Isolation of microsatellite markers from the drepanosiphid aphid Tuberculatus quercicola (Homoptera,Aphididae)

We isolated five polymorphic microsatellite loci from the drepanosiphid aphid Tuberculatus quercicola (Matsumura) that is associated with the Daimyo oak, Quercus dentata Thunberg, using the magnetic particles method. The isolated loci were polymorphic, with four to 16 alleles in 40 aphids. Expected heterozygosities ranged from 0.4 to 0.82. These loci can be used to quantify seasonal changes in clonal diversity in the metapopulation and the extent of clonal mixing in the colonies.     

Flexibility in the composition and concentration of amino acids in honeydew of the drepanosiphid aphid Tuberculatus quercicola

Abstract 1. Mutualistic interactions between aphids and ants are mediated by honeydew that aphids produce. Previous work showed that when attended by the ant Formica yessensis Forel (Hymenoptera: Formicidae), nymphs of the aphid Tuberculatus quercicola (Matsumura) (Homoptera: Aphididae) developed into significantly smaller adults with lower fecundity than did nymphs that were not ant attended.
2. This study tested the hypothesis that this cost of ant attendance arises through changes in the quality and quantity of honeydew. Ant-attended and ant-excluded aphid colonies were prepared in the field. The composition and concentration of amino acids were compared between the honeydew produced by ant-attended colonies and that produced by ant-excluded colonies.
3. The aphids excreted smaller droplets of honeydew, but also excreted them more frequently, in ant-attended colonies than in ant-excluded colonies. The honeydew of ant-attended aphids contained more types of amino acid, and a significantly higher total concentration of amino acids, than did the honeydew of ant-excluded aphids.
4. These results suggest that the increase in the concentration of amino acids in honeydew leads to a shortage of nitrogen available for aphid growth and reproduction, resulting in lower performance under ant attendance.
5. With the advance of seasons, a significant reduction was found in both the total free amino acid concentration in phloem sap and the frequency of honeydew excretion; however the total concentration of amino acids in the honeydew did not vary significantly during the seasons, suggesting that aphids keep the quality of honeydew constant in order to maintain ant visitation.     

Ant attendance reduces flight muscle and wing size in the aphid Tuberculatus quercicola

In otherwise mutualistic relationships between aphids and ants, attendance by ants often has negative impacts on aphids. For example, in a previous study using traps in the field, the aphid Tuberculatus quercicola, which exhibits mutualistic interactions with ants, showed extremely low dispersal rates, despite having long wings. This study investigates whether components of the flight apparatus (mesonotum length, flight muscle and wings) differ between aphids attended by ants and not attended by ants. Randomized block analysis of variance, using body length as a covariate, showed that ant attendance has a negative influence on aphid flight apparatus. This result indicates that aphids produce honeydew at the expense of resource investment in flight apparatus. Since the dispersal of T. quercicola is limited under ant attendance, the reduction in flight apparatus could precede a decrease in body size. This study also showed that flight apparatus was more developed in aphids under ant-exclusion conditions. This may imply that T. quercicola fly when ants are not available. The maintenance of flight apparatus in T. quercicola might therefore be partly explained by gene flow on the rare occasions that this aphid species disperses.     

Costs of ant attendance for aphids

1. Interactions between aphids and ants are considered to be mutualistic, with both partners benefiting. Costs associated with such interactions are likely to be less obvious, although they can be expected, especially if these associations are facultative.
2. It is demonstrated here that there are costs in several life-history parameters to individual aphids resulting from ant attendance. Over several generations Aphis fabae cirsiiacanthoides feeding on Cirsium arvense , at a range of developmental stages, suffered significant costs when tended by Lasius niger , e.g. in terms of a prolonged developmental time, delayed offspring production, proportionally smaller gonads, fewer well developed embryos and a reduced mean relative growth rate. These effects are similar to those observed when aphids feed on poor quality plants.
3. This is the first indication that there is a cost for aphids associated with ant attendance. The significance of this for the evolution of ant attendance in aphids is discussed.     

