Breviora

US ISSN 0006-9698

Cambridge, Mass. 3 June 2015 Number 545

EFFECTS OF ECTOPARASITISM ON BEHAVIORAL THERMOREGULATION IN
THE TROPICAL LIZARDS ANOLIS CYBOTES (SQUAMATA: DACTYLOIDAE) AND

ANOL1S ARMOURI (SQUAMATA: DACTYLOIDAE)

Asa E. Conover,12 Ellee G. Cook,1 2 3 Katherine E. Boronow,4-5 and Martha M. Munoz6

Abstract. A febrile response, or a raised body temperature in response to infection, has been widely documented in
various species of reptiles in laboratory trials. However, whether and how behavioral fever is achieved in nature remains almost
entirely unknown. Here, we examine whether two species of lizard in the cybotoid clade of Hispaniolan trunk-ground anoles
( Anolis cybotes and Anolis armouri ) change their basking behavior in response to infestation by the chigger mite, Eutrombicula
alfreddugesi. We examined body temperature and basking behavior in wild populations of A. cybotes and A. armouri from four
localities that spanned a 2,000-m elevational transect in the Sierra de Baoruco, Dominican Republic. Although basking rate
increased with elevation, we found that it did not correlate with mite load. Body temperature was also unrelated to parasite
load. Thus, we found that E. alfreddugesi infestation did not induce behavioral fever in these anoles. We found a strong
altitudinal pattern in chigger infestations: Infestations levels were highest in lizards from mid-elevation and dropped
dramatically at low and high elevation (particularly in the latter). We discuss possible mechanisms for this altitudinal pattern in
chigger infestation and discuss the relationship between infection and behavioral thermoregulation in lizards.

Key words: behavioral fever; parasitism; lizard; chigger mites; behavioral thermoregulation; anole

1 Stuyvesant High School, New York, New York, 10282,
USA.

2 Department of Biological Sciences, University of
Southern California, Los Angeles, California 90089,
U.S.A.; e-mail: aeconove@usc.edu

' Division of Biological Sciences, University of Missouri,
Columbia, Columbia, Missouri 65211, U.S.A.; e-mail:
egcrg7@mail.missouri.edu

4 Department of Organismic and Evolutionary Biology,
Harvard University, Cambridge, Massachusetts 02138,
U.S.A.; e-mail: kboronow@fas.harvard.edu

5 Museum of Comparative Zoology, Harvard Universi-
ty, Cambridge, Massachusetts 02138, LJ.S.A.

6 Ecology, Evolution, and Genetics, Australian National
University, Acton, Australian Capital Territory, Aus-
tralia 0200; e-mail: martha.munoz@anu.edu.au.

INTRODUCTION

Many lizards respond to pathogen in-
fection through a febrile response, or
a marked increase in body temperature,
which is proposed to enhance the inflamma-
tory reaction (Vaughn et al., 1974; Bernheim
and Kluger, 1976; Bernheim et al., 1978).
Unlike endothermic animals such as birds
and mammals, ectotherms rely heavily on
thermoregulation to induce heightened body
temperatures (Huey, 1982; Angilletta, 2009).
Laboratory studies on lizards (Bernheim and

© The President and Fellows of Harvard College 2015.

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?

Kluger, 1976; Muchlinski et al, 1989; Ortega
et al. , 1991; Ramos et al ., 1993; Scholnick
et al., 2010), crocodilians (Lang, 1987;
Merchant et al, 2007), turtles (Monagas
and Gatten, 1983; Amoral et al, 2002), and
snakes (Burns et al, 1996) have found that
individuals injected with bacteria exhibit
elevated set-point body temperatures, mean-
ing that they attain warmer temperatures
than uninfected individuals when placed in
a temperature gradient and allowed to
choose where to sit.

