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Disruption to Recovery Metabolism in the Fence Lizard Sceloporus occidentalisInfected with the Malarial Parasite Plasmodium mexicanumAuthor(s): David A. Scholnick , Nathan T. Gilpin , and Richard V. ManivanhSource: Journal of Herpetology, 46(4):643-647. 2012.Published By: The Society for the Study of Amphibians and ReptilesDOI: http://dx.doi.org/10.1670/11-146URL: http://www.bioone.org/doi/full/10.1670/11-146

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Journal of Herpetology, Vol. 46, No. 4, 643–647, 2012Copyright 2012 Society for the Study of Amphibians and Reptiles

Disruption to Recovery Metabolism in the Fence Lizard Sceloporus occidentalis Infectedwith the Malarial Parasite Plasmodium mexicanum

DAVID A. SCHOLNICK,1 NATHAN T. GILPIN, AND RICHARD V. MANIVANH

Department of Biology, Pacific University, Forest Grove, Oregon 97116 USA

ABSTRACT.—Western Fence Lizards, Sceloporus occidentalis, are frequently parasitized by the malaria-causing protozoan Plasmodiummexicanum, reducing hemoglobin concentrations, increasing reliance on anaerobic metabolism, and elevating the cost of recovery. We examined

the influence of malarial infections in Fence Lizards on aerobic capacity, blood metabolites, and cardiopulmonary activity following activity (<2

min of maximal activity) on a treadmill at 35.0 6 1.08C. Aerobic capacity was determined from resting and maximal oxygen uptake. Blood

glucose and lactate were measured before activity and at 15 min intervals during 60 min of recovery. Heart rate and ventilation rate weredetermined from electrocardiograph tracings. Maximal aerobic capacity was over 35% higher in uninfected lizards compared to both malaria-

infected lizards and anemic-uninfected animals. Malarial infection decreased lizard resting blood glucose levels, yet induced hyperglycemia

during recovery; blood glucose levels were elevated by about 27% from resting in malaria-infected lizards after 60 min of recovery. Malarialinfection significantly increased anaerobic metabolism during activity; blood lactate levels in infected lizards were elevated above those in

uninfected animals for 45 min of recovery. Heart rate was limited severely in malaria-infected lizards following activity; mean heart rate was

over 20 beats per minute lower (170 6 6.7 vs. 193 6 5.0) in infected lizards compared to uninfected animals. The major disruptions to recovery

metabolism in malaria-infected lizards, glucose, lactate, and cardiac dysfunction, are similar to those reported for severe Plasmodium infectionsin mammals.

In Western Fence Lizards, Sceloporus occidentalis, infectionswith the malaria-causing parasite Plasmodium mexicanum arecommon, with infections of up to 30% of animals in apopulation having been reported from California and Oregon(Schall and Marghoob, 1995; Scholnick et al., 2010). Lizardmalaria results in numerous pathologies including anemia(Schall et al., 1982), hypoglycemia (Dunlap and Schall, 1995),tissue damage (Ayala, 1970), and mortality of subadults (Schall,1983). Lizard malarial infections appear to have importantconsequences for metabolism and behavior, especially duringactivity and recovery when energy demands are elevated(Schall and Sarni, 1987). Fence Lizards infected with P.mexicanum exhibit reduced hemoglobin concentrations of upto 25% (Schall et al., 1982), which elevate lactate levels followingactivity and increase the cost of recovery (Scholnick et al., 2010).

Recovery costs are high in lizards where metabolic ratesremain elevated above resting levels for extended periodsfollowing even brief activity (Hancock et al., 2001; Hancock andGleeson, 2002). In Desert Iguanas, Dipsosaurus dorsalis, postex-ercise oxygen uptake can remain elevated above resting levelsfor over an hour following 15 sec of activity, and elevatedoxygen uptake during recovery can account for over 90% of thetotal cost of activity (Nedrow et al., 2001). Vigorous activity inlizards is supported primarily by anaerobic metabolism whileextended recovery periods must be supported by elevatedoxygen uptake (Bennett and Dawson, 1972). Long periods ofelevated oxygen uptake during recovery in lizards are used toincrease production of ATP, resaturate hemoglobin and myo-globin with oxygen, convert accumulated lactate to glucose, andgenerate ATP through lactate oxidation (Hancock and Gleeson,2008). Given the limited aerobic scope and extensive recoverytimes for lizards (Bennett and Dawson, 1972), Plasmodiuminfection may have a dramatic impact on metabolites andcardiopulmonary functions during recovery.

