butterflies scratch and imbibe from
YI-KAI TEA ,
JONATHAN WEI SOONG ,
ETHAN P. B EAVER
AND DAVID J. LOHMAN
Manuscript received 16 February 2021; revised 15 June 2021;
accepted 8 July 2021; final version received 5 September 2021.
Corresponding Editor: John Pastor.
School of Life and Environmental Sciences, University of
Sydney, Sydney, New South Wales 2006 Australia.
Department of Ichthyology, Australian Museum Research
Institute, Australian Museum, 1 William Street, Sydney, New
South Wales 2010 Australia.
829 Upper Bukit Timah Road, Singapore, 678187
Biological and Earth Sciences, South Australian Museum,
Adelaide, South Australia 5000 Australia.
Biology Department, City College of New York, City
University of New York, New York, New York 10031 USA.
Ph.D. Program in Biology, Graduate Center, City University
of New York, New York, New York 10016 USA.
Entomology Section, National Museum of Natural History,
1000 Manila, Philippines.
Citation: Tea, Y.-K., J. W. Soong, E. P. Beaver, and D. J.
Lohman. 2021. Kleptopharmacophagy: Milkweed butterflies
scratch and imbibe from Apocynaceae-feeding caterpillars.
Ecology 00(00):e03532. 10.1002/ecy.3532
Key words: behavior; leaf-scratching; pharmacophagy; pyrroli-
Milkweed butterflies (Lepidoptera: Nymphalidae:
Danainae) are chemically defended and aposematic
(Ackery and Vane-Wright 1984). The chemical ecology
of several species have been studied extensively, includ-
ing the iconic and migratory Monarch Butterfly, Danaus
plexippus (Brower and Glazier 1975, Boppr
Danaine larvae feed on chemically defended plants from
which they also extract phytochemical protection. Adult
males of many species supplement their existing bio-
chemical deterrents with pyrrolizidine alkaloids (here-
after, alkaloids) obtained by scratching alkaloid-
containing substrates and imbibing the resulting exu-
dates. These alkaloids impart additional protection to
males, serve as a biochemical precursor for mating pher-
omones, and function as a nuptial gift to females
delivered in the spermatophore (Boppr
e 1990). Here, we
report novel observations from Sulawesi of adult male
danaine butterflies scratching other danaine butterfly
larvae and imbibing the exudates with their proboscis,
presumably to steal their host-plant-derived alkaloids.
While the use of alkaloids as chemical defenses in
insects is not uncommon, it is most conspicuous in the
Lepidoptera, especially in the Danainae, which com-
prises three tribes: Danaini, Ithomiini, and Tellervini
(considered by some to be subfamilies; Lamas 2004).
Danaine species use alkaloids for defense and phero-
mone production (Edgar and Caulvenor 1974, Boppr
1986, Orr et al. 1996). Host-plant-derived chemical
defense is ubiquitous among the Danainae, and mem-
bers of this group participate in diverse mimicry rings
involving poisonous models and palatable non-danaine
mimics wherever they occur (Parsons 1998, Joshi et al.
2017, Nishida 2017).
Pyrrolizidine alkaloids are naturally occurring hepato-
toxic plant secondary metabolites commonly found in
the families Boranginaceae, Apocynaceae, Asteraceae,
Fabaceae, Orchidaceae, and Solanaceae (Wink 1988,
2003, El-Shazly and Wink 2014). Danaine butterflies
either feed on these plants as larvae or seek and imbibe
alkaloids as adults for purposes other than primary
metabolism (“pharmacophagy”; Boppr
e 1984). In the
Ithomiini, larval host plants are frequently species of
Solanaceae and Apocynaceae (Trigo et al. 1996, Will-
mott and Freitas 2006), whereas in the Tellervini and
Danaini, these are mostly plants from the families
Apocynaceae and Moraceae (Ackery and Vane-Wright
1984). Adult pharmacophagy is less taxon-specific, and
alkaloids are sequestered from a wide variety of sources,
including flowers, damaged or withered leaves, and dried
seed pods of alkaloid-producing plants (all authors per-
sonal observations; Edgar and Caulvenor 1974, Trigo
et al. 1996). Plants in the genera Senecio (Asteraceae),
Heliotropium (Boraginaceae), and Crotalaria (Fabaceae)
are among the most popular targets, consisting mostly
of the alkaloids retronecine and heliotridine (Smith and
Culvenor 1980, Boppr
e 1990). Individual plants in the
Asteraceae genus Senecio, for example, may comprise as
much as 18% in alkaloids by dry mass (Molyneux and
For adult butterflies, alkaloids are used for more than
just chemical defense. They are important precursors for
pheromone production, particularly for the biosynthesis
of danaidone and hydroxydanaidal (Schulz 1998). In
danaine butterflies, males may possess two types of
androconial organs: a pair of eversible abdominal hair-
pencils and a pair of alar glands (sex brands; Ackery and
Vane-Wright 1984, Boppr
e and Vane-Wright 1989).
