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BIOTROPICA 35(3): 356–364 2003

Does Mu llerian Mimicry Work in Nature? Experiments withButterflies and Birds (Tyrannidae) 1

Carlos E. G. Pinheiro 2

Departamento de Zoologia, Instituto de Biologia, Universidade de Brasılia, 70910-900, Brasılia, DF, Brazil

ABSTRACTThe selective advantage of Mullerian mimicry in nature was investigated by releasing live mimetic and nonmimeticbutterflies close to wild, aerial-hunting tropical kingbirds (Tyrannus melancholicus) and cliff-flycatchers (Hirundineaferruginea) in three Amazon habitats (rain forest, a city, and ‘‘canga’’ vegetation). Only mimetic butterflies elicitedsight-rejections by birds, but protection conferred by mimicry was restricted to sites in which both predators andmimics co-occurred, as in the case of six mimicry rings at a forest site and two at a city site. Most other Mullerianmimics released at city and canga vegetation were heavily attacked and consumed by birds. These results appear toreflect the birds’ previous experiences with resident butterfly faunas and illustrate how birds’ discriminatory behaviorvaried among habitats that differed in butterfly species and mimicry ring composition.

Key words: Brazil; Mullerian mimicry; prey choice; tropical rain forest; tyrant-flycatchers; unpalatability.

LABORATORY EXPERIMENTS HAVE DEMONSTRATED THAT

SEVERAL PREDATORS, especially birds, can be condi-tioned to avoid (on sight) unpalatable butterfliesand their mimics (Batesian or Mullerian) after tast-ing or eating a few individuals (Brower 1958a, b,c; Brower et al. 1963, 1971; Platt et al. 1971; Bow-ers 1983; Chai 1990, 1996). These results lead usto believe that a similar learning process also occursamong wild predators. The predators’ ability to dis-criminate mimetic butterflies in most field experi-ments, however, has been assessed almost exclu-sively through indirect evidence, usually the recap-ture rates of moths painted to resemble butterflymodels or mimics (Brower et al. 1964, 1967; Cooket al. 1969; Sternburg et al. 1977; Jeffords et al.1979), or butterflies painted or introduced to sitesin which they are not mimetic (Benson 1972, Mal-let & Barton 1989).

Insectivorous birds may be able to distinguishunpalatable prey under natural conditions in threevery distinct ways, each occurring at a differentstage in the predation process. They may rejectprey: (1) on sight (prey are detected but not at-tacked by predators); (2) on taste (prey are detect-ed, attacked, captured, but rejected before con-sumption); and (3) after consumption, when pred-ators suffer the negative effects of prey chemicaldefenses and may exhibit several aversive behaviors(examples of birds suffering these symptoms are

1 Received 4 October 2002; revision accepted 27 July2003.2 E-mail: cegp@unb.br

given in Brower 1984). Previous laboratory exper-iments have shown that sight-rejections usually oc-cur at the final stage of a bird’s learning process,when it has already associated butterfly unpalat-ability and color patterns and is then able to iden-tify a model and its mimics as non-profitable items.Conversely, taste-rejections and rejections afterconsumption are more commonly observed in na-ive predators, which attack and sample prey to as-sess palatability. The behaviors used by birds to re-ject unpalatable butterflies and their mimics there-fore may indicate how experienced they are relativeto butterfly palatability and mimicry (Boyden1976, Brower 1984, Chai 1986).

