Seeing through the static: the temporal dimension of plant–animal mutualistic interactions

Most studies of plant–animal mutualistic networks have come from a temporally static perspective. This approach has revealed general patterns in network structure, but limits our ability to understand the ecological and evolutionary processes that shape these networks and to predict the consequences of natural and human‐driven disturbance on species interactions. We review the growing literature on temporal dynamics of plant–animal mutualistic networks including pollination, seed dispersal and ant defence mutualisms. We then discuss potential mechanisms underlying such variation in interactions, ranging from behavioural and physiological processes at the finest temporal scales to ecological and evolutionary processes at the broadest. We find that at the finest temporal scales (days, weeks, months) mutualistic interactions are highly dynamic, with considerable variation in network structure. At intermediate scales (years, decades), networks still exhibit high levels of temporal variation, but such variation appears to influence network properties only weakly. At the broadest temporal scales (many decades, centuries and beyond), continued shifts in interactions appear to reshape network structure, leading to dramatic community changes, including loss of species and function. Our review highlights the importance of considering the temporal dimension for understanding the ecology and evolution of complex webs of mutualistic interactions.     

Interactions between functionally diverse fungal mutualists inconsistently affect plant performance and competition

Plants form mutualistic relationship with a variety of belowground fungal species. Such a mutualistic relationship can enhance plant growth and resistance to pathogens. Yet, we know little about how interactions between functionally diverse groups of fungal mutualists affect plant performance and competition. We experimentally determined the effects of interaction between two functional groups of belowground fungi that form mutualistic relationship with plants, arbuscular mycorrhizal (AM) fungi and Trichoderma, on interspecific competition between pairs of closely related plant species from four different genera. We hypothesized that the combination of two functionally diverse belowground fungal species would allow plants and fungi to partition their symbiotic relationships and relax plant–plant competition. Our results show that: 1) the AM fungal species consistently outcompeted the Trichoderma species independent of plant combinations; 2) the fungal species generally had limited effects on competitive interactions between plants; 3) however, the combination of fungal species relaxed interspecific competition in one of the four instances of plant–plant competition, despite the general competitive superiority of AM fungi over Trichoderma. We highlight that the competitive outcome between functionally diverse fungal species may show high consistency across a broad range of host plants and their combinations. However, despite this consistent competitive hierarchy, the consequences of their interaction for plant performance and competition can strongly vary among plant communities.     

Abundance drives broad patterns of generalisation in plant–hummingbird pollination networks

Abundant pollinators are often more generalised than rare pollinators. This could be because abundant species have more chance encounters with potential interaction partners. On the other hand, generalised species could have a competitive advantage over specialists, leading to higher abundance. Determining the direction of the abundance–generalisation relationship is therefore a ‘chicken‐and‐egg’ dilemma. Here we determine the direction of the relationship between abundance and generalisation in plant–hummingbird pollination networks across the Americas. We find evidence that hummingbird pollinators are generalised because they are abundant, and little evidence that hummingbirds are abundant because they are generalised. Additionally, most patterns of species‐level abundance and generalisation were well explained by a null model that assumed interaction neutrality (interaction probabilities defined by species relative abundances). These results suggest that neutral processes play a key role in driving broad patterns of generalisation in animal pollinators across large spatial scales.     

Consequences of grazing on the vertical transmission of a fungal Neotyphodium symbiont in an annual grass population

