and hibernation have known effects on thesize and activity of digestive organs in some species. For ex-ample, during hibernation, thirteen-lined ground squirrels(Spermophilus tridecemlineatus) experience significant reduc-tion in intestinal mass and mucosal surface area due to thedecline in intestinal villus height and abundance (Carey 1990;Carey and Sills 1992). However, mass-specific uptake rates ofsugars (glucose, 3-O-methylglucose) and the amino acid l-proline are actually higher during hibernation, resulting in noloss of intestinal nutrient uptake capacity (Carey and Sills 1992).Thus, thirteen-lined ground squirrels appear to maintain themachinery necessary for high transport rates year around. Sim-ilar findings have been reported for other Spermophilus species(Musacchia and Westhoff 1964; Karasov and Diamond 1983a).

In contrast to ground squirrels, hibernation induces a re-duction in active and passive transport of sugars and aminoacids for the lizard Uromastyx hardwickii (Latif et al. 1967;Qadri et al. 1970) when compared to active animals. Theseresults, although determined by methods substantially differentfrom ours, are similar to our findings for chuckwallas. Com-bined, these three studies suggest that herbivorous lizards re-duce intestinal performance during hibernation.

Fasting alone can induce changes in gut size and nutrientuptake rates in mammals, birds, amphibians, and reptiles. Todate, most vertebrates studied have shown a decrease in intes-tine mass related to fasting (Starck 1999), including mammals(Diamond and Karasov 1984; Dunel-Erb et al. 2001), birds(Levey and Karasov 1992; Karasov and Pinshow 1998; Piersmaet al. 1999), reptiles (Csaky and Gallucci 1977; Secor and Dia-mond 1995, 1997a, 1997b, 2000; Secor 2001), amphibians (To-loza and Diamond 1990; Secor 2001; Secor and Faulkner 2002),and fish (Buddington et al. 1987).

However, the nature of the pattern for nutrient uptake ratesis less clear. For mammals, fasting has been reported to increasenutrient uptake rates (Steiner and Gray 1969; Axelrad et al.1970; Levinson and Englert 1972), decrease nutrient uptakerates (Adibi and Allen 1970; Levin 1970; Debnam and Levin1975; Kotler et al. 1980, 1981; Diamond and Karasov 1984;Bardocz et al. 1991), or even increase nutrient uptake rates inone part of the intestine and decrease them in another (Sanfordand Smyth 1974). For birds, the results are also conflicting,with reports of either increased (Levin 1984) or decreased nu-trient uptake rates with fasting (Levin and Mitchell 1982). Dia-mond and Karasov (1984) describe that the interaction betweenchanges in intestinal mass and transporter activity can resultin one experiment reporting both trends depending on whetheruptake rates were normalized to intestine mass, intestine length,

or intestine surface area (Diamond and Karasov 1984). Despitethis confusion, recent studies suggest that, in mammals, fastingresults in changes to intestine morphology and function thatare similar to those induced by hibernation (Carey 1990, 1992;Hume et al. 2002).

For amphibians and reptiles, fasting induces the character-istic decrease in small intestinal mass and for some species adecrease in intestinal nutrient transport (Csaky and Gallucci1977; Secor et al. 1994; Secor and Diamond 1995, 1997a, 1997b,2000; Secor 2001). Snakes that naturally feed infrequently ex-hibit the largest fasting-induced changes in gut structure andfunction of any species studied to date (Secor and Diamond2000). For example, fasting pythons reduce intestinal mass by50% and reduce intestinal nutrient uptake following meal di-gestion. Consequently, feeding triggers a doubling of small in-testine mass and a 10–20-fold increase in intestinal nutrientuptake rates (Secor and Diamond 1995, 1997a, 1997b). In con-trast, frequently feeding snakes, other reptiles, amphibians, and




Table 2: Results of pairwise comparisons of least squares means of total uptake capacity of glucose (abovediagonal) and proline (below diagonal) for all combinations of elevation and feeding/activity level

Low Elevation High Elevation

Fed (6) Fasted (6) Hibernating (6) Fed (5) Fasted (8) Hibernating (6)

Low elevation:Fed (6) … !.001* !.001* !.001* !.001* !.001*Fasted (6) .064� … .053� .772 .324 .012*Hibernating (6) !.001* .002* … .048* .294 .531

High elevation:Fed (5) .052� .866 .006* … .210 .006*Fasted (5) !.001* .007* .707 .010* … .064�

Hibernating (3) !.001* .001* .402 .001* .227 …

Note. Numbers given are P values from t-tests on least squares means, using body mass as a covariate. Sample size for glucose is given

in parentheses across the top, sample size for proline is given in parentheses at left. See also Figure 2 for values of least squares means.� .0.1 ≥ P ≥ 0.05

* .P ! 0.05

mammals exhibit much more modest responses with feeding,increasing small intestinal mass by 50% and only doublingnutrient transport (Secor and Diamond 1998; Secor 2001).

