Joint evolution of mutualistic interactions, pollination, seed dispersal mutualism, and mycorrhizal symbiosis in trees.

Mycorrhizal symbiosis, seed dispersal, and pollination are recognized as the most prominent mutualistic interactions in terrestrial ecosystems. However, it remains unclear how these symbiotic relationships have interacted to contribute to current plant diversity. We analyzed evolutionary relationships among mycorrhizal type, seed dispersal mode, and pollination mode in two global databases of 699 (database I) and 10 475 (database II) tree species. Although database II had been estimated from phylogenetic patterns and therefore had lower certainty of the mycorrhizal type than database I, whose mycorrhizal type was determined by direct observation, database II allowed analysis of many more taxa from more regions than database I. We found evidence of joint evolution of all three features in both databases. This result is robust to the effects of both sampling bias and missing taxa. Most arbuscular mycorrhizal-associated trees had endozoochorous (biotic) seed dispersal and biotic pollination, with long dispersal distances, whereas most ectomycorrhizal-associated trees had anemochorous (abiotic) seed dispersal and wind (abiotic) pollination mode, with shorter dispersal distances. These results provide a novel scenario in mutualistic interactions, seed dispersal, pollination, and mycorrhizal symbiosis types, which have jointly evolved and shaped current tree diversity and forest ecosystem world-wide.

Aphids increase their rate of survival on emergent aquatic plants through niche construction.

Flooding or rain is a threat to many insects in nature, including herbivorous invertebrates whose hosts are emergent aquatic plants. They may thus have developed particular adaptations to withstand the flooding that is a feature of emergent plants' environment. The aphid Hyalopterus pruni (Hemiptera: Aphididae) modifies the physical and chemical conditions of its habitat by periodically spreading wax around itself with its hind legs. This behaviour constitutes a form of niche construction. We hypothesized that the aphid decreases its risk of death of own or around other individuals when submerged in water by spreading wax powder secreted from its body onto the leaves of its host plant, Phragmites australis. We compared the hydrophobicity of waxed and normal leaf surfaces. Next, we compared the survival rates of wax-powdering and nonwax-powdering aphids under submerged and rainy conditions in the laboratory and in the field. Finally, we examined whether the aphids' wax-powdering behaviour increased as a result of experiencing brief submergence or rain. The surface of the waxed area was significantly more water-repellent than the surface of unwaxed leaves. The waxed areas held air bubbles when under water. In experiments, aphids without wax around themselves exhibited lower survival rates: 22.9% in laboratory conditions and 15.7% in field conditions after 48 hr underwater. In contrast, aphids that secreted wax had higher survival rates, with 41.5% and 38.2% under laboratory and field conditions, respectively, after the same duration. Aphids exposed to rainfall showed similar results. Moreover, aphids that had experienced rain or submersion for 24 hr engaged in increased wax-powdering behaviour. These results indicate that aphids reduce their risk of drowning by powdering secreted wax onto the surface of leaves around them. Our findings suggest that niche construction by herbivorous invertebrates supports their ability to utilize host plants that grow under stressful conditions, such as emergent plants that are subject to periodic inundation.

Defence plasticity in the spiny plant Aralia elata (Miq.) Seem. in response to light and soil fertility.

BACKGROUND AND AIMS: Plants have evolved various defences against herbivores, including direct chemical and structural defences and co-opted biological defences by predatory insects. However, the effects of abiotic habitat conditions on the quantitative expression of defence traits of spiny species have not been elucidated. METHODS: Here, we investigated whether a spiny deciduous tree, Aralia elata (Miq.) Seem., changes its defence expression across light and nutrient gradients. We measured allocation to spines and C-based secondary metabolites (condensed tannins and total phenols) on A. elata plants growing across light and nutrient gradients in situ in natural landscapes in Japan. Second, we examined the effects of light and soil nutrient condition on allocation to shoot organs, spines and chemical defences of juveniles of two genotypes of the species, respectively spiny (mainland population) and non-spiny (island population), grown in a glasshouse. KEY RESULTS: In the field investigation, absolute spine mass, spine mass fraction, total phenols and condensed tannins all responded positively to canopy openness. Total phenol content was also negatively related to soil N. In the glasshouse, spiny genotype individuals had less total biomass, had lower stem allocation and were shorter than non-spiny genotype individuals. In spiny genotype trees, both spine mass fraction and total phenols decreased under low light conditions. Nutrient additions had negative effects on spine mass fraction and total phenols, but no effect on absolute spine mass. CONCLUSIONS: These results suggest that development of spines is costly for A. elata and receives greater allocation when carbohydrate supply is more plentiful. Thus, light is a more important determinant of spine allocation than soil nutrients for A. elata.

