Nonselective oviposition by a fastidious insect: the laboratory host range of the melaleuca gall midge Lophodiplosis trifida (Diptera: Cecidomyiidae)

Invasion by the Australian paperbark, Melaleuca quinquenervia, has degraded large areas of south Florida wetlands. Restoration of these wetlands requires the removal of expansive monocultures of this large tree while simultaneously curtailing its spread. Management strategies developed by federal and state agencies include biological control to halt the spread of this species and to prevent reinfestation of cleared areas. This requires biological agents able to reduce flowering, seed production, and growth while increasing mortality of seedlings and saplings. Two of the three introduced agents (Oxyops vitiosa Pascoe and Boreioglycaspis melaleucae Moore) partially meet these needs but outcomes are not spatially or temporally consistent. Thus, additional agents are needed. The bud-gall fly Fergusonina turneri Taylor, with its mutualistic nematode Fergusobia quinquenerviae Davies and Giblin-Davis, is actively being released but has not established. A fourth promising agent, the gall midge Lophodiplosis trifida Gagné, manifested an extremely narrow host range during laboratory testing. Oviposition was indiscriminant in caged environments. Small, incipient, unilocular galls were initiated on Melaleuca viminalis, but larval development ensued only on M. quinquenervia. The unilocular galls on M. viminalis did not grow and produced no adult flies. As a result, M. viminalis test plants suffered only minor cosmetic damage. Observations from both Australia and Florida attest to the ability of this midge to impede M. quinquenervia growth and kill small plants. Thus, L. trifida is safe to release and will likely contribute to management objectives for control of this pernicious wetland invader.     

A gall-forming biological control agent suppresses vegetative growth of an invasive tree

Attack by the gall-forming biological control agent Lophodiplosis trifida Gagné (Diptera: Cecidomyiidae), reduced Melaleuca quinquenervia sapling height by 10.1%, leaf biomass by 42%, woody biomass by 42.7%, and root biomass by 30.3%. This provided the first quantitative evidence of the potential of L. trifida to suppress pre-reproductive M. quinquenervia.     

Physiological host range of two highly specialised mutualistic symbiotes: the fly Fergusonina turneri and its obligate nematode Fergusobia quinquenerviae,potential biocontrol agents of Melaleuca quinquenervia

In Australia, galls develop on Melaleuca quinquenervia (Cav.) S.T. Blake (Myrtaceae) as a result of the mutualistic association between the fly Fergusonina turneri Taylor (Diptera: Fergusoninidae) and its obligate nematode Fergusobia quinquenerviae Davies & Giblin-Davis (Tylenchida: Sphaerulariidae). The nematode induces gall formation, whereas the fly promotes gall maturation. Together they exploit M. quinquenervia buds and may inhibit stem elongation and flower formation. We delimited the physiological host range of this pair to determine their suitability as biological control agents of invasive M. quinquenervia populations in Florida, USA. Host use was assessed for eight species of Myrtaceae native to Florida, eight phylogenetically related ornamental species and oviposition alone on five non-myrtaceous species. Although oviposition was less specific, galls developed and matured only on M. quinquenervia. After establishment, galls are predicted to prevent flower and seed production, thereby reducing the regenerative potential of M. quinquenervia. This is the first example of an insect/nematode mutualism released as biological control agents of an invasive plant.     