Secor and Diamond (1998, 1999, 2000) hypothesized thatwide regulation of gut performance is energetically advanta-geous when meals are separated by long intervals of fasting;thus, the magnitude of gut regulation is evolutionarily corre-lated with feeding frequency. While this hypothesis appears tohold for amphibians and reptiles (Secor 2001), it does notexplain the maintenance of digestive machinery in hibernatingground squirrels. The maintenance of uptake capacity in theseendotherms may reflect their higher overall metabolic demands(compared with ectotherms). The costs of maintaining trans-porters may be lower than maintaining the entire intestinalsystem; thus, ground squirrels might be able to maintain min-imum transport levels while still saving energy by reducingoverall gut mass.

To date, there has been very little work on the regulation ofgut function in herbivorous ectotherms. One might expect her-bivorous animals to show similar patterns of gut regulation tothose of frequently feeding carnivores. Most herbivores main-tain a full gut to preserve the symbiotic microflora that fermentingested cellulose. Fermentation of plant material requireslonger retention times of digesta than digestion of a carnivorous(or insectivorous) diet. Even though actual meals may be pe-riodic or even infrequent, herbivore digestive systems may be-have functionally like those of frequently feeding carnivoresbecause of the long retention time. Chuckwallas in this studyshowed relatively small increases in gut activity between hi-bernating and feeding animals; glucose uptake rates for feedingchuckwallas were about two times those of fasting chuckwallas(low elevation: 2.2 times; high elevation: 1.7 times), and prolineuptake rates were about three times fasting levels (low elevation:2.8 times; high elevation: 3.2 times). These factorial rates fallwell within the range of increases measured in frequently feed-

ing, carnivorous reptiles fed a single meal and are much lowerthan those for infrequently feeding snakes (Secor 2001).

The liver, kidney, heart, and spleen masses did not showpatterns consistent with our predictions (Table 4). While therewere some differences in organ size, they were slight and werenot all statistically significant. These organs are used in variousaspects of postabsorption processing and distribution of nu-trients and have been shown to increase in size after feedingin snakes (Secor and Diamond 2000), during refueling stopsin migratory birds (Piersma et al. 1999), and during lactationin mice (Hammond et al. 1994; Hammond and Kristan 2000).However, some frequently feeding snake species did not showincreased organ size with feeding (Secor and Diamond 2000).It is unclear whether this represents a pattern for frequentlyfeeding reptiles (including herbivores like chuckwallas) orwhether it simply reflects a small sample of these species.

Unfortunately, it was impossible to deprive chuckwallas inthe fasting and hibernating groups for an equal amount of timebecause of the long duration of hibernation. Thus, it is im-possible to completely separate the effects of prolonged fastingwhile cold from any additional effects of hibernation, and there-fore, it is possible that any significant reductions in the hiber-nation group compared to the fasting group are simply theresult of the additional time these animals were deprived offood. Regardless, the differences we have highlighted hereshould reflect ecologically relevant distinctions between short-duration fasts that occur while chuckwallas are warm and activeduring the summer and longer-duration fasts (hibernation) thatoccur over the cooler winter months.

Evolutionary and Adaptive Implications of Variation forChuckwallas

Low-elevation chuckwalla populations experience very shortgrowing seasons, followed by a dormancy period that is hot




Table 3: Digestive organ lengths and masses, corrected for body size

High Elevation Low ElevationSignificantEffectsaFed Fasted Hibernating Fed Fasted Hibernating

Stomach:Length (mm) 109ab � 7 89c � 5 79c � 4 105ab � 6 110a � 7 92bc � 6 e*, t**Wet mass (g) 4.0a � .4 2.8bc � .2 2.8bc � .2 3.4ab � .3 2.6c � .2 2.8bc � .3 t**Dry mass (g) .70a � .06 .55b � .04 .54b � .04 .62ab � .05 .51b � .04 .51b � .04 t*Dry (%) 17.6 19.2 19.6 18.1 19.6 18.5