In ectotherms and endotherms, the pathology of malaria isassociated with severe anemia and the many accompanyingdisruptions to aerobic metabolism. In humans with severe

malarial infections, usually with Plasmodium falciparum, malaria-

associated anemia is a major contributor to mortality (Lam-

ikanra et al., 2007). Respiratory distress is a frequent clinical

presentation in malarial-infected humans, particularly in chil-

dren and pregnant women (Greenwood, 1997), although other

associated risk factors including hypoglycemia (Ogetii et al.,

2010) and myocardial depression are common (Yacoub et al.,

2010). Thus, the pathophysiology of malarial infection appears

to be closely linked to aerobic capacity, and the physiological

consequences of malarial infections may be most pervasive

when aerobic demand is elevated such as during activity and

recovery.

We examine the possibility that disruptions resulting from

malarial infection may impact the factors that contribute to

elevated aerobic metabolism that occur during prolonged

recovery in lizards. We measured aerobic capacity, blood lactate,

blood glucose, and quantified cardiac and ventilatory activity

during recovery in Fence Lizards infected with P. mexicanum.

Each variable was compared to uninfected lizards that were

collected from the same populations.

MATERIALS AND METHODS

Adult Western Fence Lizards were collected from southern

Oregon. Plasmodium infections were determined at the site of

collection from blood smears prepared from a small drop of

blood collected via toe clip. Blood was fixed with methanol

before staining with Giemsa (pH 7.0). Blood cells were

examined for the presence of P. mexicanum at · 1,000 according

to methods described by Scholnick et al. (2010) and Bromwich

and Schall (1986).

Lizards infected with P. mexicanum (N = 13) and 15 uninfected

lizards from the same collecting sites were transported to Pacific

University and maintained in individual thermal gradient cages

(22–458C using a heat lamp) for 2 to 3 weeks before they were

returned to the collecting sites at the end of the study. Animals

were maintained under a 10 : 14, L : D photoperiod and fed 3- to

4-week-old crickets three times weekly. Water was provided ad

libitum. All experiments were conducted during daylight hours

1Corresponding Author. E-mail: david.scholnick@pacificu.eduDOI: 10.1670/11-146

on lizards that had been fasted for 24 h. Lizards were placed in adark 358C incubator for at least 1 h before experimentation.

Aerobic Scope.—To determine the influence of malarial infectionon aerobic capacity, we measured oxygen uptake at rest andduring maximal activity using flow-through respirometry. Beforeactivity, animals were fitted with a latex mask and placed on astationary thermostated 358C treadmill for at least 30 min.Oxygen uptake was measured from resting lizards for at least 2 hprior to activity, and the lowest mean metabolic rate over a 20-min period was used as a measure of resting oxygen uptake.Maximal oxygen uptake was measured from animals that wereinduced to run to exhaustion (less than 2 min of activity) byprodding the tail and hindquarters while treadmill speed wascontrolled to match lizard performance (maximum tread speed2.5 m sec-1). Expired gases were drawn through an AppliedElectochemistry S-3/A oxygen analyzer following methods fromScholnick et al. (2010). Tread speed and oxygen concentrationdata were collected by a Lab-NB data-acquisition board (NationalInstruments, Austin, TX) connected to a PC, and instantaneousmeasurements of oxygen uptake and performance were com-puted with LabView program equations according to Scholnickand Gleeson (2000).

To better understand the physiological consequence ofmalaria-induced anemia on aerobic scope, we reduced hemo-globin concentrations of eight uninfected lizards by 25% andmeasured performance, resting, and maximal oxygen uptake asdescribed above. To reduce hemoglobin concentrations, bloodwas collected via toe clip into heparinized microcapillary tubes(about 100–150 ll) and replaced with equal volumes of lizardRinger’s (in mM: 157.5 NaCl, 4.6 KCl, 12.0 NaHCO3

-, 1.45CaCl2, 2.6 NaH2PO4, and 1.1 MgSO3; Guillette, 1982) injectedintraperitoneally until hemoglobin concentrations were reducedby 25%. Lizards were allowed to recover for 24 h prior tooxygen uptake and performance measurements. Blood hemo-globin levels were determined spectrophotometrically using thecyanmethemoglobin method at 540 nm (Brown, 1973) directlybefore experimentation.

