The Peninsula SkollyA tale of Skollys, pugnacious foster parents and addiction by André Claassens he fynbos environment presents many intricate examples of symbiotic relationships between insects and plants. The close association between the larvae of certain species of butterfly of the large family Lycaenidae (blues and coppers) and certain species of ants is so essential that the butterflies would not be able to survive without the ants. The relationship between ants and other species of insects is known as myrmecophily. Insects that manage, by hook or by crook, to live in ants’ nests either as welcome or uninvited guests are called myrmecophiles or myrmecophilous insects. In past editions of Veld & Flora I have described the intricate relationship between the larvae of certain ‘blue’ butterflies such as the Trimen’s Blue and their host-ant, the large Spotted Sugar Ant, as well as the association of the larvae of the Red Copper butterfly with the small Black Sugar Ant. This is the story of yet another remarkable form of mutualism that exists between the larvae of a butterfly named the Peninsula Skolly and the Pugnacious Ant. Ants like other social insects are generally unfriendly towards other creatures, nevertheless they occupy a unique position in the habitats in which they occur because of their nest-building and food-gathering habits as well as their brood-care that includes feeding their larvae, all of which is aimed at the survival of their colonies. Less secure insects such as certain Lycaenid butterflies have taken advantage of one or more of the survival techniques of certain ants and have developed methods of appeasing their hostants’ naturally aggressive nature. The Peninsula Skolly (Thestor yildizae) is the only butterfly endemic to the Cape Peninsula. It dwells high up on Table Mountain, on the Saddle between the main mountain and Devil’s Peak from where most of the material used in the study of this butterfly was obtained. It also occurs, 124 VeLD&FLOrA | SEPTEMBER 2011 Brown, also known as Table Mountain Brown (Pseudonympha hippia). To meet this deepbrown butterfly with its silver-grey underside, one has to climb from the Saddle halfway up Devil’s Peak, sometimes even higher, where it flies from about early December until early March. Its larvae feed on certain grasses. As the name suggests, Burchell’s Brown was first caught by the famous English explorer William Burchell, who caught it at the top of Table Mountain in 1811 The Peninsula Skolly Females of other myrmecophilous butterflies usually choose ovipositing sites on or close to their larval food-plants that grow near their larvae’s future host-ant nests. Skolly butterfly larvae, however, do not feed on plants at all and depend on Pugnacious Ants for their survival from the moment they emerge from the eggs. For that reason Skolly butterflies oviposit randomly on rocks, bare ground, dry twigs and debris; but only in habitats where Pugnacious Ants abound. What happens to the newly hatched Peninsula Skolly larvae in their natural environment has never been observed, but later instar larvae and pupae are often found in Pugnacious Ants’ nests under rocks. The only way to find out more about the Peninsula Skolly’s newly hatched larvae was to allow captive females to oviposit in a formicarium and watch the interactions of the newly hatched larvae with their ‘adoptive’ ants. Observations in a formicarium Female Peninsula Skolly butterflies were placed in the arena (a spacious enclosure) attached to the main plaster of Paris nest of a formicarium housing a colony of Pugnacious Ants. They readily oviposited on the floor and sides of the arena regardless of the presence or absence of ants. In fact females placed in boxes without ants also oviposited without host-ants being anywhere near them. The larvae took about ten days to hatch, but what happened to these tiny, 1.5 mm long larvae baffled myself and Alan Heath who, in addition to the Peninsula Skolly, also studied the similar Riley’s Skolly (Thestor rileyi), that he caught on the Helderberg Mountain near Somerset West. The newly hatched larvae behaved in exactly the same manner as those of the Peninsula Skolly. Once hatched the tiny larvae crawled about, instinctively lifting their head and anterior end of their body well above the ground to enhance their chances of being found by a hostant. Ants soon noticed the larvae and after touching them with their antennae seemed to recognize them as ant-friendly beings. They picked them up and carried them to the nest where they deposited them on T Skollys LEFT: Peninsula Skolly upper side of male, top, and female, below. ABOVE: A male specimen of Claassens’ Skolly. BELOW: Fynbos on the Saddle between Table Mountain and Devil’s Peak – habitat of the Peninsula Skolly. Photos: André Claassens. or it least did occur, in places on the slopes of the Twelve Apostles, Orange Kloof, Little Lion’s Head, Karbonkelberg, Constantia Nek and Vlakkenberg. Further afield it flies on Silvermine and Muizenberg mountains as well as on Red Hill above Simon’s Town. Adults of the Peninsula Skolly are on the wing from about mid November until about mid February, while their early stages (larvae and pupae) are spent in close, and indeed obligatory, association with the common Pugnacious Ant (Anoplolepis custodiens). The following description of the lifecycle of the Peninsula Skolly is based on