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Antipredator Responses by Texas Horned Lizards to TwoSnake Taxa with Different Foraging and Subjugation StrategiesAuthor(s): Wade C. SherbrookeSource: Journal of Herpetology, 42(1):145-152. 2008.Published By: The Society for the Study of Amphibians and ReptilesDOI: http://dx.doi.org/10.1670/07-072R1.1URL: http://www.bioone.org/doi/full/10.1670/07-072R1.1

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Antipredator Responses by Texas Horned Lizards to Two Snake Taxawith Different Foraging and Subjugation Strategies

WADE C. SHERBROOKE1

Southwestern Research Station, American Museum of Natural History, Portal, Arizona 85632, USA;

E-mail: wcs@amnh.org

ABSTRACT .—The discrimination ability of Texas Horned Lizards (Phrynosoma cornutum) during

antipredator responses was tested with snakes of two genera having distinctly different prey foraging and

subjugation strategies; Western Diamondback Rattlesnakes (Crotalus atrox) are ‘‘sit-and-wait’’ predators

with a venomous strike from ambush, whereas whipsnakes (Masticophis spp.) are nonvenomous, rapid

pursuit-and-grasp predators. Neither snake constricts prey; both ingest prey whole. Lizards were watched for

reactions during close approaches by moving snakes. All unapproached and some approached lizards

remained alert and motionless. Approached lizards that reacted either (1) ran rapidly to a distant point in the

large enclosure, or (2) maintained their position but dorsoventrally flattened their body and tilted their

stance, orienting a ‘‘dorsal shield’’ posture toward the snake. The distinctly contrasting responses of the

lizards to the two snakes were significantly different, relocation running from rattlesnakes and stationary-

body reorientation toward whipsnakes. For slow-running, broad-bodied Texas Horned Lizards, running is

an appropriate escape response to a nonpursuing venomous predator, whereas the nonrunning body-

conformation/orientation change is an appropriate defensive response, advertising size and spiny defenses,

to a rapid-pursuit snake that must grasp prey with its jaws to effect capture and subjugation. Apparently

horned lizards visually recognized, probably innately, the two snake taxa as different categories of predator

threat.

The outcomes of predator-prey interactionsare significant selective forces in the evolutionof behavioral responses, both of predators andtheir prey (Lima and Dill, 1990; Abrams, 2000).Predation has been discussed as having sequen-tial components, actions (predators) and reac-tions (prey), by various authors (Edmunds,1974; Curio, 1976; Endler, 1986, 1991; Caro,2005). In sequence, predators must (1) encoun-ter, (2) detect, (3) identify, (4) approach, (5)subjugate, and (6) consume prey for predationto be successful. A wide variety of defensivetactics at each attack stage are used by preyspecies to successfully thwart predation at-tempts and enhance survival (Endler, 1986,1991; Caro, 2005). To maximize chances ofescape, prey would be well served to correctlyidentify predator categories so as to employdeterrence strategies, be they general (earlysequence, crypsis) or narrow (late sequence,chemical resistance to subjugation by a specificpredator), that are most successful with thecapabilities of particular predators at an appro-priate stage(s) of the predator-prey sequence.

In this paper, I consider the responses ofa single prey species, the Texas Horned Lizard(Phrynosoma cornutum) to two predatory snake

types (genera), one a venomous sit-and-wait(ambush) predator (Crotalus; Secor, 1995), hereexemplified by the Western DiamondbackRattlesnake (Crotalus atrox), and one a pursuitforager that subjugates prey by jaw grasping(Masticophis: Ruben, 1977; Jones and Whitford,1989; Stebbins 2003), here exemplified by twowhipsnakes (Masticophis flagellum and Mastico-phis bilineatus). Snakes in these two generaexhibit body-form characteristics (heavy-bodiedvs. slim-bodied; wide head vs. slender head)that are correlated with their divergent foragingstrategies and prey-subjugation skills (venom-ous strike vs. nonvenomous jaw capture; Poughand Groves, 1983; Cundall and Greene, 2000).

