28 June 2020

Life History of the Ciliate Blue

Life History of the Ciliate Blue (Anthene emolus goberus)


Butterfly Biodata:
Genus: Anthene Doubleday, 1847
Species: emolus Godart, 1824
Subspecies: goberus Fruhstorfer, 1916
Wingspan of Adult Butterfly: 24-30mm
Caterpillar Local Host Plants: Saraca thaipingensiss (Fabaceae, common name: Yellow Saraca), Saraca indica (Fabaceae, common name: Ashoka Tree), Bauhinia sp. (Fabaceae), Smilax setosa (Smilacaceae, common name: Sarsaparilla Vine), Senna fistula (Fabaceae, common name: Golden Shower), Senna alata (Fabaceae, common name: Candle Bush), Syzygium zeylanicum (Myrtaceae).



A female Ciliate Blue.

A male Ciliate Blue.

Physical Description of Adult Butterfly:
On the upperside, the male is dark purplish blue with narrow black borders. The female is brown, paler at discal areas and is iridescent blue at the basal areas of the both fore- and hindwings. On the underside, both sexes are pale greyish brown with a series of white striations on both wings. On the hindwing underside, there is a prominent black spot on the dorsum, an orange-crowned tornal spot in space 2. Also on the hindwing, there are short fine tails at the end of veins 1b, 2 and 3. These fine tails are an extension of the cilia. The tail at the end of vein 3 is the shortest of the three and  barely noticeable.

Short fine tails at the end of veins 1b, 2 and 3.




Field Observations:
Ciliate Blue is common in Singapore. It is essentially an urban butterfly, but can occasionally be found in forested areas. Adults have been observed flowers for their carbohydrate intake. Males are often encountered puddling on damp footpaths, and is partial to human perspiration. The adults have a rapid and erratic flight, but tend to fly short distances if not unduly alarmed.




Early Stages:
The caterpillar of the Ciliate Blue is polyphagous, and is known to utilize multiple plants  in a number of families as larval food plant in its range of distribution across the region. Locally in Singapore, we have recorded seven plants to date. The most popular of these is the Yellow Saraca from Fabaceae. Other plants are Saraca indica (Fabaceae), Senna fistula (Fabaceae), Senna alata (Fabaceae), Smilax setosa (Smilacaceae), Syzygium zeylanicum (Myrtaceae) and one Bauhinia sp. (Fabaceae). The caterpillars feed on young and immature leaves of these plants.

Host plant #1: Saraca thaipingensiss (Yellow Saraca).

Host plant #2: Saraca indica.

Host plant #3: Syzygium zeylanicum.

The caterpillar of the Ciliate Blue has a close obligate myrmecophilous relationship with the weaver ant (Oecophylla smaragdina). In the wild, the caterpillars of the Ciliate Blue invariably appear in the company of the weaver ants (primary worker ants). The attending ants are attracted to the lycaenid larvae by the carbohydrate-rich secretions released by the caterpillar, and their presence offer protection to the caterpillar from parasitoids and predators. As with other lycaenid caterpillars, the caterpillar of the Ciliate Blue has pore cupola organs (specialized epidermal glands on its body surface) which can release appeasement substances to suppress the ant aggressiveness towards it.

A weaver ant attending to a final instar caterpillar of the Ciliate Blue. A droplet can be seen secreted from the dorsal nectary organ.


Besides featuring pictures of the immature stages of the Ciliate Blue in the wild, this life history article also documents the full development of a large number of Ciliate Blue caterpillars from the egg stage to the adult stage, without any attending weaver ants in an indoor breeding environment. The caterpillars were given young leaves of the Yellow Saraca to feed on.


A video clip showing the caterpillars of the Ciliate Blue in various instars living in the company of the weaver ants in the wild on a tree of the Yellow Saraca.

Weaver ants attending to a pre-pupa (right) and a pupa (left) of the Ciliate Blue on the underside of a leaf of Saraca indica.

In the wild, caterpillars of the Ciliate Blue can sometimes be observed to share the same feeding site with caterpillars of the Common Tit (Hypolycaena erylus teatus) which are also constantly attended by weaver ants.

Weaver ant attending to final instar caterpillars of the Ciliate Blue and the Common Tit on a young leaf of the Yellow Saraca.

