The distribution and density of a lycaenid butterfly in relation to Lasius ants

Summary Larvae and pupae of lycaenid butteflies are often associated with ants: this is usually a mutualism in which ants guard the lycaenids from natural enemies, and the lycaenid larvae and pupae provide sugars and amino acids for the ants. A possible consequence of the interaction is spatially correlated ant and lycaenid distributions, but the phenomenon is poorly documented. We examined the lycaenid Plebejus argus, which is tended by Lasius ants. Within habitat patches, P. argus eggs, larvae and pupae were all spatially associated with Lasius. On a larger scale, the densities of butterflies in different habitat patches and populations, and whether the butterfly was present or not, were correlated with Lasius ant densities. The association of P. argus with Lasius ants is consistent among populations, and occurs at several spatial scales. Other aspects of the ecology of P. argus are more variable.     

Specificity of an ant-lycaenid interaction

Summary Many lycaenid butterflies are believed to be mutualists of ants — the butterfly larvae secrete sugars and amino acids as rewards for the ants, and the ants protect the larvae from predation or parasitism. We examined the specificity of the relationship between the lycaenid Plebejus argus and ants in the genus Lasius. Eggs were not attractive to Lasius ants until the emerging larvae had broken through the chorion. First instar larvae were palpated and picked up by Lasius workers and taken to the nest. First instars were mostly ignored by Myrmica sabuleti ants and they were rarely detected by Formica fusca. Older larvae were more attractive to Lasius than to the other ant genera. Pupae were very attractive to Lasius, moderately so to Myrmica, and were ignored by Formica fusca. Teneral adults were palpated by Lasius, but were attacked by Myrmica and Formica workers. We conclude that P. argus is a specialist associate of Lasius ants. Two populations of Plebejus argus were compared: one is naturally associated with Lasius niger, and the other with Lasius alienus. In reciprocal trials, larvae were slightly more attractive to their natural host ant species. Since test larvae were reared on a single host plant species in captivity, this differentiation probably has a genetic basis.     

Behavioral strategy of a lycaenid (Lepidoptera) caterpillar against aggressive ants in a Brazilian savanna

Myrmecophily is widespread in lycaenid butterflies, in which ants receive food resources and, in turn, protect caterpillars against natural enemies. This interaction ranges from obligate myrmecophily, in which immatures are invariably associated with ants and are dependent on ants for survival, and facultative myrmecophily, in which larvae are not dependent on ants for survival, but the presence of the latter may increase larvae survival. Lycaenids also include non-myrmecophilous butterflies, which do not have positive associations with ants and have developed strategies to avoid being attacked or preyed upon by them. In this study, we examined the relationship between the lycaenid Michaelus ira and two ant species associated with Distictella elongata (Bignoniaceae). This plant has extrafloral nectaries and is patrolled by Camponotus crassus and Ectatomma tuberculatum. Morphological analyses revealed that M. ira larvae have ant organs, such as dorsal nectary organs and perforated cupolas, structures associated with myrmecophily. We performed larval exposure experiments in the field, predicting that, in the absence of myrmecophily, the butterfly larva would present strategies to avoid ant attack. Results showed that larvae were attacked by both ant species. To escape ant molestation, larvae lived and fed inside silk-sealed D. elongata flower buds. We concluded that the M. ira bud-sheltering behavior was a defensive strategy against these ant species, while the dorsal nectary organs were apparently nonfunctional. Nonetheless, myrmecophily, in general, cannot be excluded in M. ira since relationships with other ant species may exist.     

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.     

Of crazy-ants and Curetinae: are Curetis butterflies tended by ants?

The larvae of the lycaenid subfamily Curetinae have never been reported to be associated with ants. Observations on Curetis regula Evans from Brunei are presented which show that this species may be tended by ants both as larvae and adults. The observations are discussed in relation to a recent review on lycaenid/ant associations, u is suggested that the Curetinae will be found to be associated with ants when more species have been reared, on evidence of the larval tentacle organs and apparent ‘pore cupolas’, both of which are ant adaptations. More studies are needed on Curetis biology and larval morphology to resolve the relationships of this enigmatic genus within the Lycaenidae.     