Considerable evidence exists demonstratingthat both Crotalus and Masticophis consumehorned lizards, a genus of 13–17 species(Hodges and Zamudio, 2004; Leache andMcGuire, 2006), including Texas Horned Liz-ards (Pianka and Parker, 1975; Beavers, 1976;Tyler, 1977; Whiting et al., 1992). Horned lizardshave a diverse array of defensive strategies(Pianka and Parker, 1975; Sherbrooke, 2003).Their cranial horns are raised when touchedand in response to attacks by some snakes(Sherbrooke, 1987; W. C. Sherbrooke and C. J.May, unpubl. data), thus visually presenting tosnakes structures that are potentially lethal oningestion (Speed and Ruxton, 2005). Lacking theability to dismember prey, prey size becomes

1 Present address: 3040 South Donald Avenue,Tucson, Arizona 85735, USA

Journal of Herpetology, Vol. 42, No. 1, pp. 145–152, 2008Copyright 2008 Society for the Study of Amphibians and Reptiles

a significant issue during prey selection forsnakes with limited jaw gape and esophagealpassage (Cundall and Greene, 2000). Unsuccess-ful predation following initial ingestion of TexasHorned Lizards has resulted in the deaths ofboth Western Diamondback Rattlesnakes andCoachwhips (M. flagellum), with lizard hornspenetrating postcranial tissues of the snake andpreventing further ingestion or regurgitation(Sherbrooke, 1981, 2003).

Examples of early identification of predatorcategory during predator-prey sequence en-counters and execution of appropriate antipred-ator behaviors are largely confined to alarmcalls of mammals and birds, facilitated by theirvocalizations and social interactions duringinitial detection of predators (Curio, 1975;Hirsch and Bolles, 1980; Seyfarth et al., 1980;Pereira and Macedonia, 1991; Greene andMeagher, 1998; Templeton et al., 2005). Califor-nia Ground Squirrels (Spermophilus beecheyi;Hennessy and Owings, 1978) differentiate be-tween predatory snakes (Crotalus viridis andPituophis melanoleucus), as apparently do Black-Tailed Prairie Dogs (Cynomys ludovicianus; Ow-ings and Loughry, 1985). In squamates, wherecommunication of predator threat to conspeci-fics is often unlikely, specificity of predatorcategorization is more likely to be detected bycorrelation of different individual defensiveresponses to predators having distinct prey-capture skills. Most studies have been confinedto snake or lizard detection and differentiationof snake odors prior to visual encounter (Thoenet al., 1986; Greene, 1994; Downes and Shine,1998; Bealor and Krekorian, 2002).

In this study, I focus on asking: Are TexasHorned Lizards able to distinguish between twoof their known predators, Western Diamond-back Rattlesnakes and whipsnakes? I attempt toevaluate their ability to do so by means ofdetermining whether they have different re-sponses to the two predators during visualencounters. Also, I predict that any differentresponses of the lizards will be appropriate tothe predatory skills of the respective categoriesof snakes.

MATERIALS AND METHODS

Adult male and female P. cornutum (N 5 68)were collected in Cochise County, Arizona, andHidalgo County, New Mexico (Sherbrooke,2002). They were maintained in large outdoorenclosures and watered and fed harvester ants(Pogonomyrmex spp.) and crickets (Sherbrooke,1990a, 1995). Large Crotalus atrox (N 5 19), onloan from B. Tomberlin (Hatari Invertebrates,Portal, AZ), were maintained in other largeoutdoor enclosures where experiments were

also conducted, as were Masticophis. Small C.atrox (N 5 9) were collected in the countiesindicated above and were maintained in smalleroutdoor enclosures prior to testing in the largerenclosures. Masticophis flagellum, Coachwhip, (N5 5) and M. bilineatus, Sonoran Whipsnake, (N5 2) were collected in the same counties (andOtero County, NM).

