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.     

Post-biological control invasion trajectory for Melaleuca quinquenervia in a seasonally inundated wetland

The recruitment and mortality of Melaleuca quinquenervia seedlings were evaluated over a 3-year period in a seasonally inundated wetland in the western Everglades region. The mean (±SE) density of seedlings/saplings m^?1 declined from 64.8 (±4.5) to 0.5 (±0.2) over the 3 years, a population reduction of 99.2%. Four distinct water regimes characterized this site: dry, dry to wet transition, flooded, and wet to dry transition. Seedling recruitment was highest in the dry to wet transition and lowest in the flooded water regime, while mortality was highest under flooded and dry water regimes. The mean estimate of population growth (λ) across water regimes was 0.64 ± 0.05 indicating negative population growth. Elimination of introduced insect herbivores using insecticides did not reduce mortality of recruited M. quinquenervia seedlings/saplings indicating that direct herbivory was not responsible for the decline in seedling density. On the other hand, a mean of only 0.2 (±0.03) viable seeds m^?2 d^?1 fell into the plots, an amount considerably lower than in previous studies. We submit that change in the invasion trajectory M. quinquenervia was most likely caused by reduced seed inputs from aerial seed banks depleted by insect herbivory rather than direct herbivory on seedlings. This may indicate a fundamental alteration of M. quinquenervia population dynamics ultimately resulting in a less invasive and, therefore, less ecologically damaging species.     

Within-plant distribution of the Melaleuca quinquenervia biological control agent Lophodiplosis trifida

The gall-producing midge Lophodiplosis trifida Gagné (Diptera: Cecidomyiidae) is an established biological control agent of the exotic tree Melaleuca quinquenervia (Cav.) Blake, which invades wetland systems of Florida (USA). Host use patterns within the tree canopy were investigated. Plant height affected within-plant distribution of galls as L. trifida attack rates were greater in lower versus higher portions of the M. quinquenervia canopy. Nonetheless, galls occurred even at tree-top levels of 13 m.     

The molecular basis of host plant selection in Melaleuca quinquenervia by a successful biological control agent

Melaleuca quinquenervia (Cav) S.T. Blake (broadleaf paperbark) is an Australian tree that has become a serious weed in many places around the world. Two insects Oxyops vitiosa (the melaleuca weevil), and Boreioglycaspis melaleucae (the melaleuca psyllid), which were introduced to Florida as part of a biological control programme, have been very effective in reducing survival and reproduction of this weed. There are two terpene chemotypes of M. quinquenervia; one rich in the sesquiterpene E-nerolidol whereas the other is rich in viridiflorol. Viridiflorol is a strong feeding deterrent for the melaleuca weevil and retards larval development. The larvae therefore avoid the viridiflorol-rich chemotype, in contrast, female melaleuca psyllids prefer to oviposit on these leaves. To identify the molecular basis of these preferences, we isolated and characterised two terpene synthases from the viridiflorol-rich chemotype, both of which utilise farnesyl pyrophosphate and have the same product profile. Chemotypic variation in terpenes in M. quinquenervia is under strong genetic control and the reproductive potential of each chemotype is limited by a different insect. These insects could, therefore, be selective agents for the maintenance of chemotypic variation in M. quinquenervia.     

Maintenance of a narrow host range by Oxyops vitiosa; a biological control agent of Melaleuca quinquenervia

