Table Of Content.
82 Journalofthe Lepidopterists' Society
JournaloftheLepidopterists'Society
60(2),2006,82-85
SOME DISTASTEFULASIAN PAPILIONINAE (PAPILIONIDAE)
Peter Smetacek
TheRetreat,JonesEstate, Bhimtal, Nainital26.3136,Uttaranchal, India,email: [email protected]
ABSTRACT.Western HimalayanpopulationsofdireeAsiaticPapiho L. speciesappeartobedistastefulinvaryingdegreestobirds.These
include the polymorphic Papilio polytes L. which was considered a classic Batesian mimic ofdistasteful Pachliopta Reakirt. The Indian
populationofpolytes,withthreefemaleforms,isacaseofsympatricpolymorphisminadistastefulspecieswithwarningcoloration.
Additional kevwords: Miillerianmimicry;Papilio;polymorphicmodel
Introduction Whistling Thrushes (Myiophonus caeruleus) and a
Batesian mimicry, referring to a system comprising YellowcheekedTit (Panisxanthogenys)
palatable species and unpalatable models, and Laughing Thrushes are not known to attack
Miillerian mimicry, involving similar-looking, butterflies on the wing. They feed on insects, berries
unpalatable species, are well known examples of and other vegetable matter (Ali 1962). White Crested
adaptive evolutionbynatural selection. Ofthe over200 andWhite Throated LaughingThrushes spend most of
species of Papilio L. known, at least one W. African their foraging time turning over dead leaves on the
species (antimachus Drury ) is known to be chemically ground and investigating the bark and foliage oftrees
protected in the adult stage (Watson & Whalley 1983). (Whistler 1935; Ali 1949).
Several species are believed to be Batesian mimics of Theyareveryfond oflive moths (pers. obs.). Initially
chemically defended moths and butterflies (Clarke & the birds in this studywerewaryofdead butterflies but
Sheppard 1960, 1962 Brower & Brower 1962 Clarke theysoon developedataste forthem, especiallycontrol
etal. 1968 Watson &;Whalley 1983;etc.). Altho;ugh the speciesbelongingto Nymphalinae, ofwhich 100%were
;
larvae of all Papilio butterflies are believed to be eaten.
chemically protected by unpleasant taste and smell The lack ofexperience on the part ofthe birds and
(Wynter-Blvth 1957; Klots & Klots 1959), this was not their evidentwillingness to learn proved advantageous,
believed to be carried over to the adult stage except in since they examined and tried to eat (at least once)
every species presented, including known unpalatable
the case ofantimachus.
species belonging to Delias Hiibner, Danaus Latreille
Materials & Methods and Pachliopta Beakirt. White Crested Laughing
In apilot study undertaken at Jones Estate, Bhimtal, Thrushes displayedahigh degree ofpreyrecognitionat
in Nainital district, Uttaranchal, India (elevation 1500 the species level. Many White Throated Laughing
m; latitude 29°20'41" N and longitude 79°36T5" E) in Thrushes ignoredthebutterflies completelythroughout
the outermost range of the Kumaon Himalaya, I the study. The birds were observed from a distance of
presented >560 freshly collected, wild butterflies 3—4 m, initiallythrough awire mesh screen and laterin
the open.
belonging to 86 species to wild, free ranging, foraging
parties ofbirds in > 256 encounters over a period of4 Besults
years (1999-2002). One or more of three Papilio
species, i.e. polyctor Boisduval, protenor Cramer and Entire butterflies were offered, except on three
polytes L. formed part of the presentation on 109 different occasions when, after repeated rejections, die
occasions. A total of 10 polyctor (96, 19), 9 protenor wingscales of1polyctorand2protenorspecimenswere
(E8a6ch, s1p9ec)iamnend,1i8fnpootlydteevsou(r1e2d6,, w6as9)pwreesreentperdesseenvteerda.l wpoispseidbleofpfraencodndtihteiowniendgvsishuaapleavaletresrieodn toonctihrecpuamrvtenotf
times,sometimesonthesameday,untilitwastoodryto thebirds. Thepolyctorwas eaten butboth theprotenor
be attractive tothebirds. continuedtobe ignored.
The birds consisted ofone family ofWhite Crested One6 19polyctor, 16protenor and4629polytes
Laughing Thrushes (Garrnlax leucolophus), whose wereentirelyeaten. Theprotenorwas theonlybutterfly
composition varied from 2 to 7 birds duringthe period eaten by aYellow-cheeked Tit on its single visit to the
ofobservation andWhite Throated LaughingThrushes site. Tenpercento£polyctor, 0% o{protenorand 11.1%
Gamdax albogularis) in groups varying from 4 to >60 of polytes were partially eaten, usually the head and
asonally. Casual foraging species included Blue either thorax or abdomen. In all, 30% of polyctor,
..
