The effect of host-plant quality on the survival of larvae and oviposition by adults of an ant-tended lycaenid butterfly, Jalmenus evagoras

Abstract.

• 1 Juveniles of the Australian lycaenid butterfly, Jalmenus evagorus (Donovan), secrete to ants a solution of sugars and amino acids, primarily serine. The attendant ants protect the larvae and pupae from parasites and predators.
• 2 The effect of caterpillar nutrition on the defence provided by ants was investigated. Potted food plants of Acacia decurrens were either given water containing nitrogenous fertilizer or were given water alone. Fertilized plants had a higher nitrogen content than unfertilized plants.
• 3 Fifth instar larvae of J.evagoras feeding on fertilized plants attracted a larger ant guard than those feeding on unfertilized plants. In the absence of caterpillars, ants were not differentially attracted to fertilized and unfertilized plants.
• 4 In the presence of ants, over a 10-day period, larvae on fertilized plants survived better than larvae on unfertilized plants. In the absence of ants larvae survived equally on fertilized and unfertilized plants. It is concluded that larvae on fertilized plants attracted a larger ant guard, and thereby survived better, than larvae on unfertilized plants.
• 5 Adult females of J. evagoras preferred to lay egg batches on fertiized, rather than unfertilized plants, but they did not lay larger egg batches.

     

Local distribution of the lycaenid butterfly,Jalmenus evagoras,in response to host ants and plants

Summary The caterpillars of Jalmenus evagoras are tended by ants as they feed upon Acacia trees. In the area of Brisbane, Australia, J. evagoras require ants of the Iridomyrmex anceps species group; predation and parasitism are so intense that larvae and pupae deprived of attendant ants cannot survive (Pierce 1983). We investigated the efficiency with which J. evagoras locate and exploit the host ant resource by sampling 737 quadrats in 30 sampling grids and six study sites containing appropriate host plants; ants were collected at baits located in the center of each quadrat. J. evagoras was found in all habitats where I. anceps cooccurred with host Acacia. Nine of the ten sampling grids which had three or more I. anceps/Acacia host quadrats also had colonies of J. evagoras present (or immediately adjacent), including sites as far as 35 km apart. Of 19 sampling grids on which host quadrats were rare (i.e., less than three quadrats), none had J. evagoras (P<0.001). Within sample grids, I. anceps was distributed indepedently from Acacia trees, suggesting that they are not dependent for their survival on either Acacia or on J. evagoras. Within montane pasture habitats, I. anceps and at least one other ground-dwelling Iridomyrmex species were distributed in mutually exclusive ant mosaic territories which were stable during a one month period. I. anceps did not colonize or tend pupae of J. evagoras experimentally placed in adjacent territories of a different, nontending species of Iridomyrmex, demonstrating the integrity of territory boundaries. Sampling of ants in Acacia trees revealed that, in the absence of J. evagoras, Iridomyrmex workers are not common above ground level, and that their numbers decline in larger trees (P=0.02). In I. anceps territories, eight of nine J. evagoras pupae placed in trees over 3.0 m tall were not found after 24 h whereas all ten controls placed in low trees were found and tended (P=0.00012). This may explain why J. evagoras tends to oviposit in trees less than 2.0 m tall. An alternative hypothesis, that smaller trees have higher content of total nitrogen, and are threfore more nutritious, was not supported. We conclude that the local distribution and host tree selection by J. evagoras is dependent upon the distribution, patchiness, and foraging behavior of the host ant, I. anceps, and its spatial overlap with a number of species of host Acacia.     

Effects of Argentine ants (Hymenoptera: Formicidae) on myrmecophilous lycaenid butterfly,Narathura bazalus (Lepidoptera: Lycaenidae), in western Japan

Effects of the invasive Argentine ant, Linepithema humile (Mayr), on a myrmecophilous butterfly, Narathura bazalus (Hewiston), were investigated in the field in western Japan. Larvae of N. bazalus were attended by workers of Argentine ants in invaded parks and of ten native and one cosmopolitan ant species in uninvaded parks. The abundance of eggs and larvae were not significantly different between invaded and uninvaded parks. Pupal weight and parasitized ratio by tachinid flies were also not different between the two types of parks. These results indicate that the role of Argentine ants for the butterfly might be almost equivalent to the native ants.     

