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RE V I O R A 



jyi uiseuim oi v^onnpairaitiTe z^oology 



us ISSN 0006-9698 



Cambridge, Mass. 



26 March 2010 



Number 519 



CRUISE FORAGING OF INVASIVE CHAMELEON (CHAMAELEO JACKSONII 

XANTHOLOPHUS) IN HAWAI'I 

Travis J. Hagey,i Jonathan B. Losos,^ and Luke J. Harmon^ 

Abstract. We quantified the foraging behavior of the Jackson's chameleon (Chamaeleo jacksonii xantholophus), 
an invasive insectivorous Hzard species in Hawai'i. Using video taken in the field, we focused on percent time moving, 
moves per minute, and movement speeds. Our results supported previous findings that chameleons are "cruise 
foragers" {sensu Butler, 2005), a foraging behavior unlike almost all other species of lizards. 

Key words: foraging mode; behavior; chameleon; Hawai'i; invasive species 



Classically, lizard feeding behavior has 
been described in terms of foraging mode, 
i.e., how an animal gathers food in a 
particular environment (e.g., Huey and 
Pianka, 1981; Schoener, 1971). Foraging 
mode is an important aspect of a species' 
predator-prey interactions and can affect 
prey behavior and community structure 
(Schmitz, 2008; Simmons et al, 2005). 
Previous studies have identified two distinct 
foraging modes in lizards: active and ambush 
(sit-and-wait) foraging (Huey and Pianka, 



' Department of Biological Sciences, University of 
Idaho, PO Box 443051, Moscow, Idaho 83844-3051, 
U.S.A.; e-mail: thagey@vandals.uidaho.edu 
^ Department of Organismic and Evolutionary Biology, 
Harvard University, 26 Oxford Street, Boston, Massa- 
chusetts 02138, U.S.A. 



1981; McLaughlin, 1989; Regal, 1983; Scho- 
ener, 1971). Other researchers have suggested 
a continuum with active and ambush forag- 
ing as opposite extremes (e.g., Anderson, 
2007; Cooper, 2005, 2007; Cooper et al, 
2001; Perry, 1999; Perry and Pianka, 1997; 
ToUestrup, 1980). Evidence also suggests 
that foraging mode is retained in related 
species (Johnson et al, 2008; Perry, 1999). 
Both active and ambush foraging behaviors 
can be associated with a suite of organismal 
traits, including morphology, behavior, hab- 
itat use, and prey type (Miles et al, 2007; 
Perry et al, 1990; Vitt and Congdon, 1978). 
For example, some active foragers have 
higher activity levels, caloric intake, and 
body temperatures compared with ambush 
foragers (Anderson and Karasov, 1981; 



® The President and Fellows of Harvard College 2010. 



BREVIORA 



No. 519 




Figure 1. Adult male Chameleo jacksonii from an introduced population in Nairobi. Photo by J. B. Losos. 



Webb et al, 2003). In the absence of other 
data, foraging mode could be a useful 
indicator of other organismal traits, possibly 
even predicting the effect an invasive species 
might have on an ecosystem (Phillips et al, 
2003; Watari et al, 2008; Wiles et al, 2003). 
Chameleons have unusual morphological 
and behavioral traits (Bickel and Losos, 
2002; Burrage, 1973; Losos et al, 1993; 
Parcher, 1974; Peterson, 1984), possibly 
influencing how these predatory lizards 
gather food. Butler (2005), using behavioral 
data from a single species, Bradypodion 
pumilum, suggested chameleons be included 
in a third foraging class, "cruise forager," 
because of their unusual, slow-moving for- 
aging behavior. The term "cruise forager" 
was first suggested by Regal (1978) as an 
intermediate stage between active and am- 
bush foraging, "a species that moves, stops, 
and merely scans the environment, then 
moves, stops, and scans, and so on" (Regal, 
1983, p. 114). In this study, we quantify a 
second chameleon species' foraging behav- 
ior, the Hawai'ian invasive Chamaeleo jack- 
sonii. We make comparisons to B. pumilum 



and other lizard species to investigate wheth- 
er chameleons do exhibit a novel hunting 
strategy (Butler, 2005). 