Volume 60, Number 2 83
11.1% ofprotenor and 44.4 % oipolytes were entirely Pachliopta hector L. and both are restricted to India
eaten, compared widi 77% to 100% (mean 95%) for and Sri Lanka. The nomino-typical form primarily
control species (Colias fieldii Menetries 77%; resembles Pachliopta aristolochiae Fabricius and the
Graphiumsarpedon Felder90%; Vanessa indica Herbst two exhibit similarvariation inwingpattern diroughout
100%; Kaniska canace Linne 100%; Symbrenthia lilaea their range from the Himalayas to Sri Lanka, Japan and
Hewitson 100% Precis iphita Cramer 100% Junonia Sulawesi. In addition, the typical from also resembles
lemonias Linne ;100 % Lethe rohria Fabrici;us 90%; Pachliopta polyphontes Boisduval and Pachliopta
;
Melanitisleda Linne 100 % Deudonjxepijarbas Moore polydonis L. in part ofS.E. Asia. The form theseus of
;
95%) presented alongwidi the Papilio species. polijtes resembles the black form ofaristolochiae and
On one occasion, aWhite Crested LaughingThrush both occur in parts of the Philippines and parts of
diat ate die abdomen and hindwings ofac5polytes and Indonesia, while Pachliopta atropos Staudinger is a
nothing else exhibited signs of distress immediately possible additional co-model on Palawan (Clarke &
afterwards, opening its beak repeatedly as ifto call but Sheppard 1972). In die present study, although diree
not emitting any sound. Such behavior was never female formsofpolijtes occurinthearea, onlythecyrus
observedin connectionwith die controls. form and males were used to preclude possible
preconditionedvisual aversion to the mimetic forms on
Discussion
the part of the birds. The possibility of significant
P. polyctor is not known to be mimetic, while differences in palatability between the female forms is
protenor females have been proposed as Batesian unlikely, since all the forms in a given area (three in
mimics of the Atrophaneura vanina White group India and Sri Lanka) are obtainable from asingle batch
(Batwings) and diree of the four female forms of die ofeggs (Fryer 1913; Clarke & Sheppard 1972).
polymorphic polijtes are considered classic Batesian The above data strongly suggest that these diree
mimics ofPachliopta (Evans 1932; Wynter-Blyth 1957; Papilio species are distasteful and that polytes is a
Clarke & Sheppard 1972; Larsen 1987). Peile (1937), Miillerian co-model rather a Batesian mimic of
quoting from T.R.D. Bell's series "Common Butterflies Pachliopta, at least in parts ofits range. P. polyctorand
ofthe Plains ofIndia" published in theJournal ofthe polytes appear to be moderately distasteful while
Bombay Natural History Society, stated that "the protenor is quite distasteful to birds at the studv site
(Pachliopta) groupisprotectedbyveryunpleasantsmell (Table 1).
and taste. Birds will not eat them nor will lizards In the larval stage, these three species feed on
willingly or readily. P. polijtes, of a different group, is membersofdie citrus family(Rutaceae). P. polyctorand
without these qualities .". However,hedidnotqualify protenor feed on Xanthoxylum armatum DC, while
..
this statement further. polytes feeds on a variety ofmtaceous plants and has
The male of polijtes and one female form, cyrus, been bred on Murraya konigii Spreng. and cultivated
which occurs throughout the insect's range, are non- Citrus L. in the studv area. Troidine swallowtails are
J
mimetic. The second female form, romulus, resembles known to sequester aristolochic acids from dieir
Table 1. PooledresponsesofWhiteCrestedandWhiteThroatedLaughingThrushestofreshlycollected,wild, deadbutterflies. Butterflies
thatweremanipulatedfor+5secondsbyoneormorebirdsandthen rejectedarerecordedincolumn6.Theresponsescore I,column7)was
calculated from scores recorded for individual presentations: = ignored, flung aside, pecked briefly or repeatedly but not eaten this
informationwasrecordedinwords); 1=thebutterflywaspartiallyeaten,usuallytheheadandeitherthoraxorabdomen(specimenspreserved
inmycollection)and2 = theentirebody,butnotnecessarilythewings,waseaten. SpecimenswerecollectedatdiestudysiteinJonesEstate
andatRanibagh(altitude600m),20km.southbyroadfromJonesEstate,mainlyinMarch-AprilandOctober-November.
1 2 3 4 5 6 7
Species Specimens #of # entirelyeaten # partiallyeaten #oftimesrejected Response Score
Presented encounters
%of Max
Spe>cimens % Specimens % Specimens encounters possible Actual %
Control 123 133 117 95.1 3 2.4 3 2.2 246 23S 95.9
polyctor 10 33 2 20 2 20 4 12 20 6 30
protenor 9 32 1 11 4 12.5 IS 2 11.1
polytes 18 49 6 33 4 22 7 14 36 16 44.4
84 Journalofthe Lepidopterists' Society
Although extrapolation ofthe results obtained from
100 95.9 the small number ofPapilio specimens offered in this
study must be done with caution, there is little doubt
that at least some populations of the three Papilio
species are distasteful invaryingdegrees tosomebirds.