This study investigated the efficacy of mimicryin nature by observing the reaction of wild, aerial-hunting tropical kingbirds (Tyrannus melancholicus)and cliff-flycatchers (Hirundinea ferruginea) to livemimetic butterflies released close to birds in threeAmazon habitats (rain forest, a city, and ‘‘canga’’vegetation). The co-occurrence of predators andmimics in the same habitat and locality has longbeen recognized as a basic condition for the evo-lution of mimicry (Bates 1862, Muller 1879, Fish-er 1930). Several studies have shown strong spatialand temporal associations of butterflies in mimicryrings (Brown & Benson 1974, Beccaloni 1997,DeVries et al. 1999), but attempts to relate thediscriminatory behaviors of predators to the occur-rence of mimetic butterflies in their foraging sitesare rare. Given that both bird species visit a re-stricted number of hunting perches to which theyrepeatedly return and usually stay for several hours,and that butterfly species composition and mimicry

Butterflies and Birds 357

FIGURE 1. Butterflies and mimicry rings utilized in six recognition trials at three experimental sites. Numbersindicate the sequence of presenting butterflies to birds. Species with a strong sexual dimorphism are indicated (m �male, f � female). An index of the occurrence for each butterfly species at Carajas city (Cc), canga (Ca), and forestsite (F) is given after species names (A � abundant, seen on three to six occasions; R � rare, seen on one or twooccasions; N � not seen).

358 Pinheiro

rings occur unevenly at the three study sites, twohypotheses were tested: (1) protection conferred bymimicry for butterflies in seven mimicry rings isrestricted to sites in which both predators andmimics occur together; and (2) bird species’ dis-criminatory behavior varies among habitats differ-ing in mimicry rings and butterfly species com-position.

MATERIALS AND METHODS

BUTTERFLIES AND MIMICRY RINGS. All mimetic but-terflies utilized in the experiments have been re-garded as unpalatable (Brower 1984, Chai 1986,Pinheiro 1996) and for simplicity will be referredto hereafter as Mullerian mimics. The mimicryrings (groups of species exhibiting a similar mi-metic color pattern; Fig. 1) include: (1) monarch(M), composed of two members of the Danainaethat store cardiac glycosides (Brower 1984, Cohen1985) and pyrrolizidine alkaloids (Kelley et al.1987, Malcolm et al. 1989); (2) orange (O), (3)blue and yellow (BY) and (4) black and red rays(BRR), all composed of Heliconius and other He-liconiinae that store cyanogenic glycosides (Davis& Nahrstedt 1985, Nahrstedt 1985); (5) tiger (T),which includes Heliconius ethilla (Heliconiinae)and Lycorea cleobaea (Danainae), but is composedmostly by members of the Ithomiinae that usepyrrolizidine alkaloids as defensive chemicals (Bro-wer 1984, Brown et al. 1991, Trigo et al. 1996);and (6) black and red spots (BRS), composed ofthree Parides species that store aristolochic acid andvarious compounds (Rothschild et al. 1970, Brownet al. 1991). Also included is the (7) Adelpha-Do-xocopa ring (AD), for which no evidence of unpal-atability or defensive chemicals has been found, al-though some have proposed that mimicry in thisring is related to their ability to escape predators(Mallet & Singer 1987, Srygley 1994). Except forthe AD and BRS rings at Carajas (which includeda few females), all other mimics released to birdsat three sites were males.

Nonmimetic butterflies included 11 nymphalidspecies that are well known to be palatable (Brower1984; Chai 1986, 1990; Pinheiro 1996). Most arecryptic when perched, making them difficult forpredators to detect. For species that exhibit strongsexual dimorphism (Catonephele acontius, C. nu-milia, Nessaea obrinus, and Hamadryas laodamia)both sexes representing distinct cryptic patternswere included in the experiment (N � 15). Whenit was impossible to obtain all butterflies neededfor a trial, as in the case of some butterflies in the

nonmimetic group released to kingbirds in the city,other cryptic and palatable nymphalids such asAnartia jatrophae, Colobura dirce, Napeocles jucun-da, or Nessaea batesii were offered to the birds.