MATERIALS AND METHODS 

Jackson's chameleon, Chameleo jacksonii 
xantholophus (Fig. 1), was originally intro- 
duced into Hawai'i in 1972 from Mt. Kenya, 
Kenya, as a result of the pet trade. This 
species has since reached the islands of Oahu, 
Maui, Hawai'i, and Kauai and is typically 
found in disturbed habitats (Eason et al, 
1988; McKeown, 1991; Waring, 1997). 

We observed adult C. jacksonii individuals 
from 3 to 21 August 2001, in the countryside 
near the town of Makawao on the Hawai'ian 
island of Maui. Chamaeleo jacksonii were 
located using a haphazard search method 
only on sunny days and observed from the 
ground using a standard video recorder for 
approximately 30 min. Individuals were not 
disturbed before or during the observation. 
After the video data were gathered, we 
captured each subject when possible and 
noted sex, snout-vent length (SVL), and 
mass and measured habitat parameters such 



2010 



CHAMELEON FORAGING MODE 



Table 1 . Statistical tests, descriptions, and results used in this article. 



Test Description 



Test 



Test Statistic 



Mass vs. sex/age class in C. jacksonii 
SVL vs. sex/age class in C jacksonii 
PTM vs. chameleon species 
MPM vs. chameleon species 
MPM vs. PTM in C. jacksonii 
MPM vs. PTM in B. pumilum 
MPM vs. PTM 
MPM vs. chameleon species 
MPM vs. SVL in C. jacksonii 
PTM vs. SVL in C jacksonii 
MPM vs. sex/age class in C. jacksonii 
PTM vs. sex/age class in C. jacksonii 
MPM vs. SVL in B. pumilum 
PTM vs. SVL in B. pumilum 
MPM vs. sex/age class in B. pumilum 
PTM vs. sex/age class in B. pumilum 
MPM and PTM in chameleons vs. 

active vs. ambush foragers 
MPM and PTM in chameleons vs. 

active foragers 
MPM and PTM in chameleons vs. 

ambush foragers 
MS and AS in active vs. ambush foragers 
MS and AS in C jacksonii vs. active vs. 

ambush foragers 



F-test 

F-test 

F-test 

F-test 

linear regression 

linear regression 

ANCOVA 

ANCOVA 

linear regression 

linear regression 

F-test 

F-test 

linear regression 

linear regression 

F-test 

F-test 

MANOVA 

MANOVA 

MANOVA 
MANOVA 

MANOVA 



F3,2i = 1.74 




0.19 


F3.22 = 1-74 




0.19 


F,,49 = 0.03 




0.9 


F,,49 = 6.01 




0.02* 


MPM = 0.59 X PTM + 0.08, r'- = 


= 0.50 


«0.01* 


MPM = 0.49 X PTM + 0.23, r'- = 


= 0.23 


0.02* 


F,.48 = 25.0 




<0.01* 


F,.48 = 8.95 




<0.01* 


MPM = -0.22 X SVL + 1.23, r^ 


= 0.06 


0.3 


PTM = -0.37 X SVL + L90, r^ = 


= 0.14 


0.07 


F,,23 = 1.42 




0.3 


F3,23 = 1.05 




0.4 


MPM = -0.18 X SVL + 1.07, r'- 


= 0.03 


0.5 


PTM = 0.18 X SVL - 0.52, r^ = 


0.04 


0.4 


F2,2i = 3.21 




0.07 


F2,2i = 1.90 




0.2 


Wilk's lambda F4,9o = 32.1 




«0.01* 


Wilk's lambda F2, 13 = 7.10 




<0.01* 


Wilk's lambda F2,32 = 29.3 




«0.01* 


Wilk's lambda F2,48 = 105 




«0.01* 



Wilk's lambda F4,96 = 49.5 



«0.01* 



*F < 0.05. 



as perch height and diameter by cUmbing 
trees or using a long pole with calibrated 
markings. We then released the animal at the 
site of capture. To estimate movement 
distances, we used the animal's snout-vent 
length (SVL). Chameleons were marked with 
nontoxic paint to prevent observation of the 
same individual more than once. 