Effects of sclerophylly and host choice on gall densities and herbivory distribution in an Australian subtropical forest

We hypothesize that upper canopies contrast with the understorey vegetation in gall density and survival because of greater mortality in the latter. We expect that high sclerophylly rates in the upper canopy leaves are a main cause of such pattern, and more important than other environmental traits, for instance related to altitude. The study was conducted in Lamington National Park, Queensland, Australia. Four independent vertical cylindrical transects through the forest canopy and one equivalent, horizontal understorey transect (20 m long and 1 m in diameter) were sampled at different altitude (300, 700, 900 and 1100 m above sea level) during two seasons. Total and damaged leaves were counted, and galls were collected and opened to determine if they were alive or what may have been the cause of death. Sclerophylly was estimated as specific foliar mass. Out of 72 sampled plant species, 29 presented galls, of which the greatest densities were concentrated on seven host species. A significant increase in sclerophylly with increasing canopy stratum height was observed, but had no direct effect on gall distribution. Total and live galls were more abundant in the canopy than in the understorey for all altitudes but 300 m, where a specific infestation on saplings of the canopy tree Arytera divaricata occurred. We found a positive gall establishment and survivorship in the upper canopy, along with a decrease in chewing herbivory, which resulted in decreasing risks of gall death by herbivory. An overall high sclerophylly rate in both canopy and understorey and the total number of galled host species suggest that the plant community studied is prone to gall establishment and evolution. However, a few hosts species with extreme infestation, such as A. divaricata and Ficus watkinsiana, override the community‐wide effect of sclerophylly. Our results emphasize how scarce and patchy distributed galls are.     

Stem‐galling moths provide cetoniine beetles with feeding sites via sap exudation of invasive alien plants

The alien moth Epiblema sugii (Lepidoptera: Tortricidae) induces stem galls on an invasive alien weed, Ambrosia trifida. During summer, along riverbanks in central Japan, the native insects Protaetia brevitarsis, P. orientalis submarumorea (Coleoptera: Scarabaeidae: Cetoniinae), and Camponotus vitiosus (Hymenoptera: Formicidae) feed on the sap exuded from the galls. The cetoniine beetles are highly aggregated among the galls and make wounds on the galls to facilitate sap exudation. Feeding on gall sap may be beneficial to the beetles due to the efficient intake of water and sugar, and the beetles’ inflicting wounds and feeding on the sap seem to have little effect on the gallers. This is a unique finding, where alien plant–galler interaction provides a feeding site for native insects.     

Non-random distribution among a guild of parasitoids: implications for community structure and host survival

Abstract 1. Immature stages of the gall midge, Asphondylia borrichiae, are attacked by four species of parasitoids, which vary in size and relative abundance within patches of the gall midge’s primary host plant, sea oxeye daisy (Borrichia frutescens). 2. In the current study, a bagging experiment found that the smallest wasp, Galeopsomyia haemon, was most abundant in galls exposed to natural enemies early in the experiment, when gall diameter is smallest, while the wasp with the longest ovipositor, Torymus umbilicatus, dominated the parasitoid community in galls that were not exposed until the 5th and 6th weeks when gall diameter is maximal. 3. Moreover, the mean number of parasitoids captured using large artificial galls were 70% and 150% higher compared with medium and small galls respectively, while stem height of artificial galls significantly affected parasitoid distribution. Galls that were level with the top of the sea oxeye canopy captured 60% more parasitoids compared with those below the canopy and 50% more than galls higher than the plant canopy. 4. These non‐random patterns were driven primarily by the differential distribution of the largest parasitoid, T. umbilicatus, which was found significantly more often than expected on large galls and the smallest parasitoid of the guild, G. haemon, which tended to be more common on stems level with the top of the plant canopy. 5. Large Asphondylia galls, especially those located near the top of the Borrichia canopy, were more likely to be discovered by searching parasitoids. Results using artificial galls were consistent with rates of parasitism of Asphondylia galls in native patches of sea oxeye daisy. Gall diameter was 19% greater and the rate of parasitism was reduced by almost 50% on short stems; as a result, gall abundance was 24% higher on short stems compared with ones located near the top of the plant canopy. 6. These results suggest that parasitoid community composition within galls is regulated by both interspecific differences in ovipositor length and preferences for specific gall size and/or stem length classes.     

