Beachgoing Butterflies: Marine Puddling on Black Sand Beaches of Tangkoko Batuangus Nature Reserve, North Sulawesi

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VOLUME 74, NUMBER 2
127
Journal of the Lepidopterists’ Society
74(2), 2020, 127–131
BEACHGOING BUTTERFLIES: MARINE PUDDLING ON BLACK SAND BEACHES OF TANGKOKO
BATUANGUS NATURE RESERVE, NORTH SULAWESI
Additional key words: behavior, Indonesia, island, nutritional ecology, volcanic sand
Puddling is a common and widespread behavior of
Lepidoptera and other arthropods in which fluid is
imbibed from mud puddles or other sources to obtain
sodium and perhaps other micronutrients (Downes
1973; Molleman 2010). While there have been sporadic
observations of puddling on seawater, the phenomenon
seems to be uncommon or under-reported (Pola &
García-París 2005; John & Tennent 2012). We
document frequent marine puddling by a diverse
community of butterflies on volcanic sands in Sulawesi,
Indonesia, and speculate on the prevalence of the
behavior at this locale.
Puddling is common in several insect orders but is
most conspicuous in Lepidoptera, particularly
butterflies (Papilionoidea). Puddling butterflies extend
their proboscis into a moist substrate and use their
cibarial pump to ingest aqueous solution. Desired
micronutrients are absorbed in the hindgut (Smedley &
Eisner 1995), and an anal jet of filtered water is ejected
every few seconds—sometimes shooting around half a
meter or more (John & Tennent 2012; all authors,
personal observation). Puddling butterflies are nearly
always male and sometimes form large aggregations
comprising hundreds or thousands of individuals
(Downes 1973; Beck et al. 1999; Burger & Gochfeld
2001; Molleman et al. 2005). While presumably coined
in reference to mud puddles, “puddling” is also used to
describe supplementary feeding (i.e., non-nectar
feeding) from stream banks, feces, urine, perspiration
and tears from living mammals, carrion, and—rarely—
seashores (Downes 1973; John & Tennent 2012; Plotkin
& Goddard 2013).
Most evidence suggests that puddling Lepidoptera
seek and sequester sodium (Arms et al. 1974; Adler &
Pearson 1982; Pivnick & McNeil 1987; Smedley &
Eisner 1995, 1996), though there is evidence that
nitrogenous compounds are preferred by some taxa
(Beck et al. 1999; Boggs & Dau 2004; Molleman 2010).
More than 99% of Lepidoptera species consume only
living plant tissue during their larval stages (Pierce
1995), and most plant tissues—particularly the leaves of
terrestrial plants—are a poor source of sodium (Slansky
& Rodriguez 1987). Both sodium and nitrogen are a
scarce resource for most herbivorous insects, including
nectivorous adult butterflies (Seastedt & Crossley 1981;
Liu et al. 2003). In many Lepidoptera species, sodium
accumulated by males through puddling is transferred
to females with their spermatophore during mating
(Pivnick & McNeil 1987; Smedley & Eisner 1996). In
various butterfly species where it has been studied,
sodium increases female longevity and fecundity,
decreases females’ need to forage, and increases male
mating success (Pivnick & McNeil 1987; Molleman et
al. 2004). However, not all butterfly species experience
fitness benefits from supplemental sodium (Molleman
et al. 2004). While it has been suggested that sodium
obtained through puddling enhances neuromuscular
function, as neurons and flight muscles require sodium
ions (Arms et al. 1974), there is little direct evidence for
this hypothesis (Molleman et al. 2005; Molleman 2010).
Interestingly, male Battus philenor butterflies that
consumed sodium courted females differently and more
vigorously than males deprived of the nutrient,
potentially proving an honest signal for females to assess
a male’s sodium titer (Mitra et al. 2016).
Despite the abundance of sodium in seawater, there
are few reported observations of puddling in coastal
marine environments. Pola and García-París (2005)
reported ca. 20 individuals of Papilio polytes drinking
from exposed reef shelves in Guam, providing
unequivocal evidence of direct marine puddling in
butterflies. John and Tennent (2012) reviewed the
occurrence of marine puddling in butterflies, including
published reports and previously unpublished personal
communications documenting this phenomenon. They
note observations of marine puddling near the water’s
edge, but also describe several observations of
butterflies gliding over the ocean and imbibing seawater
with their proboscis while in flight. They concluded that
observations of marine puddling remain rare or under-
reported. The phenomenon has been observed in
Papilionidae, Hesperiidae, Pieridae, Nymphalidae, and
Lycaenidae (Pola & García-París 2005; John & Tennent
2012), though the prevalence of this behavior within the
respective families and its geographical extent remain
poorly known.