The present findings prompt a re-interpretation of
the relationship betweenpolytes and Pachliopta The
.
classic Batesian interpretation of polytes-Pachliopta
mimicry predicted that only polytes benefits at the
expense of Pachliopta, which it "parasitises", and
predators, which it deceives into shunning palatable
prey. The new Miillerian interpretation suggests that
the shared aposematic signals ofthe co-models {polytes
Control Polyctor Protenor Polytes
and Pachliopta spp.) result in enhanced predator
Species learning and the benefits of this accrue to all the
butterflyspeciesinvolved. The relationshipbetweenthe
Figure 1. Palatabilityindexforthepercentageofbutterfliesentirely
orpartiallyeatenbywildbirds,basedonresponsescoredescribedin butterflies is one of asymmetrical Miillerian mimicry,
Table 1. Butterflieswerepresentedrandomly. since polytes appears to be only moderately distasteful
hostplants (Brown et al. 1991) and it is possible that whilethe Pachliopta genusis certainlymore distasteful,
some Papilio butterflies, such as the species considered with aristolochic acids in the bodvtissue.
in this paper, have retained the ability to sequester The distastefulness of polytes also explains the
aromatic or distasteful compounds from their larval persistence ofthe non-mimetic female formcyrus over
hostplants. Although some Papilio species are knownto the entire range of the species. Although cyrus
be palatable to birds, such as the N. American glaucus comprises only 5% of the total female population in
L. and palamades Drury, which have been used as parts ofsouthern Indiawhere aristolochiae hectorand
,
&
controls (95% eaten) in another study (Ritland the corresponding female forms of polytes are very
Brower 1991),bothspecies donotfeedon Rutaceaebut common (Larsen 1987), it predominates inthewestern
on Rosaceae, Oleaceae, Salicaceae, Betulaceae, Himalayan foothills where hector is absent and
Lauraceae and Magnoliaceae (Scriber et al. 1975 aristolochiae scarce orabsent (Peile 1937;Wynter-Blyth
;
Watson &Whalley 1983; Daccordi et al . 1988). In the 1957) butwherepolytes is as common as in otherparts
present study, Graphium Scopoli species that feed on ofits range. Indeed, the presence or absence ofits co-
Lauraceaewere foundtobe attractivelypalatabletothe models hardly affects the abundance ofpolytes overits
birds (unpublished) andonewas used as acontrol. range, as in the Himalayan foothills of Himachal
In this study, the spring and summer broods of Pradesh, India, where it is not uncommon despite the
polyctor, the spring brood ofprotenor and spring and fact that none ofits co-models occur (DeRhe-Philippe
autumnbroods ofpolyteswere used. The results do not 1931).
suggest any noticeable difference in distastfulness Polymorphism in distasteful species with warning
between the broods. coloration is an unusual phenomenon (Joron & Mallet
The present study was carried out using wild, free- 1998 Kapan 2001), since genetic analysis ofMiillerian
;
ranging birds which are not habitual predators on mimicry indicated that selection is for monomorphism
butterflies but generalized insectivores. The study rather than polymorphism (Turner & Crane 1962;
involved the random presentation of wild butterflies. Sheppard 1963; Emsley 1964). In other known
Thebirdscouldbeobservedonlywhiletheywereatdie polymorphic Miillerian co-models, such as Heliconius
studysite. Sincedieyusuallydepartedsoon aftereating, cydno Doubleday & Hewitson and Heliconius erato L.,
possible distress behavior or even regurgitation could different forms ofdie same species are rarelysympatric
not always be observed. Rigorous measurements of (Joron & Mallet 1998). In the very likely event that all
manipulation time, number oftimes pecked and other populations ofpolytes are as distasteful as the western
minutiae were not always possible in the melee caused Himalayan one, the case ofpolytes in southern Indiais
bya large number ofbirds feeding on a small patch of unusual, since the two mimetic forms of die female
ground. The birds at times arrived and devoured which occur there are roughlyequally abundant (Peile
everything in sight and at other times ignored 1937), eg. /iecfor-like form 50.4% andaristolochiae-\ike
everything, including controls, having evidently found form 45.7% atasingle location (Larsen 1987).
ficientfoodelsewhere. Ithas beenproposed (Kapan 2001) thatgeographical
Volume 60. Number 2 85
variation in selection for mimicry coupled with weak 383.
selection against formswhentheyare common explains DeRhe-Philippe. G.W.V. 1931.ThebutterfliesoftheSimlaHills.J.
Bomb. Nat. Hist.Soc.35: 172-183.
the existence of polymorphic Miillerian co-models. Emsley, M. G. 1964. Thegeographicaldistributionofthecolor-pat-
.Although this proposition is applicable to certain cases, terncomponentsofHeliconiuseratoandHeliconiusmelpomene
notablyHeliconius Kluk, itcannotbe appliedtothecase wthiethtwgeonsepteicciaels.evZiodoelnocgeicfaor49t:he24s5y-s2t8e6m.aticrelationshipbetween
ofsympatricpolymorphisminpolytes insouthernIndia. Evans,W.H. 1932. TheIdentificationofIndian Butterflies.2nded..
BombayNat. Hist. Soc. 10+454pp.
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