The influence of plant size on attack rates of Oxyops vitiosa,an introduced herbivore of Melaleuca quinquenervia

Oxyops vitiosa Pascoe (Coleoptera: Curculionidae) was released in Florida in 1997 as a biological control agent of the invasive tree Melaleuca quinquenervia (Cav.) S.T. Blake. Three years after release, the weevil’s dispersal into three replicated M. quinquenervia stands was monitored to determine if O. vitiosa preferentially selects larger trees during patch colonisation. Data indicated that tree size did not influence the likelihood of an attack by O. vitiosa and smaller individuals within host patches did not escape herbivory through enemy-free space.     

Root development and competitive ability of the invasive species Melaleuca quinquenervia (Cav.) S.T. Blake in the South Florida flatwoods

Melaleuca quinquenervia (Cav.) S.T. Blake is an aggressive, invasive species in sub-tropical Florida that is considered a serious threat to the existing biological integrity of many subtropical ecosystems in south Florida. It prevents other species from thriving through its high rate of seed production/germination and the formation of a dense tree canopy. However, its ability to take over a site between initial seedling establishment and crown closure is not well understood. The objective of this study was to determine (i) the nature of root development with time and soil depth, and (ii) the ability of M. quinquenervia to invade and absorb nutrients from soil already occupied by native vegetation. The working hypotheses were that M. quinquenervia captures a site either by (i) tolerating competition by prolifically growing roots into soil already occupied by native plants, or (ii) avoiding competition by rooting to depths where inter-root competition is less and water supply during a drought is available. Soil trenches and in-growth trays were used to measure root distribution and growth. Root number (# m^–2), root length density (m root m^–3 soil volume), and root biomass (g root m^–3 soil) were determined. This study demonstrated that M. quinquenervia (1) is a prolific rooter with or without the presence of competing vegetation; (2) can develop root densities higher than many mature native species at an early age; (3) can develop roots in the soil surface during soil drying periods, even while competitive grasses are dying out; (4) can develop a deep root system at an early age; and (5) is an effective rooter in both moist and dry water regimes in this fluctuating water table soil. The data suggested that this species is a strong competitor through the use of both competition avoidance and tolerance mechanisms and that the rooting habit of M. quinquenervia should be an important consideration when evaluating its ability as an invasive species.     

A gall-inducing arthropod drives declines in canopy tree photosynthesis

Mature forest canopies sustain an enormous diversity of herbivorous arthropods; however, with the exception of species that exhibit large-scale outbreaks, canopy arthropods are thought to have relatively little influence on overall forest productivity. Diminutive gall-inducing mites (Acari; Eriophyoidae) are ubiquitous in forest canopies and are almost always highly host specific, but despite their pervasive occurrence, the impacts of these obligate parasites on canopy physiology have not been examined. We have documented large declines in photosynthetic capacity (approx. 60%) and stomatal conductance (approx. 50%) in canopy leaves of mature sugar maple (Acer saccharum) trees frequently galled by the maple spindle gall mite Vasates aceriscrumena. Remarkably, such large impacts occurred at very low levels of galling, with the presence of only a few galls (occupying approx. 1% of leaf area) compromising gas-exchange across the entire leaf. In contrast to these extreme impacts on the leaves of adult trees, galls had no detectible effect on the gas-exchange of maple saplings, implying large ontogenetic differences in host tolerance to mite galling. We also found a significant negative correlation between canopy tree radial increment growth and levels of mite galling. Increased galling levels and higher physiological susceptibility in older canopy trees thus suggest that gall-inducing mites may be major drivers of “age-dependent” reductions in the physiological performance and growth of older trees.     

