White and black circles indicate the paired and the unpaired treatments in E and G. The effect of prior exposure to the caterpillar on ant tending behavior toward A the cuticular extract, B the hydrocarbon HCs fraction and C the non-HCs fraction. D The experimental protocol for each run of associative learning assays.
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E The time spent tending by workers trained with N. F The effect of prior exposure to caterpillars of L. G Tending time of workers trained with L. Recent evidence has demonstrated that cuticular hydrocarbons are detected by chemosensilla in the antennae that have trajectories to the primary olfactory center of the brain  — . Lycaenid secretions containing carbohydrates and amino acids are perceived by gustatory receptor cells on the taste sensilla  , .
These findings suggest that ants learn to associate lycaenid secretions with cuticular hydrocarbons of N. To test this, we conducted associative learning assays using artificial secretions and cuticular extracts of N. Chemical analyses revealed that the secretions of N.
Based on this result, we made an artificial secretion that was used for learning assays Table S2. In the learning assay, we alternately presented a control dummy and a dummy coated with cuticular chemicals of N. These results indicate that the ant tending behavior toward the caterpillars is based on simple associative learning of secreted rewards and cuticular hydrocarbon profiles of the caterpillars.
Insect cuticular hydrocarbons are used by most insects to prevent water loss . Thus non-ant-associated lycaenid butterflies also secrete hydrocarbons on their cuticles. To test this hypothesis, we investigated the effect of previous experience with a non-ant-associated caterpillar on the ant tending behavior using another lycaenid butterfly species, Lycaena phlaeas.
The caterpillars of L. When we reared the workers with the L. In addition, the associative learning experiments using artificial secretions based on N. The amount of time that workers spent tending dummy models in paired treatments was also significantly different between models treated with N. These results indicated that the cuticular hydrocarbons of N. Analyses of cuticular hydrocarbons of both lycaenid species revealed that the total amount of hydrocarbons of N. Caterpillars of L. These results suggest that the behavioral differences exhibited by the ants were not caused by a difference in the amount of hydrocarbons, but rather on their qualitative traits.
Because cuticular hydrocarbons of P. Several studies have shown that the ant workers appear to use specific hydrocarbon classes in nest-mate recognition cues  — . It is also known that the ability of social insects to learn hydrocarbon profiles is affected by the structure of the hydrocarbons  — . Further learning assays using synthetic hydrocarbons and comparative studies using different lycaenid species are needed to understand the importance of hydrocarbon classes on recognition and maintenance of ant associations.
A Narathura japonica hydrocarbons consisted of a mixture of n -alkanes, n -alkenes and n -alkadienes, whereas B L. Previous studies of ant-protection mutualisms have reported that the ant partners can change the rates, concentration and composition of their reward secretions depending upon the need to regulate ant attendance  ,  ,  ,  ,  , .
We showed that learning to associate the cuticular hydrocarbon profile with food rewards plays an important role in mediating cooperative behaviors between ants and their symbionts. Because the quality of lycaenid secretions varies depending on various biotic and abiotic factors, learning to associate the hydrocarbon profile with reward secretions should serve as a good indicator of the quality of the partner species for the attendant ants. Several ant species can learn to recognize cuticular hydrocarbons  ,  , and a recent study reported that cuticular hydrocarbons are used as recognition cues in ant-aphid mutualisms .
We believe that the regulation of the relationship with ants based on associative learning of cuticular hydrocarbons is not restricted to associations with lycaenids, but may be common among various ant-protection mutualisms. For mutualistic partners, advertising by investing in more complex hydrocarbon signals is useful to attract attendant ants, especially when there is competition for ant partners.
We suggest that variation in hydrocarbon profiles of lycaenid larvae may reflect degree of ant association. At the same time, selection may have also favored ant sensory systems that can recognize and efficiently learn the odors of the most profitable lycaenid partners. Many species of lycaenid butterflies have evolved complex adaptations enabling them to live in association with ants  , . Further analyses of lycaenid signalling and perception by ants will provide valuable insight into the evolution of interspecific communication in mutualisms.
Narathura japonica Theclinae is native to oak woods in Japan, Taiwan and Korea. Caterpillars feed on species of Quercus Fagaceae and are usually associated with ants. We collected eggs and early instar caterpillars feeding on Q. Early instar caterpillars of Lycaena phlaeas daimio Lycaeninae were collected at Kyoto city in , and reared on cuttings of their host plant, Rumex japonicus. Colonies of the ant, Pristomyrmex punctatus have no queen, but workers reproduce through parthenogenesis. We collected three colonies of P. All colonies were collected in areas that did not contain host plants of N.
Therefore, to the best of our knowledge, the ants had never previously encountered caterpillars of N. No specific permit was required to collect these ant and butterfly species, which is not endangered or protected. Mealworms, maple syrup solution and Bhatkar-Whitcomb diet  were provided as food in the foraging area twice each week.