We used the recorded videos to quantify 
each individual chameleon's foraging behav- 
iors. We counted all behaviors (e.g., move- 
ments, position adjustments, displays, and 
eating events; see Butler, 2005) and noted the 
amount of time to complete each task. With 
these values, we calculated the number of 
moves the animals made per minute (MPM), 
percent time the animal spent moving 
(PTM), position adjustments per minute 
(PAPM), percent time adjusting position 



(PTAP), and number of eating events per 
hour (EPH). Movements were defined as any 
event in which there was physical displace- 
ment of the animal's body. We used the 
video in conjunction with our habitat mea- 
surements to calculate two different mea- 
surements of speed: moving speed (MS) and 
mean or average speed (AS; see Cooper, 
2007). Moving speed represents the speed of 
the animal while it was actually moving, 
analogous to instantaneous speed (distance 
moved, taken from habitat measurements, 
divided by the length of time required to 
complete the movement, calculated by 
counting frames in the videotapes). Mean 
speed was calculated by adding the entire 
distance moved during the observational 
period divided by the length of the observa- 
tional period. These values were compared 



BREVIORA 



No. 519 



CU 
■»-• 

Z5 



CD 
Q. 
on 
CU 
> 
O 



3.5 - 

3.0 - 

2.5 - 

2.0 - 
1.5 

1.0 - 

0.5 - 

0.0 ®^' 
0% 



10% 



A Q 



E Chameleo jocksonii 

X Chameleo jocksonii Mean 

o Bradypodion pumilum 

A Bradypodion pumilum Mean 



CP 



S 



20% 30% 40% 50% 
Percent Time Moving 



60% 70% 80% 



Figure 2. Percent time moving (PTM) versus moves per minute (MPM) for Bradypodion pumilum (Butler, 2005) 
and Chameleo jacksonii (this study). Species A' ± 1 SE. Error bars present on the F-axis are obscured by 
point markers. 



with data from Cooper's (2007) literature 
review of lizard speeds for 51 species. All 
variables were natural log or arcsine trans- 
formed for normality before statistical anal- 
yses. We compared our calculated behavior 
parameters to data from two previous studies 
(Butler, 2005; Cooper, 2007). 

RESULTS 

All values presented are means plus or 
minus standard errors. We collected data on 
27 chameleons: 14 males, 12 females, and 
two juveniles with mean male SVL 106.5 ± 
6.3 mm, mean mass 37.2 ± 7.1 g; mean 
female SVL 107.5 ± 6.6 mm, mean mass 
43.9 ± 10.0 g; mean juvenile SVL 77 ± 
1.0 mm, mean mass 12 ± 1.0 g. Neither mass 
nor SVL was dependent on sex/age class 
(Table 1). Chamaeleo jacksonii perched 4.5 ± 
0.4 m off the ground on 2.42 ± 0.57 cm 
perches, adjusted position 0.22 ± 0.04 times 
per minute, spent 4.75 ± 0.99% of their time 



adjusting position, and ate 1.85 ± 0.53 times 
per hour. We did not observe any display 
events. 

PTM and MPM values were similar 
between C jacksonii (PTM = 19.7% ± 
4.0%, MPM = 0.24 ± 0.05) and B. pumilum 
(PTM = 20.8% ± 4.1%, MPM = 0.44 ± 
0.07, data from Butler, 2005; Fig. 2), al- 
though values varied greatly among individ- 
uals. Chamaeleo jacksonii did, however, 
move significantly less often than B. pumilum 
(Table 1). In both species, MPM was posi- 
tively correlated with PTM (Table 1; species 
X PTM interaction term not significant, P = 
0.65, and omitted from analysis). Neither 
MPM nor PTM was significantly dependent 
on SVL or sex/age class in both C. jacksonii 
and B. pumilum (Table 1). 

