Lycaenid Butterflies and Ants

Lycaenid Butterflies and Ants

In many ways, ants are the greatest cooperators on earth. As eusocial insects, they are well known for their highly cooperative and coordinated societies, but they also cooperate with other organisms.  Ants engage in mutualisms—aka symbiotic, cooperative, or mutually beneficial interactions—with plants, fungus, and other insects. They serve as effective protectors, fertilizers, seed dispersers, tenders, cleaners, and farmers. Ants are such prolific cooperators, that an entire class of species interactions exists to describe cooperative associations with ants: myrmecophily (meaning ‘ant love’). But wait, this is a butterfly article, right?

A caterpillar of the Centaur Oakblue being attended by Weaver Ants.

A pupa of the Centaur Oakblue still getting the attention of a number of Weaver Ants.

A Centaur Oakblue adult.

Right: butterflies. As you well know, butterflies are a wonderful group to study for both scientific and artistic purposes. Butterflies are beautiful and fascinating, and as far as I'm concerned, the butterfly family Lycaenidae is the most beautiful and fascinating of them all. With more than 6,000 estimated species, the Lycaenidae is a huge family (second in number only to Nymphalidae), and lycaenid butterflies occur in nearly every habitat where a butterfly could conceivably occur. They exhibit an incredibly broad hostplant range, feeding on numerous plant families, as well as fungi, lichen, and yes, other insects. But what really makes them the most interesting butterfly group is their larval association with ants.

A Common Red Flash displaying its striking upperside.

Caterpillars of the Common Red Flash in the company of attending ants.

A Long Banded Silverline adult.

Caterpillars of the Long Banded Silverline interacting with ants eager to get a taste of its nectary excretion.

More than 75% of the world’s lycaenid species engage in highly specialized larval interactions with ants. In its most basic form, the interaction looks something like this: caterpillars produce nutritious secretions (honeydew) from specialized organs for the ants to eat, and in exchange the ants protect the caterpillars from predators and parasitoids. There are many aspects of this interaction that are tantalizing to a biologist, not least of which are the behavioural and communicative adaptations that must take place in order for the association to work. Caterpillars use a variety of mechanisms, including chemical mimicry and acoustic signaling, to elicit the favor to ants.

A 2nd instar caterpillar being tailed by an ant which is eyeing the nectary fluid excreted by the caterpillar.

A sequence of three pictures showing an ant receiving its pay packet of a nectary droplet from the 2nd instar caterpillar.

Moreover, the interactions can be highly variable, with different lycaenid species engaging in different ‘flavors’ of ant association. Some lycaenids do not associate with ants at all, and among those that do the interaction can range from generalist, facultative mutualism (meaning that the caterpillars don’t need ants to survive, but they’ll associate with them if they’re available) to species-specific, obligate associations (a caterpillar’s survival absolutely requires being adopted by the correct ant species).  The interaction is not always a truly cooperative one either: there are many species of lycaenids that have evolved to parasitize their ant partners. In these cases the ants still care for the lycaenid caterpillars, but instead of feeding on plants like the majority of lepidopteran larvae, the caterpillars switch to carnivorous food sources such as ant brood or other insects that are within the ants’ care. Amazing!

A Quaker adult.

A Quaker caterpillar being tended by an ant.

However, despite the fascinating life histories and the commonness of lycaenids worldwide, they remain some of the most mysterious butterflies in many places.  For example, if you look through the lycaenid section of a good butterfly field guide, you might be amazed to see how often the larval food source is unrecorded. Moreover, many times we think we know what a species eats, we're dead wrong! Hostplant records are often based on anecdotal field observations or on rearing experiments in captivity, but what a caterpillar will eat versus what is does eat are two different stories. Horace recently told me that he's successfully reared the Ciliate Blue (Anthene emolus), a species known to be carnivorous throughout SEA, on plants, and that he has also observed "known" herbivores munching on treehoppers. Go figure.

A mother Singapore Four-line Blue laying an egg on its host plant.

Several caterpillars of the Singapore Four-line Blue with ants in attendance.

Close-up view of one caterpillar (and one ant) in the picture above.