Species-specific effects of tending ants on the development of lycaenid butterfly larvae

The transfer of nutrients between organisms is a common feature of mutualism. The production of these food rewards is often assumed to be costly. Estimation of the costs of producing food rewards is important for understanding the overall effects of the interaction on fitness. When food rewards are harvested by several species differing in foraging behavior, costs to the producer may differ. The larvae of many species in the butterfly family Lycaenidae produce secretions consumed by tending ants. Here I report that three North American ant species, Formica perpilosa, Dorymyrmex sp. (smithi complex), and Forelius foetida, had no negative effect on the duration of development and adult size of the lycaenid Hemiargus isola. Moreover, tending by the ant Formica perpilosa significantly enhanced larval growth, resulting in butterflies that were 20% heavier than their untended counterparts. Tending by the ants Dorymyrmex sp. (smithi complex) and Forelius foetida had no effect on butterfly weight. Tended, nonfeeding larvae lost 69% more weight than untended, nonfeeding larvae. Taken together, the results suggest that, although ant tending imposes a physiological cost, H. isola larvae use behavioral or physiological mechanisms to compensate or overcompensate for nutrients lost to ants.     

Associations between lycaenid butterflies and ants in Australia

A comprehensive and critical review of all available literature on associations between Australian lycaenid butterflies and ants was undertaken to establish an accurate database of the partners involved. Collections and observations of lycaenids and ants were used to augment this review, resulting in a significant number of newly documented association (and non-association) records. Twenty published records considered to be erroneous or doubtful are noted, with justifications given for their deletion from the association database. In total, 265 different associations between lycaenids and ants, plus 65 non-attendance records are documented for Australia. Nearly 80% of the lycaenid species in Australia, for which the early stages are known, are recorded associating with ants and half of these are obligately ant-associated. Patterns of association are examined from the perspective of both lycaenids and ants, with a focus on ant systematics and ecology. Lycaenids are recorded with five ant subfamilies, including the first record of an association with the Pseudomyrmecinae. The Dolichoderinae, and to some extent the Formicinae, have a disproportionately high percentage of genera that associate with lycaenid butterflies. All ant species that tend lycaenids spend at least some portion of their time foraging on vegetation to collect plant and insect nectar. There is a robust relationship between the competitive status of ants within a community, and their frequency and degree of association with lycaenids. Obligate ant-association is accompanied by a high degree of specificity for ant partner, but two notable exceptions, Ogyris aenone and O. amaryllis are discussed. Facultative myrmecophiles tend to associate with a broad range of ants, although interactions with ecologically dominant ants are less frequent than might be expected based on the abundance of dominant ant species in Australian communities.     

Mutualistic ants and parasitoid communities associated with a facultative myrmecophilous lycaenid,Arhopala japonica,and the effects of ant attendance on the avoidance of parasitism

Herbivorous insects have evolved various defensive strategies to avoid their primary enemies, parasitoids. Many species of Lycaenidae (Lepidoptera) have food‐for‐protection mutualism with ants in their larval stages, where larvae produce nectar for ants and in return ants exclude parasitoids as well as predators. Myrmecophilous relationships are divided into two categories, obligate and facultative, by degrees of myrmecophily. Although parasitoids attacking obligate lycaenids always encounter lycaenid‐specific ant species, parasitoids that use facultative lycaenids are likely to encounter diverse ant species showing various defense systems. However, we know little about the parasitoid community of facultative lycaenid larvae. In this study, we investigated the mutualistic ant and parasitoid communities of a facultative myrmecophilous species, Arhopala japonica, in seven localities in Japan. The present field observation newly recorded four ant species attending A. japonica larvae, and combined with the previous data, the number of attending ant species reached 16, which is nearly the maximum number of reported attending ant species among myrmecophilous lycaenids. However, the present study revealed that almost all parasitized A. japonica larvae were attacked by a single braconid species, Cotesia sp. near inducta. We also assessed the efficiency of facultative ant defense against the parasitoid in the laboratory and revealed that oviposition by Cotesia sp. near inducta females was almost completely hindered when A. japonica larvae were attended by ants. This suggests that the dominant parasitoid does not have effective traits to overcome defensive behavior of ants and that the female wasps oviposit mainly in A. japonica larvae without intensive attendance.     