Symbiosis between cool‐season grasses and vertically transmitted fungal endophytes are common and significantly impact on ecosystem function. This makes the understanding of the underlying mechanisms to symbiotic individuals frequency in local populations much more interesting. Most studies have been focused on the differential fitness between symbiotic and non‐symbiotic counterparts (relative fitness), barely considering other mechanisms. We performed a microcosms experiment to evaluate whether grazing alters the dynamics of the endophyte Neotyphodium occultans in the annual grass Lolium multiflorum by simultaneously modifying the relative fitness and the endophyte efficiency to be transmitted from host plants to seeds. Grazing was simulated by means of clipping and trampling on symbiotic and non‐symbiotic plants growing separately, in soils obtained from paddocks, differing in their agronomic management history (natural grassland vs. ryegrass promotion). Seed production showed a complex pattern as it depended on the symbiotic status of the plants, the level of grazing and the agro‐ecological context. Grazed plants produced three times fewer seeds than ungrazed plants only in microcosms with endophyte‐symbiotic plants in soils from ryegrass promotion. Endophyte benefits on seed production were exclusively observed in ungrazed plants in the same soil. Symbiotic plants produced symbiotic and non‐symbiotic seeds in all the treatments. While the production of non‐symbiotic seeds by these plants was not affected by grazing and the soil, grazing reduced the production of symbiotic seeds in both contexts. Grazing negative effect on the density of fully infected spikes determined a significant increment in the transmission failures which were not modified by agro‐ecological contexts. Therefore, grazing can modulate symbiosis dynamics through reducing seed production and endophyte transmission efficiency. Transmission has been disregarded, but it is a context‐dependent process that could lead to a gradual reduction in the symbiotic plants frequency in a population if the mutualism effectiveness does not outweigh transmission failures.     

Ants suppressing plant pathogens: a review

Ant–plant mutualisms are usually regarded as driven by ants defending plants against herbivores in return for plant‐produced food rewards and housing. However, ants may provide additional services. In a review of published studies on ant–pathogen–plant interactions, we investigated whether ants’ extensive hygiene measures, including the use of ant‐produced antibiotics, extend to their host plants and reduce plant pathogen loads. From 30 reported species combinations, we found that the presence of ants lead to reduced pathogen levels in 18 combinations and to increased levels in 6. On average, ants significantly reduced pathogen incidence with 59%. This effect size did not differ significantly from effect sizes reported from meta‐analyses on herbivore protection. Thus, pathogen and herbivore protection could be of equal importance in ant–plant mutualisms. Considering the abundance of these interactions, ecological impacts are potentially high. Furthermore, awareness of this service may stimulate the development of new measures to control plant diseases in agriculture. It should be noted, though, that studies were biased toward tropical ant–plant symbioses and that the literature in the field is limited at present. Future research on plant pathogens is needed to enhance our understanding of ant–plant mutualisms and their evolution.     

Developmental Changes in Direct and Indirect Defenses in the Young Leaves of the Neotropical Tree Genus Inga (Fabaceae)

Plant fitness is affected by herbivory, and in moist tropical forests, 70 percent of herbivore damage occurs on young leaves. Thus, to understand the effects of herbivory on tropical plant fitness, it is necessary to understand how tropical young leaves survive the brief, but critical, period of susceptibility. In this study, we surveyed three species of Inga during young leaf expansion. Three classes of toxic secondary metabolites (phenolics, saponins, and tyrosine), extrafloral nectar production, leaf area, and extrafloral nectary area were measured at randomly assigned young leaf sizes. In addition, all defenses were compared for potential trade‐offs during leaf expansion. No trade‐offs among defenses were found, and the concentration of all defenses, except tyrosine, decreased during leaf expansion. We suggest that plants continued to increase phenolic and saponin content, but at a rate that resulted in decreasing concentrations. In contrast, tyrosine content per leaf steadily increased such that a constant concentration was maintained regardless of young leaf size. Nectar production remained constant during leaf expansion, but, because young leaf area increased by tenfold, the investment in extrafloral nectar per leaf area significantly decreased. In addition, nectary area did not change during leaf expansion and therefore the relative size of the nectary significantly decreased during young leaf expansion. These results support the predictions of the optimal defense hypothesis and demonstrate that the youngest leaves have the highest investment in multiple defenses, most likely because they have the highest nitrogen content and are most susceptible to a diversity of herbivores.     