In 1993, the mean snout–vent length (SVL) ofthe P. cornutum was 83.6 6 5.6 mm (mean 6 1S.D., range 71–95), and in 1994, the mean SVLwas 80.5 6 7.4 mm (range 57–98). The meanSVL of large C. atrox was 135.7 6 11.6 cm (range110–162 cm), and mean SVL of small C. atroxwas 82.7 6 9.9 cm (range 63–94 cm). Mean SVLof Masticophis spp. was 93.6 6 11.8 cm (range78–109). Two species of Masticophis were usedbecause of the limited number of individualsavailable of any one species and because of theirbehavioral similarities as predators. The Masti-cophis exhibited greater individual levels ofactivity, frequent movements, around the trialenclosure than did the large Crotalus. AllCrotalus experiments were conducted in 1993(large, 20–28 July; small, 5–7 August), approx-imately 1600–1700 h. All Masticophis experi-ments were conducted in 1994 (29 Augustthrough 2 September), approximately 0930–1130 h. Temperatures during trials were asfollows: large Crotalus 28–31uC, small Crotalus23–25uC, and Masticophis 27–29uC. Live snakeswere used in trials because models would nothave exhibited the proper locomotor andapproach patterns necessary for causing thelizards to switch from their primary immobilitydefense to secondary defensive behaviors.

All trials (N 5 20) were conducted in theAnimal Behavior Observatory of the Southwest-ern Research Station (1,620 m elevation), Amer-ican Museum of Natural History, Cave CreekCanyon, Chiricahua Mountains, Cochise Coun-ty, Arizona. Experimental enclosures were 7 mlong, 3.8 m wide, and 2.4 m high, with a view-ing hide (with one-way mirrored observation-windows) at the south end. The lower walls ofthe experimental enclosures were internallycovered by sheet metal from ground level(sandy soils) to 60 cm. Above, the interior ofthe cage (walls and top) was covered withaviary wire (galvanized, 1.5 3 2 cm). Exteriorlythe cage was covered with welded wire (1 32.5 cm); the two-layer wire walls were 13 cmapart, preventing access of predators. In theMasticophis experiments, an additional layer ofwindow screening was added above the galva-nized metal to the interior aviary wire surfacefor 91 cm above the sheet metal to prevent thesesnakes from penetrating the aviary wire.

Trials with large Crotalus and Masticophis (N5 7 and 10, respectively) were all conducted

146 W. C. SHERBROOKE

with four P. cornutum in the experimentalenclosure that housed the snakes. Individualhorned lizards were used only in a single trial.For visual identification, each lizard wasmarked with a small piece of plastic tape, ofdistinctive color (5 3 10 mm), folded around itstail and joined above as a tiny flag. Narrowlengths of wood 30 cm long were placed in thecage to help estimate approach distances ofsnakes to lizards. Trials (N 5 3) with smallCrotalus were conducted with 22 lizards (6 or 8/trial) previously run in trials with large Crotalus.The purpose of the small Crotalus trials was toattempt to control for size difference betweenlarge mass Crotalus and the smaller massMasticophis. In trials using four or more lizards,each lizard is considered an independentstatistical unit because the species is not highlysocial, individuals were widely spaced, andlizards failed to exhibit any interactions.

All trials lasted 1 h and were initiated when Iplaced the lizards in the cage with the desig-nated group of snakes and exited to makeobservations from the hide windows. Myactivity in leaving the cage frequently causedthe lizards to run, following which they froze inplace where they remained, apparently inresponse to observing the presence of thesnakes. With very few exceptions, they re-mained motionless thereafter throughout thetrial unless provoked to activity by the close(,30–50 cm) approach of a snake that wasactively exploring the cage. Lizards were neverstalked nor attacked, and with some frequency,the lizards failed to respond to an approachingsnake even when snakes passed over lizards.Note was made only of responses involvingmovements by the lizards to closely approach-ing snakes. Two classes of response wererecorded: (1) a relocation run (always overa meter and usually to a far end of the cage);and (2) a stationary-body reorientation of thebody posture (usually involving raising the farside of the abdomen from the approachingsnake and lowering the near side or reorienting