Host range expansion in insect herbivores is often thought to be mediated by several factors, principal among them are secondary plant metabolites. In weed biological control, the host range of a prospective agent is one of the most important considerations in its implementation. Extensive host testing tests seek to determine the behavioral acceptance and nutritional value of different test plant species to the potential agent. A list of test plants is compiled that comprises species that are close taxonomic relatives of the target weed plus other species of economic or ecologic importance. The host testing of the Melaleuca quinquenervia biological control agent Oxyops vitiosa indicated that larvae would accept and complete development on the Australian target weed M. quinquenervia, two Australian ornamental species, Callistemon citrina, Callistemon viminalis (all Myrtaceae). However, the larvae did not complete development when fed a North American species Myrica cerifera (Myricaceae). The study reported here confirms these results and examines the nutritional and performance differences in O. vitiosa larvae fed leaves of these species. The leaf quality factors, percent moisture, percent nitrogen, toughness, and terpenoid content were related to larval survival, performance and digestive indices. The results indicate that plant quality among the Myrtaceae species was generally similar and correspondingly larval survival, performance and digestive indices differed little when larvae were fed leaves of these species. However, significant differences occurred in the plant quality of the North American M. cerifera compared with the Australian species which had leaves with the lowest percent moisture, lowest leaf toughness, highest percent nitrogen. This species, however, is not a physiological host as none of the neonates survived to pupate. When third instars were switched to M. cerifera from their normal host M. quinquenervia reductions were found in survival, biomass gain, digestive efficiency, and conversion of digested food to insect biomass. The marginal acceptance of this North American native plant in laboratory bioassays appears related to the terpenoid chemistry that has similarities to the taxonomically unrelated host M. quinquenervia. However, the high larval mortality corresponds to several novel terpenoids that are not present in the host. For weed biological control host testing these results indicate that M. cerifera is a poor host for O. vitiosa. Additionally, future test plant lists should include plants with secondary metabolites similar to the target weed as these compounds may constitute behavioral cues that are relevant to these specialized herbivores.     

Reticulate evolution in the natural range of the invasive wetland tree species Melaleuca quinquenervia

The Melaleuca leucadendra complex (broad-leaf paperbarks; Myrtaceae) is a dominant component of the tropical and sub-tropical biota of Australia, particularly in wetlands of high conservation significance. In Florida and other parts of the Americas, however, one member of the group (Melaleuca quinquenervia) is a serious ecological and economic weed. Understanding the relationships and evolution of the group is integral to both conservation and biocontrol efforts. Although the complex is currently considered to include up to 14 species, there has been some concern over taxonomic boundaries within the complex because most species are circumscribed only by combinations of characters, each of which also occurs in other species. Here, DNA sequence data derived from the chloroplast and two nuclear regions are used to explore the relationships of M. quinquenervia. We find little evidence for clear species boundaries within the M. leucadendra complex in general, with regional sharing of chloroplast haplotypes across morphologically defined taxa, indicating asymmetrical introgression or retention of ancestral haplotypes (lineage sorting). Phylogenies were further confounded by the recovery of multiple copies of both nuclear regions sequenced (ITS and rpb2) from many individuals. There was no clear evidence of polyploidy or pseudogenes, but multiple duplications of rpb2 could not be ruled out. Parsimony networks of the nuclear ITS region show some clustering of haplotypes by morphospecies but there is also evidence of both hybridisation and recombination. Signals of introgression were also evident in rpb2, supporting an hypothesis of recent or ongoing gene flow between M. quinquenervia and other members of the M. leucadendra complex. Both relaxed and fixed molecular-clock dating estimate the introgression to have occurred sometime within the past seven million years (95% CI: 0.7-18). The New Caledonian population of M. quinquenervia appears to have been established by dispersal from Australia during this period. M. quinquenervia is found to have alleles closely related to multiple different morphotaxa within the M. leucadendra complex, suggesting considerable past introgression into this taxon from some other members of the M. leucadendra complex, and this has implications for biocontrol efforts. The M. leucadendra complex appears to reflect early to intermediate stages of speciation, possibly driven by different ecologies.     