Biocontrol without borders: the unintended spread of introduced weed biological control agents

An underlying assumption of classical biological control implies that intentionally introduced natural enemies will remain within the boundaries that delineate the program’s area of implementation. A weed biological control program targeting Melaleuca quinquenervia in Florida, USA has resulted in the release and establishment of Oxyops vitiosa and Boreioglycaspis melaleucae. An international survey of M. quinquenervia populations in 13 other states or countries where the insects have not been intentionally introduced was initiated to monitor the long range dispersal of O. vitiosa and B. melaleucae beyond the herbivores’ intended geographic range (Florida). Surveys in 2006 resulted in the discovery of B. melaleucae within the canopies of several M. quinquenervia trees near San Juan, Puerto Rico. In 2007, O. vitiosa was observed on the island of New Providence in the Bahamas but neither herbivore was detected on nearby Grand Bahama or Andros islands. In 2009, B. melaleucae was observed attacking M. quinquenervia trees in Los Angeles, California (USA). The herbivores have not been detected on other surveyed M. quinquenervia populations in Cuba, Jamaica, Texas (USA), Costa Rica, Brazil, Hawaii (USA) or South Africa. There is no evidence to suggest that herbivore colonization of New Providence, Puerto Rico, or California was influenced by linear distance between Florida and the recipient M. quinquenervia stand. While the dispersal pathway(s) remains unknown, biological control agents were detected from 200 to >3500 km from their original release location (Florida) and at locations that have strong links via tourism and trade as indicated by the number of airline flights connecting south Florida with colonized tree populations. Implications of this unintended spread are discussed in relation to permeability of biogeographical barriers and risk assessment of biological control agents.     

Host range of Boreioglycaspis melaleucae Moore (Hemiptera: Psyllidae), a potential biocontrol agent of Melaleuca quinquenervia (Cav.) S.T. Blake (Myrtaceae), under quarantine

Research on the natural enemies of the Australian tree Melaleuca quinquenervia, a dominant, adventive weed of wetland habitats in south Florida, USA began in the late 1970s. Since then host-range tests have been conducted in Australia and Florida on three insect species: a weevil, a sawfly, and a psyllid. Herein we discuss the host-range studies of the psyllid, Boreioglycaspis melaleucae conducted in quarantine in Florida. Tests showed that the host range is very narrow, limited to one Melaleuca species, M. quinquenervia. One time, a few psyllids developed on a different species, Callistemon (=Melaleuca) citrinus, broad-leaf form, but repeated efforts to rear it again failed. In its Australian homeland, B. melaleucae has been collected on 5 closely related broad-leaved Melaleuca species including M. quinquenervia; it developed on 2 of 4 species tested, M. viridiflora (28%) and M. quinquenervia (37%). There was also 2% development on a 6th narrow-leaved Melaleuca species, M. nodosa. In the New World, there are no native Melaleuca species; in the United States, there is one introduced group, Callistemon (=Melaleuca), which is of commercial value and just one naturalized species, M. quinquenervia, which has no commercial value. Because of the near absence of Melaleuca species and B. melaleucae’s narrow host range and ability to severely damage or kill M. quinquenervia, we concluded that field release of B. melaleucae in south Florida would be safe. The first releases were made in February 2002.     

An evaluation of the impact of Melaleuca quinquenervia invasion and management on plant community structure after fire

Two questions were asked in this study: after a fire, does the choice of invasive plant management strategy, namely herbicidal or biological, alter (1) plant community assemblages and (2) the re-invasion potential of the Australian tree Melaleuca quinquenervia? Plant species richness was highest in the non-invaded and herbicide sites compared to the biological site with 10.5, 10.8, and 8.25 species m⁻² found in each site, respectively. Although the total count of live and dead seedlings was highest in the biologically controlled site at 22.8 and 13.6 plants m⁻², respectively, M. quinquenervia seedlings were recruited in all sites. While the ultimate goal of management programs is to restore ecosystem integrity, this work provides evidence that passive restoration may not be enough to restore plant community structure in this system.     

