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Conservation Biology, Pages 1142–1143Volume 12, No. 5, October 1998

Comments

Tameness of Insular Lizards and Loss ofBiological Diversity

MIGUEL DELIBES* AND M. CARMEN BLÁZQUEZ

Estación Biológica de Doñana, Consejo Superior de Investigaciones Científicas, Apdo. 1056, 41080 Sevilla, Spain

Stone et al. (1994) call attention to the threats to a “sub-tle and perhaps overlooked component of biological di-versity,” behavioral diversity. They argue that behavioraldiversity is lost when organisms delete evolved behav-iors from their repertoire, and they use as an examplethe increased wariness (loss of “unusual tame behavior”)of lava lizards (genus

Tropidurus

) on islands where do-mestic cats (

Felis

catus

) have been introduced.The authors quantified wariness by analyzing the re-

sponses of lizards of nine populations in eight islands ofthe Galapagos archipelago to a slowly approaching ob-server. They found a correlation between the presenceof feral cats (but not of rats [

Rattus

rattus

] or snakes [

Al-sophis

sp.]) and the distance lizards allowed the ob-server to approach before fleeing (approach distance),and the distance they fled in one continuous movement(flight distance; Snell et al. 1988). Stone et al. (1994)concluded that their results clearly suggest that feral catsare responsible for a reduction of lizard tameness, whichin fact should represent a reduction in behavioral diver-sity and thus a reduction in biological diversity.

We agree with Stone et al. (1994) that a reduction inbehavioral diversity may also represent a reduction ingenetic diversity, which is at the basis of all biological di-versity (Noss 1990). We think, however, that the in-creased wariness (reduced tameness) in insular lizardsfollowing the introduction of exotic predators is not agood example of loss of biological diversity.

At least two aspects of the loss of tameness must be con-sidered to accept that it represents a reduction of biologicaldiversity: (1) whether the decline of tameness is actually aloss and (2) whether this “lost” tameness can be restored.

Tameness and wariness, as they are commonly esti-mated—by measuring approach distance, distance to a ref-uge, time devoted to vigilance, and so forth—are not dis-crete behaviors but the extremes of a continuum. Hence, itis possible to discuss whether naive animals have devel-

oped tameness or rather have lost wariness. The commoncondition in ecological communities is that animals live un-der the risk of predation and have evolved behaviors of vig-ilance and escape (Schall & Pianka 1980). The “enemy-free” situation on some islands is rather exceptional, andthe development there of tameness probably should be in-terpreted not as the acquisition of a new behavior but asthe loss of an escape behavior that was included in the be-havioral repertoire of the founders of the island populationand their ancestors. In other words, when predators disap-pear from a community, the presumably tame prey result-ing will not be behaviorally richer, but poorer.

The second question refers to the possibility of recov-ering the lost tameness. Biological diversity is the resultof the evolutionary process (Wilson 1992), and evolu-tion does not go backwards—extinction is forever. Thismeans that, by definition, extinct biological materials, in-cluding genetically based discrete behaviors, cannot berecovered. Nevertheless, much circumstantial evidencesuggests that apparently lost tameness and wariness canbe restored in populations as well as individuals.

Spiny-tailed iguanas (

Ctenosaura

hemilopha

) comingfrom populations of continental Mexico were introducedto mainland Baja California Peninsula and the nearby Cer-ralvo island before European settlement (Murphy 1983).Despite the presence of cats, introduced in the last 20years, iguanas on Cerralvo island are very tame. The dis-tance from basking places to refuges, the distance to anobserver at which iguanas disrupt their activity, and theapproach distance are statistically smaller on the islandthan on the mainland (Blázquez et al. 1997). Becausespiny-tailed iguanas were an important food resource fornatives (Mocquard 1899), we can speculate that in theoriginal population they were probably hunted; there-fore, they should be wary. If so, in some centuries the in-troduced iguanas in Cerralvo island, which is inhabitedand without terrestrial predators, would have lost most oftheir ability to recognize and escape from predators. Onthe contrary, on the mainland the presence of humansand natural ground predators would have kept the igua-nas as wary as at the time of introduction.

*

email decastro@ebd03.ebd.csic.esPaper submitted October 28, 1997; revised manuscript acceptedMarch 12, 1998.

Conservation BiologyVolume 12, No. 5, October 1998

Delibes & Blázquez Tameness and Biological Diversity

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There is other empirical evidence, related to variationsin predation pressure, of rapid changes of tameness andwariness in lizards. Green iguanas (

Iguana

iguana

) areeasily domesticated and become very tame. Black igua-nas (

Ctenosaura

similis

) in Palo Verde, a protected areaof Costa Rica, have become habituated to the presenceof people and often ignore it, whereas in the nearby for-est they escape into burrows or trees whenever they seea person (Burger et al. 1991). But the iguanas of PaloVerde were more wary in 1992 than in 1990, probablybecause of increasing harassment by humans (Burger &Gochfeld 1993). The increased wariness of lava lizardson islands with cats, reported by Stone el al. (1994), isalso a good example.

Stone et al. (1994) assume a genetic basis for tameness,but it may be irrelevant to discuss here how much of theescape behavior is genetic or based on learning. The abil-ity to recognize, judge the intentions of, and decide whento escape from a potential predator requires some experi-ence (Endler 1986) and a genetic basis (Hobson et al.1988). Buitron (1983) suggested that a variety of birds havean innate fear response to a variety of stimuli and graduallylearn which objects warrant continued alarm. Even tameanimals try to escape in some circumstances (Kruuk &Snell 1981). Based on this evidence, Maloney and McLean(1995) taught naive birds predator-coping skills, and Milleret al. (1994) did the same with captive-reared black-footedferrets (

Mustela

nigripes

). Most available information sug-gests that the ability to assess the level of predation riskand the presence of flexibility in the decision-making pro-cess are adaptive characteristics of escape behavior, regard-less of their genetic basis.

We do not mean to suggest that the introduction ofexotic predators to oceanic islands is unimportant forthe conservation of biological diversity. We are wellaware that almost all the worldwide extinctions of am-phibians and reptiles over the last four centuries havebeen of insular taxa (Case et al. 1992) and have been re-lated to the arrival of humans and the introduction of ex-otic predators (Atkinson 1989; Olson 1989). Also, it isevident that the loss of wariness in the absence of preda-tors makes possible the evolution of rare structures andbehaviors (e.g., flightless birds; McNab 1994). In thissense, the introduction of exotic predators on islands al-ters the evolutionary trajectories of prey, as stated byStone et al. (1994), reducing the possibilities of futureevolution and thus eliminating a potential source of bio-logical diversity. Hence, the conservation of naive spe-cies or races on islands must be a subject of concern, al-though tameness per se is not a particular behaviorwhose loss must be regretted.

Acknowledgments

We are grateful to Drs. F. Alvarez, P. Ferreras, and F. Pal-

omares for their critical comments on a previous versionof the manuscript.

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