Responses of Melaleuca quinquenervia seedlings to flooding

Abstract Studies were conducted on effects of flooding for 15, 30, 60, and 90 days on morphological changes, stomatal aperture, water potential, and growth of seedlings of Melaleuca quinquenervia, a species often planted for reclamation of swamps. Flooding rapidly induced formation of many hair-like adventitious roots as well as a few thick adventitious roots that originated on the original root system. Some adventitious roots also formed on submerged portions of the stem. Melaleuca seedlings were very tolerant of flooding as shown by only slight reduction in dry weight increment of shoots after 30 days of flooding in stagnant water. Although flooding for 60 or 90 days significantly reduced dry weight increment of leaves, dry weight increment of roots was not inhibited by any flooding treatment, reflecting both degeneration of some of the original roots and compensatory growth of adventitious roots. On certain days flooding induced stomatal closure on both adaxial and abaxial leaf surfaces. Extensive production of adventitious roots and some stomatal reopening after a critical period of flooding appeared to be important factors in the flooding tolerance of Melaleuca and are consistent with its aggressiveness and vigorous growth on wet sites.     

Chemotype variation of the weed Melaleuca quinquenervia influences the biomass and fecundity of the biological control agent Oxyops vitiosa

Host plant nutritional and non-nutritional variability can have a significant effect on herbivore populations by influencing survival, larval performance, and fecundity. The effect of chemical and physical variation of the leaves of two chemotypes of the weed Melaleuca quinquenervia was determined on the biomass and fecundity of the biological control agent Oxyops vitiosa (Coleoptera: Curculionidae). M. quinquenervia chemotypes were distinguished by the principal terpenoids E-nerolidol and viridiflorol using gas chromatography and mass spectroscopy. Not only were the terpenoid profiles of the two chemotypes different but the viridiflorol leaves had greater toughness (1.2-fold) and reduced nitrogen (0.7-fold). When the larvae and adults were fed leaves of the E-nerolidol chemotype increased adult biomass (1.1-fold) and fecundity were found (2.6- to 4.5-fold) compared with those fed leaves of the viridiflorol chemotype. Regardless of the larval diet, when adults were fed the E-nerolidol chemotype leaves they had greater egg production compared with those adults fed the viridiflorol leaves. Moreover, adult pre-oviposition period was extended (1.5-fold) when individuals were fed the viridiflorol leaves compared with those fed the E-nerolidol leaves. By rearing the O. vitiosa weevil on the more nutritious chemotype plants these results assisted in the mass production and establishment of the M. quinquenervia biological control agent.     

Field colonization,population growth,and dispersal of Boreioglycaspis melaleucae Moore,a biological control agent of the invasive tree Melaleuca quinquenervia (Cav.) Blake

Invasion of native plant communities by the Australian paperbark tree (“melaleuca”), Melaleuca quinquenervia, complicates restoration of the Florida Everglades. Biological control, within the context of a comprehensive management program, offers a means to suppress regeneration of melaleuca after removal of existing trees and a mechanism to forestall reinvasion. To meet this need, a biological control program commenced in 1997 upon the release of an Australian weevil (Oxyops vitiosa [Pascoe] [Coleoptera: Curculionidae]). Release of a second biological control agent, the melaleuca psyllid (Boreioglycaspis melaleucae Moore), followed in February 2002 at field sites containing mixed age-class melaleuca stands or coppicing stumps. Each site was inoculated with 7000–10,000 adult psyllids, with one exception where 2000 nymphs were released on seedlings the following December. Psyllid populations established everywhere irrespective of colony source, site conditions, or the quantity released, although numbers released and, to a lesser degree, colony age influenced the numbers of colonies produced. Quantity included in the release was the major determinant of the resultant number of colonies, although the duration of their tenure in quarantine culture may have also influenced this. One site, comprised mainly of coppicing stumps, contained 3.3 million psyllids per ha within 3 months after release. Less than 1% of the coppices at a similar site harbored psyllid colonies 2 months after release (May 2002), but this rose to 75% in October then to 100% by December. The census population exceeded 715,000 adults and nearly 11 million nymphs by late January 2003. Psyllid populations dispersed 2.2–10.0 km/year, with the slower rates in dense, continuous melaleuca stands and faster rates in fragmented stands. Over 1 million psyllids had been redistributed to 100 locations as of December 2005. This species now occurs throughout much of the range of melaleuca in south Florida due to natural range expansion as well as anthropogenic dissemination.     