The laboratory studies discussed above
suggest that behavioral thermoregulation
mechanistically underlies fever, but this
remains unconfirmed in wild populations of
naturally infected lizards. In a semi-natural
experiment, Muchlinski et al (1989) found
that, when injected with Aeromonas bacteria,
free-ranging chuckwallas ( Sauromalus obe-
sus) exhibit heightened body temperatures,
supporting the hypothesis that shifts in
basking behavior are important for inducing
fever. Malvin and Kluger (1979) found that
iguanas do not increase their internal heat
production to raise their core temperature
during infection, further supporting the idea
that extrinsic behavioral shifts are critical to
achieving fever in lizards.

Here we tested whether infestations by
chigger mites induced behavioral fever in
anoles from the Dominican Republic. Ecto-
parasites such as chigger mites are known to
affect lizard metabolism negatively (Booth
et al, 1993) and induce immune responses by
skin inflammation (Goldberg and Bursey,
1991). Previous studies in lizards have found
that ectoparasite infestation is associated
with reduced body condition (Dunlap and
Mathies, 1993; Klukowski and Nelson, 2001;
Cook et al, 2013), and reduced sprint speed
(Main and Bull, 2000). In a previous study
of Anolis brevirostris, an anole from the
Caribbean island of Hispaniola, Cook et al
(2013) found that individuals with greater

infestations of the chigger Eutrombicula
alfreddugesi exhibited poorer body condi-
tion, had duller colored dewlaps (extensible
throat fans), and displayed less frequently
than individuals with lower parasite loads.
Fence lizards with malaria also exhibit
shifts in coloration (Ressel and Schall,
1989) and reduced body condition (Dunlap
and Mathies, 1993), suggesting that ectopar-
asites have negative effects on their lizard
hosts, either through the effects of the
parasites themselves or through pathogens
transmitted by the chiggers. Given the
negative effects of chiggers, it is possible that
lizards respond to infestation by these para-
sites through behavioral fever; by increasing
their core temperature through increased
basking, lizards may combat pathogens
transmitted by the chiggers or cause the
mites to drop off. The relationship between
basking behavior and parasite infestation
may further vary with altitude: In a study of
three Hispaniolan anoles ( Anolis coelestinus,
Anolis cybotes, and Anolis olssoni ), Zippel et al.
(1996) found that chigger infestation levels
increased dramatically with elevation. Given
that basking frequency also tends to increase
with elevation in some anoles from Hispaniola
(Hertz and Huey, 1981; Munoz etal., 2014), the
use of behavioral fever may be expected also to
vary across altitude.

The goal of this study was to assess whether
chigger infestations induce behavioral fever in
wild populations of two species of Anolis
lizards ( Anolis armouri and A. cybotes) from
the Dominican Republic, Hispaniola, arrayed
across a 2,000-m elevational gradient. Specif-
ically, we tested three hypotheses: (1) chigger
infestation reduces lizard body condition; (2)
lizards with greater parasite loads also have
higher core body temperatures (i.e., exhibit
a fever) and bask more than less infested
lizards; (3) behavioral fever should be most
pronounced at high elevation, where chigger
infestations and basking rates are highest.

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Table 1. Summary Data are Given for Each Population for Study Sites in the Southwestern Region of the

Dominican Republic.

Los Patos

Guayuyal

Polo

Zapoten

Coordinates

17° 57' 36"N,

18° 3' 36"N,

18° 10' 12"N,

18° 18' 0''N,

71° 11' 24"W

71° 8' 24"W

71° 15' 0''W

71° 42' 0"W

Elevation (m)

13

727

1,236

2,020

Mean annual temperature (°C)a

26.0

22.4

23.5

13.9

Sample size

18

18

20

22

Prevalence6

100

100

100

78.3

Infestation intensity11

29.4 ± 4.3

99.4 ± 18.4

108.4 ± 19.1

15.2 ± 4.4

Infestation ranged

4—78

18-354

12-274

0-75

Observation time (min)e

58.2

57.7

59.1

57.2

Basking ratef

14.6 ± 1.0

44.4 ± 1.9

70.1 ± 2.1

90.3 ± 1.0

Body temperature (°C)s

30.9 ± 0.3

27.8 ± 1.7

26.7 ± 2.5

28.2 ± 2.3

aMean annual temperature was extracted from the WorldClim database (Hijmans et al., 2005).

bPercentage of individuals with at least one mite.

cMean number of mites per individual (± 1 SEM).

dRange of infestation intensities for a population.

cMean behavioral observation time.