the head to bring the cranial horns toward theapproaching snake). This body reorientationresembles a ‘‘dorsal shield’’ defensive displaynoted in predator-prey interactions with Great-er Roadrunners (Geococcyx californianus; Sher-brooke, 1990b), Southern Grasshopper Mice(Onychomys torridus; Sherbrooke, 1991), andLong-Nosed Leopard Lizards (Gambelia wislize-nii; unpubl. data). Horned lizard responses tosnakes were viewed and recorded directly fromvisual observations. During trials, lizards failedto show any signs of distress following eitherrunning responses, after which they resumeda position flattened against the substratum, orfollowing reorientation responses, after whichthey resumed their former substrate-flattenedimmobile stance.

Chi-square analyses (Zar, 1999) were used tostatistically determine whether the responses tothe two snakes were different. Means are given6 1 S.D.

RESULTS

Of 28 lizards, only one did not react inresponse to the large Western DiamondbackRattlesnakes. The other 27 lizards respondedwith a relocation run as their first response to anapproaching rattlesnake (Table 1). These lizardscontinued to respond similarly (total relocationruns 5 135, mean 5 5.0 6 2.8 lizard21, range 1–11), except for one individual who, amongseven responses (its final two), exhibited twoweak stationary-body reorientations (Table 1).

In whipsnake trials, all 40 lizards respondedat least once, with first responses of 35 lizardsexhibiting stationary-body reorientations andfive exhibiting relocation runs (Table 1). Of thefive lizards that ran as a first encounter re-sponse, all five subsequently reacted to whip-snake approaches with stationary-body reorien-tations. Only one lizard responded witha relocation run after having already respondedwith an initial stationary-body reorientation,and it only did this in one of three responses. Of

TABLE 1. Numbers of relocation runs and stationary-body reorientations as first responses, and total trialnumber of these responses in ( ) in the table below, by Texas Horned Lizards (Phrynosoma cornutum) toapproaching (1) large Western Diamondback Rattlesnakes (Crotalus atrox), (2) whipsnakes (Masticophis spp.), or(3) small Western Diamondback Rattlesnakes. First responses, relocation runs versus stationary-bodyreorientations, by Texas Horned Lizards are significantly different (P , 0.001) for both categories ofrattlesnakes compared to whipsnakes but are not significantly different between the small and large rattlesnakes.

Texas Horned Lizard responses—first (all)

Approaching predator Horned lizards (N 5 ) Relocation runsStationary-bodyreorientations Total responses

(1) Rattlesnakes (large) 28 27 (135) 0 (2) 27 (137)(2) Whipsnakes 40 5 (6) 35 (208) 40 (214)(3) Rattlesnakes (small) 22 15 (22) 0 (0) 15 (22)

HORNED LIZARD RESPONSES TO SNAKE PREDATORS 147

the total lizard responses during the trials (214),there were 208 stationary-body reorientations(mean 5 5.2 6 4.3 lizard21, range 1–20) and sixrelocation runs (Table 1).

In trials with small Western DiamondbackRattlesnakes all responding lizards exhibitedrelocation runs (15 for first responses, 22 fortotal responses; mean 5 1.5 6 0.7 lizard21,range 1–3), with no stationary-body reorienta-tions. Seven lizards did not exhibit responsesin these categories but remained immobile(Table 1).

Comparing the lizards’ first responses to thelarge Crotalus and to the Masticophis, there wasa highly significant difference (X2

1 5 49.91;P , 0.001). Comparing the lizards’ first re-sponse to the small Crotalus and to the Mastico-phis, again there was a highly significant differ-ence (X2

15 32.41; P , 0.001). Chi-square com-parisons between first responses of lizards tolarge and small Crotalus were not used becauseall responses were runs (no differences betweenthe two groups).