Predator discrimination of prey promotes the predator-mediated coexistence of prey species.

The predator discrimination of prey can affect predation intensity and the prey density dependence of predators, which has the potential to alter the coexistence of prey species. We used a predator-prey population dynamics model accounting for the predator's adaptive diet choice and predator discrimination of prey to investigate how the latter influences prey coexistence. The model revealed that (i) prey species that are perceived as belonging to the same species by a predator are attacked in the same manner, and it is more difficult for them to coexist than those that are recognized as different prey species, and (ii) prey species that are not discriminated by a predator-and therefore cannot coexist-may coexist in the presence of an alternative predator that does discriminate between them. These results suggest that prey diversity, which favours the predator discrimination of prey, and the different capabilities of predators to identify prey species both enhance prey coexistence.

Plant-plant interaction by Aster leiophyllus affects herbivory by Sika deer, Cervus nippon.

Changes in leaf traits in response to plant-plant interactions affect feeding by insect herbivores. However, the effects of such changes on feeding by vertebrate herbivores remain unclear. We examined the effects of interactions of Aster leiophyllus collected in the field (growing with plants of the same species [aggregated] or with plants of different species [solitary]) or grown in pots (with another A. leiophyllus [intraspecific] or with Carex aphanolepis or Thalictrum baicalense [interspecific]) on the concentration of total phenolics in A. leiophyllus leaves and on sika deer (Cervus nippon) grazing preference in Japan. Deer were presented for 30 s with the first A. leiophyllus leaf (from either aggregated plants or solitary plants) and then for 30 s with the second leaf (solitary or aggregated, respectively). All of the deer presented first with a leaf from a solitary plant ate it, but when deer were presented first with a leaf from an aggregated plant, which had a higher concentration of total phenolics, 50% rejected or left it. About a third of the deer that had been presented first with a leaf from an aggregated plant subsequently rejected the leaf of a solitary plant. The leaves in the intraspecific interaction pot treatment had higher total phenolic concentration and were rejected more by deer than the leaves in the interspecific treatments. Plant-plant interactions affected deer preference, which was also influenced by learning. These results should improve our understanding of both plant grazing by deer and environmental management.

Effects of indirect plant-plant interaction via root exudate on growth and leaf chemical contents in Rumex obtusifolius.

Belowground plant-plant interactions can affect the concentrations of leaf chemicals, but the mechanism is not clear. Here, we investigated the effects of intra- and interspecific root exudates on the growth and leaf chemical content of Rumex obtusifolius. Seedlings of R. obtusifolius were grown with exposure to root exudates collected from other R. obtusifolius plants or from Trifolium repens, Festuca ovina, or Plantago asiatica plants, and the total phenolic, condensed tannin, dry biomass, and chlorophyll contents of the leaves were examined. The root exudates from conspecific plants had no effect on the total phenolic, condensed tannin, and chlorophyll contents of the leaves but did significantly reduce the dry leaf biomass. Root exudates from heterospecific plants had different effects depending on the species. These results were different from the results of a previous study that examined the effects of direct plant-plant interaction in R. obtusifolius. Thus, indirect interaction via root exudates induces different effects in leaves from direct interaction.

Night interruption provides evidence for photoperiodic regulation of bud burst in Japanese beech, Fagus crenata.

Some of trees in cool and temperate regions regulate bud burst by perceiving photoperiod. However, it is not clear whether the difference in bud burst timing between the two photoperiod conditions is due to differences in perception of day length or the daily light integral (DLI) because majority of studies concerning the photoperiodic regulation of bud burst make use of an experimental design that compares the differential timing of bud burst between long and shortday length. We conducted night and day interrupt experiments using twig cuttings of Japanese beech, Fagus crenata, to investigate the effect of photoperiod on bud burst. Twigs with leaf buds were collected in winter (February 2020) and maintained in four conditions: 1) long day length (16L8D; LD), 2) short day length (8L16D; SD), 3) day interruption for 2-h in the middle of the 16-h light period and a 6-h dark period (DI; total time of light period is the same as LD), and 4) night interruption with 2-h of light in the middle of the dark period and a 6-h light period (NI; total time of light period is the same as SD) for a duration of 40 d. We then measured the number of days until burst for each bud. Timing of bud burst was delayed in the SD treatment compared to the LD, DI, and NI treatments. These results demonstrate that the difference in bud burst phenology observed between SD and LD conditions is mainly due to day length perception rather than DLI, and an uninterrupted night period plays a major role in the perception of photoperiod. Our results provide the experimental evidence of perception of photoperiod regulating bud burst in spring.