Small intestine:Length (mm) 350a � 40 300ab � 30 330ab � 30 310ab � 30 260bc � 30 200c � 20 e**, t*Wet mass (g) 3.0ab � .2 2.2c � .1 2.4bc � .2 3.3a � .2 2.4c � .2 1.5d � .2 e # t # b*, e # b*,

t # b�, e # t*, e*, t�

Dry mass (g) .64a � .06 .46b � .03 .42bc � .03 .74a � .06 .62a � .05 .37c � .03 e # t*, e # b**, e**,t***

Dry (%) 21.2 21.1 17.3 22.4 25.4 24.1Cecum:

Length (mm) 69a � 6 41c � 3 39c � 3 79a � 6 50b � 4 40c � 3 e�, t***Wet mass (g) 2.3 � .4 1.6 � .2 1.9 � .3 2.5 � .4 1.8 � .3 2.0 � .3 t�

Dry mass (g) .39ab � .05 .29b � .03 .30ab � .03 .40a � .04 .31ab � .03 .28b � .03 t*Dry (%) 17.2 17.5 15.6 15.7 17.5 14.1

Large intestine:Length (mm) 49bc � 7 56abc � 6 47c � 5 65ab � 8 74a � 9 60abc � 8 e**Wet mass (g) 1.0 � .1 1.2 � .1 1.3 � .2 1.3 � .2 1.0 � .1 1.1 � .2Dry mass (g) .17ab � .02 .20ab � .02 .22a � .02 .22a � .02 .17ab � .02 .16b � .02 e # t*Dry (%) 17.4 16.8 16.6 17.6 17.5 14.3

Total gastrointestinal tract:Length (mm) 590a � 50 450bc � 30 500ab � 40 570a � 50 490ab � 40 390c � 30 e # t�, t**Wet mass (g) 10.2ab � 1.1 8.1bc � .7 8.4abc � .8 10.5a � 1.0 7.1c � .7 7.8bc � .8 t**Dry mass (g) 1.9a � .2 1.6b � .1 1.6b � .1 1.9a � .2 1.5b � .1 1.4b � .1 t # b*, e**, t**Dry (%) 19.0 19.3 18.4 18.5 21.4 17.5

Note. Measurements are given as the least squares means from two-factor ANCOVA, with body mass as the covariate. The initial analysis used log-transformed

organ body masses; least squares means were back-transformed (antilog). Superscript letters indicate statistically distinguishable groups within each measurement,

using post hoc pairwise contrasts at , without correction for multiple comparisons.P ! 0.05a Main effects and interaction terms from the ANCOVA; , /feeding level, mass covariate.e p elevation t p activity b p body� .0.1 ≥ P ≥ 0.05

* .P ! 0.05

** .P ! 0.01

*** .P ! 0.0001

during part of the time and may last through the entire fol-lowing year. For these populations, selection would favor theability to take advantage of resources quickly when available,as well as conserve energy (by minimizing energy expenditures)during periods when food resources are scarce. Thus, lizardswould be more likely to survive extended periods of fastingand be better prepared to grow and reproduce when food doesbecome available.

Chuckwallas from lower elevations possess a suite of char-acters that are seemingly adaptive for inhabiting more extremeenvironments. Compared to high-elevation lizards, low-elevation chuckwallas are smaller (Case 1976; Tracy 1999),which reduces their total energy requirements compared tolarger, high-elevation chuckwallas. Low-elevation lizards alsohave large fat-bodies (Case 1976), providing them with amplestored energy for the long periods when food is unavailable.

Furthermore, low-elevation juveniles grow more quickly thantheir high-elevation counterparts, allowing them to reach sexualmaturity in the same number of growing seasons as high-elevation chuckwallas, despite experiencing shorter growingseasons (Tracy 1999). Once reaching sexual maturity, low-elevation lizards grow very slowly, presumably because energyallocation is shifted from growth to fat storage. Our studydemonstrates that low-elevation chuckwallas have a greater ca-pacity to regulate digestive performance, thus facilitating thislifestyle. When food is available, low-elevation chuckwallas up-regulate intestinal nutrient uptake, and when food is scarce,they downregulate intestinal performance.