observations made in the field as well as in homemade ants’ nests. Climbing the Saddle. After zigzagging up and up the slope leading from Tafelberg Road to the top of the Saddle it is quite a relief reaching the peaceful, large, flat, open fynbos-covered area. I have often visited the Saddle either on my own or with the late Charlie Dickson in whose company I found the first known pupa of the Peninsula Skolly in January 1975. It is also the place where I found that butterfly’s first known final instar larva in December l979. Both the larva and the pupa were found under rocks covering nests of the Pugnacious Ant. In later years I visited the Saddle often in the company of Alan Heath, a lepidopterist of ant-associated larvae and pupae-digging fame, to collect Skolly larvae and pupae together with numbers of host-ants to place in a formicarium for investigation. On one memorable occasion I slogged up the Saddle accompanied by the late farmer and lepidopterist Victor Pringle of Bedford, who, although well in his seventies, was anxious to experience for himself the Peninsula Skolly and its early myrmecophilous stages in their natural environment. On few occasions, while on the Saddle, I was closely watched by one or two of the then still common Himalayan Tahrs that tolerated me in their usually undisturbed grazing area as long as I kept my distance. Sometimes, to avoid being caught in fast approaching thick mist, I had to quickly gather my collecting gear and run down the winding mountain path back to the road where I had parked my car. Many other butterflies occur on the Saddle, including several blues such as the beautiful Peninsula Blue (Lepidochrysops oreas oreas) whose larvae are associated with the Black Marsh Ant (see Veld & Flora, December 2007) as well as several browns such as Burchell’s ABOVE: Cape Town’s only endemic butterfly, the Peninsula Skolly. Photo: André Claassens. BELOW: Burchell’s Brown. Photo: Steve Woodhall. BOTTOM: Peninsula Blue. Photo: Steve Woodhall. Skolly butterflies belong to the genus Thestor of the family Lycaenidae. The genus is made up of 27 species, only one of which, the Basuto Skolly (Thestor basutus basutus) is not endemic to South Africa. They are colloquially known as Skollys*, because of their sombre, rather scruffy appearance. (Skolly is a South African slang term for gangster or ragamuffin.) In some the upper side is almost black, but others have colours varying from light to dark yellow or even greenish. Taking their upper wing colours into consideration lepidopterists for convenience sake refer to black Skollys and yellow Skollys. The underside of the wings of Skollys is mainly light to dark grey with dark to black markings and patterns that are usually helpful in identifying different species, but comparisons of their internal sex organs are sometimes necessary to separate very similar individuals. Unlike other butterflies, Skollys do not feed on flower nectar, nor do they survive on any other diet. Their sucking mouth parts are poorly developed and they therefore rely on food reserves stored in their bodies during their larval stage. It has been found that the larvae of all Skollys examined so far are dependent on the common Pugnacious Ant for their survival and that the Skolly butterflies only occur in habitats where these ants occur in abundance. *Incidentally at first I did not like the name Skolly for these harmless butterflies, even though they acquired their common name long before their life-history involving ants was known, but since one of them, Claassens’ Skolly (Thestor claassensi), shares my name I have dropped my objections. ‘My’ Skolly butterfly occurs near Stilbaai. the floor, mostly near the entrance, and left them to their own devices, never feeding them. This experiment was repeated on several occasions but always with the same unsatisfactory result. All the Peninsula Skolly larvae and Riley’s Skolly larvae died after a few days wandering about searching for food. The ants picked the little corpses up and deposited them in a corner of the nest where they usually dumped other debris. What was missing in our artificial nests that would ensure the survival of the Skolly larvae in their natural environment? The diet of the newly hatched larvae Lepidopterists researching the life-history of other Skolly butterflies have found that the earliest stages of some species like the Basuto Skolly (Thestor basutus capeneri) and Boland Skolly (Thestor protumnus aridus) feed on coccids (scale insects) and psyllids (jumping plant lice). Both insects belong SEPTEMBER 2011 | VeLD&FLOrA 125 to the family Homoptera that feed on plant juices and excrete excess sugars onto their bodies and immediate surroundings. It is also known that Pugnacious Ants visit the plant-sucking insects to imbibe their sweet excretions. How the newly hatched Skolly larvae arrive at a site where coccids and psylids are present has so far remained unanswered. Having observed the behaviour of the ants towards newly hatched larvae in a formicarium, it is my strong belief that under natural conditions, ants pick up the tiny Skolly larvae, wherever they meet them while foraging outside their nest, and place them among the plant-sucking bugs; which most probably constitute the diet of the early Peninsula Skolly larvae. How the ants ‘know’ how to save the larvae that initially have nothing to offer them is another unanswered