Blood Metabolites.—In a separate set of experiments, wedetermined blood lactate and blood glucose for animals at restand during 60 min of recovery from activity, as described above.Approximately 10 ll of blood were collected via toe clip fromlizards at rest and every 15 min of recovery. Animals were placedin individual containers in a darkened incubator set to 358Cduring recovery. Sampling typically took less than 30 sec and asingle toe clip was usually sufficient for collecting blood for theentire recovery period. If animals struggled or sampling tooklonger than 30 sec, the samples were discarded. Resting bloodsamples were collected after animals had been acclimated to 358Cfor at least 2 h and recovery samples collected immediatelyfollowing activity and every 15 min for 60 min from infected (N= 6) and uninfected (N = 8) animals. Blood metabolites weremeasured using small-volume (<2 ll), handheld blood lactate(Scout, EKF Diagnostic, Germany) and glucose (Abbott, Alame-da, CA) analyzers. Prior to lizard studies, handheld analyzerswere compared to colormetric blood lactate and glucose assays(Sigma Technical Bulletins no. 862 and 7119, respectively). Withinthe range of glucose and lactate measured in the currentexperiment, there was no discernable difference in glucose orlactate concentrations between the two analysis methods.

Cardiac and Ventilatory Activity.—An electrocardiograph (ECG)with two small alligator clips as leads was used to measure heartand ventilation rates during rest and recovery. Leads were placedat a diagonal on the anterior aspect of the right shoulder to the

posterior aspect of the left shoulder with a single ground. ECGactivity was monitored using a Thornton Bio-Amplifier (Thorn-ton Associates, Inc., Waltham, MA, USA) and an iWorx dataacquisition system (iWorx Systems, Inc., Dover, NH, USA). Theoutput showed large spikes that represented ventricular contrac-tions and regular baseline oscillations that represented movementof chest and abdomen which corresponded to inhalation andexhalation.

Statistical Analysis.—Comparisons between resting and recov-ery groups were made by analysis of variance (ANOVA) withrepeated measures followed by a paired post hoc test (Fisher’sprotected least-significant difference test for multiple compari-sons) adjusted to an experimental wise error of P < 0.05 in orderto compare groups at each recovery time. Statistical comparisonsbetween infected and uninfected animals and anemic-uninfectedanimals were performed by paired t-test or ANOVA. Allstatistical analyses were performed using SigmaStat 3.5 (SystatSoftware Inc., Pint Richmond, CA). Data are reported as mean 6

SE unless noted otherwise.

RESULTS

Aerobic Scope.—Aerobic scope, the difference between restingand maximal oxygen uptake, differed significantly betweeninfected and uninfected lizards (F2,33 = 17.51, P < 0.001; Fig. 1).Maximal aerobic capacity was over 35% higher in uninfectedlizards compared to malaria-infected lizards. Uninfected lizardswith experimentally reduced hemoglobin concentrations hadaerobic capacities similar to malaria-infected animals (Table 1).Performance measures such as burst speed and distance traveledwere not influenced by malaria parasite infection, although therewas a strong relationship between anemia and maximal oxygenuptake (Table 1).

Blood Glucose and Lactate.—Malaria-infected lizards had signif-icantly lower blood glucose levels at rest than did uninfectedlizards (189 6 6 vs. 206 6 7 mg dl-1; F1,14 = 9.81, P = 0.012; Fig.2A). Blood glucose levels during recovery increased steadily inmalaria-infected lizards compared to uninfected lizards. Unin-fected animals maintained stable blood glucose levels directlyafter activity and throughout 60 min of recovery. Blood glucoselevels increased from about 200 mg dl-1 directly after activity toover 250 mg dl-1 following 60 min of recovery in malaria-infected lizards. Overall, malaria infection induced a 20%increase in blood glucose after 60 min of recovery compared touninfected lizards that were able to maintain stable blood glucoselevels throughout recovery (F1,14 = 7.84, P = 0.021).

Following activity, malaria-infected lizards had significantlyhigher blood lactate levels than the uninfected lizards (F1,14 =28.35, P < 0.001; Fig. 2B). Malarial infection had no influence onresting blood lactate (F1,14 = 1.75, P = 0.20; Fig. 2B). Directlyfollowing activity, lizards infected with P. mexicanum had bloodlactate levels significantly higher than the uninfected animals(16.0 mmol L-1 vs. 10.5 mmol L-1) and lactate remainedelevated above uninfected animals for 45 min of recovery. Inboth infected and uninfected animals, blood lactate decreasedthroughout the 60 min of recovery to near resting levels; after 45min in uninfected animals and 60 min in infected.