The greater average rainfall and lower temperatures at higherelevations allow a longer growing season and the possibility ofsheltered pockets where food is available, even during normallydry periods. In some areas of the chuckwallas’ range, there is




Table 4: Visceral organ masses corrected for body size

High Elevation Low Elevation SignificantEffectsaFed Fasted Hibernating Fed Fasted Hibernating

Liver:Wet mass (g) 4.8ab � .4 3.9a � .5 5.5b � .5 5.6b � .5 4.7ab � .5 4.8ab � .5Dry mass (g) 1.5 � .1 1.3 � .2 1.5 � .2 1.8 � .2 1.6 � .2 1.8 � .3 e # b*, e�

Dry (%) 31.1 33.3 26.7 32.8 34.5 38.0Kidney:

Wet mass (g) .77a � .04 .62a � .13 1.06b � .10 .94b � .06 .80a � .06 .86ab � .11 e # t # b*,e # t*

Dry mass (g) .16cd � .01 .13bcd � .03 .21ab � .02 .19abd � .01 .16abcd � .01 .16abcd � .02 e # t # b*,e # t*

Dry (%) 21.0 20.7 19.8 20.6 20.6 18.5Heart:

Wet mass (g) .37a � .02 .38ab � .03 .37ab � .02 .39ab � .02 .44b � .03 .37ab � .03Dry mass (g) .076ab � .004 .076ab � .007 .080a � .005 .080a � .005 .086a � .006 .066b � .005 e # t�

Dry (%) 20.5 19.9 21.4 20.4 19.5 17.9Spleen:

Wet mass (g) .11 � .02 .08 � .03 .09 � .02 .07 � .02 .09 � .03 .06 � .01Dry mass (g) .026 � .005 .020 � .007 .026 � .006 .017 � .004 .027 � .008 .012 � .003 e # t�

Dry (%) 22.7 24.2 29.9 24.3 29.5 21.0

Note. See Table 1 for explanation of values.a , /feeding level, mass covariate.e p elevation t p activity b p body� .0.1 ≥ P ≥ 0.05

* .P ! 0.05

also the possibility of a second growing season followingsummer monsoonal rains. Chuckwallas from high elevationsshowed patterns of size and function of digestive organs con-sistent with a more predictable habitat with extended or mul-tiple growing seasons. Those lizards reduced intestine size andnutrient uptake at lower magnitudes compared to low-elevationlizards. The occasional pockets of food or second growing sea-sons at high elevations are likely to be relatively short lasting,so chuckwallas that did not maintain the digestive machineryto process it could miss an important source of energy becauseof the potential time lags involved in upregulating the digestivesystem. This argument hinges on the consideration that thereis a delay after feeding has resumed before the gut is fullyupregulated.

The argument that differences in strategies of gut regulationdepend on energy savings could also be strengthened by mea-suring the differences in metabolic rate associated with eithermaintaining a large, active digestive system or up- and down-regulating the digestive system with use. Secor and Diamond(2000) compared daily energy expended on maintenance anddigestion for two species of snakes that differ in their feedingfrequencies. They found that, when feeding frequently, the spe-cies that maintained gut function when fasting was at an en-ergetic advantage because of reduced costs of digestion. How-ever, when feeding infrequently, the species that severelydownregulated gut performance while fasting had an energetic

advantage due to lower maintenance cost when fasting. It wouldbe interesting to test, by measurements of metabolic rate,whether this energetic advantage between two species can alsooccur within one species, like Sauromalus obesus, whose pop-ulations vary in strategy of gut regulation.

In summary, we have shown that S. obesus does have theability to regulate digestive organ size and function. Further,we have shown that within this single species, there is variationin the pattern of regulation. Although this variation is small incomparison with differences between species, the fact that thereare differences between populations within a species makes thevariation intriguing. The physiological regulation is consistentwith adaptive patterns of variation in life-history traits that aredriven by variation in local environmental conditions, thoughwe cannot as yet rule out phenotypic plasticity as an explanationfor these differences.

Acknowledgments

This research was conducted under permit from the AnimalCare and Use Committee of the University of Wisconsin (pro-tocol A-48-9700-L00233-2-05-96). It was partially funded byNational Institutes of Health grant GM14772 (J.D.), a JohnJefferson Davis research award from the University of Wiscon-sin Department of Zoology (C.R.T.), and a Vilas Professional




Development Fellowship from the University of WisconsinGraduate School (C.R.T.). Thanks to Warren Porter (and hislab group), Dick Tracy, Pamela Mueller, and Steven Secor fortheir help at all stages of this research. Annette Gendron andStephen Gammie provided equipment and expertise with thehistological preparation, interpretation, and presentation. Spe-cial thanks to Mandy Lam for her invaluable help with evertedsleeves and Bill Karasov (and his lab group) for help and gen-erous access to facilities and expertise.

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