Absence of cuticular alkenes allows lycaenid larvae to avoid predation by Formica japonica ants

Chemical mimicry and camouflage based on cuticular hydrocarbons (CHCs) are adaptive strategies that are frequently observed in myrmecophilous insects. The larvae of several lycaenid butterfly species that exhibit obligate associations with specific ant species have been reported to use chemical mimicry. However, little is known about the strategies used by the larvae of species that have facultative associations with multiple ant species. We attempted to reveal the effects of larval CHC profiles on interactions with Formica japonica workers, using three lycaenid species, two facultative ant‐associated (Lycaeides argyrognomon and Zizeeria maha) and one non‐ant‐associated (Lycaena phlaeas), which commonly possess n‐alkanes as the major CHCs. In field bioassays, the lycaenid larvae were attacked by ant workers less often than larvae of Papilio polytes (Papilionidae), the CHCs of which were rich in 7‐alkenes. Treating the lycaenid larvae with 7‐heptacosene and 9‐heptacosene significantly activated ant aggression (biting), whereas treating them with n‐heptacosane, n‐octacosane and 13‐methylheptacosane had little effect. Furthermore, larvae of Pieris rapae (Pieridae), possessing n‐alkanes as the dominant CHCs, suffered an intermediate level of ant biting between the lycaenid and Pa. polytes larvae. However, treatments of the P. rapae larvae with 7‐heptacosene and 9‐heptacosene significantly affected the frequency of ant biting. These findings suggest that the absence of alkenes in larval CHC profiles is an effective means of circumventing predation by ants and allows lycaenid larvae to inhabit the foraging territory of predaceous ants, at least to some extent.     

The effect of ant association on the population genetics of the Australian butterfly Jalmenus evagoras (Lepidoptera: Lycaenidae)

Populations of the myrmecophilous lycaenid Jalmenus evagoras Donovan were assessed for genetic structure at three hierarchical spatial scales: sites, geographically-defined subpopulations, and subpopulations defined by species of mutualistic ant-associate. Estimates of Wright's FST generated from multilocus electrophoretic data revealed low, though significant, amounts of genetic structure. Most structure was observed at the level of geographic subpopulations, suggesting that adult butterflies do not exhibit preferential mating and oviposition along the lines of ant associate. The genetic structure data, together with estimates of Nei's genetic distance (D) for pairwise site and subpopulation comparisons, suggest that J. evagoras populations are spatially and temporally dynamic. These patterns are considered in the context of extinction and recolonization models. The extreme patchiness of J. evagoras populations stems from the stringent requirements of both host plant and host ant, contributing to an extinction/ recolonization process. We discuss the key parameters influencing genetic cohesion versus differentiation under an extinction/recolonization regime, including mode of butterfly dispersal, site turnover rate, and the effects of host dispersal and phenology. This system provides a model of population-level consequences of certain mutualistic interactions as well as of a class of patterns arising from an extinction/recolonization process.     

Comparative study of the morphology of stridulatory organs of the Iberian lycaenid butterfly pupae (Lepidoptera)

We compared the pupal stridulatory organs of 35 species and one subspecies of Iberian Lycaenidae using scanning electron microscopy. The studied species belong to the tribes Theclini, Eumaeini, Lycaenini, and Polyommatini. Nine species do not show stridulatory organs on the pupae but all other species possess them. Stridulatory organs are formed by a stridulatory plate (pars stridens) placed on the fifth abdominal segment and a file (plectron) in the sixth abdominal segment. The plate has tubercles in the Theclini and Lycaenini, tubercles, ridges, or undulations in the Eumaenini, and tubercles, teeth, or unspecialized structures in the Polyommatini. Morphological differences can be found in the files of the different tribes, regarding the number of teeth, their form and size. Cuticular formations of the organs were studied on a surface of 2,500 µm² and the average of ridges, tubercles, and teeth was measured searching for relevant taxonomic information. Stridulatory organs were thought to be an adaptation to myrmecophily but we show that they are present both in myrmecophilous and nonmyrmecophilous species; therefore, we suggest that this trait probably did not evolve in relation with myrmecophily, but may be used to enhance relationships with ants. J. Morphol. 275:414–430, 2014. © 2013 Wiley Periodicals, Inc.     