Cardiac and Ventilatory Activity.—Malaria parasite infection hada negative effect on mean recovery heart rate (HR; Fig 3A).Recovery HR in uninfected animals was significantly elevatedabove that of infected animals after 30 min of recovery andremained elevated over 60 min of recovery (F1,16 = 6.20, P =0.028). During recovery, malaria-infected animals had recovery

644 D. A. SCHOLNICK ET AL.

HR over 20 beats min-1 slower than the uninfected animals

(mean recovery HR was 170 6 6.7 for infected vs. 193 6 5.0 for

uninfected animals). Maximal recovery HR for uninfected

animals reached 203 beats min-1 after 40 min of recovery while

maximal recovery HR remained below 180 beats min-1

throughout 60 min of recovery for infected lizards. Malarial

infection had no significant impact on mean resting HR (113 6 8

beats min-1 for uninfected and 120 6 9 beats min-1 for infected;

F1,16 = 0.34, P = 0.565).

Mean resting ventilatory rates (VR) were not significantly

different between uninfected (28 6 2 breaths min-1; N = 9) and

malaria-infected animals (26 6 2 breaths min-1; N = 6; F1,15 =0.825, P = 0.382; Fig. 3B). The presence of malaria parasite

infection had no significant effect on VR at rest or following

activity. Activity increased VR about 5 breaths min-1 for

infected and uninfected animals.

DISCUSSION

Our results suggest that P. mexicanum infection in Fence

Lizards can limit maximal aerobic capacity and disrupt blood

metabolites and cardiac function during recovery. At rest,

malaria-infected lizards exhibited a slight blood hypoglycemiawhereas blood lactate, heart rate, and ventilation rate wereunaltered when compared to uninfected animals. Maximaloxygen uptake was significantly reduced due to malarialinfection, resulting in a lower maximal aerobic capacity. Duringrecovery, malarial infection limited cardiac function; mean HRof infected lizards was more than 20 beats min-1 slower than inuninfected lizards. Blood glucose steadily increased from 200mg dl-1 at the end of activity to over 250 mg dl-1 after 60 min ofrecovery in malaria-infected lizards. Our results suggest thatmalarial infections, and the accompanying anemia, increase thereliance on anaerobic metabolism during activity and increasethe aerobic costs of substrate recycling and energetic costsneeded to return to homeostasis during recovery.

Malarial infections in S. occidentalis decreased maximalaerobic capacity by almost 40% compared to uninfected lizards.Uninfected animals with experimentally reduced hemoglobinconcentrations had aerobic capacities comparable to malaria-infected animals. These results suggest that changes inhemoglobin concentrations are a major contributing factor foroxygen limitations during maximal activity and explaindifferences in aerobic scope between treatment groups. Schallet al. (1982) reported similar decreases in aerobic scope due tomalaria-associated anemia and found a positive correlationbetween blood hemoglobin concentrations and maximal oxygenconsumption for both infected and uninfected S. occidentalis.

Malaria-infected lizards have a small but significant depres-sion in plasma glucose at rest and a continual increase in bloodglucose during 60 min of recovery. Hypoglycemia is oftenassociated with severe malaria in mammals (Aghenyega et al.,2000) and has been reported previously in Fence Lizards(Dunlap and Schall, 1995; Vardo-Zalik and Schall, 2008). Inmammals, parasite-infected erythrocytes utilize glucose at ahigher rate than do uninfected cells (Roth et al., 1988) andappear to indirectly obstruct glucose utilization in uninfectedred cells (Mehta et al., 2005). Decreased resting glucose andhyperglycemia postactivity would be consistent with a Plasmo-dium parasite influencing host glucose metabolism to enhanceparasite reproductive success (Mehta et al., 2005).

In the present study, malarial infection limited cardiacfunction during recovery (Fig. 3). Malaria-associated cardiacdisruptions are known to play a role in the pathophysiology ofPlasmodium infection in mammals (Yacoub et al., 2010). Childrenwith severe malaria infections have decreased blood flow(Dondorp et al., 2008), elevated lactic acid production (Englishet al., 1997), and increased concentrations of circulating cardiac

FIG. 1. Maximum aerobic capacity for malarious (N = 13),uninfected (N = 15), and uninfected-anemic (N = 8) S. occidentalisduring sprint activity (<2 min) on a treadmill at 358C. Uninfected lizardshad significantly higher aerobic capacity (*) than did lizards infectedwith Plasmodium mexicanum and uninfected with experimentallylowered hemoglobin levels (25% reduction). Mean values 6 SE areshown.