During pre-copulation, males hover over receptive
Article e03532; page 1
The Scientific Naturalist
Ecology, 0(0), 2021, e03532
©2021 by the Ecological Society of America
females with hairpencils extruded and splayed, dissemi-
nating pheromones that are detected by females (Brower
et al. 1965, Honda et al. 2016). Courtship success corre-
lates with mating success and fecundity (Edgar and
Caulvenor 1974, Honda et al. 2018), and males often
transfer alkaloids to females through spermatophores as
nuptial gifts (Boppr
e 1990). While alkaloids are often
ingested in leaves consumed by caterpillars during the
larval stages, they may be stored as intermediary com-
pounds (Orr et al. 1996) and are not always transferred
to the adult stage (Boppr
e 1990). Withered and dried
parts of alkaloid-producing plants are a favorite of
danaine butterflies, possibly due to higher concentra-
tions and retention of alkaloids. Fresh leaves and other
vegetative parts are also a target in the absence of dried
or withered leaves. Unique to the danaine butterflies
is the unusual behavior known as “leaf-scratching”
e 1983), in which adult butterflies damage plant
parts with their sharp tarsal claws, liberating plant juices
and sap to imbibe.
Rarely, danaines have been reported imbibing fluids
directly from carcasses of alkaloid-storing insects, though
this phenomenon has been reported infrequently. For
example, in Africa, Danaus chrysippus has been observed
to feed on juices of moribund pyrgormorphid grasshop-
pers that have previously fed on alkaloid-producing
plants, apparently taking advantage of their carcasses as
an alternative source of alkaloids (Owen 1971, Bernays
et al. 1977). This behavior has been observed indepen-
dently by the authors Y. K. Tea and J. W. Soong in Singa-
pore. Both observations involved adults of Parantica
agleoides agleoides (Nymphalidae: Danainae) feeding
from dead lepidopteran carcasses, the pupa of another
danaine species in one case, and a dead arctiine moth in
the other (Fig. 1A). Whether the butterflies were actively
imbibing alkaloids from these sources is unclear, but
danaine pupae and arctiine moths are both chemically
defended by alkaloids (Rothschild et al. 2008).
On 9 December 2019, however, Y. K. Tea and J. W.
Soong observed adult male danaine butterflies scratch-
ing at living butterfly caterpillars in coastal forests of
Tangkoko Batuangus Nature Reserve, North Sulawesi,
Indonesia (1°34033.2″N, 125°09036.1″E) and apparently
imbibing fluid from them. The behavior was similar to
danaine leaf-scratching, but the butterflies instead
scratched live Idea blanchardii blanchardii larvae that
were feeding on Parsonsia spp. (Apocynaceae; Fig. 1B–
E). Adult butterflies of multiple danaine species were
observed scratching many caterpillars along a stretch of
coastal vegetation (˜500 m long), with mid-to-late-instar
caterpillars appearing to be the preferred targets. The
larvae would contort their bodies rapidly in what
appeared to be futile attempts to deter the persistent
scratching of adults. Adult danaine butterflies were
observed actively imbibing from the wounded and ooz-
ing caterpillars, sometimes in mixed species groups that
would congregate for several hours (Fig. 1D). Feeding
butterflies were often so engrossed that they were oblivi-
ous to being touched by human observers. Subsequent
observations over three days revealed repeated visits by
danaine butterflies to the same wounded larvae. Adults
were also observed scratching and imbibing from dead
FIG. 1. Danaine butterflies imbibing from dead and living Lepidoptera. (A) Parantica agleoides agleoides feeding on an arctiine
moth carcass in Singapore. (B–F) Various species of danaine observed in Tangkoko Batuangus Nature Reserve, North Sulawesi
scratching and imbibing from living and dead caterpillars of Idea blanchardii blanchardii. Note everted proboscis in all individuals.