A single lycaenid caterpillar gets an ant‐constructed shelter and uninterrupted ant attendance

Ant‐lycaenid associations range from mutualism to parasitism and the caterpillars of some species of lycaenids are reported to enter ant nests for shelter, diapause, or pupation. The present study aimed to examine the nature of the association between Euchrysops cnejus (Fabricius) (Lepidoptera: Lycaenidae) and Camponotus compressus (Fabricius) (Hymenoptera: Formicidae) worker ants on the extrafloral nectary‐bearing cowpea plant, Vigna unguiculata (L.) Walp. (Fabaceae). The abundance patterns of the ants and the lycaenid caterpillars together with the spatial patrolling patterns of the ants on the plants revealed that ant abundance increased with the occurrence of the lycaenid caterpillars and the ants preferred the lycaenids over the extrafloral nectar. Camponotus compressus worker ants constructed a shelter at the cowpea plant base after interaction with one or more lycaenid caterpillar(s) and tended the caterpillars and pupae till the emergence of the butterfly. The ant‐constructed shelters (ACSs) inhabited by the minor caste workers (13 ± 1.3 ants per ACS), were utilized by the caterpillars to undergo pupation. The ants confined their activities predominantly to tending the pod‐feeding caterpillars and the solitary pupa within each ACS. It appears that the behavior of the tending worker ants is modulated by the lycaenid vulnerable stages.     

Ant attendance of the cotton aphid is beneficial for okra plants: deciphering multitrophic interactions

相似文献   

Impacts of Argentine ants on mealybugs and their natural enemies in California's coastal vineyards

Abstract 1. The Argentine ant, Linepithema humile, tends honeydew‐excreting homopterans and can disrupt the activity of their natural enemies. This mutualism is often cited for increases in homopteran densities; however, the ant’s impact on natural enemies may be only one of several effects of ant tending that alters insect densities. To test for the variable impacts of ants, mealybug and natural enemy densities were monitored on ant‐tended and ant‐excluded vines in two California vineyard regions. 2. Ant tending increased densities of the obscure mealybug, Pseudococcus viburni, and lowered densities of its encyrtid parasitoids Pseudaphycus flavidulus and Leptomastix epona. Differences in parasitoid recovery rates suggest that P. flavidulus was better able to forage on ant‐tended vines than L. epona. 3. Densities of a coccinellid predator, Cryptolaemus montrouzieri, were higher on ant‐tended vines, where there were more mealybugs. Together with behavioural observations, the results showed that this predator can forage in patches of ant‐tended mealybugs, and that it effectively mimics mealybugs to avoid disturbance by ants. 4. Ant tending increased densities of the grape mealybug, Pseudococcus maritimus, by increasing the number of surviving first‐instar mealybugs. Parasitoids were nearly absent from the vineyard infested with P. maritimus. Therefore, ants improved either mealybug habitat or fitness. 5. There was no difference in mealybug distribution or seasonal development patterns on ant‐tended and ant‐excluded vines, indicating that ants did not move mealybugs to better feeding locations or create a spatial refuge from natural enemies. 6. Results showed that while Argentine ants were clearly associated with increased mealybug densities, it is not a simple matter of disrupting natural enemies. Instead, ant tending includes benefits independent of the effect on natural enemies. Moreover, the effects on different natural enemy species varied, as some species thrive in the presence of ants.     

Ant-partners play a minor role on occurrence of the myrmecophilous butterfly <Emphasis Type="Italic">Leptotes cassius</Emphasis> in its host plant

Ant-related oviposition in facultatively myrmecophilous lycaenid butterflies is common, but not universal. In fact, our knowledge of ant-related oviposition in lycaenids is based on some common species (e.g., Rekoa marius, Allosmaitia strophius, Parrhasius polibetes), which limits generalizations about these systems. In this study, we experimentally investigated whether the oviposition pattern of the florivorous lycaenid Leptotes cassius was influenced by the presence of Camponotus ants and whether larvae were attended, rather than attacked, by ants. This might be evidence of myrmecophily. Both L. cassius and Camponotus ants occur on Bionia coriacea, an extrafloral nectaried legume shrub that grows in the Brazilian cerrado. Plants were randomly assigned to ant-present and ant-excluded treatments and were observed twice throughout the short reproductive season. Larvae of L. cassius were tended by ants, whose attendance was characterized by active antennation on the last body segments of the caterpillars. Therefore, Camponotus can be considered a partner of L. cassius. Lycaenid abundance was on average 1.9- and 1.21-fold higher in plants with ants in each sampling period, respectively, indicating a tendency of L. cassius to occur in plants with ants. Nonetheless, results were not statistically significant, suggesting that in this case ants are not a major cue for lycaenid oviposition. In many ant–lycaenid mutualisms, butterfly immatures benefit from reduced parasitism rates. However, no L. cassius immature, regardless of ant presence or absence, was parasitized. Furthermore, larvae may occur inside flower buds that may provide protection from natural enemies; thus, ants may not be required for immature protection.     