I suspect that carnivory is more widespread than we think. I often come across species descriptions that say something along the lines of "Lives in ant shelters, larval hostplant unknown," and my first suspicion is parasitism. Then again, there are also plenty of species that live inside ant shelters during the day when predators are active, but leave the nests at night to feed on plants under the watchful guard of their ant escorts. In order to describe species' diets and ant associations with confidence, we need systematic observations and study. In lieu of that, the life histories and diets of these species will remain mysterious.

Two early instar caterpillars of the Ciliate Blue (Anthene emolus) with Weaver ants in attendance.

A late instar caterpillar of the Dark Tit (Hypolycaena thecloides).

A final instar caterpillar of the Vinous Oakblue (Arhopala athada).

So, what exactly would we like to know about lycaenid-ant interactions, and why don’t we know it already? For closely ant-associated species, it can be difficult to access lycaenid larvae. Excavating ant nests to search for caterpillars is tough work, and not many people are so inclined to spend their leisure time being attacked by ants. Imagine spending your days opening up weaver ant nests to look for caterpillars--no thank you! But there is some really good stuff in there! The caterpillars of the Moth Butterfly (Liphyra brassolis), one of the coolest lycaenid species in the world, are found only inside weaver ant nests, and a few other lycaenid species have been found in these nests as well. My gut feeling tells me that if more crazy people were out there opening up weaver ant nests we'd be fascinated to find what other animals they host inside. We'd also have a lot of ant bites….

A final instar caterpillar of the Copper Flash (Rapala pheretima sequeira).

A final instar caterpillar of the Pale Mottle (Logania marmorata damis).

But luckily we don’t need to scour every ant nest to answer important questions about lycaenid ecology. We can answer many outstanding questions simply through careful observation - something members of ButterflyCircle truly excel at. By documenting and keeping records of observed associations, we can start to fill in the gaps in our current knowledge. Below is a preliminary list of some easy ways in which the members of ButterflyCircle can contribute important ecological data about Singapore’s lycaenid (and even non-lycaenid) butterflies:

A Branded Imperial adult sipping fluid from the young shoot of its host plant.

Three Branded Imperial caterpillars caught the attention of a large black ant.

• Photograph interactions between ants and lycaenid larvae whenever possible. These photographs can be considered data, and with enough data we can start to understand fundamental aspects of ant-lycaenid interactions: How often do different lycaenid species associate with ants in the wild? Are certain ant species (or genera) preferred over others? What hostplants do these interactions take place on? Are specific behaviours observed?
• Note the habitats that these interactions occur in. Do you only find certain species in certain habitats? How might ant distributions affect lycaenid distributions?
• Photograph ants and hostplants so that they can be identified later.
• Record GPS coordinates along with photos. This goes for non-lycaenid butterflies as well. Having reliable location data can be useful for understanding butterfly dispersal, population dynamics, and habitat use.
• Collect DNA material. Many modern zoological museums are shifting their collections away from dried, pinned specimens toward DNA and tissue collections. Rather than donating spread adults to museums like the Raffles Museum of Biodiversity Research, consider donating larvae, pupae, or adults preserved in ethanol instead. Specimens preserved in this way provide a valuable resource for understanding evolutionary relationships, population genetics, and species delineations of Singapore’s butterflies (and moths too!). While I understand and appreciate that collecting is not an important component of ButterflyCircle’s work, if anyone is interested in learning more about DNA collections please feel free to contact me.

About the author:

Dr. Melissa Whitaker is a postdoctoral fellow at the Harvard Museum of Comparative Zoology, where she studies the evolution and ecology of ant-lycaenid associations. She recently visited Singapore to collaborate with Horace Tan on research focusing on Singapore's lycaenid fauna (funded by the Wildlife Reserves Singapore Conservation Fund). She is a huge fan of the ButterflyCircle’s approach to butterfly study and appreciation. For more information about Dr. Whitaker's research, or to contact her, please visit www.melissawhitaker.net.

Text by Dr Melissa Whitaker; Photos by Khew SK, Horace Tan; Videos by Horace Tan.