DISCUSSION

Statistical analyses of trial results providea clear indication that the antipredator re-sponses of Texas Horned Lizards (P. cornutum)to two different categories of predatory snakes(C. atrox and Masticophis spp.) are distinct. Thisconfirms the hypothesis that this prey species isable to distinguish differences between twosnakes, one venomous and one nonvenomous,with a high degree of fidelity.

An explanation as to how the lizards are ableto differentiate the two snakes, and the breadthof characteristics used for those identificationcategories (be they morphological, based onpossession of venom, or otherwise) is notreadily apparent. Texas Horned Lizards arethought to use visual cues to distinguish KitFoxes (Vulpes macrotis), to which they respondwith a blood-squirting, chemical defense that isalso employed with other canids (Sherbrookeand Middendorf, 2001, 2004; Sherbrooke andMason, 2005). Similarly, vision may be used todistinguish the two snake categories. Use of thetongue, for taste or trigeminal chemoreceptors,or vomeronasal organs (Schwenk 2000), todistinguish between the two snakes, is possible(as shown in other lizard studies involvingnonvisual encounters; Thoen et al., 1986;Downes and Shine, 1998; Bealor and Krekorian,2002) but seems unlikely in this study. Lizardsnever tongue flicked the air or substratumduring the trials. Also, although P. cornutumare highly accurate during prehension of antprey with their tongue (Ott et al., 2004), andapparently receive chemical cues regarding

sexual status from other individuals by tonguesampling of anal scales (Tollestrup, 1981), theydo not normally sample the environment fortongue or vomero-nasal chemoreception as dosome other lizards and snakes (Schwenk, 2000;pers. obs.). Also, because of the usually sparseoccurrence of these lizards across the land-scapes they inhabit, and their presumed in-frequent social contacts (Munger, 1984; Sher-brooke, 2002), it seems unlikely that the lizardslearn antipredator responses to different cate-gories of snakes from observations of conspe-cifics. Therefore, I conclude that the abilityexhibited by Texas Horned Lizards to differen-tiate the two snakes in these trials was mediatedby visual identification and that this ability ofpredator categorization is innate.

Sensory-systems collected and nervous-system processed information about potentialpredators should allow prey to employ preda-tor-specific escape strategies that enhance theirprobability of successfully avoiding death whenchallenged by predators having specific anddifferent attack-subjugation abilities. Thus, thekey to prey survival in many predator-preyencounters is (1) accurate predator identifica-tion or categorization and (2) linked responsepatterns that are appropriate to the abilities andlimitations of particular predator types. Suchinformation processing and decision-makingmechanisms involving learned or innate behav-ioral responses to predators reflect fundamentalcomponents of the prey’s cognitive skills (Ka-valiers and Choleris, 2001).

Texas Horned Lizards die from WesternDiamondback Rattlesnake envenomation (un-publ. data). Running from the proximity ofa rattlesnake allows a lizard to disengage froma predator-prey interaction. The swift actionrisks little chance of attack (strike) becauserattlesnakes do not use pursuit and jaw-medi-ated subjugation for prey capture. In trials,Texas Horned Lizards responded 159 times toapproaches by Western Diamondback Rattle-snakes (large and small). In 157 responses(99%), the lizards ran and in only two casesdid a lizard remain in place and alter bodyorientation. This suggests that in the rattlesnaketrials the lizards consistently exhibited a behav-ioral response that had a high likelihood ofresulting in successful escape from a specificlife-threatening encounter, rattlesnake enveno-mation.