The Contribution of Extrafloral Nectar to Survival and Reproduction of the Predatory Mite Iphiseius Degenerans on Ricinus Communis

The phytoseiid mite Iphiseius degenerans (Berlese) is an effective predator of western flower thrips, Frankliniella occidentalis (Pergande), in Dutch greenhouses. In the Mediterranean area, castor bean, Ricinus communis L., is known as a year-round host plant for this predatory mite. On flowering castor bean plants in greenhouses, I. degenerans can be found in densities of more than 100 per leaf. For this reason, the plant is being used as a banker plant to augment biological control. It has been shown that pollen produced by the large apical flowers sustains reproduction and development for these mites. The objective of this study was to measure the contribution of the extrafloral nectar of this plant to the reproductive success of this predatory mite. A study conducted at 25°C in presence of free water showed that (1) I. degenerans is unable to develop beyond the protonymphal stage when fed only nectar and leaf tissue, (2) its ovipositional rate is higher when pollen is supplemented with nectar, (3) its reproduction ceases within a few days when fed on nectar only, but the predator can survive for several weeks and resume oviposition when fed pollen again and (4) the feeding of young females for one or two weeks with nectar only extends their longevity by approximately the same period and only slightly diminishes their lifetime reproductive potential (R0), as compared to mites continuously fed pollen. It can be concluded that extrafloral nectar can provide an important contribution to population growth and maintenance of I. degenerans on R. communis, particularly in pre- and post-blooming periods. Assuming these predators are beneficial to the plant in clearing them of herbivorous mites and thrips, this relationship may be regarded as an example of plant–predator mutualism. The combination of pollen and extrafloral nectar makes castor bean an ideal rearing and banker plant for I. degenerans.     

Root volatiles in plant–plant interactions II: Root volatiles alter root chemistry and plant–herbivore interactions of neighbouring plants

Volatile organic compounds (VOCs) emitted by plant roots can influence the germination and growth of neighbouring plants. However, little is known about the effects of root VOCs on plant–herbivore interactions of neighbouring plants. The spotted knapweed (Centaurea stoebe) constitutively releases high amounts of sesquiterpenes into the rhizosphere. Here, we examine the impact of C. stoebe root VOCs on the primary and secondary metabolites of sympatric Taraxacum officinale plants and the resulting plant‐mediated effects on a generalist root herbivore, the white grub Melolontha melolontha. We show that exposure of T. officinale to C.stoebe root VOCs does not affect the accumulation of defensive secondary metabolites but modulates carbohydrate and total protein levels in T. officinale roots. Furthermore, VOC exposure increases M. melolontha growth on T. officinale plants. Exposure of T. officinale to a major C. stoebe root VOC, the sesquiterpene (E)‐β‐caryophyllene, partially mimics the effect of the full root VOC blend on M. melolontha growth. Thus, releasing root VOCs can modify plant–herbivore interactions of neighbouring plants. The release of VOCs to increase the susceptibility of other plants may be a form of plant offense.     

昆虫共生菌的垂直传播

共生菌普遍存在于昆虫体内,它们能够为宿主昆虫提供生长发育所必需的氨基酸、固醇类等营养物质,还能提高昆虫适应高温、寄生虫、病毒等不利环境因素的能力,昆虫则为共生菌提供稳定的生存环境和营养物质,昆虫与共生菌相互依存。多数情况下,共生菌通过垂直传播在宿主代次间进行传播,即共生菌由母代传递给子代。结合最近几年相关研究,本文综述了不同昆虫共生菌的垂直传播模式。除极少数肠道共生菌通过污染卵壳被宿主幼虫取食得以垂直传播外,垂直传播的共生菌多为经卵传播。根据侵染时期的不同,共生菌经卵传播模式多数可分为以下4种：侵染宿主昆虫幼虫中的生殖干细胞、侵染宿主昆虫年轻雌成虫中的生殖干细胞、侵染宿主昆虫雌成虫中的成熟卵母细胞以及侵染宿主昆虫囊胚期胚胎。其中,有些共生菌是以共生菌菌胞整体侵染的方式进入到宿主卵巢。另外,少数肠道共生菌也通过卵巢进行垂直传播,此类共生菌先侵染卵巢侧输卵管并在侧输卵管聚集,待卵排放至侧输卵管时再进入到卵中。在文中,我们也探讨了昆虫共生菌垂直传播过程中的细胞机制和免疫机制,包括共生菌避开宿主免疫反应、共生菌通过内吞作用进入卵巢以及不同共生菌间的协同作用等。     