Of crazy-ants and Curetinae: are Curetis butterflies tended by ants?

The larvae of the lycaenid subfamily Curetinae have never been reported to be associated with ants. Observations on Curetis regula Evans from Brunei are presented which show that this species may be tended by ants both as larvae and adults. The observations are discussed in relation to a recent review on lycaenid/ant associations, u is suggested that the Curetinae will be found to be associated with ants when more species have been reared, on evidence of the larval tentacle organs and apparent 'pore cupolas', both of which are ant adaptations. More studies are needed on Curetis biology and larval morphology to resolve the relationships of this enigmatic genus within the Lycaenidae.     

Ants benefit from attending facultatively myrmecophilous Lycaenidae caterpillars: evidence from a survival study

Workers of three ant species (Lasius niger, Lasius flavus, Myrmica rubra) were caged in the laboratory together with caterpillars and pupae of five species of lycaenid butterflies. Mortality of ants was 3–5 times higher when the ants were confined with larvae lacking a dorsal nectar organ (Lycaena phlaeas, Lycaena tityrus) rather than with caterpillars which possess a nectar gland (Aricia agestis, Polyommatus bellargus, P. icarus). For all five species, ant survival was always lower at the pupal stage (where a nectar organ is always absent) than at the caterpillar stage and was largely equivalent for the butterfly species tested. The experimental data confirm earlier estimates that ants can derive nutritive benefits from tending facultatively myrmecophilous lycaenid caterpillars, even though these caterpillars produce nectarlike secretions at low rates.     

Aggregation as a cost-reducing strategy for lycaenid larvae

If a mutualistic relationship entails providing services ata cost, selection will favor individuals that maximize the netbenefits of the interaction and minimize the costs. Larvae ofmany species of lycaenid butterflies secrete nutritious foodrewards to attending ants and, in return, receive protectionagainst predators and parasitoids. Because ants typically recruitmore workers to larger resources, by forming groups the larvaemay ensure more reliable access to ants and thereby gain betterprotection. A further consequence of aggregating should be achange of the cost-benefit relationship for individual larvae.The larger the group, the smaller a single larva's influencewill be on total ant density, which could lead to a smallerinvestment in secretion, thus reducing the per capita cost ofcooperation. In this study, die influence of ant attendance,group size, and companion quality on larval investment was investigated.The interaction between the obligately ant-dependent lycaenid,Jalmanus evagoras, and its attendant Iridomyrmax ants was manipulatedand the effect on larval secretion measured. As the level ofant attendance increased, the delivery of food rewards increased,bodi for solitary and for aggregated larvae. When aggregated,larvae provided less food rewards to ants dun when solitary,and secretion rate decreased with increasing group size. Furthermore,larvae had lower secretion rates when paired with a bigger,more attractive larva than when paired with a smaller one. Theconsiderable reduction in secretion rates for larvae in groupssuggests that gaining protection at a lower secretion cost couldbe one factor that promotes aggregation in myrmecophilous lycaenids.     

Species‐specific levels of ant attendance mediate performance costs in a facultative myrmecophilous butterfly

Trophobiont butterfly larvae offer caloric rewards to ants through specialised glands and, in return, gain ant‐derived protection from natural enemies. Thus, from the larva's perspective, the major cost of myrmecophily comprises the reward production. Larvae of the butterfly Parrhasius polibetes (Stoll) (Lycaenidae) are facultatively tended by several ant species, which might differ in the intensity of tending behaviour. The performance costs (development time, survival, pupal mass and adult dry mass) of P. polibetes are examined when tended by two ant species differing in size and foraging strategies (Camponotus melanoticus Emery and Camponotus crassus Mayr), along with the corresponding intensity of tending behaviour towards late instars. Untended larvae serve as controls. Larvae tended by C. melanoticus take longer to pupate compared with both C. crassus and control larvae. By contrast, pupae whose larvae are tended by C. crassus are lighter than control larvae but do not differ from those tended by C. melanoticus. No differences are found in the adult stage, indicating compensation in all cases. Both at short‐ and long‐term scales, C. melanoticus tends larvae of P. polibetes more intensely than C. crassus. The increase in tending activity of C. melanoticus presumably delays the development time of larvae tended by this ant species. The results of the present study show that tending intensity varies depending on the ant species, and that P. polibetes has compensatory mechanisms to minimise myrmecophily costs, regardless of tending intensity. To the authors' knowledge, this is the first experimental evidence that intensity of ant‐tending behaviour is species‐specific and affects performance in a trophobiont insect.     