STUDY SITES. Experiments were conducted duringJune–July 1994 in the Serra dos Carajas, in thesouthern portion of the state of Para, Brazil (5�54�–6�33�S, 49�53�–50�34�W). Tests with tropicalkingbirds were conducted in a small city (Carajas)surrounded by undisturbed rain forest. All birdstested at this site were found in groups of threeindividuals 100–150 m distant from each otheralong a large avenue that circled the city, wherethey perched on electric lines (ca 8 m high). Testswith cliff-flycatchers were conducted at two othersites more than 30 km away. One group of threebirds was found in a rocky mountain covered by alow plant formation locally known as ‘‘canga’’ veg-etation. Birds were always present on wires or onthe roofs of abandoned houses. Another group ofthree birds was found close to a reservoir (Represado Esteril Sul) in a small open area surrounded bynative rain forest (forest site). Birds at this site al-ways perched on three posts 7 m high and 15 mapart from each other.

RECOGNITION TRIALS. A set of 39 live butterfliesrepresenting the 7 mimicry rings and 15 cryptic,distinct color patterns was released close to eachexperimental bird (10 birds in the city, 3 birds inthe canga, and 3 in the forest) in six recognitiontrials carried out on different days. Each trial con-sisted of several butterflies (up to 8 individuals)including both mimetic (different rings) and non-mimetic species offered to birds (Fig. 1). The se-quence of presenting mimics and nonmimics variedamong trials, but always ended with a nonmimeticbutterfly. This design helped control for lack ofappetite and the possibility of satiation when amimic was previously sight-rejected.

Butterflies were released 2 m above the ground,inside an open area within 8 to 12 m of a bird thatwas apart from the rest of its group to help avoiddisputes for butterflies and to minimize the possi-bility that birds could observe another bird’s reac-tions (some Tyrannidae learn new feeding tacticsby watching companions; Alcock 1969). With twoassistants, it was possible to follow all individualbirds in a given group until all of them were suc-cessfully tested, thus avoiding replications. Theproportion of butterflies attacked or sight-rejected,consumed, or taste-rejected by birds was recordedand compared among bird groups through contin-

Butterflies and Birds 359

FIGURE 2. Pooled responses of birds relative to attacked or sight-rejected butterflies. Number of butterflies offeredto birds (N) at Carajas city (Cc), canga (Ca), and forest (F) is given along with X2 values and significance levels.

gency tables (Sokal & Rohlf 1995). To interpret abird’s responses to Mullerian mimics, a survey ofthe butterflies in the three habitats within a radiusof 40 m around bird hunting perches was carriedout on six occasions during the recognition trials

(3–5 hours/site). The frequency of a particular spe-cies in each of the six surveys was utilized to pro-duce an index of its abundance (Fig. 1). Whetherbirds attacked, captured, or consumed passing but-terflies was recorded.

360 Pinheiro

TABLE 1. Butterflies taste-rejected by tropical kingbirds(Carajas city) and cliff-flycatchers (canga andforest site). (N � number of butterflies releasedto birds).

Ring SpeciesC. city

(N � 10)*Canga

(N � 3)Forest

(N � 3)

M

O

BY

D. eresimusD. plexippusD. junoE. alipheraH. saraH. wallacei

221121

011000

000000

BRR

T

H. eratoH. melpomeneE. talesH. ethillaL. cleobaeaH. daphnis

211022

100211

001000

BRS

H. ninoniaM. mazeus.M. polymniaP. lysanderP. neophilusP. panthonus

112864

001222

000102

* Except for H. ethilla (N � 2) and P. panthonus (N �5).

RESULTS

ATTACKS AND SIGHT-REJECTIONS. Pooled responsesof birds to released butterflies at the three experi-mental sites showed three patterns (Fig. 2). First,all butterflies in the nonmimetic group (150 in thecity, 45 in canga, and 45 in the forest) were at-tacked. Second, only butterflies in the M, O, BY,BRR, T, and BRS mimicry rings elicited sight-re-jections by birds. Third, the proportion of sight-rejections in these rings varied significantly amonghabitats (P � 0.0001 for all rings above; GI x GII x G III contingency tables in Fig. 2).

The highest proportion of sight-rejections oc-curred at the forest site where cliff-flycatchers se-lectively attacked cryptic and palatable species andavoided almost all Mullerian mimics on sight. Thisincluded all representatives of the M, O, BY andT rings, eight of nine butterflies (88.9%) in theBRR (except one Eueides thales), and six of ninebutterflies (67%) in the BRS ring (except one Pa-rides lysander and two P. panthonus).