Invasion theory and biological control

Recent advances in the mathematical theory of invasion dynamics have much to offer to biological control. Here we synthesize several results concerning the spatiotemporal dynamics that occur when a biocontrol agent spreads into a population of an invading pest species. We outline conditions under which specialist and generalist predators can influence the density and rate of spatial spread of the pest, including the rather stringent conditions under which a specialist predator can successfully reverse a pest invasion. We next discuss the connections between long distance dispersal and invasive spread, emphasizing the different consequences of fast spreading pests and predators. Recent theory has considered the effects of population stage-structure on invasion dynamics, and we discuss how population demography affects the biological control of invading pests. Because low population densities generally characterize early stages of an invasion, we discuss the lessons invasion theory teaches concerning the detectability of invasions. Stochasticity and density-dependent dynamics are common features of many real invasions, influencing both the spatial character (e.g. patchiness) of pest invasions and the success of biocontrol agents. We conclude by outlining theoretical results delineating how stochastic effects and complex dynamics generated by density dependence can facilitate or impede biological pest control.     

Laboratory life history and field observations of Poliopaschia lithochlora (Lower) (Lepidoptera: Pyralidae), a potential biological control agent for Melaleuca quinquenervia (Myrtaceae)

Abstract  Melaleuca quinquenervia (Cav.) S.T. Blake, Australian broad-leaved paperbark, has become a serious weed in southern Florida. Poliopaschia lithochlora (Lower) is a promising candidate as a potential biological control agent, and this study describes laboratory and field observations of the life history of this moth. Eggs are laid in small batches, mainly on the surface of leaves, and larvae are voracious leaf feeders, concealed in tubes that are usually found in small colonies attached to leaves and stems. Larvae move from these tubes to feed on surrounding leaves, and saplings and suckers are frequently defoliated. Prepupae form sealed bulbs in the larval tubes in which they pupate. Adult females are mainly active and oviposit at night. Development from egg to adult occurs in approximately 80 d. Field populations appear to be regulated by several egg and larval parasites. Because this moth severely damages saplings and suckers of M .  quinquenervia , prefers low-lying humid sites, and can be successfully mass reared, it is rated highly for its potential as a biological control agent.     

Biology, distribution and host-range of the sawfly,Lophyrotoma zonalis (Hym. pergidae), a potential biological control agent for the paperbark tree,Melaleuca quinquenervia

Since its introduction into southern Florida at the beginning of this century, the Australian paperbark tree,Melaleuca quinquenervia (Cav.) S. T. Blake, has become a major economic and environmental pest. A project to develop biological control agents for this tree in Australia began in 1986. Among a number of potential agents, a defoliating sawfly,Lophyrotoma zonalis (Rohwer) (Hymenoptera: Pergidae), was selected for further study. The larvae of this sawfly are conspicuous defoliators ofMelaleuca trees in northern Queensland. We collected these sawflies from Cairns to Mackay in northern Queensland, and they are also known from the Northern Territory and New Guinea. The life-cycle from egg to adult takes about 12 weeks. The egg, larval and pupal stages are parasitized by dipteran and hymenopteran parasites. We conducted 2234 larval no-choice feeding tests on 46 plant species from 20 families. Although feeding occurred on 35 of these plant species,M. quinquenervia and its close relative,M. leucadendra (L.) L., were preferred. In oviposition tests, larvae only emerged from egg cases laid onM. quinquenervia andM. leucadendra. Our extensive field surveys of nearly 70 tree species foundL. zonalis eggs and larvae only on several closely relatedMelaleuca species. The potential effectiveness of this sawfly as a biocontrol agent is discussed and estimated using the Goeden-Harris scoring system. Quarantine studies of this insect began in Florida in early 1994.     