Functional roles of ants in a temperate grassland.

Ants in temperate grasslands are consumers and ecosystem engineers, influencing biodiversity and potentially grassland productivity. However, the effects of ant exclusion or suppression on resource removal and the biological community in temperate grasslands have yet to be fully explored. We conducted ant-suppression experiments and evaluated the effects of ants on ground-dwelling arthropod communities in the field by using pitfall and bait traps. In the laboratory, we evaluated the effects of ants on the ant-attended aphid Aphis rumicis, which is a honeydew resource for ants, and the slug (Deroceras laeve), an aphid predator. Aboveground arthropod communities were not affected by the ant-suppression treatment. However, slugs (D. laeve and Ambigolimax valentianus) visited bait resources more frequently in the ant-suppression treatment area. In the ant-absence condition in the laboratory experiment, there were fewer aphids on the plants compared to the ant-presence condition owing to predation by D. laeve. Our results suggest that ant abundance in temperate grasslands influences the predation activity of slugs toward honeydew sources such as aphids.

Aboveground plant-to-plant communication reduces root nodule symbiosis and soil nutrient concentrations.

Aboveground communication between plants is well known to change defense traits in leaves, but its effects on belowground plant traits and soil characteristics have not been elucidated. We hypothesized that aboveground plant-to-plant communication reduces root nodule symbiosis via induction of bactericidal chemical defense substances and changes the soil nutrient environment. Soybean plants were exposed to the volatile organic compounds (VOCs) from damaged shoots of Solidago canadensis var. scabra, and leaf defense traits (total phenolics, saponins), root saponins, and root nodule symbiosis traits (number and biomass of root nodules) were measured. Soil C/N ratios and mineral concentrations were also measured to estimate the effects of resource uptake by the plants. We found that total phenolics were not affected. However, plants that received VOCs had higher saponin concentrations in both leaves and roots, and fewer root nodules than untreated plants. Although the concentrations of soil minerals did not differ between treatments, soil C/N ratio was significantly higher in the soil of communicated plants. Thus, the aboveground plant-to-plant communication led to reductions in root nodule symbiosis and soil nutrient concentrations. Our results suggest that there are broader effects of induced chemical defenses in aboveground plant organs upon belowground microbial interactions and soil nutrients, and emphasize that plant response based on plant-to-plant communications are a bridge between above- and below-ground ecosystems.

Assessing temporal dynamics of predation and effectiveness of caterpillar visual defense using sawfly larval color and resting posture as a model.

Caterpillars (Lepidoptera and Symphyta larvae) employ diverse visual defensive tactics, and effectiveness of such tactics may be highly dynamic across time due to seasonal changes in the predator assemblages and their preferences. However, this has rarely been studied especially in tropical regions. Here we assessed temporal changes in the defensive value of caterpillar color and shape, using six types of plasticine dummy caterpillars: three colors (green, black, and white) × two shapes (curled and straight). These dummy caterpillars were deployed five times over different seasons in tropical forests of Xishuangbanna (China) and, as a comparison, twice in a temperate forest of Hirosaki (Japan). The colors and shapes of dummy caterpillars simulate visual traits of black sawfly larvae which take the curled resting posture in tropical rainforests of Xishuangbanna, apparently masquerading excrements commonly found on plants, while in Hirosaki there is no black-curled sawfly larvae and few excrements on plants. We found no significant effects of caterpillar colors or shapes on predation in Hirosaki. In contrast, black and curled caterpillars received significantly lower predation by birds in Xishuangbanna constantly across time. However, we were unable to provide evidence that the black-curled sawfly larvae are masquerading as excrements. Shapes of the dummy caterpillars also affected the predation by ants and parasitoid wasps at certain times. This is the first report on ecological function of the curled posture of sawfly larvae, and we demonstrated the importance to assess the temporal dynamics of predation and effectiveness of defensive tactics in tropical forests.

Intraspecific Adaptation Load: A Mechanism for Species Coexistence.