Conversely, cliff-flycatchers in the canga didnot discriminate among butterflies and attackedmost mimetic and nonmimetic species. Only 5 of72 mimetic butterflies (6.94%) released at this sitewere sight-rejected, including Heliconius melpomene(BRR), Hypothyris daphnis and Mechanitis mazeus(T), and P. lysander and P. neophylus (BRS).

Tropical kingbirds in Carajas city also attackedmost mimetic species. Exceptions were 3 of 20 but-terflies (15%) in the M (1 Danaus eresimus and 2D. plexippus), and 12 of 52 butterflies (23.1%) inthe T ring (3 Hypothyrus ninonia, 2 L. cleobaea, 2Mechanitis polymnia, 3 M. mazeus, and 2 H. daph-nis); however, significant differences in the propor-tion of attacks and sight-rejections between tropicalkingbirds and canga cliff-flycatchers were foundonly for the BRR and BRS rings (P � 0.05 in bothcases; G I x G II contingency tables in Fig. 2).

Observations on the responses of birds to pass-ing butterflies (not released in the trials) were ob-tained only in the forest. Here, cliff-flycatcherswere observed to sight-reject one D. plexippus (M),one Agraulis vanillae (O), two Heliconius sara or H.wallacei (BY, not identified in flight), three H. eratoor H. melpomene (BRR), one M. polymnia (T), andto attack one H. laodamia and one Pyrrhogyra neae-rea (both escaped attacks).

CONSUMPTIONS AND TASTE-REJECTIONS. Except forthe BRS ring that was predominantly taste-rejectedby all birds, most other Mullerian mimics and allnonmimics captured by birds were consumed (Ta-

ble 1; Fig. 3). The proportion of taste-rejections inall rings did not differ significantly among birdgroups (P � 0.05 in all cases; GI x GII x GIIIcontingency tables in Fig. 3). One exception wasin the BRR ring, in which forest cliff-flycatchersseemed to differ from the other groups; however,small sample size (N � 1 for forest cliff-flycatchers)and empty cells did not allow a conclusive statis-tical test. Comparisons involving only tropicalkingbirds and canga cliff-flycatchers also showed nosignificant differences in the proportion of taste-rejections (P � 0.05 for M, O, BY, BRR, and Trings; Fig. 3).

Despite many distasteful and chemically de-fended species consumed by birds, aversive behav-iors like vomiting were never observed (at least for15 min after a butterfly was ingested or taste-re-jected). On five occasions, however, head shaking(Gillan 1979) was observed in three cliff-flycatchersand two kingbirds, all occurring after eating or justhandling the Parides (BRS). Among these birds,two forest cliff-flycatchers knocked the butterfliesseveral times against the perch before droppingthem dead on the ground.

DISCUSSION

Mullerian mimicry clearly provided protection forbutterflies at the forest site where such mimics were

Butterflies and Birds 361

FIGURE 3. Pooled responses of birds relative to consumed or taste-rejected butterflies. Number of butterflies cap-tured and tasted by birds (N) at Carajas city (Cc), canga (Ca), and forest (F) is given along with X2 values andsignificance levels.

predominantly sight-rejected by birds. Moreover,the joint occurrence of birds and the six mimicryrings observed at this site (Fig. 1), and the fact thatpassing mimetic butterflies (not released in the tri-als) were also sight-rejected, strongly suggest that

birds at the forest were already experienced relativeto butterfly unpalatability and mimicry.