(B) Parantica cleona luciplena; (C) Danaus ismare alba; (D) Danaus ismare alba,Euploea algea kirbyi, and Ideopsis juventa tontolien-
sis; (E) Ideopsis vitrea vitrea; (F) Idea blanchardii blanchardii. Caterpillars are dead in panels C, D, and F, but alive in panels B and
E. Photographs by Akio Takatsuki, G€
oran Pettersson, Yi-Kai Tea, Jonathan Wei Soong, and Cheong-Weei Gan.
Article e03532; page 2 THE SCIENTIFIC NATURALIST Ecology, Vol. xx, No. xx
caterpillars, although whether these mortalities were a
direct consequence of harassment and scratching is
unclear. Although multiple danaine species were abun-
dant at this locale, adult butterflies were only observed
scratching larvae of I. blanchardii blanchardii. No larvae
of other danaine species were found. Pupae of I. blan-
chardii blanchardii were also observed in situ, but these
remained unmolested and appeared to be of no interest
to adult butterflies. We also include a photograph of
Idea blanchardii blanchardii feeding on a larval carcass of
its own species taken in 2017 at the same location by an
amateur naturalist (Fig. 1F).
In total, we observed seven danaine butterfly species
scratching larvae, both dead and alive. These were
Danaus ismare alba,Euploea algea kirbyi,Idea blan-
chardii blanchardii,Ideopsis juventa tontoliensis,Ideopsis
vitrea vitrea,Parantica cleona luciplena, and Tirumala
ischmoides ischmoides. All of these species, along with
adults of four other danaines (Danaus genutia leucoglene,
Euploea eupator eupator,Euploea hewitsonii hewitsonii,
and Euploea westwoodii meyeri), were also observed
scratching leaves (Fig. 2A–L). All 11 danaine species
scratched leaves intermittently during our hours of
observation, between 09:00 and 14:00, mostly on lactif-
erous vines in the genus Parsonsia and other unidentified
apocynaceous plants. Leaf-scratching was also observed
on trees in the genus Premna (Lamiaceae). While species
of Premna (and most other Lamiaceae) are not known
to produce pyrrolizidine alkaloids, they contain isoxa-
zole alkaloids (Barik et al. 1992) and icetexane diterpe-
nes (Dianita and Jantan 2017). We do not know whether
these compounds are attractive to danaine butterflies or
play roles similar to pyrrolizidine alkaloids. Of the doz-
ens of adult butterflies observed scratching plants or
caterpillars, only one was female (Fig. 2B). Observations
of females engaging in leaf-scratching are unusual, since
it is almost exclusively males that engage in this behav-
ior, often gathered in large aggregations (sometimes
numbering in the hundreds) where they imbibe alkaloids
from suitable plants with fervor (Fig. 2M, N).
Why danaine butterflies harass and scratch caterpillars
at this locale remains unclear. Similarly, it is not known
whether the scratching butterflies are attracted by the lar-
vae, their host plants, or both. One possibility is that
caterpillars feeding on apocynaceous plants at this site
are a more concentrated source of alkaloids compared to
their host plants (see Orr et al. 1996). In addition, the
thin larval integument of Idea blanchardii blanchardii may
permit easier access to alkaloid-containing exudate than
through leaf or pupal scratching. The congeneric Idea
FIG. 2. Danaine butterflies exhibiting leaf-scratching on living or dead plants. Observations from Tangkoko Batuangus Nature
Reserve, North Sulawesi. Observations (M–N) from Singapore. (A) Danaus genutia leucoglene; (B) Danaus ismare alba; (C) Euploea
hewitsonii hewitsonii; (D) Euploea eupator eupator; (E) Euploea algea kirbyi; (F) Euploea westwoodii meyeri; (G) Idea blanchardii
blanchardii; (H) Idea blanchardii blanchardii (aberrant coloration); (I) Ideopsis juventa tontoliensis; (J) Ideopsis vitrea vitrea; (K)
Parantica cleona luciplena; (L) Tirumala ishmoides ishmoides; (M) Parantica agleoides agleoides; (N) Danaus genutia genutia. The
Danaus ismare alba individual pictured here (B) is the only female that we observed leaf-scratching in North Sulawesi. Photographs
by Yi-Kai Tea, Jonathan Wei Soong, Cheong-Weei Gan, and Lena Chow.