Evolutionary ecological theory suggests that selection arising from interactions with conspecifics, such as sexual and kin selection, may result in evolution of intraspecific conflicts and evolutionary 'tragedy of the commons'. Here, we propose that such an evolution of conspecific conflicts may affect population dynamics in a way that enhances species coexistence. Empirical evidence and theoretical models suggest that more abundant species is more susceptible to invasion of 'selfish' individuals that increase their own reproductive success at the expense of population growth (intraspecific adaptation load). The density-dependent intraspecific adaptation load gives rise to a self-regulation mechanism at the population level, and stabilizes species coexistence at the community level by negative frequency-dependence.

Outcome of interspecific competition depends on genotype of conspecific neighbours.

The outcome of interspecific competition is affected by numerous abiotic and biotic factors. However, the effects of genetic relatedness of conspecific neighbours have not been elucidated. Here, we demonstrate that the genotype of a conspecific neighbour determines the outcome of interspecific competition. We investigated effects of genotype of neighbour sibling or non-sibling Plantago asiatica plants on competition with Trifolium repens plants. Pairs of P. asiatica, sibling or non-sibling, were grown in competition with T. repens. Sibling P. asiatica plants, but not non-sibling plants, increased leaf placement towards competitor T. repens plants, and that placement was correlated negatively with the biomass of T. repens and positively with seed production by P. asiatica. Seed production by P. asiatica plants competing with T. repens was greater in individuals paired with siblings than in those paired with non-siblings. Thus, our results show that the genotype of conspecific neighbours can alter the outcome of interspecific competition.

Correction to: Extraforal nectary-bearing plant Mallotus japonicus uses diferent types of extraforal nectaries to establish efective defense by ants.

The article Extraforal nectary-bearing plant Mallotus japonicus uses diferent types of extraforal nectaries to establish efective defense by ants, written by Akira Yamawo.

Damage to leaf veins suppresses root foraging precision.

PREMISE: Plants generally increase root growth in areas with high nutrients in heterogeneous soils, a phenomenon called foraging precision. The physiology of this process is not well understood, but it may involve shoot-root signaling via leaf veins. If this is true, then damage to leaf veins, but not to nearby mesophyll, would reduce plant foraging precision. METHODS: To test this hypothesis, we imposed two leaf damage treatments on Plantago asiatica and Prunus jamasakura, removing either the tip of each main vein or mesophyll tissue between the veins with a 3-mm-diameter hole punch. After 30 days or 20 weeks of plant growth, we measured root biomass in the soil in response to soil nutrient concentration. RESULTS: When leaf mesophyll was damaged, root biomass of both species was greater in nutrient-rich patches than in nutrient-poor patches. However, when leaf veins were damaged, root biomass was similar between patches. CONCLUSIONS: These results suggest the importance of shoot-root signaling in plants, emphasizing that physiological processes are not necessarily restricted to single organs. The idea that herbivores that damage leaf veins may affect a plant's ability to selectively forage in high-nutrient patches is novel, with implications for natural and managed systems.

Extrafloral nectary-bearing plant Mallotus japonicus uses different types of extrafloral nectaries to establish effective defense by ants.

Extrafloral nectary (EFN)-bearing plants attract ants to gain protection against herbivores. Some EFN-bearing plants possess different types of EFNs, which might have different effects on ants on the plants. Mallotus japonicus (Thunb.) Muell. Arg. (Euphorbiaceae) bears two types of EFNs, including a pair of large EFNs at the leaf base and many small EFNs along the leaf edge. This study aimed to determine the different roles of the two types of EFNs in biotic defense by ants. A field experiment was conducted to investigate the effect of leaf damage on EFN production and on the distribution pattern of ants. After leaf damage, the number of leaf edge EFNs increased in the leaves first-produced. The number of ants on the leaves also increased, and the foraging area of ants extended from the leaf base to the leaf tip. An EFN-covering field experiment revealed that leaf edge EFNs had a greater effect than leaf base EFNs on ant dispersal on leaves. The extended foraging area of ants resulted in an increase of encounter or attack rate against an experimentally placed herbivore, Spodoptera litura. These results suggest that M. japonicus plants control the foraging area of ants on their leaves using different types of EFNs in response to leaf damage, thus achieving a very effective biotic defense against herbivores by ants.

Self-discrimination in vine tendrils of different plant families.