question, but it appears that the larvae soon develop glands that secrete honeydew. This sweet secretion is much sought after by the ants, and they keep visiting these larvae as well as the plant-sucking insects on which the larvae feed. Some time during late summer ABOVE: Riley’s Skolly. Photo: André Claassens. BELOW: Peninsula Skolly – the penultimate (fourth) instar larva in the host-ant’s nest situated under a rock. Photo: Alan Heath. Pugnacious Ants Pugnacious Ants are small to medium sized, reddish brown insects. The workers are polymorphic (they appear in various sizes) ranging from a length of about 2 mm to about 10 mm. There are no soldiers. The queens, of which there are usually more than one – sometimes several – present in a colony, measure up to 13 mm in length. Often winged males as well as winged, virgin females are present. There are two closely related and very similar species of Pugnacious Ant respectively known as Anoplolepis custodiens and A. steingroeveri. Both species are very common in fynbos environments but do also occur in other habitats at low and high altitudes; and it is assumed that both host Skolly larvae. They usually nest under large, flat rocks ABOVE: A Riley’s Skolly larva seeking the attention of a Pugnacious Ant. BELOW: A Pugnacious Ant (Anoplolepis custodiens) about to pick up a Riley’s Skolly larva. Photos: Alan Heath. but where these are not available, also dig out subterranean passages and chambers in the soil. They are intolerant of other insects, including other ants, and indeed any intruders, as well as lepidopterists interfering with their nests in which case they crawl up their legs and arms and attack with fierce bites. Pugnacious Ants live on a mixed diet of flower nectar, certain seeds, honeydew secreted by various plant-sucking insects, dead insects and other dead animal material. Like certain other species of ant, the Pugnacious Ants collect elaiosomebearing seeds of fynbos plants, for example, proteas, and in doing so play a very important role in the dispersal of seeds of these plants. Seed collecting by ants is known as myrmecochory. Notwithstanding their hostile nature, the Pugnacious Ant or Malmier (crazy ant) as it is known in Afrikaans, allows certain insects such as the larvae of Skollys and certain other Lycaenid butterflies into its nest, where they are treated well and fed as if they were the ants’ own brood. This is only in return for their guests’ sweet secretions to which they appear to have become addicted. Pugnacious Ants easily adapt to an artificial nest in which they survive on sugar solutions, bits of meat and dead insects. Unfortunately, like several other fynbos-friendly ants, the Pugnacious Ants, especially those occurring at lower altitudes, are driven out of their nest by the introduced Argentine Ants (Linepithema humile) invading their habitats, robbing them of their food reserves and devouring their brood. In doing so, they have a very detrimental effect on the survival of plants that depend on these ants for seeddispersal. The Argentine Ants is not yet a threat to the Peninsula Skolly associated with the Pugnacious Ant because the invasive ants appear to avoid higher altitudes where this butterfly and its hostant occur. as they feed their own larvae begging for food. After caring for the larvae from the moment they hatched from the eggs by physically taking them to a food source, the ants behaved again as devoted ‘foster parents’ of the Peninsula Skolly’s larvae. Hungry larvae crawled about between the ants with their heads stuck out far and raised above the floor of the nest while approaching an ant, begging for food. An ant responding to a larva’s begging behaviour then placed its mouthparts on the unusually small mouth parts of the larva and fed it by regurgitating food into its mouth, a method of feeding known as trophallaxis (from the Greek words trophe, meaning nourishment and allaxis, meaning interchange). Ants feed their own larvae and their nest-bound queens as well as non-foraging sister-ants in the same manner. It must be noted that under natural conditions all these activities take place in complete darkness and one wonders how the larvae become aware of the proximity of an ant willing to feed it. immunity against potential attacks by the ants. Towards the end of October and during November larvae, after reaching a length of about 20 mm, pupated. The pupae were also visited by the ants that obviously derived some desired secretion from the pupal skin as well. It is thought that the larvae and possibly the pupae, in addition to honeydew, secrete a nest pheromone, which is a kind of communication hormone that allows ants as well as their guests to recognize each other as belonging to the same colony. Nest invaders not equipped with these glands or other methods of appeasement are fiercely attacked and killed. Pupae found in Pugnacious Ants’ nests were also introduced into the arena of the formicarium and when found by foraging ants were dragged into the main nest, where they completed their development into adult butterflies. enough to expand its small, crumpled-up wings, and was attacked and even killed by the ants. ACKNOWLEDGEMENTS Thanks to Alan Heath and to Steve Woodhall for the use of their photographs. READING Claassens, A.J.M. & Dickson, C.G.C. l980. Butterflies of the Table Mountain Range. Struik, Cape Town. Claassens, A.J.M. & Heath, A. l997. Notes on the myrmecophilous early stages of two species of Thestor Hubner (Lepidoptera: Lycaenidae) from South Africa. Metamorphosis 8(2). Claassens, A.J.M. 2007. The butterfly, the ant and the wasp. Veld & Flora 93(4). Claassens, A.J.M. 2009. The Red Copper and the Black Sugar Ant. Veld & Flora. 