Indirect interactions between two aphid species in relation to ant attendance

The influence of foraging by the ant, Lasius niger, on the population growth of two aphid species, Lachnus tropicalis and Myzocallis kuricola, on chestnut trees, Castanea crenata, was examined. The ant-tending effect was divergent depending on the aphid density per ant: it was positive when there were few aphids per ant, but negative when there were many aphids per ant. In addition, the density of one aphid species also influenced the ant-tending effect on the other aphid. Furthermore, the influences were asymmetrical: an increase in L. tropicalis density per ant reversed the ants effect on this species and on M. kuricola, while an increase in M. kuricola per ant did not significantly influence the ants effect on L. tropicalis. Thus, the ant seems to stabilize the L. tropicalis population density and keep this species from extinction, while the ants effect on M. kuricola depends on the density of L. tropicalis and may lead M. kuricola to extermination. This change in the ant-tending effect corresponds to the previously detected density-dependent change in predation activity of the ants on aphids. In contrast, the density-dependent change in the protection effect of the ants against natural enemies does not explain the results.     

The cost of ant attendance and melezitose secretion in the black bean aphid Aphis fabae

1. The aphid Aphis fabae (Scopoli) is facultatively tended by Lasius niger (Linnaeus) ants. Previously, we found that A. fabae colonies can be made up of several clones, and that clones display significant differences in the composition of their honeydew sugars, especially in the amount of the ant attractant sugar melezitose that they produce. 2. These clonal differences could greatly impact the strength of the mutualistic interaction with ants as well as the aphids' fitness. 3. Hence, the aim of this study was to compare the fitness of different A. fabae clones that differed in their melezitose secretion, and whether or not they were tended by ants. 4. Individual fitness indices, colony growth, and alate production of single‐clone aphid colonies were analysed. 5. The results demonstrate that the fitness consequences of ant attendance critically depend on an interaction between levels of melezitose production. In particular, we show that high‐melezitose secreting clones produce fewer alates and hence might have a lower dispersal ability in the presence of ants. 6. Furthermore, these data confirm previous evidence that ant attendance is costly and results in the production of fewer apterae.     

Cheating on a mutualism: indirect benefits of ant attendance to a coccidophagous coccinellid

Coccinellids (Coleoptera: Coccinellidae) are generally unable to prey on ant-tended prey. However, particular coccinellid species have morphological, behavioral, or chemical characteristics that render them immune to ant attacks, and some species are even restricted to ant-tending areas. The benefit gained from living in close association with ants can be twofold: (1) gaining access to high-density prey areas and (2) gaining enemy-free space. Here, the myrmecophily of Azya orbigera Mulsant (Coleoptera: Coccinellidae), an important predator of the green coffee scale, Coccus viridis (Green) (Hemiptera: Coccidae), is reported. In this paper, three main questions were studied. (1) Are the waxy filaments of A. orbigera larvae effective as defense against attacks of the mutualistic ant partner of C. viridis, Azteca instabilis F. Smith (Hymenoptera: Formicidae)? (2) Does A. instabilis reduce the rate at which A. orbigera larvae prey on scales? (3) Do A. orbigera larvae gain enemy-free space by living in close association with A. instabilis? Laboratory and field experiments were conducted to answer these questions. We found that, because of the sticky waxy filaments of A. orbigera larvae, A. instabilis is incapable of effectively attacking them and, therefore, the predation rate of A. orbigera on C. viridis does not decrease in the presence of ants. Furthermore, A. instabilis showed aggressive behavior toward A. orbigera's parasitoids, and the presence of ants reduced the parasitism suffered by A. orbigera. This is the first time that this kind of indirect positive effect is reported for an ant and a coccidophagous coccinellid. Furthermore, this indirect positive effect may be key to the persistence of A. orbigera's populations.     

Success of aphid parasitoids and their hosts varies with ant attendance: A field study

Aphid–ant associations are often described as mutually beneficial interactions in which honeydew is traded for protection from predators and parasitoids. The aim of the present study was to determine parasitization avoidance in ant‐tended aphid colonies. Field experiments were carried out on two host plants: hoary cress Lepidium draba (Brassicaceae) and Canadian teasel Cirsium arvense (Asteraceae). Lepidium was host to Acyrthosiphon gossypii (Aphididae) tended by the ant Lasius turcicus (Formicidae) and attacked by two parasitoids, Trioxys asiaticus (Braconidae) and Lysiphlebus fabarum (Braconidae). Cirsium was host to Brachycaudus cardui tended by Crematogaster sordidula and attacked by L. fabarum and Aphidius colemani (Braconidae). The per capita population growth rate of A. gossypii was significantly higher in the presence of ants, while B. cardui was negatively affected, albeit non‐significantly. The parasitism rate of A. gossypii decreased significantly when tended by Lasius turcicus, but the presence of Crematogaster sordidula in colonies of B. cardui significantly increased parasitism. Our results indicate that the effects of ant attendance vary between different aphid–ant interactions. Moreover, parasitoids can benefit from the presence of ants under some conditions.     