Trade‐off between fecundity and survival generates stabilizing selection on gall size

Complex interactions within multitrophic communities are fundamental to the evolution of individual species that reside within them. One common outcome of species interactions are fitness trade‐offs, where traits adaptive in some circumstances are maladaptive in others. Here, we identify a fitness trade‐off between fecundity and survival in the cynipid wasp Callirhytis quercusbatatoides that induces multichambered galls on the stem of its host plant Quercus virginiana. We first quantified this trade‐off in natural populations by documenting two relationships: a positive association between the trait gall size and fecundity, as larger galls contain more offspring, and a negative association between gall size and survival, as larger galls are attacked by birds at a higher rate. Next, we performed a field‐based experimental evolution study where birds were excluded from the entire canopy of 11 large host trees for five years. As a result of the five‐year release from avian predators, we observed a significant shift to larger galls per tree. Overall, our study demonstrates how two opposing forces of selection can generate stabilizing selection on a critical phenotypic trait in wild populations, and how traits can evolve rapidly in the predicted direction when conditions change.     

Going undercover: increasing canopy cover around a host tree drives associational resistance to an insect pest

Neighbouring heterospecific plants are often observed to reduce the probability of herbivore attack on a given focal plant. While this pattern of associational resistance is frequently reported, experimental evidence for underlying mechanisms is rare particularly for potential plant species diversity effects on focal host plants and their physical environment. Here, we used an established forest diversity experiment to determine whether tree diversity effects on an important insect pest are driven by concomitant changes in host tree growth or the light environment. We examined the effects of tree species richness, canopy cover and tree growth on the probability of occurrence, the abundance, and volume of galls caused by the pineapple gall adelgid Adelges abietis on Norway spruce. Although tree diversity had no effect on gall abundance, we observed that both the probability of gall presence and gall volume (an indicator of maternal fecundity) decreased with tree species richness and canopy cover around host spruce trees. Structural equation models revealed that effects of tree species richness on gall presence and volume were mediated by concurrent increases in canopy cover rather than changes in tree growth or host tree density. As canopy cover did not influence tree or shoot growth, patterns of associational resistance appear to be driven by improved host tree quality or more favourable microclimatic conditions in monocultures compared to mixed‐stands. Our study therefore demonstrates that changes in forest structure may be critical to understanding the responses of herbivores to plant diversity and may underpin associational effects in forest ecosystems.     

Carbon isotope discrimination in leaves of the broad‐leaved paperbark tree,Melaleuca quinquenervia,as a tool for quantifying past tropical and subtropical rainfall

Quantitative reconstructions of terrestrial climate are highly sought after but rare, particularly in Australia. Carbon isotope discrimination in plant leaves (Δ_leaf) is an established indicator of past hydroclimate because the fractionation of carbon isotopes during photosynthesis is strongly influenced by water stress. Leaves of the evergreen tree Melaleuca quinquenervia have been recovered from the sediments of some perched lakes on North Stradbroke and Fraser Islands, south‐east Queensland, eastern Australia. Here, we examine the potential for using M. quinquenervia ?_leaf as a tracer of past rainfall by analysing carbon isotope ratios (δ¹³C) of modern leaves. We firstly assess Δ_leaf variation at the leaf and stand scale and find no systematic pattern within leaves or between leaves due to their position on the tree. We then examine the relationships between climate and Δ_leaf for a 11‐year time series of leaves collected in a litter tray. M. quinquenervia retains its leaves for 1–4 years; thus, cumulative average climate data are used. There is a significant relationship between annual mean ?_leaf and mean annual rainfall of the hydrological year for 1–4 years (i.e. 365–1460 days) prior to leaf fall (r² = 0.64, P = 0.003, n = 11). This relationship is marginally improved by accounting for the effect of pCO₂ on discrimination (r² = 0.67, P = 0.002, n = 11). The correlation between rainfall and Δ_leaf, and the natural distribution of Melaleuca quinquenervia around wetlands of eastern Australia, Papua New Guinea and New Caledonia offers significant potential to infer past rainfall on a wide range of spatial and temporal scales.     