‘Percentage of time lizards were observed basking (± 1 SEM).

^Temperature ± 1 SEM.

METHODS AND MATERIALS

We conducted our study on the two
cybotoid anoles, A. cybotes and A. armour i,
in June and July 2012 in the Dominican
Republic. The term “cybotoid” refers to the
clade of anoles containing the widespread
species A. cybotes and its relatives from the
Caribbean island of Hispaniola (Glor et al ,
2003). Though A. armouri shares many over-
lapping morphological features with A. cybotes
(Schwartz, 1989), this high-elevation specialist
is considered a separate species (Glor et al.,
2003; Wollenberg et al., 2013). Within the
adaptive radiation of Caribbean anoles, the
cybotoids all belong to the same “ecomorph”
or habitat specialist category, meaning that
they overlap substantially in behavioral, eco-
logical, and morphological characteristics
(Losos, 2009). Specifically, the cybotoids are
“trunk-ground” anoles; as such, they perch
close to the ground, especially on tree trunks,
have stocky builds with long hindlimbs, and

forage actively on the ground (Schwartz, 1989;
Glor et al., 2003; Losos, 2009).

We worked at four different localities ranging
between 13 and 2,020 m in the Sierra de
Baoruco in the southwestern region of the
Dominican Republic (Table 1; Fig. 2). Study
sites were located at Los Patos (13 m above sea
level [masl]; 17° 57' 36"N, 71° 11' 24"W),
Guayuyal (727 masl; 18° 3' 36"N, 71° 8'
24"W), Polo (1,236 masl; 18° 10' 12"N, 71°
15' 0"W), and Zapoten (2,020 masl, 18° 18'
0"N, 71° 42' 0"W). Anolis cybotes is found at
the three low-elevation sites (Los Patos,
Guayuyal, and Polo), where it occupies mesic,
semi-disturbed habitats, especially near agricul-
tural sites (plantain, coconut, and coffee planta-
tions). The high-elevation specialist A. armouri
is found in Zapoten. At this montane locality
the habitat is composed of monodominant pine
forest and open fields with rocky outcrops.

Eutrombiculid mites are known to parasitize
anoles from low- to mid-elevation (~ 520 masl)
on Hispaniola (Zippel et al., 1996). These

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Figure 1. A male Anolis cybotes infested with
Eutrombicula alfreddugesi mites on its dewlap
(throat fan).

small, orange-colored mites are most com-
monly found in densely vegetated areas with
high humidity and moderate ambient temper-
ature (Clopton and Gold, 1993; Bulte et al. ,
2009). The larvae attach to anoles through
direct contact and typically cluster in skin
folds, especially behind the front and back
limb joints and on the dewlap, an extensible
throat fan used extensively in Anolis commu-
nication (Fig. 1). Mites can cause lesions,
blood loss, and skin inflammation in lizards
(Goldberg and Bursey, 1991; Goldberg and
Flolshuh, 1992) and can transmit pathogens.
In Asia, chigger mites are known to transmit
scrub typhus (Traub and Wisseman, 1974),
and, more generally, mites might be vectors for
bloodbome parasites known as haemogregar-
ines, which are known to reduce burst speed in
lizards (Oppliger et al, 1996; Garrido and
Perez-Mellado, 2014).