Butterfly of the Month - November 2014

Butterfly of the Month - November 2014
The Malayan Eggfly (Hypolimnas anomala anomala)

"It's beginning to look a lot like Christmas..." as the song goes. The eleventh month of 2014 is upon us, as shopping malls and office buildings in Singapore get decorated in anticipation of the year-end holidays and Christmas season. Many shopping malls are getting in on the act early to take advantage of the end of school season and people who would like to do their Christmas shopping early. Even the theme at our Gardens by the Bay already feature Christmas decor and lights to mesmerize its visitors with the colours of the season.

It's been an interesting year of ups and downs, both in the local and global scenes, as Singapore looks ahead towards celebrating its 50th year of independence since 1965. The year 2015 looks like it's going be a pretty busy year for Singapore with many commemorative celebrations and events planned by numerous organisations, both from the public and private sectors. Even ButterflyCircle is also planning on a special 'present' for Singapore's 50th birthday, but let's leave that for later. ;)

On the butterfly conservation and research front, we are encouraged to see more people interesting in butterflies - setting up butterfly gardens and sanctuaries, as well as learning more about butterflies through observing them and photographing them. As the Lee Kong Chian Natural History Museum, one of the region's first custom-designed building for a natural history museum readies itself for completion, several exciting initiatives and projects, in collaboration with ButterflyCircle, are in the works.

A typical example of form-nivas of the Malayan Eggfly

ButterflyCircle members have continued to contribute to conservation initiatives and promoting butterfly-friendly projects in collaboration with the National Parks Board. In support of Ubin Day, ButterflyCircle will be conducting a butterfly watching and photography session next Sunday, 30 Nov 2014. The registration for participants is now closed, and we thank all the interested parties for registering and joining us. Weather permitting, we hope that you will have an enjoyable morning at Butterfly Hill on Pulau Ubin!

Upperside of a form-anomala of the Malayan Eggfly

This month, our feature butterfly is the Malayan Eggfly (Hypolimnas anomala anomala). This low-profile and relatively sombre coloured butterfly doesn't usually create much excitement amongst butterfly watchers, when compared to its more colourful and attractive cousins. In fact, it is often mistaken for one of the drab "Crows" from the Danainae family, due to its close resemblance to its distasteful models.

A form-anomala of the Malayan Eggfly feeding on the flowers of the Red Leea

The Malayan Eggfly displays mimetic behaviour, in that it mimics the Crows for protection against predators. It also flies in an unhurried and slow manner, copying the flight of the Crows to fool predators to avoid them as they would for the distasteful Danainaes. From the number of mis-identifications of this species by beginners and casual nature enthusiasts, we can almost conclude that the Malayan Eggfly is a passable mimic of the Crows (at least from the human perspective!).

The Malayan Eggfly is relatively common in Singapore. Seasonally, several individuals can be observed together at various locations, particularly in the vicinity of its caterpillar host plant, Pipturus argenteus, a secondary forest bush that grows quite commonly in the forested areas of Singapore.

A form-nivas with reduced white markings on the hindwing

The species is observed to display territorial behaviour - particularly the males. Individuals select favourite perches amongst shrubbery and low foliage, and perch with wings held upright. Whenever an 'intruder' breaches its domain, it will fly out and try to 'attack' the newcomer. At other times, it returns repeatedly to its favourite perches even when disturbed.

In the typical form, the Malayan Eggfly is reddish brown on the upperside, with a series of post-discal and submarginal white spots on both wings. The underside is usually darker and bears the white spots as on the upperside. The species is subject to considerable variation in the extent of additional white markings on the hindwings, although two distinct forms are documented for this species.

Form-anomala is the typical brown form where the hindwing post-discal area is unmarked, both on the upper- and undersides. This form is the more commonly observed one, and is quite widespread in distribution, from urban parks and gardens to the forested sanctuary of the nature reserves.

Typical form-nivas with prominent white post-discal patches of varying degrees on the hindwing on both the upper and undersides

The other form, which is slightly less encountered, features a series of white post-discal streaks on the hindwings. This is form-nivas. Between the two forms, is a wide spectrum of variations from totally no postdiscal markings, to a few obscure streaks, to a prominent white patch on the hindwings.