Variation in behavior of lycaenid larvae when attended by different ant species

Partner quality can be crucial for the outcome of a mutualistic interaction. In multi-species associations, the characteristics of potential partners can vary substantially and thus the associated benefits. As a consequence of such variation, one might expect strategies of adjusting investments to the characteristics of a partner. Lycaenid butterfly larvae often interact mutualistically with several ant species of different size and aggressiveness and thereby different ability to protect the larvae. Attending ants are rewarded with nutritious secretions. Both ant behavior and a larva's need for protection are known to influence larval investment in the relationship. This study investigates the effect of six ant species on larval behavior in the lycaenid butterfly, Glaucopsyche lygdamus. The overall level of secretion, as well as the response to varying number of attending ants, were found to be influenced by ant species. This revised version was published online in November 2006 with corrections to the Cover Date.     

Pupation site choice of a North American lycaenid butterfly: the benefits of entering ant nests

Abstract.

• 1 Larvae of the North American lycaenid butterfly Hemiargus isola Reakirt tended by the ant Formica perpilosa Wheeler often enter nests of this ant species, and pupate in tunnels and chambers near the surface. Untended larvae and those tended by the ants Dorymyrmex Forel sp. (smithi complex), Forelius foetida (Buckley), and Myrmecocystus mimicus Wheeler pupate in crevices in the ground, under bark, and on leaves; but rarely inside ant nests.
• 2 The location and structure of F.perpilosa nests facilitates discovery by H.isola prepupae. At the southeast Arizona study site, F.perpilosa nests are located at the base of H.isola's host plant, whereas other species’nests are in open ground. Also, F.perpilosa nest openings are wide, whereas those of other species may be too narrow for prepupae to enter.
• 3 Prepupae associated with F.perpilosa spent 67% less time on the ground searching for pupation sites than prepupae associated with other ant species. Pupae in artificial chambers connected to F.perpilosa nests were 4–5 times less likely to disappear overnight, presumably due to predation, than those not connected to nests.
• 4 Formica perpilosa ants tend pupae inside nests. However, in the laboratory experiments tended pupae did not lose more weight prior to eclosion than untended ones, suggesting that chemicals or sounds produced by pupae as ant attractants are inexpensive, or are produced whether or not ants are present.
• 5 Newly-eclosed butterflies exited nests unmolested by ants in the field, but were attacked if confined with ants for several minutes after eclosion in the laboratory.

     

Animal-fed plants: an investigation into the uptake of ant-derived nutrients by the far-eastern epiphytic fern Lecanopteris Reinw. (Polypodiaceae)

The epiphytic fern genus Lecanopteris (Polypodiaceae) is regularly inhabited by five species of Iridomyrmex and Crematogaster, which nest and deposit debris in the hollow rhizomes. These epiphytes gain nutrients from ants in two ways: by root absorption from carton runways which surround plants, and by uptake of solutes from ant faeces and debris through the inner rhizome walls. The rhizome cavity surface is black, minutely pitted and bears no specialized absorptive structures. Nutrients containing 14-glucose, 86-rubidium and 32-phosphorus injected into the rhizome cavity were translocated through the plant. Ants inhabiting Lecanopteris were fed glycine and urea containing 15-nitrogen, and this label was incorporated into the fern tissues. Thus ant-derived nutrients can be incorporated into Lecanopteris tissues. The ferns may gain other benefits from the ants such as defence against herbivores, nurture of juveniles or spore dispersal.     