Although horned lizards easily outdistancenonpursuing rattlesnakes, their speed is rela-tively slow compared to a whipsnake (Piankaand Parker, 1975; Bonine and Garland, 1999).Therefore, during a visual encounter betweena whipsnake and a Texas Horned Lizarda running escape by the lizard is unlikely to

148 W. C. SHERBROOKE

greatly reduce its risk of capture. Flight oftenelicits chase in pursuit predators (Cyr, 1972).The snake is likely to pursue and grasp thelizard’s dorsoventrally flattened body betweenits upper and lower jaws, thus effecting efficientprey capture. In contrast, if the lizard remains inposition, there is no chase, and the predatorremains in the lizard’s view, and vice-versa.Then, by altering its body position in relation tothe snake’s head (with its eyes and jaws), thelizard is able to bring several aspects of itsdefenses into position such that it might displaythem to the predator and enhance its probabilityof survival. Raising the distant side of its bodyfrom the substratum, while lowering the sidenearest the snake, enhances the lizard’s appar-ent-size as does the rotation of its ribs forwardto spread and widen its back. This dorsal-shieldposturing, visually enhanced by the enlargedlateral-fringe scales, which are jaggedly ar-ranged down both sides of the lizard’s body(Sherbrooke, 2003), and motion generated bybackward and forward rocking, visually presentthe predator with potential prey capture, sub-jugation and ingestion problems (Taylor et al.,2000). Additionally, the change in prey body-orientation, from a horizontal to a near verticalsurface is inhibitory of horizontal jaw opening/grasping by a whipsnake for effective preycapture. One adult Sonoran Whipsnake, videorecorded in captivity, was unable to grasp anadult Texas Horned Lizard displaying a dorsal-shield defense (repeatedly rocking anteriorly/posteriorly about once per second) and ceasedits efforts after five jaw grasping attempts failedover 40 sec (unpubl. data.)

The snake’s view is of a broadly oval prey oflarge cross-sectional diameter, a considerationin swallowing for a predator unable to dismem-ber its prey (Cundall and Greene, 2000). Thesnake is also presented with a view of thelizard’s prominent cranial horns protrudingfrom the rear and sides of its head and aboveits eyes, another aspect of the prey’s defensesthe snake may use in selecting appropriate preyfor swallowing (Inbar and Lev-Yadun, 2005;Speed and Ruxton, 2005). Prey ingestion bysnakes is usually from the head end (de Queirozand de Queiroz, 1987; Cundall and Greene,2000). Thus, by remaining in position for anencounter with certain predators, a hornedlizard is able to effect prominent display of itsdefensive morphology (Taylor et al., 2000;Speed and Ruxton, 2005), features not aseffectively displayed during an attempted run-ning escape.

In this study, Texas Horned Lizards re-sponded 214 times to approaches by whip-snakes. In 208 responses (97%), the TexasHorned Lizards responded by remaining in

place and changing their body conformationand orientation in relationship to the approach-ing/passing snake. This suggests that in whip-snake trials lizards consistently exhibited be-havioral responses that enhanced their ability tothwart the prey capture, subjugation and in-gestion abilities of the whipsnakes. Concomi-tantly, they refrained from responding witha running escape that may have had a lowerlikelihood of successful escape.

Given the distinctly different nature of thethreats presented by the two snakes (Crotalusand Masticophis), and the apparent appropriate-ness of the lizard’s responses to each predationscenario, I conclude that the lizards behaviorallyrespond to each threat in a manner thatenhances the likelihood of their survival. Addedto the blood-squirting defense used effectivelyin response to attacks by canids (Sherbrookeand Middendorf, 2001, 2004; Sherbrooke andMason, 2005), Texas Horned Lizards are knownto identify three distinct categories of predatorsand employ specific defenses during the latterstages of predator-prey sequences to enhancesurvival. The blood-squirting defense is notused during encounters where it would beentirely ineffective, with Greater Roadrunners(Geococcyx californianus; Sherbrooke, 1990b),Southern Grasshopper Mice (Onychomys torri-dus; Sherbrooke, 1991), Long-Nosed LeopardLizards (Gambelia wislizenii; unpubl. data), orrattlesnakes and whipsnakes (Crotalus atrox andMasticophis spp.; this study).