Environmental filtering structures fungal endophyte communities in tree bark

The factors that control the assembly and composition of endophyte communities across plant hosts remains poorly understood. This is especially true for endophyte communities inhabiting inner tree bark, one of the least studied components of the plant microbiome. Here, we test the hypothesis that bark of different tree species acts as an environmental filter structuring endophyte communities, as well as the alternative hypothesis, that bark acts as a passive reservoir that accumulates a diverse assemblage of spores and latent fungal life stages. We develop a means of extracting high‐quality DNA from surface sterilized tree bark to compile the first culture‐independent study of inner bark fungal communities. We sampled a total of 120 trees, spanning five dominant overstorey species across multiple sites in a mixed temperate hardwood forest. We find that each of the five tree species harbour unique assemblages of inner bark fungi and that angiosperm and gymnosperm hosts harbour significantly different fungal communities. Chemical components of tree bark (pH, total phenolic content) structure some of the differences detected among fungal communities residing in particular tree species. Inner bark fungal communities were highly diverse (mean of 117–171 operational taxonomic units per tree) and dominated by a range of Ascomycete fungi living asymptomatically as putative endophytes. Together, our evidence supports the hypothesis that tree bark acts as an environmental filter structuring inner bark fungal communities. The role of these potentially ubiquitous and plant‐specific fungal communities remains uncertain and merits further study.     

Soil conditioning effects of Phragmites australis on native wetland plant seedling survival

Interactions between introduced plants and soils they colonize are central to invasive species success in many systems. Belowground biotic and abiotic changes can influence the success of introduced species as well as their native competitors. All plants alter soil properties after colonization but, in the case of many invasive plant species, it is unclear whether the strength and direction of these soil conditioning effects are due to plant traits, plant origin, or local population characteristics and site conditions in the invaded range. Phragmites australis in North America exists as a mix of populations of different evolutionary origin. Populations of endemic native Phragmites australis americanus are declining, while introduced European populations are important wetland invaders. We assessed soil conditioning effects of native and non‐native P. australis populations on early and late seedling survival of native and introduced wetland plants. We further used a soil biocide treatment to assess the role of soil fungi on seedling survival. Survival of seedlings in soils colonized by P. australis was either unaffected or negatively affected; no species showed improved survival in P. australis‐conditioned soils. Population of P. australis was a significant factor explaining the response of seedlings, but origin (native or non‐native) was not a significant factor. Synthesis: Our results highlight the importance of phylogenetic control when assessing impacts of invasive species to avoid conflating general plant traits with mechanisms of invasive success. Both native (noninvasive) and non‐native (invasive) P. australis populations reduced seedling survival of competing plant species. Because soil legacy effects of native and non‐native P. australis are similar, this study suggests that the close phylogenetic relationship between the two populations, and not the invasive status of introduced P. australis, is more relevant to their soil‐mediated impact on other plant species.     

Invasive ants disrupt frugivory by endemic island birds

Biological invasions can alter direct and indirect interactions between species, generating far-reaching changes in ecological networks that affect key ecological functions. We used model and real fruit assays to show that the invasion and formation of high-density supercolonies by the yellow crazy ant (YCA), Anoplolepis gracilipes, disrupt frugivory by endemic birds on Christmas Island, Indian Ocean. The overall handling rates of model fruits by birds were 2.2–2.4-fold lower in ant-invaded than in uninvaded rainforest, and pecking rates by two bird species declined by 2.6- and 4.5-fold, respectively. YCAs directly interfered with frugivory; their experimental exclusion from fruiting displays increased fruit handling threefold to sixfold, compounding indirect effects of ant invasion on resources and habitat structure that influence bird abundances and behaviours. This invasive ant, whose high densities are sustained through mutualism with introduced scale insects, rapidly decreases fruit handling by endemic island birds and may erode a key ecological function, seed dispersal. Because most other invasive ant species form expansive, high-density supercolonies that depend in part on association with hemipteran mutualists, the effects that we report here on avian frugivore–plant associations may emerge across their introduced ranges.     