At the other sites, mimetic butterflies were pre-dominantly attacked and consumed by birds. Al-though bird responses may have been due to hun-

362 Pinheiro

ger, the absence of all released species of butterfliesat the canga and most of them at the city site (Fig.1) suggest that birds at these sites had no previousexperience and attacked the butterflies to assesstheir palatability. A few sight-rejections of Mulle-rian mimics were obtained for two rings (M andT) at Carajas city, and three at canga (BRR, T, andBRS). Sight-rejections obtained at canga occurredmostly in the last trials, suggesting that a birdlearned to avoid mimics during the recognition tri-als, after attacking and eating other co-mimics. AtCarajas city, however, sight-rejections were not re-stricted to the last trials and at least one speciesrepresentative of each ring was commonly found atthe city site (D. plexippus and M. polymnia; Fig. 1).It is possible, therefore, that at least part of thatpopulation of tropical kingbirds was already ableto discriminate among rings. In fact, of all ringscommonly observed close to the birds in the city(M, O, and T; Fig. 1) only the butterflies in theO ring did not elicit sight-rejections by kingbirds.

The large number of attacks on nonmimeticbutterflies provided no indication of birds’ discrim-inatory behavior. Both experienced and naive birdsmay have attacked palatable and cryptically coloredbutterflies, as the former could have had experiencewith their profitability, and the latter could havebeen sampling novel prey. Such attacks, however,indicate that sight-rejections of Mullerian mimicsin this study were not likely due to a lack of ap-petite or satiation, but rather to the birds’ abilitiesto discriminate mimetic butterflies.

Among all mimicry rings tested, only butter-flies in the AD ring did not elicit sight- or taste-rejections by birds. A previous experiment involv-ing these and other Adelpha and Doxocopa speciesdid not indicate unpalatability or any special abilityof butterflies to escape attacks by tropical kingbirds(Pinheiro 1996). It is conceivable, however, thatother predators are involved and both possibilitiesshould be further investigated in order to under-stand the similarities of color patterns found be-tween butterflies in these two genera.

In contrast, naive tropical kingbirds and cliff-flycatchers seemed unable to taste-reject most Mul-lerian mimics (butterflies were often entirely eaten,including the wings that may contain larger

amounts of defensive chemicals than other bodyparts; Brower & Glazier 1975). It is possible thatcompounds such as cyanogenic glycosides in theHeliconiinae, alkaloids in the Ithomiinae, and car-denolides and alkaloids in the Danainae act onbirds through delayed effects and are not tastedimmediately after the butterflies are consumed, orthat both bird species are more tolerant to defen-sive chemicals than other insectivorous birds. Col-lins and Watson (1983) also observed predation byother Tyrannidae on chemically defended arctiidmoths, and W. W. Benson (pers. comm.) fed twocliff-flycatchers with seven H. erato without ob-serving any aversive behavior. These observationssuggest that only after repeated sampling do birdsassociate butterfly chemical defenses and color pat-terns. Until birds learn to avoid butterflies on sight,as required in mimicry theory, many mimics maydie.

The ability to discriminate unpalatable butter-flies shown by birds in the forest suggests that theymay learn many different mimetic and cryptic col-or patterns; however, there are other potential stim-uli in live butterflies such as size, shape, smell,sounds, flight pattern, and other behavioral traitsthat could also be utilized by birds to discriminateunprofitable prey. Among these traits, flight patternseems to be especially relevant since most unpal-atable and mimetic butterflies fly slowly and reg-ularly, and tend to exhibit similar flight patterns(Srygley 1994, 1999). Discriminatory ability andall other aspects related to the birds’ memory andlearning process, including the possibility of sociallearning among birds (Alcock 1969), remain un-known and should be viewed as important factorsfor future research.

ACKNOWLEDGMENTS

I thank the Companhia Vale do Rio Doce for facilities inthe Serra dos Carajas. O. R. Silva (UnB) and E. L. Araujo(CVRD) helped in the field. K. S. Brown Jr helped iden-tify butterfly species. D. S. Smith, G. McGavin, P. J.DeVries, J. D. Hay, and an anonymous reviewer readdifferent phases of the manuscript and furnished helpfulcomments. Financial support to the author was providedby the Conselho Nacional de Desenvolvimento Cientıficoe Tecnologico–CNPq, Brazil (proc. no. 202081/91-5).

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