Xxxxx 0000 THE SCIENTIFIC NATURALIST Article e03532; page 3
leuconoe from Japan is similar in having larvae that feed
exclusively on Parsonsia. Under laboratory conditions,
the pyrrolizidine alkaloids ideamine A and B N-oxides
have been isolated from adults, eggs, and host plants,
demonstrating the acquisition and transfer of alkaloids
directly from the host to the larva in this species (Nishida
et al. 1991, ideamine B is a nor-derivative of parsonsine).
Whether a parallel situation occurs in the Sulawesi ende-
mic I. blanchardii blanchardii is unknown, though this
could explain the preference for live and dead caterpillars
of I. blanchardii blanchardii by adults of the same species,
as well as those of other danaine butterflies at this locale.
We note that while our observations of scratching by
adult butterflies at this locale have been limited to leaves
and caterpillars, we are aware of at least one incident
where this behavior has been performed directly on an
adult butterfly (video available online).
The video, taken
at the same locale in 2017 by Samaisukh Sophasan,
clearly shows a male Ideopsis vitrea vitrea harassing,
scratching, and probing the wings of an adult I. blan-
chardii blanchardii with its proboscis.
The population density of danaine butterflies in the
vicinity may also contribute to more frequent observa-
tions of this previously unknown phenomenon. The
coastal habitat of Tangkoko Batuangus Nature Reserve
in Sulawesi is bordered by dense coastal vegetation that
is replete with Apocynaceae. Species of Danaini were the
dominant group of diurnal Lepidoptera, particularly
those of the genera Danaus,Euploea,Idea,Ideopsis,
Parantica, and Tirumala. One alternative hypothesis is
that the butterflies are attracted to the damaged leaves
left by feeding caterpillars, and as a result are in close
proximity to caterpillars that they inadvertently wound
through leaf-scratching. The wounded caterpillars and
their alkaloid-rich exudates then act as a beacon, draw-
ing the attention of butterflies already in the vicinity.
Continuously overlapping generations in this tropical
habitat may also allow newly eclosed adult butterflies to
observe and learn the larval scratching behavior from
older individuals, resulting in cultural transmission of
this unusual behavior (Whiten 2019). Although we
report the occurrence of 11 species, seven of which were
observed feeding on caterpillars, it is likely that this list
will increase with additional observation.
As far as we are aware, these are perhaps the first
observations of milkweed butterflies apparently obtain-
ing alkaloids from the caterpillars of living, closely
related species rather than plants or the dead carcasses
of insects from different orders. We presume that alka-
loids are transferred from the larvae to the adults, but
this hypothesis requires chemical verification, and we
therefore exercise caution interpreting our observations.
Since the larvae appear to be unwilling participants in
this presumed exchange, we suggest this behavior be
termed “kleptopharmacophagy,”which highlights that
the chemicals consumed by the adults are stolen from
others. However, since it is not clear whether the cater-
pillar wounds and fatalities were caused by scratching,
the alternative neologisms “kairopharmacophagy”(feed-
ing on defensive chemicals from wounded caterpillars
detected via “eavesdropping”)or“necropharma-
cophagy”(feeding on defensive chemicals from dead
caterpillars) might also be appropriate. It is not known
whether this behavior occurs elsewhere in the tropics or
is truly restricted to this region. Danaus species of the
Americas, for example, are apparently not known to per-
form leaf-scratching (Ramos et al. 2020, Lawson et al.
2021). It is possible that the dearth of natural history
observations on Sulawesi may have precluded observa-
tions elsewhere on the island (but see Tea et al. 2020).
No specimens were collected during the course of observa-
tions on Sulawesi. Field observations were made with accompa-
niment of our guides, Saka and Yulen, whom we thank.
Cheong-Weei Gan accompanied Y. K. Tea and J. W. Soong dur-
ing field work and provided additional photographs. We thank
Michael F. Braby (ANU, Canberra) for discourse regarding the
observed behavior, and two anonymous reviewers for the con-
structive comments. We thank Akio Takatsuki, G€
tersson, Cheong-Weei Gan, and Lena Chow for providing
additional photographs used in this manuscript. The research
of D. J. Lohman is supported by National Geographic Society
grant WW-227R-17 and NSF grant DEB-1541557.
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