We surveyed 4 sites near Kyoto city on ten occasions from May to October in We investigated every young leaf on Q. Each observation was made in the afternoon 1PM to 6PM.
The caterpillars had never been exposed to other ants before being used in the experiment. Tending assays see below were conducted soon after the introduction on Day 0 when workers from both treatments had not yet contacted the caterpillar. Rearing cases were checked and cleaned every day, and if a caterpillar became a pre-pupa, we replaced it with another 5th instar caterpillar. This exchange did not interrupt the feeding condition treatment of ants because preliminary observation confirmed that N. Preliminary observation confirmed that the nail polish was sufficient to prevent secretion. We also confirmed that observed both ant and caterpillar behaviors were not disrupted by the nail polish application, by putting nail polish on other areas of the caterpillars.
The experienced and inexperienced treatments are the same as those described above. Ten workers were randomly chosen from a nest box and moved to a plastic petri dish 4. A fresh caterpillar intact or reward-less, depending on the experiment was introduced to the petri dish, and behavioral interactions were recorded for 15 min using a video camera IXY DV M5, Canon. We measured three behavioral responses: 1 the total time tended by ants, measured in ant min i. After each assay, the workers were not returned to the original colony or nest boxes to avoid social learning.
We used different individual caterpillars for each tending assay. To make the cuticular chemical extract, a caterpillar was immersed in approximately 2 ml of n -hexane for 2 min. For hydrocarbon and non-hydrocarbon fractions, the crude extract was chromatographed on ca. Hydrocarbons were eluted with 2 ml of n -hexane and non-hydrocarbon compounds were eluted with 2 ml of methylene chloride.
The extracts from different individual caterpillars were used for each assay. All beads were used after the evaporation of solvent approximately 30 min after application. After the 0 and 3 days, the glass bead coated with cuticular extract was gently placed on the center of the petri dish 4. We measured tending time ant min toward the glass dummy and compared this for experienced and inexperienced ants.
A 5th instar caterpillar of N. When the workers antennated the dorsal nectary organ, the caterpillar secreted a droplet. These droplets were collected using 0. For the sugar analysis, samples 0. For sugar analysis, samples were analysed by high performance liquid chromatography using a 5NH 2 -MS packed column 4. It has been known for centuries that floral and extra-floral nectar secreted by plants attracts and rewards animals.
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Extra-floral nectar is involved in so-called indirect defense by attracting animals generally ants that prey on herbivores, or by discouraging herbivores from feeding on the plant. Floral nectar is presented inside the flower close to the reproductive organs and rewards animals that perform pollination while visiting the flower. In both cases nectar is a source of carbon and nitrogen compounds that feed animals, the most abundant solutes being sugars and amino acids.
Plant—animal relationships involving the two types of nectar have therefore been used for a long time as text-book examples of symmetric mutualism: services provided by animals to plants in exchange for food provided by plants to animals.
Cheaters in Mutualisms
A more subtle way of exploiting mutualism was recently highlighted. Several substances other than sugars and amino acids have been found in nectar and some affect the foraging behavior of insects and potentially increase the benefits to the plant. Such substances can be considered plant cues to exploit mutualism. Mutualistic inter-species relationships, i. Mutualism has a pivotal role in the functioning of all current ecosystems and in key events of the evolutionary history of life on our planet, such as the evolution of eukaryotic cells, colonization of land by plants and the radiation of angiosperms Bronstein et al.
According to this theory natural systems tend to remain in a stable equilibrium where natural forces prevent species from becoming too abundant or becoming extinct Egerton, Mutualism, regarded as reciprocal cooperation between species, was therefore perfectly framed in this theory. These conflicts challenge the maintenance of mutualisms and selection may favor exploitation or the abandonment of such relationships.
However, possible conflicts can be managed and mutualism stabilized in different ways, from special rewards for cooperatives and sanctions for cheaters to strict specificity in partner choice Douglas, , From this point of view, mutualisms can best be regarded as reciprocally exploitative interactions that provide a net benefit to both parties. The net effect to each partner is highest when the benefit is maximized in relation to investment Bronstein, and references therein.
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Plants are involved in a myriad of mutualistic interactions with very diverse organisms such as bacteria, fungi and animals. Mutualisms with bacteria nitrogen-fixing bacteria and fungi mycorrhiza increase nutrient uptake by plants as well as providing organic matter and a suitable ecological niche to the heterotrophic counterpart.
Pollen, the male gametophyte of seed plants containing the male gametes, needs to be transported from the anther to the stigma of a compatible carpel, a process called pollen dispersal or pollination that is the first step toward fertilization in all seed plants. According to a recent global estimate, Insects are the most numerous and diverse animals involved in pollination Ollerton, Being sessile and having limited movements, plants have developed an array of defense strategies against predation by herbivores Schoonhoven et al.