On December 9, 2019, the first three authors (YKT,
JSW, and CWG) observed marine puddling along the
black sand beaches of Tangkoko Batuangus Nature
Reserve, North Sulawesi, Indonesia (1° 34′33.2″N,
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125° 09′36.1″E; Fig. 1). The butterflies were initially
seen descending from the canopy before flying up and
down the shoreline patrolling the beach. Occasionally,
individuals flew above the water close to the surface,
where they appeared to drink mid-flight. Similar reports
of aerial seawater drinking have been documented for
Papilio ulysses in Honiara, Solomon Islands (Tennent
1997). Mostly, however, butterflies were observed
puddling on the sand 0–10 m from the waterline, often
flying away only when disturbed by waves (Fig. 1).
Subsequent observations over the span of the next three
days revealed that this was a common and frequent
behavior.
We observed multiple male individuals of 27
Papilionidae, Hesperiidae, Pieridae, Nymphalidae, and
Lycaenidae species engaging in marine puddling
between 09:00 – 12:00 h and up to 14:00 h at this one
marine site (Fig. 2; Table 1). While we observed no
puddling Riodinidae, we note that there are only four
riodinids out of 557 butterfly species known from
Sulawesi (Vane-Wright & de Jong 2003). Based on our
reading of the available literature, we observed more
butterfly species and individuals puddling on seawater
than have ever been documented before at a single
location (John & Tennent 2012). We also observed that
most butterflies puddled alone, with a maximum group
size of ca. five individuals. So-called “puddle clubs”
(Adler, 2008) in the Indo-Australian Archipelago
including Wallacea can include dozens to hundreds of
individuals in a single group (all authors, personal
observation). Small group size might be explained by
the distance between the ocean and forest cover, ca.
10–15 m. On the one hand, brightly colored butterflies
foraging on dark sand are easily spotted by predators,
and this perhaps limits the number of males willing to
stray so far from the protection of forest cover. On the
other hand, butterflies are not frequent beachgoers, and
puddling males are usually copy-cats. A butterfly is far
more likely to land at a salt source if conspecifics have
already alighted. Experimental studies exploit this
behavior by placing freshly killed, pinned specimens
next to puddles to act as decoys and attract additional
puddling males (Arms et al., 1974). Perhaps the distance
between the ocean and forest cover limits the number
of males that see other puddling males, thus preventing
the formation of large groups.
Why this phenomenon of marine puddling is locally
common at this site in Indonesia is unclear. One
possibility is that terrestrial sodium may be an especially
rare resource in this region of Sulawesi. Although most
afternoons were met with rain, we did not encounter
rivers, streams, or flooded banks—favored habitats for
puddling activity. More curiously, we were unable to
attract many butterflies with urine and fermented
shrimp paste: two baits that that are effective elsewhere,
particularly for Papilionidae and Nymphalidae. It is
possible that paucity of sodium in the terrestrial
environment has resulted in local adaptation for
obtaining the mineral from the sea. Indeed, the habitat
of Tangkoko Batuangus Nature Reserve is not dissimilar
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FIG. 1. Marine puddling butterflies on the black sand beaches of Tangkoko Batuangus Nature Reserve. Butterflies were observed
puddling at the edge of the waterline, often taking flight only when disturbed by the incoming surf. Photographs by Jonathan Soong
Wei and Yi-Kai Tea.
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to Honiara and Guam (Tennent 1997; Pola & García-
París 2005); both are tropical, coastal forests bordered
by the sea. Although seawater intake in northeast
Sulawesi is unlikely to be the only possibility for
butterflies to obtain minerals (we observed lone
individuals of Graphium, Papilio, Cepora, and Vindula
puddling in drains and swamps), it appears to be the
preferred option.
The black sands of these shores might explain why
puddling is more common on this beach than
elsewhere. Black sands are typically rich in minerals
(Mallik et al. 1987) and formed by recent volcanic
activity. Black sands are frequently composed of basalt,
which can be rich in sodium (Hughes & Brown 1972).
Thus, the sand itself may provide additional sodium or
other attractive micronutrients, and the rarity of black
sand beaches might explain the dearth of puddling
observations on beaches. Alternatively, minerals in the
sand may interact with seawater to make it more
appealing to butterflies. Carol Boggs (in John &
Tennent 2012) suggests that seawater may be
underutilized as a salt resource because it contains
unwanted or unsuitable compounds. These substances
might be buffered or chemically modified by black
sands to increase the palatability of seawater.
Apart from the species detailed herein (Fig, 2; Table
1), no other Lepidoptera species were observed
definitively engaging in marine puddling. The coastline
of Tangkoko Batuangus Nature Reserve is bordered by
dense coastal vegetation, a favored habitat for
Apocynaceae plants. Parsonsia and other lactiferous
vines dominated, and so did species of Danaini, which
specialize on these plants. Several adult males in the
genera Danaus, Euploea, and Parantica were observed
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TABLE 1. Species of butterflies observed engaging in marine puddling in Tangkoko Batuangus Nature Reserve, North Sulawesi.
Frequency of observations are denoted by (+) symbols, corresponding to the total number of days (out of four) that each species
was observed.