Following Rand (1962), we found focal
lizards through slow, random sweeps through
the habitat over the course of 2-3 days per site

during all weather conditions except rain. All
observations were made on undisturbed,
naturally behaving adult male animals fol-
lowing the methods of Johnson et al. (2010).
We performed behavioral observations either
by watching lizards with binoculars and
manually transcribing observations or with
video recordings (Sony HDR-XR500V cam-
era, set in standard definition), which we
subsequently scored. Observations lasted
from 30 to 60 min ( X = 57 min) per lizard.

During each behavioral observation peri-
od we recorded the amount of time the lizard
spent under different basking conditions. We
recorded each lizard’s basking status, which
refers to how it was exploiting weather
conditions, following Munoz et al. (2014).
During each observation period we recorded
the weather conditions as sunny, partly
sunny, or overcast. Under sunny or partly
sunny conditions lizards could be scored as
perching in the sun, in the partial sun, or in
the full shade. Under overcast conditions
lizards could only be in the shade (i.e., there
was no basking choice), and these observa-
tions were discarded from further analysis.
At the end of the observation, the relative
amount of time each lizard spent basking
was calculated as the total time spent either
in the full or partial sun divided by the length
of the total observation.

At the conclusion of each observation we
attempted to catch the lizard to obtain infor-
mation on body temperature, body condition,
and parasite infestation. We noosed lizards
using a dental floss noose tied to the end of
a 10- 12-foot (3-3.7 m) telescopic panfish
pole (Cabela’s Incorporated, Sidney, Ne-
braska). Immediately after capture, we mea-
sured the core temperature of the lizard by
inserting a thermocouple (type T, copper-
constantan; Omega Engineering) approxi-
mately 1 cm into the lizard’s cloaca. The
thermocouple was attached to a handheld

2015

BEHAVIORAL FEVER IN TWO SPECIES OF ANOLE

5

Figure 2. Images showing the four localities where this study was conducted: A. Los Patos (13 m elevation);
B. Guayuyal (727 m); C, Polo (1,236 m); and D, Zapoten (2,020 m).

6

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No. 545

reader (model HH603A; Omega Engineering),
which gave temperature measurements to the
nearest 0.1 °C.

For each lizard captured we also measured
body mass to the nearest 0.1 g, using a spring
scale, and body size as snout-vent length
(SVL), the distance from the tip of the snout
to the anterior edge of the cloaca, using digital
calipers (Mitutoyo), which gave length mea-
surements to the nearest 0.01 mm. We then
counted the total number of ectoparasites on
each anole using a handheld loupe. We
sampled individuals only once and released
them at the site of capture within 48 hours.

For each population, we calculated preva-
lence, which refers to the proportion of
individuals in a population that had at least
one mite. Following Margolis et al. (1982), we
measured infestation intensity as the number
of mites per lizard. We estimated body
condition as the residuals of body mass
regressed against SVL (Schulte-Hostedde
et al., 2005). Before statistical analyses, we
log-transformed all continuous variables and
arcsine square root-transformed the propor-
tional variable (basking rate). Given that
infestation intensity correlated strongly with
body size (Pearson’s r — 0.441, d.f. = 16, p <
0.001), we used the residuals of infestation
intensity regressed against SVL as our mea-
sure of parasite load in our examinations of
correlation with body temperature and bask-
ing rate. We assessed the Pearson correlation
between variables, and used the Bonferroni
correction to correct for multiple tests. None
of the relationships were changed when we
compared body temperature and basking rate
to infestation intensity, rather than parasite
load. We compared body temperature among
populations using the Mann-Whitney U test.

RESULTS

Prevalence was extremely high across
localities: 73 of the 78 lizards examined were

infested with E. alfreddugesi mites, and 100%
of lizards from the three lower elevation sites
were infested (Table 1). Prevalence was
slightly lower in Zapoten, where 21.7% of
lizards captured had no parasites, and most
individuals had fewer than 20 mites (Fig. 3).
On average lizards harbored 61.7 mites, and
infestation intensity ranged from 0 to 354
mites (Table 1). Despite high numbers of
ectoparasites, we found no significant rela-
tionships between infestation intensity and
lizard body condition (Table 2).