The ovipositing female typically looks for parts of the host plant densely populated by the weaver ant, and lay its eggs there.  The eggs are laid in small to large clusters on the underside of a leaf or a twig, under the watchful eyes of the weaver ants which do not attack the female. At times, the eggs are even laid directly on the nest of the weaver ant.

A female Ciliate Blue laying eggs on the underside of a leaf of Saraca indica.

A cluster of eggs of the Ciliate Blue laid on the leaf underside of Saraca indica.

A weaver ant checking the cluster of eggs (shown above).

A time lapse sequence showing a Ciliate Blue female laying eggs on the underside of a twig of Saraca indica as weaver ants wandering by.

A weaver ant checking the cluster of eggs laid on a twig.

Each egg is about 0.5mm in basal diameter, and whitish with a strong greenish undertone. It is discoid-shaped with a slightly depressed micropylar at the center of the top surface. The egg surface is reticulated with a very dense pattern of tiny ridges and pointed protrusions.

Close-up views of eggs of the Ciliate Blue. Basal diameter: 0.5mm.

It takes about 3 days for the egg to hatch. The caterpillar nibbles away the top portion of the egg shell to emerge but does not bother to completely devour the remaining egg shell. The newly hatched has a a pale yellowish body with a length of about 1mm. Its head is similarly coloured. The body also features pale yellowish  setae (hair) dorso-laterally and along the body fringe.  These young caterpillars feed by grazing on the surface of the young leaf of the host plant. The body colour could remain pale yellowish or  change to  a darker shade of yellow as growth progresses.  After about 2.5-3 days of growth in the first instar, and reaching a length of about 2mm, the caterpillar moults to the next instar. 

In the wild, it had been observed that early instar caterpillars of the Ciliate Blue were regularly picked up by the worker ants and carried back to the ant nests. It is thought that these young caterpillars feed and grow within the nests before being carried out when they reach later instars.

Hatching time! Both newly hatched caterpillars as well as those in the process of devouring egg shell.

Two views of a newly hatched caterpillar, length: 1mm.

Two views of a 1st instar caterpillar, length: 1.6mm.

A large number of early 1st instar caterpillars feasting on leaf lamina of the host plant.

Two views of a late 1st instar caterpillar, dormant prior to its moult, length: 1.95mm.

A group of late 1st instar caterpillars, dormant prior to its moult.

Both 1st and instar caterpillars being attended by weaver ants on a leaf of a Syzygium sp.

Both 1st and instar caterpillars being attended by weaver ants on a leaf of the Yellow Saraca.

In the 2nd instar, there are numerous tiny  speckles covering the body surface.  The caterpillar is pale to dark yellowish in colour. At this stage, the dorsal nectary organ on the 7th abdominal segment is present and rather prominent. The 2nd instar caterpillar reaches up to a length of about 4mm, and after about 2.5-3 days in this stage, it moults again.

Two views of a 2nd instar caterpillar, early in this stage, length: 2.5mm.

Two views of a 2nd instar caterpillar, length:2.8mm.

Two views of a late 2nd instar caterpillar, dormant prior to its moult, length:4.1mm.

Two weaver ants in a tussle over a 2nd instar caterpillar of the Ciliate Blue.

A weaver ant transporting a 2nd instar caterpillar of the Ciliate Blue.

A weaver ant attending to caterpillars of the Ciliate Blue.

The 3rd instar caterpillar has numerous speckles covering its body surface which is pale to dark yelowish green. Pale brownish to reddish dorso-lateral bands stretch from the prothorax to the 6th abdominal segment. Between these bands, the dorsum typically bears a darker shade of colours (reddish or greenish) than the body ground colour. The dorsal nectary organ and the pair of tentacular organs, on the 7th and 8th abdominal segments respectively, are now readily observed. The 3rd instar takes about 3.5 to 4 days to complete with the body length reaching about 7.5mm.

A newly moulted 3rd instar caterpillar.

Two views of a 3rd instar caterpillar, early in this stage, length: 4.6mm.

Two views of a 3rd instar caterpillar, length: 7mm.

Two views of a 3rd instar caterpillar, dormant prior to its moult, length: 7.4mm.

A group of late 3rd instar caterpillars, dormant prior to the moult to the next instar.