The use of honeydew in foraging for aphids by larvae of the ladybird beetle, Coccinella septempunctata L. (Coleoptera: Coccinellidae)

Abstract.  1. To clarify the use of honeydew in foraging for aphids by larvae of the ladybird beetle, Coccinella septempunctata L., searching behaviour of ladybird larvae for Aphis craccivora Koch and Acyrthosiphon pisum Harris and the abundance of honeydew under aphid colonies were examined in laboratory experiments.
2. More larvae responded by climbing the plants with aphids than responded to plants without aphids. When the plants were replaced with sticks, in order to exclude visual and olfactory cues from plants and aphids, more larvae of C. septempunctata climbed sticks above the area that contained honeydew than climbed sticks above the area that did not contain honeydew. Then, ladybird larvae use honeydew as a contact kairomone when foraging for aphids.
3.  Aphis craccivora deposited a larger number of honeydew droplets beneath the plants than did similar numbers of A. pisum. Thus, C. septempunctata larvae licked more frequently the honeydew of A. craccivora than that of A. pisum and spent longer searching on the area containing honeydew of A. craccivora than that of A. pisum . Consequently, a larger number of larvae climbed a stick above honeydew of A. craccivora than that of A. pisum.
4. It may be also considered that C. septempunctata larvae can distinguish honeydew of the two aphid species and respond more strongly to A. craccivora than A. pisum.     

Migration of the painted lady butterfly, Vanessa cardui, to north-eastern Spain is aided by African wind currents

1. Thousands of records of migratory butterfly species such as Vanessa cardui flying just above ground-level on fixed compass bearings have led to the common belief that these insects migrate within the so-called 'flight-boundary layer', where movements are relatively independent of the wind. 2. Given the selective advantages of windborne migration and the existence of a number of observations of flights of V. cardui from the upper levels of the atmosphere, we tested the hypothesis that migration from North Africa to southern Europe in this species is influenced by synoptic-scale wind currents. 3. Even with modern technology, it is extremely difficult to observe high-altitude flights directly, so we rely on an indirect approach that examines whether or not arrival peaks in north-eastern Spain are associated with winds blowing from Africa. 4. Arrivals of V. cardui were determined for the spring period (1 March-27 June, 1997-2006) at 79 sites in the Catalan Butterfly Monitoring Scheme. Wind patterns were described on the basis of synoptic-scale maps, transport models and back-trajectories calculated for each day of the spring period. 5. We found a strong association between migration and winds from North Africa, both for the whole data set (1997-2006; chi(2) = 4.7, P = 0.03) and for a restricted data set that excludes years in which the species was very scarce (chi(2) = 7.26, P = 0.007). 6. Episodes of massive northward migration within the species' flight-boundary layer also coincided with spells of winds from North Africa, suggesting a connection between low-altitude (observational) and high-altitude flights (inferred from wind patterns). 7. Finally, on the assumption that migration in V. cardui is windborne, a source-receptor transport model applied to spring abundance data in north-eastern Spain enables us to identify the most probable population source areas in North Africa.     

Positive and negative impact to decomposition of pig cadavers by ants (hymenoptera: Formicidae) at the Islet Yeongdo in Busan,South Korea

We observed how ants affected the decomposition process of pig cadavers. Experiments were carried out with six pig cadavers during three seasons without winter. Fifteen ant species belonging to 14 genera 3 subfamilies were recorded from pig cadavers. The species richness and species composition of ants were different significantly at bloated and decay stages from the remaining stages, regardless of season. Ant species Nylanderia flavipes, Aphaenogaster japonica, Pheidole fervida, and Ectomomyrmex javanus kept hunting a considerable amount of eggs and maggots of flies in the two stages. In particular, Lasius japonicus continually interrupted landing and ovipositing of flies and removed eggs and maggots from pig cadavers. Our observation suggests that ants may affect decomposition process of dead animals by participating in positive and negative ways by massive removal of eggs and maggots of flies.