Resource regulation of an invasive tree by a classical biological control agent

The invasive tree Melaleuca quinquenervia experienced substantial declines in growth and reproduction in response to chronic herbivory by the defoliating weevil Oxyops vitiosa. Plants subjected to unrestricted defoliation replaced leaves that were more suitable for feeding by the next generation, a process envisioned by the Resource Regulation Hypothesis which posits that attack by one generation increases the amount of the preferred host resources for the next, resulting in a positive feedback loop for the herbivore. The production of juvenile replacement leaves stimulated additional bouts of oviposition and feeding by O. vitiosa, which ultimately produced positive effects for the herbivore with negative consequences for the plant. The addition of water resources to the plant prolonged the positive feedback loop such that more than twice as many insects were produced on irrigated versus non-irrigated trees. In a more simple, reassembled food web on M. quinquenervia, the lack of biotic constraints like parasitoids may have prevented the earlier termination of the feedback loop and thus increased the impact of the biological control agent on the target. The overall effectiveness of this classical biological control program can be attributed, in part, to the phenomenon of the target plant’s induced susceptible response to a herbivore.     

Antipredatory Activity of the Weevil Oxyops vitiosa: A Biological Control Agent of Melaleuca quinquenervia

The larvae of the leaf-feeding weevil Oxyops vitiosa, a biological control agent of Melaleuca quinquenervia, are covered with a viscous orange coating that is thought to protect against generalist predators. This coating is gradually lost as the larvae drop to the ground and pupate in subterranean pupal cells. To test the antipredator activity of this species, four immature life stages (early instars, late instars, prepupae, pupae) were exposed to a common generalist predator, the red imported fire ant Solenopsis invicta. Choice tests were conducted by placing an O. vitiosa individual and a control larva of the weevil Neochetina eichhorniae into an arena containing a S. invicta colony and observing subsequent ant behaviors. S. invicta workers contacted O. vitiosa early instars, late instars, and prepupae less frequently than control N. eichhorniae larvae, and upon contact S. invicta was less likely to behave aggressively toward these O. vitiosa life stages than toward N. eichhorniae larvae. However, S. invicta contacted, attacked, and consumed naked (nonencased) O. vitiosa pupae and N. eichhorniae larvae with equal frequency. Encased O. vitiosa pupae buried in sand were not attacked compared to susceptible encased pupae on the sand surface. By shifting from a chemical defense during the larval stages to a physical defense during the pupal stage, O. vitiosa reduces the risk of attack by this generalist predator.     

Quarantine host range studies with Lophyrotoma zonalis, an Australian sawfly of interest for biological control of melaleuca, Melaleuca quinquenervia, in Florida, U.S.A.

The Australian melaleuca tree, Melaleuca quinquenervia (Cav.) S. T. Blake (Myrtaceae), has naturalized in southern Florida,U.S.A., and is now one of that regions most important weeds.Primarily a weed of wetlands, it also infests neighboring drierareas. Current efforts to restore the South Florida ecosystem arethreatened by the continuing range expansion of melaleuca andother weeds. In an effort to supplement the current chemical andcultural control methods for melaleuca, a search for potentialbiological control agents was begun in Australia in 1986. Thesawfly, Lophyrotoma zonalis, was determined after extensive fieldand laboratory studies to have potential as a biological controlagent. Larvae of L. zonalis eat leaves and occasionally defoliatelarge trees in Australia. Host range studies were conducted in aFlorida quarantine facility with native and cultivated plantspecies. Multi-choice and no-choice oviposition tests wereconducted with 36 species in the Myrtaceae and with 18 species inother families. Larvae developed to prepupae and adults from theeggs oviposited on 23 species of Myrtaceae only on 3 species ofbottlebrushes, Callistemon. Medium-sized larvae were tested forfeeding on bouquets of plant cuttings and on potted plants. Theyare the stage that might wander from defoliated trees. Noticeablefeeding, but much less than on melaleuca, was restricted to theMyrtaceae, except for a few individual larvae that fed on waxmyrtle, Myrica cerifera. Medium-sized larvae became prepupae onlyon Melaleuca decora (73%) and on wax myrtle (10%). However,neither species received eggs in the oviposition tests. Thesestudies confirmed the narrow host range of L. zonalis aspreviously reported from field and laboratory studies inAustralia.     