Two weaver ants attending to a 3rd instar caterpillar of the Ciliate Blue on a leaf of the Yellow Saraca.

A weaver ant attending to a 3rd instar caterpillar of the Ciliate Blue on a leaf of a Syzygium sp.

In the 4th instar, the caterpillar has its body ground colour featured in varying degrees of yellowish green (yellow to green, and intermediaries). Inner and adjacent to the dorsal-lateral bands (which are reddish brown in most specimens), thin whitish bands are present. In the area enclosed by the dorsal-lateral bands, the dorsum could be either reddish brown or green, and decorated with chevron markings in most body segments. In some specimens, the chevron markings are indistinct or absent, and in other specimens, reddish brown to dark brown coloration spreads beyond the dorsal bands and spanning     almost entire body surface.The dorsal nectary organ and the tentacular organs are prominent in this final instar of the larval phase of the life cycle.

A newly moulted 4th instar caterpillar.

Two views of a 4th instar caterpillar, early in this stage, length: 7.5mm.

Two views of a 4th instar caterpillar, length: 10.5mm.

An animated sequence showing twelve 4th instar caterpillars of the Ciliate Blue, showing colour/marking variations.

Two weaver ants attending to an early 4th instar caterpillar of the Ciliate Blue.

Weaver ants attending to a 4th instar caterpillar of the Ciliate Blue.

Weaver ants attending to a 4th instar caterpillar of the Ciliate Blue.

Weaver ants attending to a 4th instar caterpillar of the Ciliate Blue.

Weaver ants attending to a 4th instar caterpillar, with a 2nd instar caterpillar present nearby.

After about 4-5 days of feeding in the 4th instar and reaching a length of up to about 15.5mm, the caterpillar stops food intake and seeks out a pupation site. During this time, its body gradually shrinks and turns almost uniformly green. Typically the caterpillar chooses a spot on the underside of a leaf or a stem for its pupation site. The pre-pupatory caterpillar prepares for pupation by spinning a silk girdle and a silk pad to which it attaches itself via anal claspers.

Two views of a pre-pupa of the Ciliate Blue.

A video clip showing the pupation event of a Ciliate Blue caterpillar.

After about half a day as a pre-pupa, pupation takes place. The pupa has a typical lycaenid shape. The colour of the pupa varies drastically, ranging from the more common green colour, to colours such as pink, brown and black. A large diamond-shaped marking is present at the posterior end of the mesothorax on the dorsum. Pupal length: 9.8-11.3mm.

Two views of a green-coloured pupa of the Ciliate Blue.

An animated sequence depicing six pupae of the Ciliate Blue, showing variations in colour.

Weaver ants checking a brown-coloured pupa of the Ciliate Blue.

Weaver ants checking a green-coloured pupa of the Ciliate Blue.

About five days later, the pupa turns dark, first in the wing pad and thorax, then progressively in the abdomen. The extent of the bluish patch in the wing pads gives an early indication of the gender of the soon-to-emerge adult. The next day, the pupal stage comes to an end with the emergence of the adult butterfly.

Two views of a mature pupa of a female Ciliate Blue.

A newly eclosed male  Ciliate Blue.

A video clip showing the eclosion event of a female Cilite Blue butterfly.

References:
  • The symbiosis between the weaver ant, Oecophylla smaragdina, and Anthene emolus, an obligate myrmecophilous lycaenid butterfly, K. Fiedler and U. Maschwitz, Journal of Natural History, vol. 23, pp.833-846, 1989.
  • Differences in worker caste behaviour of Oecophylla smaragdina in response to larvae of Anthene emolus, E. V. Saarinen, Biological Journal of the Linnean Society, vol. 88, no.3, pp. 391-395, 2006.
  • Symbiotic Relationship Between Anthene emolus and Oecophylla smaragdina: An obligate mutualism in the Malaysian rainforest, E. V. Heffernan, Doctoral dissertation, University of Florida, 2004.
  • [C&P4] The Butterflies of The Malay Peninsula, A.S. Corbet and H.M. Pendlebury, 4th Edition, Malayan Nature Society, 1992.
  • A Field Guide to the Butterflies of Singapore, Khew S.K., Ink On Paper Communications, 2010.
Text by Horace Tan, Photos by Simon Sng, Ellen Tan, Nelson Ong  and Horace Tan.