Batesian mimicry in snakes: A review of recent field experiments

Elapid coral snakes of the Neotropics and Nearctic are highly venomous and frequently

brightly coloured, with rings of red, yellow (or white), and black encircling the body (Roze 1996). Predators typically avoid tricolour ringed patterns (Brodie 1993; Brodie &

Janzen 1995; Hinman et al. 1997; Pfennig et al. 2001; Harper & Pfennig 2007; Pfennig

et al. 2007; Harper & Pfennig 2008; Kikuchi & Pfennig 2010), possibly without prior experience (Smith 1975, 1977). Numerous nonvenomous colubrid snakes of the

Neotropics and Nearctic (e.g., kingsnakes and milk snakes) converge on similar tricolour ringed patterns, which has led many to suggest that these snakes are Batesian

mimics of coral snakes (reviewed in Greene & McDiarmid 1981; Brodie & Brodie 2004).

If tricolour ringed colubrids are indeed Batesian mimics of coral snakes, then such

patterns should confer protection from predation where they actually co-occur with coral snakes. This protection should break down, however, in areas where coral snakes are

absent (i.e., in allopatry) because predators would not be under selection to avoid coral

snakes or anything resembling them (Pfennig et al. 2001).

Recently, this critical prediction of Batesian mimicry theory has been tested with field experiments (Pfennig et al. 2001; Harper & Pfennig 2007; Pfennig et al. 2007; Harper &

Pfennig 2008; Kikuchi & Pfennig 2010). In these experiments, researchers constructed

artificial replicas of snakes expressing different “phenotypes” (i.e., with patterns mirroring either a presumed mimetic or nonmimetic phenotype). These replicas were

placed in natural habitat (Fig. 1) and attacks on different phenotypes by free-ranging, naturally occurring predators were measured. Replicas were constructed of cylinders of

either precoloured, nontoxic plasticine or polymer clay, which was threaded onto an S-

shaped wire for stability; fishing line was then attached to the wire on one end and a nail on the other, which was driven into the ground in the field. Replicas were coated with a

thin film of clear, low-odour spray latex enamel to minimize any smell emitted by the plasticine or clay.

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Figure 1. A replica of a scarlet kingsnake (Lampropeltis elapsoides) in situ.

By placing replicas in natural habitat, the researchers were able to record predation attempts by observing the imprints left in the soft plasticine/clay by natural predators

(Fig. 2). This method has been employed successfully to document both avian and mammalian predators on at least three continents (e.g., see Madsen 1987; Brodie 1993;

Brodie & Janzen 1995; Hinman et al. 1997; Pfennig et al. 2001; Wuster et al. 2004;

Niskanen & Mappes 2005; Buasso et al. 2006; Harper & Pfennig 2007; Pfennig et al. 2007; Harper & Pfennig 2008; Kikuchi & Pfennig 2010). Thus, this approach appears to

be robust to different predator guilds and environments.

Figure 2. A control (brown) replica that had been attacked, probably by a black bear.

In the initial experiments, Pfennig et al. (2001) tested whether scarlet kingsnakes

(Lampropeltis elapsoides), which resemble eastern coral snakes (Micrurus fulvius), and

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sonoran mountain kingsnakes (L. pyromelana), which resemble western coral snakes

(Micruroides euryxanthus), are Batesian mimics. They specifically tested whether

predators avoid harmless lookalikes of coral snakes only where coral snakes occur.

In these experiments, three phenotypes were exposed to predators: (1) a tricolour (red-black-yellow (or white)) ringed pattern, (2) a striped pattern with identical colours and

proportions as ringed replicas, or (3) a plain brown pattern. Ringed replicas were

modeled after either L. elapsoides (yellow rings) or L. pyromelana (white rings). Striped and brown replicas acted as controls. The former controlled for the possibility that

predators might just avoid bright colours, whereas the latter controlled for the possibility that predators might avoid any object that resembles a snake.

The researchers arranged three different replicas (triplets) 2 m apart in natural habitat (each replica was used once only). At each site, 10 triplets were placed 75 m apart in a

line. After 2-4 weeks, the replicas were collected from the field, and a person who had no knowledge of the replica’s location scored attacks by noting any impressions

corresponding to a likely predator (marks left by insects, lizards, rodents and other

noncarnivore mammals were excluded from the analysis, because “attacks” by these animals would not have represented actually attempts at predation on a live snake).