Temporal and structural effects of stands on litter production in Melaleuca quinquenervia dominated wetlands of south Florida

Melaleuca quinquenervia dominates large areas of the Florida Everglades in the southeastern USA where it has transformed sedge-dominated marshes into melaleuca forests. Despite its prevalence, very little is known about the ecology and stand dynamics of this invasive tree. We delineated large-, intermediate-, and small-tree stands in non-flooded, seasonally flooded and permanently flooded areas of Florida in 1997, measured their biological attributes, and then quantified litterfall components for 3–4 year periods. Melaleuca wood components and mature seed-capsules comprised the largest and the smallest portions of aboveground biomass, respectively, while leaves, fine stems, mature fruits, bud scales, floral structures, and residues represented decreasingly smaller fractions of the litter during the succeeding year. Dry weight proportion of leaves in litter was greatest (80.9%) in non-flooded and least (69.1%) in permanently flooded habitats. It was also greatest in small (85.6%) and least in large (64.7%) tree stands. Reproductive structures and mature-fruit fractions in litter were highest in large-tree stands whereas the bud-scale fraction showed no relationship to tree size. Seasonally flooded habitats had the most litterfall, wherein small-, intermediate-, and large-tree stands generated 0.662, 0.882, and 1.128 kg m⁻² yr⁻¹, respectively. Dry weight of stems, leaves, bud–scales, floral structures, and mature fruit fractions in litter increased as the predominant size of the trees in the stand increased. Total annual litter production was highest during 1999–2000. Leaf fall occurred year-round with maximal amount during April, July, and October. Highest amounts of bud scales and floral structures fell during October–January, which corresponded with flushes of vegetative growth and major flowering events. Overall, melaleuca alone accounted for nearly 99% of the total litterfall dry weight in all habitats and months sampled. The amount of non-melaleuca litter was greater in small-tree stands than in intermediate- or large-tree stands. Litterfall data of this nature will be helpful in detecting changes occurring in melaleuca canopies in response to biological control impact and in prescribing site-specific management strategies.     

If and when successful classical biological control fails

Classical biological control of insects has a long history of success, with high benefit–cost ratios. However, most attempts to introduce a biological control agent have been unsuccessful, largely because the agent does not establish in the new environment. This perspectives paper discusses the possibility that even successful biological control may eventually fail, although records show that this is far from a common event. A documented example of eventual biological control failure is discussed and the prospect for future failures analyzed. Part of this analysis is based on an introduced weevil pest in New Zealand and its successful parasitoid biological control agent. The potential fragility of this host–parasitoid relationship is considered, as well as why it may indeed be starting to show signs of instability; this is particularly from the point of view of New Zealand’s often species-poor agricultural ecosystems.     

Biological control of <Emphasis Type="Italic">Melaleuca quinquenervia</Emphasis>: an Everglades invader

A massive effort is underway to restore the Florida Everglades, mainly by re-engineering hydrology to supply more water to the system at appropriate times of the year. However, correcting water flow patterns alone will not restore the associated plant communities due to habitat-transforming effects of invasive species, in particular the Australian wetland tree Melaleuca quinquenervia (Cav.) S. T. Blake (Myrtales, Myrtaceae), which has invaded vast areas and transformed sawgrass marshes into dense, biologically impoverished, structurally altered forest habitats. To address this threat, an invasive species reduction program was launched that combined mechanical removal and herbicidal control to remove mature trees with the release of specialized insects to suppress seed production and lower seedling survival. Melaleuca has now been removed from most public lands while biological control has limited its ability to regenerate and reinvade from nearby infestations often located on unmanaged privately held lands. This case illustrates how restoration of highly modified ecosystems may require both restoration of physical conditions (water flow), and suppression of high impact or transformative invaders, showing well the need to integrate biological control into conservation biology.