A female variant with iridescent blue forewings resembling a Striped Blue Crow

The two forms are passable mimics of the Danainae species that are also found in Singapore - Striped Blue Crow (for form-anomala) and Lesser Striped Black Crow (for form-nivas). However, not infrequently, a third "form", with iridescent blue forewings on the upperside, is seen. This variant is usually female, featuring the attractive blue forewings and we believe it mimics the male Striped Blue Crow. Ecologically, it also makes sense that the female has a series of alternative mimetic strategies to ensure a higher chance of survival to prolong its lifespan to be able to lay as many eggs as possible before it falls prey to a predator or dies of natural causes. However, why this is not considered a different form or documented in any research paper as such, is still not fully understood.

A female Malayan Eggfly standing guard over her eggs

Speaking of egg-laying, the Malayan Eggfly displays a very unique behaviour where the female, after ovipositing from anything between 50 to 100 eggs on the underside of the leaf of its host plant, "stands guard" over the eggs. This behaviour has been documented by researchers and papers have been written about it, but it is not really known why the female does that, because a butterfly does not possess the means nor arsenal of offensive weaponry to fend off any potential predators of her eggs.

Another shot of a form-anomala female Malayan Eggfly standing guard over her future babies

In some instances, the female stands guard over her eggs until the first instar caterpillars hatch and start eating the leaf. The adult butterfly, in at least two of our observations, died in that position, "protecting" her eggs till her last breath. In a controlled environment on one occasion, we physically removed the female butterfly from her perch, only to see it fly back the moment it was released, back to stand guard over her progeny!

The Malayan Eggfly is partial towards human sweat as can be seen here, feeding on a sweaty camera body and a sweaty finger.  The top photo shows the species puddling at sandy streambanks

The Malayan Eggfly has also been observed puddling at sandy streambanks and muddy footpaths. It also has a liking for human sweat and there have been instances where it stays on the hands and arms of ButterflyCircle members, sipping sweat.

A mating pair of form-anomala Malayan Eggfly

The life history of the Malayan Eggfly has been fully documented here in Singapore, feeding on the caterpillar host plant, Australian Mulberry (Pipturus argenteus). The detailed life history of this species can be found here.

Text by Khew SK : Photos by Sunny Chir, Goh EC, Huang CJ, Koh CH, Khew SK, Loke PF, Jonathan Soong, Horace Tan, Nelson Ong and Anthony Wong.

Life History of the Full Stop Swift

Life History of the Full Stop Swift (Caltoris cormasa )

Butterfly Biodata:
Genus: Caltoris Swinhoe, 1893
Species: cormasa Hewitson, 1876
Wingspan of Adult Butterfly: 32-34mm
Caterpillar Local Host Plants: Ottochloa nodosa (Poaceae), Panicum maximum (Poaceae, common name: Guinea Grass), Ischaemum ciliare (Poaceae, common name: Smut Grass).

Physical Description of Adult Butterfly:

On the upperside, the wings are dark brown with hyaline spots in spaces 2,3 and 4, subapical spots in spaces 6 and 7 and two cell spots in the forewing. The upper cell spot is typically either absent or small in comparison to other Caltoris spp. On the underside, the wings are ferruginous brown, usually with a purplish tinge.

A close-up view of the forewing upperside, showing two small cell spots of a Full Stop Swift.

The upperside view of a newly eclosed Full Stop Swift. The upper cell spot is absent  while the lower cell spot is small.

A Full Stop Swift visiting flower in a wasteland.

Field Observations of Butterfly Behaviour:

The Full Stop Swift is moderately common in Singapore. The adults have been sighted in multiple locations including forested areas, wastelands, urban parks and gardens across the island. The adults fly with a swift, strong and darting flight.

Early Stages:

The Full Stop Swift have been bred on a number of grass species, three of which have been identified: Ottochloa nodosa, Panicum maximum and Ischaemum ciliare. The caterpillars feed on leaves of the host plants, and live in shelters formed by joining edges of a grass blade together.

Local host plant #1:Ottochloa nodosa.

Local host plant #2:Panicum maximum.

The eggs are laid singly on the upperside of a grass blade of the host plant. Each dome-shaped egg is reddish with white fuzzy patches on the lower half. The micropylar sits atop and a number of very fine and obscure  ridges running longitudinally from it. The basal diameter is about 1.2-1.3mm.

Full Stop Swift caught in the act of ovipositing on two separate occasions.