Ants andPolyommatus icarus immatures (Lycaenidae) —sex-related developmental benefits and costs of ant attendance

Summary Third and fourth instar larvae and pupae of the facultatively myrmecophilous Palaearctic blue butterflyPolyommatus icarus showed no alteration in developmental time when reared in the presence of two species ofLasius ants. Sex differences were observed in larval growth and pupal weight, with males growing larger and faster. Sex-related differences also occurred in the costs and benefits of ant-attendance. Male pupal masses tended to be larger in individuals associated with ants, and their pupal weight loss was not enhanced by ant attendance. This positive developmental effect of myrmecophily is tentatively attributed to a stimulating influence of ants on caterpillar feeding behavior. In contrast, females associated with ants tended to lose more weight during the pupal stage. Hence there is evidence for developmental benefits, rather than costs, of myrmecophily in maleP. icarus immatures, whereas ant attendance appears to be more costly for females during the pupal stage. These findings are discussed in relation to data on other myrmecophilous lycaenid species. It is suggested that maintaining low-level myrmecophily and its related organs is a comparatively inexpensive evolutionary stable strategy among this butterfly group.     

The effect of ant attendance on the success of rosy apple aphid populations, natural enemy abundance and apple damage in orchards

1 The rosy apple aphid, Dysaphis plantaginea, is the most serious pest of apple in Europe and, although conventionally controlled by insecticides, alternative management measures are being sought. Colonies of D. plantaginea are commonly attended by ants, yet the effects of this relationship have received little attention. 2 An ant exclusion study was conducted in two distant orchards within the U.K. At both sites, ants were excluded from a subset of D. plantaginea infested trees at the beginning of the season and populations were monitored. The number of natural enemies observed on trees was also recorded and, before harvest, the percentage of apples damaged by D. plantaginea calculated. 3 Overall, the exclusion of ants reduced the growth and eventual size of D. plantaginea populations. On trees accessed by ants, greater numbers of natural enemies were recorded, presumably because aphid populations were often greater on such trees. However, this increased natural enemy presence was diluted by the larger aphid populations such that individual aphids on ant‐attended trees were subjected to a lower natural enemy pressure compared with those on ant‐excluded trees. 4 At harvest, apple trees that had been accessed by ants bore a greater proportion of apples damaged by D. plantaginea. There were also differences in cultivar susceptibility to D. plantaginea damage. 5 The present study highlights the importance of the ant–D. plantaginea relationship and it ia suggested that ant manipulation, whether physically or by semiochemicals that disrupt the relationship, should be considered as a more prominent component in the development of future integrated pest management strategies.     

Seasonal changes in the density of the symbionts Buchnera and Wolbachia of the aphid Tuberculatus macrotuberculatus on Quercus dentata

Seasonal changes in leaf traits and tannins, including hydrolysable tannins (HTs) and condensed tannins (CTs), affect aphid body size and demographic patterns. The aphid Tuberculatus macrotuberculatus Essig & Kuwana (Hemiptera: Aphididae) feeds on the leaves of the daimyo oak, Quercus dentata Thunberg (Fagaceae), does not alternate hosts, and is attended continuously by ants. Buchnera aphidicola Munson et al. (a γ‐proteobacterium, hereafter Buchnera) is the primary symbiont of most aphid species. It provides essential amino acids to host aphids. Wolbachia sp. (an α‐proteobacterium) is present in some aphid species. This study investigated the effects of seasonal tannin and leaf trait fluctuations in Q. dentata on aphid performance and Buchnera and Wolbachia densities in T. macrotuberculatus. As the season progressed, the water content and HT concentration in Q. dentata leaves decreased, CT concentration in Q. dentata leaves increased, and T. macrotuberculatus performance decreased. Buchnera density varied in accordance with host aphid performance, whereas Wolbachia density did not vary throughout the season, suggesting that although Buchnera depends on the host plant and host aphid performance for growth, Wolbachia may have a high tolerance for oligotrophic environments and may exist independent of the nutritional metabolism of the host aphid. Although the role of Wolbachia in T. macrotuberculatus remains unclear, it may be associated with resistance to parasitoid wasps and plant secondary metabolites.     