Basking behavior differed among localities
(Table 1): The proportion of time lizards
spent basking increased with elevation from
14.6% in Los Patos (13 m) to 90.1% in
Zapoten (2,020 m). Mean body temperature
ranged from 26.7°C (Polo) to 30.9°C (Los
Patos) (Table 1) and was significantly higher
in Los Patos relative to the other populations
(Mann-Whitney U test; all p < 0.01).
However, basking rate and parasite load
were not strongly correlated (Table 2). Sim-
ilarly, we found no significant relationships
between body temperature and parasite load
(Table 2).

DISCUSSION

Behavioral fever is one way that ectother-
mic animals might be able to respond to
parasite infestation. However, we found that
basking frequency and body temperature
were not correlated with parasite load
(Table 2), indicating that A. cybotes and A.
armouri did not exhibit a febrile response to
chigger infestation. One possible explana-
tion is that anoles do not exhibit behavioral
fevers. Muchlinski et al. (1995) found that
Anolis eqaestris injected with bacteria did
not exhibit elevated core temperatures
compared with uninfected individuals. In
another study, Anolis carolinensis that were
injected with bacterial lipopolysaccharide
exhibited a hypothermic response (i.e., cooler,

Count

2015

BEHAVIORAL FEVER IN TWO SPECIES OF ANOLE

7

CN

o

—

CN -
O -

^ —
CN -
O -

CO

o

J=L

_Dn

h n

Los Patos

Guayuyal

n

r

0

100

200

300

400

Number of Ectoparasites

Figure 3. Histogram showing infestation intensity frequency in each of the populations sampled.

Table 2. Results for Correlation Tests Examining Relationships Between (A) Body Condition, (B) Basking
Rate, and (C) Body Temperature and Parasite Load. Pearson’s r and P Values are Given for Each Test,

and Sample Size is Given in Parentheses.

r

P

A. Body condition ~ infestation intensitya

Los Patos (18)

-0.161

0.525

Guayuyal (18)

0.326

0.187

Polo (20)

0.231

0.328

Zapoten (22)

-0.319

0.148

B. Basking rate ~ parasite loadb

Los Patos

0.262

0.293

Guayuyal

-0.399

0.101

Polo

-0.129

0.599

Zapoten

0.033

0.896

C. Body temperature ~ parasite load

Los Patos

-0.080

0.753

Guayuyal

-0.489

0.040

Polo

-0.219

0.353

Zapoten

0.036

0.875

“Residuals of body mass/SVL and the number of ectoparasites (infestation intensity). SVL refers to the body size of
the lizard, measured as the distance from the tip of the snout to the cloaca (snout-vent length).
b(Time spent basking)/(total observation length) and parasite load (residuals of infestation intensity ~ SVL).

8

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No. 545

rather than warmer, body temperatures)
when placed in a temperature gradient and
allowed to choose where to sit (Merchant
et al., 2008). Looking more broadly, whereas
many studies have observed a febrile
response to infection in lizards (e.g., Bernheim
and Kluger, 1976; Muchlinski et al, 1989;
Ortega et al., 1991; Ramos et al, 1993),
others have failed to detect a pattern
(Laburn et al., 1981; Mitchell et al., 1990)
or have found that individuals can vary in
whether or not fever is induced (Bernheim
and Kluger, 1976).

Behavioral fever might not be prevalent in
lizards because the costs associated with
fever are too high to induce them in nature.
Almost all studies examining febrile re-
sponses in lizards were conducted using
laboratory heat gradients, where all other
ecological variables besides infection are held
constant. Given that extra time spent ther-
moregulating imposes a cost to other activ-
ities, such as foraging, predator avoidance,
and reproduction (e.g., Huey, 1974; Grant
and Dunham, 1988; Adolph and Porter,
1993), it is possible that selection does not
favor fevers in nature. It is also possible that
the chigger mites can withstand more heat
than A. cy botes and A. armouri. Tropical
lizards such as anoles tend to exhibit low
body temperatures and heat tolerances rela-
tive to other lizard species (discussed in
Sunday et al, 2010; Araujo et al, 2013); it
is possible that a febrile response is not
effective for lizards with low heat tolerances,
such as these species (critical thermal maxi-
mum: ~ 38-40°C; Munoz et al, 2014),
although it may be possible and advanta-
geous in more heat tolerant species.