Above‐ and belowground biotic interactions facilitate relocation of plants into cooler environments

One important but largely unanswered question about floristic responses to climate change is how interactions such as competition, facilitation and plant–soil feedbacks will influence the ability of species to track shifting climates. In a rugged and moisture‐limited region that has recently warmed by 2° (Siskiyou Mountains, OR, USA), we planted three species into cooler aspects and elevations than those they currently inhabit, with and without removal of neighbouring plants, and tracked them over 2 years. Two species had higher success in cooler topographic locations, and this success was enhanced by neighbouring plants, which appeared to modulate minimum growing season temperatures. One species' success was also facilitated by the higher soil organic matter found in cooler sites. These results are a novel experimental demonstration of two important factors that may buffer climate change impacts on plants: rugged topography and plant–plant facilitation.     

Plant controls on Late Quaternary whole ecosystem structure and function

Plants and animals influence biomass production and nutrient cycling in terrestrial ecosystems; however, their relative importance remains unclear. We assessed the extent to which mega‐herbivore species controlled plant community composition and nutrient cycling, relative to other factors during and after the Late Quaternary extinction event in Britain and Ireland, when two‐thirds of the region's mega‐herbivore species went extinct. Warmer temperatures, plant–soil and plant–plant interactions, and reduced burning contributed to the expansion of woody plants and declining nitrogen availability in our five study ecosystems. Shrub biomass was consistently one of the strongest predictors of ecosystem change, equalling or exceeding the effects of other biotic and abiotic factors. In contrast, there was relatively little evidence for mega‐herbivore control on plant community composition and nitrogen availability. The ability of plants to determine the fate of terrestrial ecosystems during periods of global environmental change may therefore be greater than previously thought.     

Vertical transmission of hepatitis B virus in Culex quinquefasciatus

An investigation of the vertical transmission of hepatitis B virus (HBV) in Culex quinquefasciatus Say revealed the presence of low levels of the virus in adult F1 progeny from the first ovarian cycle of mosquitoes infected by feeding on HBV positive human blood. HBV was not transmitted vertically during the second, third and fourth ovarian cycles nor to the F2 generation. The salivary glands, ovaries and faeces of the F1 generation did not contain detectable levels of HBV. Progeny of female Cx quinquefasciatus mated with F1 males were negative for HBV.     

Inclusive fitness,asymmetric competition and kin selection in plants

The findings that some plants alter their competitive phenotype in response to genetic relatedness of its conspecific neighbour (and presumed competitor) has spurred an increasing interest in plant kin‐interactions. This phenotypic response suggests the ability to assess the genetic relatedness of conspecific competitors, proposing kin selection as a process that can influence plant competitive interactions. Kin selection can favour restrained competitive growth towards kin, if the fitness loss from reducing own growth is compensated by increased fitness in the related neighbour. This may lead to positive frequency dependency among related conspecifics with important ecological consequences for species assemblage and coexistence. However, kin selection in plants is still controversial. First, many studies documenting a plastic response to neighbour relatedness do not estimate fitness consequences of the individual that responds, and when estimated, fitness of individuals grown in competition with kin did not necessarily exceed that of individuals grown in non‐kin groups. Although higher fitness in kin groups could be consistent with kin selection, this could also arise from mechanisms like asymmetric competition in the non‐kin groups. Here we outline the main challenges for studying kin selection in plants taking genetic variation for competitive ability into account. We emphasize the need to measure inclusive fitness in order to assess whether kin selection occurs, and show under which circumstances kin selected responses can be expected. We also illustrate why direct fitness estimates of a focal plant, and group fitness estimates are not suitable for documenting kin selection. Importantly, natural selection occurs at the individual level and it is the inclusive fitness of an individual plant – not the mean fitness of the group – that can capture if a differential response to neighbour relatedness is favoured by kin selection.