Previous study reported a novel type of self-discrimination in the tendrils of the vine Cayratia japonica (Vitaceae). However, whether self-discrimination in tendrils is common in vine plant species has not been elucidated. Here, we investigated whether tendrils of Momordica charantia var. pavel (Cucurbitaceae), Cucumis sativus (Cucurbitaceae) and Passiflora caerulea (Passifloraceae) can discriminate self and non-self plants. We also investigated whether the tendrils of M. charantia and C. sativus can discriminate differences in cultivars to determine the discrimination ability for genetic similarity. We found that tendrils of the M. charantia and P. caerulea were more likely to coil around non-self plant than self plants, but not in C. sativus. Our findings support the common occurrence of self-discrimination in tendrils in different plant taxa, although some species lacked it. Furthermore, tendrils of M. charantia more rapidly coil around different cultivars than around same cultivars. The tendrils of M. charantia may can discriminate differences in cultivars.

Induction and relaxation of extrafloral nectaries in response to simulated herbivory in young Mallotus japonicus plants.

The disadvantage of induced defenses compared with constitutive defenses is the time during which a plant is vulnerable to herbivory before activation. There is obvious importance in determining the costs and benefits of induced defenses. Some plants produce extrafloral nectaries (EFNs), which attract ants that protect against herbivores, and induce EFNs and extrafloral nectar in response to leaf damage. To understand induction of indirect defense by ants, we investigated the induction and relaxation of extrafloral nectar secretion and EFN formation after artificial leaf damage in young Mallotus japonicus. Plants were grown under control or leaf damage conditions a greenhouse or in the field. Following artificial leaf damage, we assessed secretion of extrafloral nectar and the number of ant workers on plants. We measured the number of EFNs on each of seven leaves produced after leaf damage. Extrafloral nectar secretion was induced within 1 day following leaf damage, resulting in the attraction of numerous ant workers, and the extrafloral nectar secretion decreased to initial levels after 7 days. The number of EFNs was largest on the first leaf and smallest on the sixth leaf produced after leaf damage, but the total number of EFNs did not differ between treatments. Thus, M. japonicus rapidly induces extrafloral nectar secretion after leaf damage, followed by relaxation. Furthermore, following induction of EFNs on newly produced leaves, it may decrease the cost of induction by reducing the number of EFNs on leaves produced later.

Seeds integrate biological information about conspecific and allospecific neighbours.

Numerous organisms integrate information from multiple sources and express adaptive behaviours, but how they do so at different developmental stages remains to be identified. Seeds, which are the embryonic stage of plants, need to make decisions about the timing of emergence in response to environmental cues related to survival. We investigated the timing of emergence of Plantago asiatica (Plantaginaceae) seed while manipulating the presence of Trifolium repens seed and the relatedness of neighbouring P. asiatica seed. The relatedness of neighbouring P. asiatica seed and the presence of seeds of T. repens did not on their own influence the timing of P. asiatica emergence. However, when encountering a T. repens seed, a P. asiatica seed emerged faster in the presence of a sibling seed than in the presence of a non-sibling seed. Water extracts of seeds gave the same result. We show that P. asiatica seeds integrate information about the relatedness of neighbouring P. asiatica seeds and the presence of seeds of a different species via water-soluble chemicals and adjust their emergence behaviour in response. These findings suggest the presence of kin-dependent interspecific interactions.

Concentration and retention of chlorophyll around the extrafloral nectary of Mallotus japonicus.

Plants need to allocate some of their limited resources for defense against herbivores as well as for growth and reproduction. However, the priority of resource allocation within plants has not been investigated. We hypothesized that plants with extrafloral nectaries (EFNs) invest more chlorophyll around their EFNs-to support a high rate of carbon fixation there-than in other leaf parts of young leaves. Additionally, this chlorophyll may remain around EFNs rather than in the other leaf parts. We used Mallotus japonicus plants to investigate the chlorophyll content at leaf centers and edges and around EFNs at four stages of leaf development: middle-expanded young leaves, fully expanded mature leaves, senior leaves, and leaves prior to abscission. These four stages of development were located at the third, fifth, eighth, and eleventh leaf positions from the apex, respectively. The results revealed that the chlorophyll content around the EFN side of the third-position leaves was higher than that at the leaf center or edge. Although the chlorophyll content in the fifth-position leaves did not differ between those at the leaf edge and around EFNs, the chlorophyll content around EFNs in the eighth-position leaves was higher than that at the leaf centre and edge. The volume of EF nectar was positively correlated with the chlorophyll content around EFN during the leaf stage, but it was not correlated with the chlorophyll content in the leaf center and edge, except in fifth-position leaves. These findings suggest that M. japonicus plants facilitate and maintain secretion of EF nectar in their young and old leaves, respectively, through the concentration and retention of chlorophyll around EFNs.