Pianka and Parker (1975) proposed a numberof morphological, physiological, and behavioralchanges that have led to the evolution of thedistinctive features of the genus Phrynosoma,a genus of ant-feeding specialists. These fea-tures include a dorsoventrally flattened body,short legs and slow locomotion, reliance onimmobility and camouflage in the presence ofpredators, cranial horns, and spiny scales. Lossof a generalized broadly effective (with manycategories of predators) high-speed runningescape, such as is found in horned lizards’closest living relatives the sand lizards (Hodgesand Zamudio, 2004; Leache and McGuire, 2006),has probably limited the effectiveness of thisantipredator strategy by horned lizards to fewerpredator categories, such as rattlesnakes. Thestationary-body reorientation (dorsal-shield)defense employed with whipsnakes, and widelyused with other predators (Sherbrooke, 1990b,1991, 2003, unpubl. data), has probably evolvedwith other benefits of dorsoventral flattening inthe genus (Heath, 1965; Pianka and Parker,1975; Sherbrooke, 1990a, 2003).

As with Texas Horned Lizards, Regal HornedLizards (Phrynosoma solare) usually run whenconfronted by a Western Diamondback Rattle-

HORNED LIZARD RESPONSES TO SNAKE PREDATORS 149

snake (W.C. Sherbrooke and C. J. May, unpubl.data). Thus, two similar-sized horned lizards,Texas and Regal, have essentially identicalresponses to Western Diamondback Rattle-snakes. But when confronted by whipsnakes,Regal Horned Lizards rapidly execute a full-body flip and immobility, a behavior thatappears to be an exaggerated form of thestationary-body reorientation that is used byTexas Horned Lizards. Both stationary defen-sive-displays have much in common, present-ing the targeted predator with visual images ofmorphological features (horns, spines, wide-diameter body, rigidly displayed appendages)that are inhibitory and dangerous during thesubjugation/consumption stages of predator/prey sequences involving gape-limited preda-tors (Taylor et al., 2000; Speed and Ruxton, 2005;Honma et al., 2006; Ruxton, 2006).

Cranial horns on horned lizards may haveevolved to their current forms (variable indifferent species: Sherbrooke, 1981, 2003; Leacheand McGuire, 2006) largely to address threatsfrom predators like snakes that ingest preywhole (Cundall and Greene, 2000). Horns mayfunction as both primary and secondary de-fenses, essentially self-advertising honest sig-nals of physical threat (Ruxton et al., 2004; Inbarand Lev-Yadun, 2005; Speed and Ruxton, 2005;Broom et al., 2006).

Young et al. (2004) have shown that predationlevels by raptorial Loggerhead Shrikes (Laniusludovicianus), which eviscerate horned lizards,are reduced on individual Phrynosoma mcalliihaving longer horns that appear to play a role ininterference with prey subjugation (Yosef, 2004).Thus, selective pressure by both snake andavian predators (whole-prey and dismember-ing-prey consumers) may have contributed tohorn elongation by enhancing survival duringresistance to subjugation and ingestion phasesof predation and by enhancing the visualimpact on decisions by these predators as towhether to attack (Taylor et al., 2000; Speed andRuxton, 2005).

Apparently, horned lizards do not have anyspecialist predators whose diets are highlydependent on them (Sherbrooke, 2003). Never-theless, even with a presumed lower intensity ofnatural selection by any specific predatorcategory, such as might be found in tightlyevolved predator-prey coevolution, they haveevolved predator identification/categorizationskills that have led to distinct antipredatorresponses to a diversity of predator threats.

Acknowledgments.—I thank C. J. May forpermission to reference unpublished data, M.Vogel for assistance with trial observations, andG. D. Ruxton for comments that significantly

enhanced the manuscript. Arizona Game andFish Department and New Mexico Departmentof Game and Fish supplied scientific-collectingpermits.

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Accepted: 14 September 2007.

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