It is also possible that mite infestations do
not negatively affect lizards enough to induce
fever in A. cy botes and A. armouri. Although
some studies have found negative correla-
tions between chigger infestation and lizard
body condition (Dunlap and Mathies, 1993;

Klukowski and Nelson, 2001; Cook et al,
2013), we did not observe any correlation
between body condition and chigger infesta-
tion (Table 2). Similarly, other studies have
found no effect of E. alfreddugesi infestation
on lizard health (Garcia-De La Pena et al,
2004, 2010; Schlaepfer, 2006; Rocha et al,
2008), and others have found positive
correlations (Amo et al, 2005), suggesting
that the health effects of mite infestation may
vary among taxa. This variable response in
host health is not limited to chiggers: Even
when infected with malaria, some anole
species exhibit negative effects, whereas
others do not (Schall, 1992; Schall and
Pearson, 2000). These findings underscore
that a more comprehensive understanding of
how ectoparasites (and the pathogens they
may transmit) affect lizard health is neces-
sary for determining whether behavioral
fever should occur.

More broadly, it is still not fully un-
derstood how ectoparasite infestation should
affect lizard body condition. For example,
the detrimental effects of ectoparasites can
be inferred from both negative correlations
between body condition and mite loads
(Dunlap and Mathies, 1993; Klukowski and
Nelson, 2001; Cook et al, 2013) and from
positive correlations (e.g., Amo et al, 2005).
In the former, the reduced body condition of
infested lizards can suggest that the ectopar-
asites reduce health and immunity, as evident
in the reduced body condition, and in the
latter it is thought that parasites reduce
survival and so only the individuals with
best body condition can survive (Amo et al,
2005). Furthermore, even when negative
correlations between body condition and
parasite load are detected, they may not be
driven by the parasites inducing lizards to
lose mass. Klukowski and Nelson (2001)
found that body condition was reduced in
infested lizards because high mite loads
appeared to prevent lizards from gaining

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BEHAVIORAL FEVER IN TWO SPECIES OF ANOLE

9

mass. In short, a deeper understanding of
how ectoparasites and their associated
bloodborne pathogens influence host health
will vastly improve our predictions for how
behavioral fever should occur, if at all.

Although basking rate was uncorrelated
with parasite load, the use of sun and shade
varied considerably across elevation. Whereas
lizards near sea level spent only a small fraction
of their time perching in the sun, those found at
high elevation (Zapoten) were almost invari-
ably observed basking (Table 1), a result that
aligns with findings from previous studies on
these species (Hertz and Huey, 1981; Munoz
et al. , 2014). Prevalence was also considerably
lower at Zapoten, and most lizards harbored
fewer than 20 parasites (Fig. 3). If increased
basking frequency were associated with warm-
er core temperatures in Zapoten, then it could
be possible that fever in A. armouri reduced
ectoparasite levels. However, this is unlikely
because mean body temperature was signifi-
cantly lower in Zapoten ( X — 28.2°C) than in
Los Patos ( X = 30.9°C), suggesting that even
though they bask continually, lizards in high-
elevation populations might not always be able
to attain body temperatures comparable to
their low-elevation counterparts, let alone
behaviorally induce a fever.