Chameleons are distinct from a range of 
other active and ambush foraging lizard 
species both in regard to MPM and PTM 
(Fig. 3, Table 1; data from Butler, 2005). We 
also compared moving speed and mean 



2010 



CHAMELEON FORAGING MODE 





3.5 


0) 




Z5 


3 


C 


2.5 


i~. 


7 


(D 




Q. 


1.5 


en 






> 


1 


O 






0.5 











^ Ambush Foragers 

• Active Foragers 

X Chameleojacksonii Mean 

^ Bradypodion pumilum Mean 






0% 10% 



<>• 

• 


• 


• 


. ^^-^^ 




1 

20% 


1 1 1 

30% 40% 50% 
Percent Time Moving 



60% 70% 80% 



Figure 3. Percent time moving (PTM) versus Moves Per Minute (MPM) for a variety of lizard species including 
Bradypodion pumilum (Butler 2005) and Chameleo jacksonii {this study). Species X ± 1 SE. Error bars present on the 
F-axis are obscured by point markers. 



speed (see Methods) for C. jacksonii (MS = 
0.33 ± 0.09 m/min, AS = 0.052 ± 0.01 m/ 
min; Fig. 4) and found, in agreement with 
Cooper (2007), that active foragers display a 
slightly lower moving speed and much higher 
mean speed (Table 1). Again, chameleons 
seem to represent a foraging mode substan- 
tially different from the standard lizard 
foraging categories (Table 1). 

DISCUSSION 

Our data suggest that C. jacksonii exhibits 
a moderate percent time moving, low moves 
per minute, and a very slow locomotion 
speed. This combination of parameter values 
is rarely seen in other lizard species and is 
strikingly similar to data from the only other 
chameleon studied, B. pumilum (Butler, 
2005). Although only two chameleon species 
have been evaluated, many lizard clades 
show little variation in foraging mode, which 



suggests that chameleons as a group might 
exhibit a unique foraging style (Perry, 2007). 
Our data support Butler's (2005) suggestion 
that chameleons be classified as cruise 
foragers. Interestingly, a second genus of 
lizards, Chamaeleolis, which lies phylogenet- 
ically with the Anolis clade and is only 
distantly related to chameleons (Townsend 
et al, 2004), might exhibit similar behavior 
(Leal and Losos, 2000). 

The morphology of chameleons is highly 
divergent from nearly all other species of 
lizards. This unique morphology may have 
facilitated a novel hunting strategy not used 
by other predators. Thus, one might expect 
chameleons to have distinct effects on prey 
behavior and their surrounding communi- 
ties, a point to consider when evaluating 
native as well as introduced ecosystem 
interactions. More research is necessary to 
better understand the implications of cha- 
meleons' novel morphological and behavior- 



BREVIORA 



No. 519 



"D 
OJ 

CD ,— . 
Q. C 

00 ^ 

I E 

o 



100 n 



10 1 



^ 1 - 



0.1 



^Ambush Foragers 

• Active Foragers 

X Chomeleo jocksonii Mean 












O^ 



oO <|^ 






h-Kh 



0.01 



0.1 1 

Average Speed (m/min) 



10 



Figure 4. Movement speed (AS vs. MS) for a set of lizard species (Cooper 2007) with the addition of Chameleo 
jacksonii (this study). Species X ± 1 SE. Error bars present on the F-axis are obscured by point markers. 



al adaptations, as well as the ramifications of 
chameleons' foraging mode on their sur- 
rounding community structure. 

ACKNOWLEDGMENTS 

We thank F. Kraus and A. Lyons for help 
in the field; G. Perry, H. Hoekstra, and one 
anonymous reviewer for comments on the 
manuscript; and M. Butler for helpful 
advice, comments on the manuscript, and 
providing her data on chameleon behavior. 

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