95(2). Parker-Allie, F., Robertson, H. & Richardson, D.M. 2008. The Argentine ant. Veld & Flora 94(1). Skaife, S.H. l961. The study of ants. Longmans, Cape Town. Slingsby, P. & Bond, W. 1981. Ants friends of the fynbos. Veld & Flora 67(4). Slingsby, P. 1982. The Argentine Ant: how much of a threat? Veld & Flora 68 (4). Williams, M.C. & Joannou, J.G. 1996. Observations on the oviposition behaviour and larvae of Thestor basutus capeneri Dickson (Lepidoptera: Lycaenidae: Miletinae) in South Africa. Metamorphosis 7(1). Woodhall, S. 2005. Field guide to butterflies of South Africa. Struik, Cape Town. partners derive benefit and neither partner is harmed. myrmecochory From Greek myrmex meaning ant and chore meaning farm. Ants collect certain seeds, store them in their nests and feed on their elaiosomes. Seeds with elaiosomes attached to them are referred to as myrmecochorous seeds, and plants that use ants for seed dispersal are referred to as myrmecochorous plants. myrmecophily The relationship between ants and other species of insects – from the Greek words myrmex meaning ant and philos meaning love. oviposit Female butterflies have a structure at the end of their abdomen known as the ovipositor, which she uses to deposit her eggs on a surface. SEPTEMBER 2011 | VeLD&FLOrA 127 or autumn, after moulting into their fourth, penultimate instar and no longer being satisfied by the plant-sucking insects that by this time may even have become scarce, they follow the ants into their nest, or they are carried there by the ants, keen to secure their source of honeydew. They spend the remainder of their larval and their pupal stages in the safety of their host-ants’ nests, only emerging as adult Skollys sometime between November and February. How do the larvae survive inside their host-ants’ nest? Did they feed on ants, ant brood or debris found on the floor of the nest, or did they perhaps leave the nest at night to feed on plants or plant-sucking insects? The answer to those questions soon became evident. The final two instars Once the larvae were inside the ants’ nest, observations were again possible. Late larval instars found in Pugnacious Ants’ nests under rocks on the Saddle were placed in the arena of a formicarium from where they followed foraging ants into the nest compartment that, being covered with glass, allowed me to view them, especially at night when the ants were most active. We found that at night the ants were not disturbed by artificial light. (When not under observation the glass top was covered with a dark cloth to imitate the normally dark nest condition.) To our surprise the larvae did not feed themselves any more. They had changed their insectivorous feeding habit into foodbegging behaviour resulting in the ants feeding them by mouth in the same manner Flying the nest Adult butterflies emerge from the pupal shells from about mid November. The mature butterflies (also referred to as imagines) The ants’ reward escaped quickly from the nest compartment Several ants were sometimes found near or into the arena, where they completed wing on top of butterfly guest larvae, which soon expansion – a process that could not, even outgrew even the largest ants in the colony. in the wild, have taken place inside the They pressed their mouth parts on the narrow confines of the nest. The abdomen larvae’s skin, obviously imbibing a desired of the emerging imagines were covered with secretion exuding from small epidermal loose, fluffy material, presumably protecting glands. The butterfly larvae thus rewarded them against attacks by the host-ants that the ants’ hospitality and ensured their no longer recognized them as members of the colony. The imagines obviously lack the TOP RIGHT: The Peninsula Skolly butterfly. Photo: Andre Claassens. ant-appeasing secretions that so successfully BELOW: Peninsula Skolly – the final (fifth) instar larva being mouth-fed by a pugnacious ant. Photo: Alan Heath. protected them during their larval and pupal BOTTOM: Peninsula Skolly pupae in a host-ant’s nest. stages. Ants chased freshly emerged Skolly Photo: André Claassens. imagines that frantically tried to find the exit to the arena, but when grabbed from behind by ants, were quickly released as the attackers, using their front-legs as brushes, tried to clear the loose, dry material covering the Skolly’s abdomen from their mouths. Rarely an imago failed to find the exit soon WHAT DOES THAT MEAN? elaiosome From Greek elaion meaning oil and soma meaning body. Some plants produce seeds with an oil-rich attachment known as an elaiosome. This attracts ants that collect these seeds and after eating the nourishing elaiosomes, leave the seeds minus their elaiosomes behind in or near their nests, safe from seed-eating birds and mice where they later may germinate. formicaria (singular: formicarium) Artificial ant nest - from the Latin word formica meaning ant. imagines (sing. imago) Mature butterflies. instar From Latin instar meaning form or stage between moults of an immature insect. mutualism A form of symbiosis in which both 126 VeLD&FLOrA | SEPTEMBER 2011