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Museum of Comparative Zoology

US ISSN 0006-9698

CAMBRIDGE, Mass.

26 Marcu 2010

NuMBER 519

CRUISE FORAGING OF INVASIVE CHAMELEON (CHAMAELEO JACKSONII XANTHOLOPHUS) IN HAWAPI

TrRAvis J. HAGEY,! JONATHAN B. Losos,? AND LUKE J. HARMON!

ABSTRACT.

We quantified the foraging behavior of the Jackson’s chameleon (Chamaeleo jacksonii xantholophus),

an invasive insectivorous lizard 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:

Classically, lizard feeding behavior has been described in terms of foraging mode, 1.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.

foraging mode; behavior; chameleon; Hawai'i; invasive species

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; Tollestrup, 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;

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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 Hawarian 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’1, 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 TABLE |. Test Description Test Mass vs. sex/age class in C. jacksonii F-test SVL vs. sex/age class in C. jacksonii F-test PTM vs. chameleon species F-test MPM vs. chameleon species F-test

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

ANCOVA ANCOVA

F-test F-test

MPM vs. sex/age class in B. pumilum F-test PTM vs. sex/age class in B. pumilum F-test MPM and PTM in chameleons vs.

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

active foragers MANOVA MPM and PTM in chameleons vs.

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

ambush foragers MANOVA

*P < 0.05.

as perch height and diameter by climbing 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

linear regression linear regression

CHAMELEON FORAGING MODE 3

STATISTICAL TESTS, DESCRIPTIONS, AND RESULTS USED IN THIS ARTICLE.

Test Statistic P. F351 = 1.74 0.19 F309 = 1.74 0.19 Fj 49 = 0.03 0.9 Fi 49 = 6.01 0.02*

MPM = 0.59 x PTM + 0.08, 72 = 0.50 <«0.01*

MPM = 0.49 x PTM + 0.23, 7? = 0.23 0.02* Fi 4g = 25.0 <0.01* Fy a3 = 8.95 <0.01*

MPM = —0.22 x SVL + 1.23, 72 = 0.06 0.3

PTM = —0.37 X SVL + 1.90, 72 = 0.14 0.07 F353 = 1.42 0.3 F353 = 1.05 0.4

MPM = —0.18 X SVL + 1.07, r? = 0.03 0.5 PTM = 0.18 x SVL — 0.52, 7? = 0.04 0.4

Fy > = 3.21 0.07 F3>; = 1.90 0.2 Wilk’s lambda F499 = 32.1 <«K0.01* Wilk’s lambda F3.,;3 = 7.10 <0.01* Wilk’s lambda F339 = 29.3 << 0.01* Wilk’s lambda F 4g = 105 «K0.01* Wilk’s lambda F495 = 49.5 «K0.01*

(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

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Chameleo jacksonii * Chameleo jacksonii Mean © Bradypodion pumilum 4 Bradypodion pumilum Mean

oO oO

40% 50% 60% 70% 380%

Percent Time Moving

3.5 3.0 =) = Ds; PE ANE Pe) 0) ro) gS : ro) WO fe) = O 05 OG 8-0 ~ 0% 10% 20% 30% Figure 2.

Percent time moving (PTM) versus moves per minute (MPM) for Bradypodion pumilum (Butler, 2005)

and Chameleo jacksonii (this study). Species ¥ + 1 SE. Error bars present on the Y-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 + 0.4m 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 5

Ambush Foragers

® Active Foragers * Chameleo jacksonii Mean

Ww um

Moves per Minute

Oo 107%" 207% 30%

4 Bradypodion pumilum Mean

80%

70%

40% 50% 60%

Percent Time Moving

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 ¥ + 1 SE. Error bars present on the

Y-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-

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Ambush Foragers ® Active Foragers X Chameleo jacksonii Mean

ll 10

Average Speed (m/min)

Figure 4. Movement speed (AS vs. MS) for a set of lizard species (Cooper 2007) with the addition of Chameleo jacksonii (this study). Species ¥ + 1 SE. Error bars present on the Y-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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