Species Family Subfamily Frequency
Papilio demoleus demoleus Papilionidae Papilioninae ++++
Papilio fuscus minor Papilionidae Papilioninae +
Papilio gigon gigon Papilionidae Papilioninae ++
Papilio sataspes sataspes Papilionidae Papilioninae +
Graphium agamemnon comodus Papilionidae Papilioninae ++++
Graphium codrus celebensis Papilionidae Papilioninae +++
Graphium eurypylus pamphylus Papilionidae Papilioninae ++++
Graphium meyeri meyeri Papilionidae Papilioninae ++
Graphium milon milon Papilionidae Papilioninae ++++
Graphium rhesus rhesus Papilionidae Papilioninae ++++
Badamia exclamationis Hesperiidae Coeliadinae ++
Appias hombroni hombroni Pieridae Pierinae +
Appias zarinda zarinda Pieridae Pierinae +++
Cepora celebensis celebensis Pieridae Pierinae ++
Cepora timnatha timnatha Pieridae Pierinae +
Hebomoia glaucippe celebensis Pieridae Pierinae ++
Catopsilia pomona flava Pieridae Coliadinae ++++
Charaxes nitebis nitebis Nymphalidae Charaxinae +
Cyrestis thyonneus celebensis Nymphalidae Cyrestinae +++
Danaus genutia leucoglene Nymphalidae Danainae +
Euploea eupator eupator Nymphalidae Danainae +
Vindula dejone celebensis Nymphalidae Helioconiinae ++
Doleschallia polibete celebensis Nymphalidae Nymphalinae +
Hypolimnas bolina bolina Nymphalidae Nymphalinae +
Anthene lycaenina Lycaenidae Polyommatinae ++
Catopyrops ancyra subfestivus Lycaenidae Polyommatinae +
Hypolycaena erylus gamatius Lycaenidae Theclinae +
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congregating in large numbers at the base of these
vines, often directly on seawater-tainted sand. While
most were likely imbibing pyrrolizidine alkaloids
(Boppré 1986), it is unclear if seawater was secondarily
or unintentionally being imbibed. For this reason, we do
not include these species as engaging in marine
puddling (except for Euploea eupator eupator [Fig. 2R]
and Danaus genutia leucoglene [not pictured], which
were seen actively drinking from seawater tainted sand).
Though extensive, this report on marine puddling
activity is likely not exhaustive. The following species
were seen patrolling the beach, but were not observed
puddling, viz: Graphium androcles androcles, Papilio
peranthus adamantius, Pachliopta polyphontes
polyphontes, Troides helena hephaestus, and Troides
hypolitus cellularis. It is likely that the list of marine
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FIG. 2. A selection of butterflies from different families engaging in marine puddling. Marine puddling was observed from mem-
bers of all butterfly families found on Sulawesi except Riodinidae (representatives of Hesperiidae not pictured). (A–J) Papilion-
idae, in order of inset letters: Papilio gigon gigon, P. demoleus demoleus, P. sataspes sataspes, P. fuscus minor, Graphium rhesus
rhesus, G. milon milon, G. eurypylus pamphylus, G. meyeri meyeri, G. codrus celebensis, and G. agamemnon comodus; (K–N)
Pieridae: Catopsilia pomona flava, Cepora celebensis celebensis, Hebomoia glaucippe celebensis, Appias zarinda zarinda; (O–R)
Nymphalidae: Vindula dejone celebensis, Cyrestis thyonneus celebensis, Doleschallia polibete celebensis, Euploea eupator eupator
(S–T) Lycaenidae: Anthene lycaenina, Catochrysops ancyra subfestivus. Photographs by Yi-Kai Tea, Jonathan Soong Wei, and
Cheong Weei Gan.
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puddlers will no doubt increase with additional
observation. Nonetheless, this study provides the most
taxonomically extensive documentation of this behavior
yet observed at a single location.
ACKNOWLEDGEMENTS
No specimens were collected during the course of this study.
We thank Rod Eastwood and an anonymous reviewer for their
insightful comments on a previous version of this manuscript.
DJL’s research is funded by grant WW-227R-17 from the Na-
tional Geographic Society Committee for Exploration and Re-
search and by NSF DEB-1541557.
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YI-KAI TEA*School of Life and Environmental
Sciences, University of Sydney, Sydney, Australia;
Department of Ichthyology, Australian Museum
Research Institute, Australian Museum, 1 William
Street, Sydney, NSW 2010 Australia. JONATHAN SOONG
WEI 892 Upper Bukit Timah Road, #04-21, Singapore
678187; CHEONG WEEI GAN Nature Society Singapore,
510 Geylang Road, #02-05, Singapore 389466. AND
DAVID J. LOHMAN Biology Department, City College of
New York, City University of New York, 160 Convent
Ave., New York, NY, 10031 USA; Ph.D. Program in
Biology, Graduate Center, City University of New York,
365 5th Ave., New York, NY, 10016 USA; and
Entomology Section, National Museum of Natural
History, T.F. Valencia Circle, Rizal Park, Ermita,
Manila, 1000 Philippines.
*Corresponding email: yi-kai.tea@sydney.edu.au
Submitted for publication 18 March 2020; revised and
accepted 5 April 2020.
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