Myrmecophilous butterflies utilise ant–treehopper associations as visual cues for oviposition

1. Selection of a safe oviposition site is important for herbivorous insects whose immature stages have limited mobility. Female herbivores rely on environmental cues for this choice, and presence of natural enemies or mutualistic partners may be important in this process. 2. Some butterflies have mutualistic interactions with ants (myrmecophily), in which caterpillars offer a nutritional liquid and gain protection against natural enemies. Participants in butterfly–ant mutualisms may utilise signals to initiate interactions, but the use of visual cues by ovipositing myrmecophilous butterflies remains uncertain. 3. Larvae of facultatively myrmecophilous Parrhasius polibetes (Lycaenidae) feed on Schefflera vinosa, and females prefer to oviposit near aggregations of the ant‐tended treehopper Guayaquila xiphias, where caterpillars survive better due to increased ant attendance. Given the conspicuousness of ant–treehopper associations, it was investigated whether butterflies use them as visual cues for oviposition and, if so, which participants of the association are used as cues: ants, treehoppers, or both. 4. Experiments using dried insects on paired branches revealed that females visually recognise ants and ant–treehopper associations, using them for egg‐laying decisions. However, presence of a treehopper aggregation alone had no effect on oviposition choices. 5. This is a first insight into the importance of visual discrimination for ovipositing myrmecophilous butterflies. The results show that facultative mutualisms can be important enough to promote a behavioural adaptation (visual detection of ants) reinforcing the interaction. Our research highlights the importance of the behavioural interface within complex multispecies systems.     

The influence of ants on patterns of colonization and establishment within a set of coexisting lycaenid butterflies in a south-east Asian tropical rain forest

In Peninsular Malaysia ten species of lycaenid butterflies use leaf flushes or inflorescences of the legume tree Saraca thaipingensis as larval hostplant. Resource partitioning among these species is regulated by a complex mixture of patterns of interaction with ants. Females of obligately myrmecophilous species lay their eggs exclusively on trees colonized by their specific host ants. On trees colonized by weaver ants, only specialist mutualists adapted to these territorial ants are able to survive, while larvae of other species are killed. The formicine ant Cladomyrma petalae, which inhabits hollow twigs of the myrmecophytic hostplant, likewise precludes oviposition by female butterflies. Lycaenid larvae confronted with this ant species never survive, but one concealed feeding species (Jamides caeruleus) escapes removal due to the cryptic life-habits of the larvae. Two facultative myrmecophiles associate in a mutualistic way with a wide and largely overlapping range of ant genera which forage at the extrafloral nectaries of leaf flushes. One species (Cheritra freja) is not myrmecophilous, but is tolerated by all but the most territorial ants. Ant-dependent hostplant selection and egg-clustering characterize the obligate mutualists, whereas facultative myrmecophiles and the non-myrmecophile distribute their eggs singly over appropriate hostplants. Signals mediating caterpillar-ant communication are highly specialized in one obligate myrmecophile (Drupadia theda), but rather unspecific in four other species tested. Altogether our observations indicate that colonization and establishment of lycaenid butterflies on S. thaipingensis trees are governed by specializations as well as opportunistic use of resources (ants and hostplant parts). Therefore, the diversity of this species assemblage is maintained by deterministic as well as stochastic factors.     

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.     

Spatial distribution of ants (Hymenoptera: Formicidae), vine mealybugs and mealybug parasitoids in vineyards

The mutualistic association between some ant species and honeydew‐producing Hemiptera has been shown to influence the distribution patterns and abundance of these hemipterans and their natural enemies. We studied the spatial distribution patterns of three ant species, mealybugs and mealybug parasitoids for two consecutive growing seasons on three wine grape farms in the Western Cape, South Africa. During the study period, no ant or mealybug controls were applied. Ant and mealybug monitoring was conducted on a total of 21 ha using a presence/absence sampling system, while parasitoids were collected from infested mealybug females. Spatial analysis by distance indices was used to analyse spatial distribution of insects and ArcView? was used to map the gap, patch and local association indices where significant association and disassociation occurred. Significant associations were found between some ants and parasitoids, while significant disassociations between the ants Crematogaster peringueyi and Linepithema humile; and also between Crematogaster peringueyi and Anoplolepis steingroeveri were found. Interspecific competition between ant species could play a role in the distribution of parasitoids and mealybugs. Our results stress the importance of monitoring for ants and mealybugs and further highlight the importance of restricted chemical applications against ants during the growing season.