黑蚁对雪松长足大蚜集群时空变化的取食反应

我们研究了黑蚁 (Lasiusniger)如何开发距离其巢不同距离的多种食物资源 ,以及黑蚁的照看活动是否与雪松长足大蚜 (Cinaracedri)种群的增长有关 ,以及 /或者受空间分布的影响。笔者定期调查了Cinaracedri集群的空间分布 ,以及在雪松树枝上黑蚁取食的时间变化 ,发现只有 2 5 %的蚜虫集群在研究后数周内保持在同样的位置 ,这表明蚜虫集群的高度运动性迫使黑蚁改变活动路线以获取事物资源。实际上 ,黑蚁集群能选择最近的食物资源以及蚜虫数量最多的地点     

Costs and benefits of hydroxamic acids-related resistance in winter wheat against the bird cherry-oat aphid, Rhopalosiphum padi L.

Estimations of infestation by the bird cherry-oat aphid (Rhopalosiphum padi) as well as measurements of grain yield in 26 Hungarian winter wheat cultivars under field conditions were correlated with the concentration of hydroxamic acids (Hx) in seedlings of those cultivars. The significant inverse relationship between infestation ratings and Hx levels in wheat showed that Hx, despite their decreased accumulation at later plant phenological stages, may be able to confer resistance against aphid infestation in the field. Since no significant relationship was found between grain yield and Hx levels in plants it is suggested that Hx accumulation does not impose a cost to the plant in terms of yield. These findings support earlier claims stressing the potential of Hx as breeding targets for aphid resistance in wheat.     

Costs and benefits of a cleaning mutualism

Juvenile Atlantic salmon or parr ( Salmo salar L.) maintain station at certain locations in flowing stream water. This position choice is assumed to involve the maximization of energy intake, based upon food availability which is usually directly related to water flow rate. Conversely energy expenditure, including station holding behaviour, foraging and defending preferred sites, is inversely related to water flow rate. Adaptations of parr to life in fast flows implies that station holding is energetically inexpensive at water speeds up to the maximum sustained holding speed, which is fish specific, thus the most important energetic consideration for parr is the ability to maximize food intake. Ten groups of three parr were each observed for 60 min within an artificial stream tank over a heterogeneous substratum. Individual position choice and behaviour were recorded continuously. For each location chosen by the parr the potential upstream line‐of‐sight (LOS), defined as the maximum distance upstream that the water surface would be visible, was calculated. At those sites where foraging behaviour was observed, the mean upstream potential LOS was significantly greater than at sites where other behaviours were observed and at 400 randomly generated sites within the tank. When foraging, parr usually take food from the stream drift and there is a significant time expenditure on food location, identification and catching. Results presented here would seem to confirm that to maximize time available to make these decisions, a fish would be expected to maximize the distance over which it can observe potential food particles.     

Lack of ant attendance may induce compensatory plant growth

Three levels in ant–plant protection systems need to be considered to fully understand how these symbiotic systems work. Here we present the effect of Oecophylla smaragdina ants on (1) the arthropod community, (2) herbivory, and (3) plant performance, within a studied mangrove ant–plant protection system. On Rhizophora mucronata trees in Thailand ants successfully colonised ant trees attached with a string to a natural ant tree, whereas they were unable to colonise control trees without this connection. Trees were monitored and arthropods (numbers and composition), leaf damage, leaf turnover and growth rates (stem diameter, tree height and total leaf area) were recorded in two surveys covering a period of 12 months. The number of herbivorous arthropods, but not the number of predators, was significantly lower on ant trees compared to control trees. Likewise, the amount of leaf damage inflicted by the four major groups of herbivores (Chrysomelidae, Tortricidae, Geometridae and Sesarminae) was significantly lower on ant trees compared to control trees and so was the leaf turnover rate. In spite of this, the released herbivore pressure on ant trees did not translate into higher growth rates. In contrast, all growth responses increased more on control trees compared to ant trees. Differences between the two groups were insignificant but leaf area increase was only marginally nonsignificant (P=0.062). The results show that ants remove herbivorous arthropods more efficiently than predators but ant-colonised mangroves do not necessarily benefit from this despite the resulting decrease in herbivory.