In the southeastern U.S. (where L. elapsoides occurs in both sympatry and allopatry

with M. fulvius), 25 (5.2%) replicas were attacked by carnivore mammals (e.g, black

bear, bobcat, coyote, fox, raccoon; none were attacked by birds). In the southwestern U.S. (where L. pyromelana occurs in both sympatry and allopatry with M. euryxanthus),

49 (6.8%) replicas were attacked by carnivores (again, none were attacked by birds). In both sites, the mean proportion of ringed replicas attacked was significantly greater in

allopatry than in sympatry (Pfennig et al. 2001), indicating that, as predicted by Batesian

mimicry theory, predators avoid mimics only in sympatry. Moreover, in both sites, protection from predation was frequency dependent. Specifically, coral snakes become

increasingly rare with increasing latitude in the southeastern U. S. and increasing elevation in the southwestern U. S. (Pfennig et al. 2001). Consequently, one might

expect that selection to avoid ringed patterns would weaken with increasing latitude and

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elevation. The data did indeed suggest that selection to avoid ringed patterns is

sensitive to coral snake abundance (Fig. 3).

Figure 3. Frequency-dependent mimicry. The proportion of carnivore attacks on ringed

replicas of scarlet kingsnakes (a mimic of eastern coral snakes) and sonoran mountain

kingsnakes (a mimic of western coral snakes) increased with (a) latitude, and (b) elevation. Horizontal dashed line: proportion of attacks on ringed replicas expected

under randomness. Vertical dashed line: maximum latitude and elevation for coral snakes in North Carolina and Arizona, respectively. From Pfennig et al. (2001).

Subsequent experiments have found:

• In a field experiment designed to assess predation on replicas of “good” mimics

(i.e., mimics that closely matched their model) versus “poor” mimics (i.e., mimics that matched their model less closely but that were still within the range of

variation of actual mimics), attacks on good mimics were significantly greater

than randomness (indicating that good mimics would likely suffer higher predation than poor mimics in allopatry), but this was only true in areas where

good mimics actually occur in nature, suggesting that predation on good mimics

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might reflect frequency-dependent (i.e., apostatic) predation (Pfennig et al.

2007).

• When free-ranging natural predators on the edge of the model’s range were given a choice of attacking replicas of good or poor mimics, they avoided only

good mimics. By contrast, those in the center of the model’s range attacked good and poor mimics equally frequently. These findings demonstrate why the

best mimics occur on the edge of their model’s range (Harper and Pfennig 2007).

• Where coral snakes are rare, intermediate phenotypes are attacked more often than cryptic and mimetic phenotypes, indicating the presence of an adaptive

valley between cryptic and mimetic phenotypes. However, where coral snakes are abundant, intermediate phenotypes are not attacked more frequently,

resulting in an adaptive landscape without a valley. Thus, high model abundance

may facilitate the evolution of Batesian mimicry (Kikuchi and Pfennig 2010).

The fact that separate experiments—conducted in different habitats, and focusing on

different mimicry complexes and on diverse suites of predators—found similar results,

supports the validity of these experiments. Nevertheless, a number of potential

concerns with these experiments might be raised.

First, some might question why bird attacks were ignored. Bird attacks were not

ignored in these studies; there were simply very few predation attempts directed by birds on these replicas (< 1% of all attacks). In general, bird predation on snakes might

be lower in temperate regions than in tropical regions, where greater attacks on snake replicas have been observed (e.g., see Brodie 1993).

Second, some might contend that, because carnivores lack of trichromatic (“true”) colour vision, and because they are generally nocturnal, they would not be able to

distinguish good mimics from poor mimics. However, the fact that carnivores possess dichromatic vision (having cones for blue and green light) does not seem to preclude

their being able to distinguish good mimics from poor mimics (Harper and Pfennig 2007;

Kikuchi and Pfennig 2010). Presumably, different pattern resemblances to coral snakes

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can be detected even without colour vision, since patterns and degrees of shading differ

among snakes that represent good, poor, and no mimics. Moreover, these patterns are

distinctive, even in dark, low-light conditions (Fig. 4).

Figure 4. A western coral snake, showing how distinctive its pattern is, even in low light

and black and white.

Third, any scent from the clay is unlikely to have affected the results, because all

replicas were made of the same material and thus would have had similar scent. Moreover, replicas were coated with a thin film of clear, low-odour spray latex enamel to

minimize any smell emanating from the clay.

Finally, some might question whether carnivores actually considered these replicas as

potential prey items rather than merely attacking the clay to, e.g., obtain minerals of fats. Such arguments cannot, however, explain why ringed replicas were attacked

significantly less frequently in sympatry than in allopatry by the same suites of predators, nor can they explain why ringed replicas were attacked less in sympatry than

striped replicas, which had the same types of clay (only arranged differently). Moreover,

attacks by mammals other than carnivores were excluded from the analysis.

Thus, these experiments strongly suggest that naturally occurring predators do indeed avoid mimetic phenotypes in sympatry, but not in allopatry.

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