Gall-inducing Pachypsylla celtidis (Psyllidae) infiltrate hackberry trees with high concentrations of phytohormones

Abstract

In order to identify phytohormones involved in the initiation and maintenance of galls on the hackberry tree, Celtis occidentalis (Ulmaceae), in the presence of the insect Pachypsylla celtidis (Psyllidae); endogenous levels of cytokinins (CKs) and abscisic acid (ABA) were measured in the tissues of leaves, galls, and larval insects using liquid-chromatography-tandem-mass-spectrometry. The CKs isopentenyl adenine, isopentenyl adenosine, trans-zeatin and cis-zeatin, were extremely concentrated in insect larvae compared to surrounding tissue of leaves and galls. ABA concentrations in the insects were also relatively high at about 3268 pmol?g-1 fresh mass – approximately 25 times higher than in leaves, and 17 times higher than in galls. This represents a novel case of high concentrations of ABA being found in a larval insect. These findings indicate that manipulation of CK and ABA are involved in the initiation and maintenance of hackberry galls in the presence of larval P. celtidis.     

Biological control increases the susceptibility of melaleuca quinquenervia to fire

A field experiment evaluating herbivory from biological control agents on Melaleuca quinquenervia saplings experienced a wildfire, which resulted in post-fire tree mortality of 64.6% and 28.1% in the unrestricted and restricted herbivory treatments, respectively. The fire did not negatively impact populations of the biological control agent Oxyops vitiosa.     

Consequences of Melaleuca quinquenervia Invasion on Soil Nematodes in the Florida Everglades

The tree Melaleuca quinquenervia invades all types of habitats of South Florida leading to up to 80% loss of aboveground diversity. To examine impacts on the belowground ecosystem, we investigated the composition and diversity of nematodes from soils dominated by the invasive tree and compared them with soils supporting native plant communities at six locations across the Florida Everglades over three years. Despite the significant differences in soil type, hydrology, and native plant composition of the sites, there were consistent differences in nematode communities between soil environments under the native and invaded plant communities. The total abundance and diversity of nematodes in soils dominated by M. quinquenervia was 60% and 80% of adjacent soils under native plants. Fungal-feeding and plant-parasitic nematodes were twice as abundant under native plants as under M. quinquenervia. Nematode communities under M. quinquenervia were bacterivore-dominated, while under native vegetation plant-parasite dominated. The overall diversity of nematodes was 20% lower under the exotic than under native plants, with plant parasites being 36% and fungivores being 30% less diverse. Soil moisture, % of Ca, Mg, and clay particles and total soil C and N were greater in M. quinquenervia soils, but plant-available concentrations of P, K, Ca, and Mg as well as CEC were reduced. Overall, data suggests that the invasion process may modify soil biotic and abiotic conditions that in turn promote the advancement of the exotic M. quinquenervia and displacement of the native plants.     

基于ISSR的豚草和三裂叶豚草遗传多样性研究

[目的]研究不同地理种群的豚草和三裂叶豚草的遗传多样性水平和遗传结构。[方法]应用筛选的13条ISSR引物对8个豚草居群和7个三裂叶豚草居群共240个样品进行分子标记。[结果]8个豚草居群128个样品,共扩增出304条带,多态性位点比率为98.68%;Shannon''s信息指数为0.6716,Nei''s基因多样性指数为0.4788。7个三裂叶豚草居群112个样品,共扩增出266条带,多态性位点比率为95.86%;Shannon''s信息指数为0.6593,Nei''s基因多样性指数为0.4670。豚草和三裂叶豚草各居群遗传距离较近。[结论]豚草和三裂叶豚草在居群间具有一定的遗传稳定性;居群内具有丰富的遗传多样性。豚草和三裂叶豚草遗传变异主要来源于居群内部。豚草各居群遗传距离和地理距离有显著相关性,三裂叶豚草各居群遗传距离和地理距离无显著相关性。