Two views of an egg of the Full Stop Swift.

Maturing eggs on the 2nd last day (left) and the last day (right) of the oval phase.

It takes about 4.5-5 days for the egg to hatch. The young caterpillar eats just enough of the shell to emerge, and has a length of about 2.2mm. Its orangy body is cylindrical in shape and has a tuff of few moderately long setae at the posterior end. The head capsule is black. A black collar mark can be found the dorsum of the prothorax. The newly hatched nibbles away most of the egg shell remnant before proceeding to construct its first leaf shelter.

Two views of a newly hatched caterpillar, length: 2.2mm

A newly hatched caterpillar in its very first leaf shelter. Further "stitching" work by the caterpillar will bring the two opposite edges together.

The body turns yellowish green after the caterpillar has a few sessions of the leaf diet. By the time the caterpillar lies dormant for its moult to the 2nd instar, its length has reached 5.5mm. The 1st instar takes a total of 3 days to complete.

Two views of a 1st instar caterpillar, length:4mm.

The 2nd instar caterpillar still has a yellowish green body, and the head capsule is still black. The black collar mark on the prothorax has faded to just to hint of its presence. This instar lasts about 4 days with the body length reaching about 7.5-8.5mm.

Two views of a 2nd instar caterpillar, length: 5.5mm.

The 3nd instar caterpillar still has a black head capsule but its body is now much paler yellowish green compared to the 2nd instar. There is no longer any trace of the black collar mark on the prothorax. This instar lasts a total of 4-5 days with the body length reaching about 12-13mm.

Two views of a 3rd instar caterpillar, early in this stage, length: 9.2.

A 3rd instar caterpillar, late in this stage, length: 11mm.

The 4th instar caterpillar resembles the 3rd instar caterpillar closely. In some specimens, the head capsule is no longer entirely black as pale brownish lateral patches can be observed. This penultimate instar lasts 4-5 days with the body length reaching up to 20-23mm.

A 4th instar caterpillar with head capsule bearing brownish lateral patches. length: 17mm.

Two views of a 4th instar caterpillar, late in this stage, length: 20mm.

The 5th instar caterpillar has a pale yellowish body. In a drastic change, its head capsule is now whitish in ground colour but reddish brown along the periphery and various sulci (groove/furrow). Two reddish brown stripes rise from the adfrontal area, giving the appearance of a chinese character 山. The anal plate is unmarked as in the all previous instars. This final instar takes about 6-8 days to complete with the body length reaching 37-38mm.

Two views of a 5th instar caterpillar, top: 27mm, bottom: 34mm.

Two views of a 5th instar caterpillar, late in this stage, length: 35mm.

Towards the end of 5th instar, the body of the caterpillar shortens in length and body colour assumes a uniform shade of pale lime green. It seeks out the underside of a leaf blade and forms a shallow but half-open shelter with silk threads at both ends. The body excretes a moderate amount of white waxy material at this stage. Within the shelter, a silk girdle and a silk pad are then spun. Once the caterpillar attaches its claspers to the silk pad, it enters the dormant prepupatory phase which lasts about one day.

Two views of a dormant pre-pupa of The Full Stop Swift.

The pupa secures itself with the silk girdle and with its cremaster attached to the silk pad. It has a short thorax, a rather long abdomen, a short and pointed rostrum. The body is uniformly deep lime green with no markings. Length of pupae: 28-30mm.

Two views of a pupa of a male Full Stop Swift, length: 29mm.

After 7 days, the pupa becomes mostly black in color in the wing pads and in the body segments. Eclosion takes place the next day.

Two views of a mature pupa of the Full Stop Swift, shortly before the eclosion event.

A newly eclosed Full Stop Swift.

References:

• [C&P4] The Butterflies of The Malay Peninsula, A.S. Corbet and H.M. Pendlebury, 4th Edition, Malayan Nature Society, 1992.
• Butterflies of Thailand, Pisuth Ek-Amnuay, 2nd Edition, 2012.
• A Field Guide to the Butterflies of Singapore, Khew S.K., Ink On Paper Communications, 2010.

Text by Horace Tan, Photos by Benjamin Yam, Koh Cher Hern, Chng CK and Horace Tan