The markedly low levels of infestation
intensity observed in A. armouri from Zapo-
ten appear to conflict with previous findings
on A. cybotes by Zippel et al (1996), who
found that intensity increased with elevation.
Both their study and ours were conducted in
the Sierra de Baoruco mountain chain in the
western Dominican Republic. However,
Zippel and colleagues did not sample A.
cybotes lizards above 520 m, and our transect
extended to 2,020 m. Consistent with Zippel
et al. (1996), we found that mite infestation
increased from sea level to mid-elevation, as
intensities were particularly high in the mid-
elevation populations at Guayuyal (727 m)
and Polo (1,236 m), where up to 354 and 274

ectoparasites were observed on a single lizard,
respectively (Table 1; Fig. 3). The inlestation
levels in Guayuyal and Polo are among the
highest recorded for mites on other species of
lizards (Amo et al. , 2005; Rocha et al. , 2008;
Garcia-De La Pena et al ., 2010; Delfino et al.,
2011; Ramirez-Morales et al., 2012; Cook
et al. ,2013, but see Garcia-De La Pena, 2011),
as well as for lizards with other types of
ectoparasites such as ticks (e.g., Ixodes ricinus
[Acari: Ixodidae]: Amore et al, 2007; Gryc-
zynska-Siemi^tkowska et al., 2007; Stuart-
Fox et al., 2009; Gomes et al, 2013).

Why do intensities drop so dramatically in
Zapoten? Habitat preference by E. alfreddugesi
may explain particularly low infestation levels
observed at high elevation. Previous work has
shown that chigger mites tend to prefer mesic
habitats with low-incident sunlight and mod-
erate temperatures (Clopton and Gold, 1993;
Schlaepfer and Gavin, 2001) and that parasite
intensity is typically higher in forest interiors
than in forest edges (Bulte et al, 2009; Rubio
and Simonetti, 2009). At elevations above
approximately 1,800 m in Hispaniola, anoles
tend to cluster in forest clearings and rocky
outcrops, presumably to access open basking
sites in this colder environment, where tem-
peratures can reach near freezing throughout
the year (Hertz and Huey, 1981; Munoz et al,
2014). Even contiguous forest tends to be more
open than at low elevation because the pine
forest lacks the closed canopy characteristic of
the broadleaf forest at lower elevations (Fig. 2)
(Martin et al., 2011). Thus, open habitat and
cold temperatures may prevent E. alfreddugesi
from reaching densities comparable to those
observed at lower elevations.

Although behavioral fever is likely a key
response to infection in lizards, we still know
little of how it occurs in nature. In the case of
A. cybotes and A. armouri, we did not find
evidence that lizards respond to ectoparasite
infestation through behavioral fever. It is
not fully known how these (and other)

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No. 545

ectoparasites influence their lizard hosts and
what pathogens they transmit (Amo
et al., 2005; Garrido and Perez-Mellado,
2014). A more detailed understanding of
how ectoparasites and bloodborne patho-
gens influence lizard health and how path-
ogen and host temperature tolerances differ
will lead to more detailed hypotheses about
the conditions under which we expect lizards
to exhibit behavioral fever.

ACKNOWLEDGMENTS

We thank I. Shields for assistance in the
field, the Ministerio de Medio Ambiente y
Recursos Naturales and the Museo Nacional
de Historia Natural for granting our research
permit requests, and J. Gastel, J. Losos, and
M. Johnson for helpful comments on this
manuscript. We thank two anonymous re-
viewers, who greatly improved this manu-
script. This study was conducted in accordance
with the Institutional Animal Care and Use
Committee at Harvard University under pro-
tocol 26-11. This project was completed by
Conover in partial fulfillment for the Intel
Science Talent Search through Stuyvesant
High School. Support for this work came from
a David Rockefeller Center for Latin Ameri-
can Studies Research Grant; a Ken Miyata
Award from the Museum of Comparative
Zoology; a Sigma Xi Grant-In-Aid Award to
M.M.M.; and a Beckman Scholar Award from
the Arnold and Mabel Beckman Foundation,
Sigma Xi Grant-In-Aid, and Explorer’s Club
Youth Activity Fund Grant to E.G.C. This
material is based on work supported by
National Science Foundation Graduate Re-
search Fellowships to K.E.B. and M.M.M.

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