TABLE 1. Influence of Plasmodium mexicanum infection and experimentally induced anemia on oxygen uptake and performance in Sceloporusoccidentalis. Values are means (6SE). Statistical comparisons are between infected and uninfected (t-test) and uninfected and anemic-uninfected(paired t-test). Anemia in uninfected animals was induced by removing red blood cells to achieve a 25% reduction in hemoglobin concentration.

Treatment

Infected (I) Uninfected (U)

I vs. U

Anemic-uninfected (A)

U vs. A

P P

Oxygen uptake (ml g-1 h-1)Number of animals 13 15 8Resting 0.34 (0.03) 0.31 (0.02) >0.05 0.34 (0.02) >0.05Maximal activity 1.20 (0.07) 1.60 (0.09) <0.05 1.24 (0.07) <0.05

PerformanceNumber of animals 8 10 7Burst speed (m sec-1) 0.88 (0.07) 1.04 (0.06) >0.05 1.08 (0.05) >0.05Meters run in 30 sec 14.2 (2.4) 16.9 (1.3) >0.05 15.5 (2.6) >0.05Meters run in 2 min 26.5 (2.4) 28.3 (2.9) >0.05 30.1 (4.0) >0.05

MALARIA INFECTION DISRUPTS LIZARD RECOVERY 645

proteins that are indicative of impaired cardiac function(Ehrhardt et al., 2005). Mice infected with Plasmodium developirreversible heart lesions that were correlated with infectionduration (Vuong et al., 1999). Limited cardiac function duringrecovery in western Fence Lizards, which typically have lifetimePlasmodium infections (Schall and Marghoob, 1995), maysuggest cardiac muscle damage and corresponding decreasedblood flow similar to those reported in mammals.

Mean ventilatory activity increased by about 5 breaths/min-1

following activity for both infected and uninfected animals andremained slightly elevated for the entire 60-min recoveryperiod. Elevated VA during recovery was estimated tocontribute only about 2% to recovery metabolism in DesertIguanas (Hancock and Gleeson, 2008), although elevated VA isnecessary to offset decreased pH due to lactic acid formationfollowing activity in the American Alligator (Hartzler et al.,2006).

In humans hypoglycemia, elevated lactic acid, associatedacidosis, and impaired cardiac function are considered serious,potentially life-threatening complications of P. falciparum infec-

tion, a situation unfortunately exacerbated by quinine therapy(Davis et al., 2002). While the causative factors of malarialmetabolic disruptions in humans remain unclear, the apparentaccelerated anaerobic metabolism resulting from malaria-associated anemia appears to be a major contributor to theconsiderable metabolic disruptions and resulting high levels ofmortality due to severe malaria. The pathophysiology of severePlasmodium infection reported in mammals is strikingly similarto the disorders reported in the current study for S. occidentalis.Disturbances to blood glucose, elevated lactate, and cardiacimpairment appear to be a common suite of disruptionsresulting from malarial infections in both ectotherms andendotherms. These disruptions appear to stem from reductionsin oxygen carrying capacity, elevated tissue hypoxia duringactivity, and the high glycolytic demands of the parasite.

Acknowledgments.—This paper was based upon work sup-ported by the M. J. Murdock Charitable Trust Research Grandfor Life Sciences 2008353:JVZ to D. Scholnick. K. Dick, V.Haynes, and W. Nelson helped with lizard collection and bloodscreening. Special thanks to the staff at Siskiyou Field Institute

FIG. 2. Effect of malarial infection on plasma levels of glucose (A)and lactate (B) in Fence Lizards, S. occidentalis. Values are means 6 SE, N= 9 for uninfected and N = 6 for infected. Zero minutes indicates valuesdirectly following exhaustive exercise on a 358C treadmill. Asterisksindicate a significant difference due to infection with the malarialparasite Plasmodium mexicanum. Resting values are for nonexercisedanimals at 358C.

FIG. 3. Effect of malarial infection on heart rate (A) and ventilatoryrate (B) in Fence Lizards, S. occidentalis. Values are means 6 SE, N = 7for both groups. Ten minutes indicates mean values for the first 10 mindirectly following exhaustive exercise on a 358C treadmill. Asterisksindicate a significant difference due to infection with the malarialparasite Plasmodium mexicanum. Resting values are for nonexercisedanimals at 358C.

646 D. A. SCHOLNICK ET AL.

at Deer Creek Center for providing laboratory space. PacificUniversity Institutional Animal Care and Use Committeeapproved all animal protocols. Lizards were collected underOregon Department of Fish and Wildlife Scientific TakingPermit (22-09 and 029-10).

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Accepted: 17 December 2011.

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