F. Allen Dray

Invasion History of Melaleuca quinquenervia (Cav.) S.T. Blake in Florida

Abstract The Australian punk tree Melaleuca quinquenervia is a notorious invasive weed that threatens the biological integrity of Floridas Everglades ecosystems. A comprehensive plan initiated to manage M. quinquenervia includes an ambitious biological control program, and as part of this program we investigated the origins and invasion history of M. quinquenervia in Florida. Scrutiny of public and private records showed that extant populations derive from more than a dozen introductions, with the earliest occurring during 1886 in Sarasota County. Six sources, some Australian and some extra-Australian, have contributed to Floridas populations. The tree became naturalized in southern Florida during the 1920s, but a paucity of records makes it difficult to determine when naturalized populations began to proliferate via an exponential growth phase. Human distribution of seeds and seedlings is a confounding factor in attempting to decipher rates of M. quinquenervia invasion.

No evolution of increased competitive ability or decreased allocation to defense in Melaleuca quinquenervia since release from natural enemies

If invasive plants are released from natural enemies in their introduced range, they may evolve decreased allocation to defense and increased growth, as predicted by the evolution of increased competitive ability (EICA) hypothesis. A field experiment using the invasive tree Melaleuca quinquenervia was conducted to test this hypothesis. Seeds were collected from 120 maternal trees: 60 in Florida (introduced range) and 60 in Australia (home range). Plants grown from these seeds were either subjected to herbivory by two insects from Australia that have recently been released as biological control agents or protected from herbivores using insecticides. Genotypes from the introduced range were initially more attractive to herbivores than genotypes from the home range, supporting EICA. However, genotypes from the introduced and home range did not differ in resistance to insects or in competitive ability, which does not support EICA. Plants from the introduced range had a lower leaf hair density, lower leaf: stem mass ratio, and a higher ratio of nerolidol: viridifloral chemotypes compared to plants from the native range. Plants with an intermediate density of leaf hairs and with high specific leaf area were more susceptible to herbivory damage, but there were no effects of leaf toughness or chemotype on presence of and damage by insects. Herbivory had a negative impact on performance of Melaleuca. Other than an initial preference by insects for introduced genotypes, there was no evidence for the evolution of decreased defense or increased competitive ability, as predicted by the EICA hypothesis. It does not appear from this study that the EICA hypothesis explains patterns of recent trait evolution in Melaleuca.

Selection on herbivory resistance and growth rate in an invasive plant.

The evolution of increased competitive ability (EICA) hypothesis proposes that invasive species evolve decreased defense and increased competitive ability following natural enemy release. Previous tests of EICA examined the result of evolution by comparing individuals from home and introduced ranges, but no previous study of this hypothesis has examined the process of evolution by analyzing patterns of selection. On the basis of EICA, there should be selection for competitive ability without herbivores and selection for defense with herbivores. Selection on competitive ability should be stronger for genotypes accustomed to herbivores (home range genotypes), and selection on defense should be stronger for genotypes unaccustomed to herbivores (introduced range genotypes). Using a field experiment, we tested these hypotheses for the invasive plant Melaleuca quinquenervia. There was a negative genetic correlation between resistance and growth, indicating a trade‐off. However, selection for stem elongation (an indicator of competitive ability) was always positive, and selection on resistance was always negative and did not depend on genotype source or the presence of herbivores. The patterns of selection found in this study contrast with predictions from EICA and accurately predict the lack of evolutionary change in growth and resistance following the introduction of this species from Australia to Florida.

Biological control of Melaleuca quinquenervia: 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.

Lessons from Unsuccessful Attempts to Establish Spodoptera pectinicornis (Lepidoptera: Noctuidae), a Biological Control Agent of Waterlettuce

We released nearly 332 000 Spodoptera pectinicornis individuals for biological control of the floating aquatic weed Pistia stratiotes (waterlettuce) at 22 sites in Florida during December 1990-December 1997. Predation (by boat-tailed grackles, fire ants, and spiders) and Allee effects (resulting from rapid dispersal of adults) prevented populations from persisting during early attempts. These efforts consisted of small releases at multiple sites, with no nurturing of the introduced populations. Modification of our initial approach resulted in a series of release strategies that consisted of multiple releases at fewer sites and employed progressively more intensive nurturing of the introduced populations. The most successful strategy incorporated: (i) cages to restrict adult dispersal and exclude flying predators; (ii) plant-free zones around the cages to exclude crawling predators; (iii) enhancement of the nutritional quality of waterlettuce in the cages; and (iv) frequent inoculation of the cages with laboratory-reared insects. Use of this strategy resulted in several provisionally-established S. pectinicornis populations, numbering as much as 23.5 S. pectinicornis individuals m -2 , and produced up to seven post-release generations. Unfortunately, all of these incipient populations declined until S. pectinicornis was undetectable. We conclude that field populations of this moth no longer persist in Florida, and offer an introspective assessment of how this project might have been improved.

Initial Impacts and Field Validation of Host Range for Boreioglycaspis melaleucae Moore (Hemiptera: Psyllidae), a Biological Control Agent of the Invasive Tree Melaleuca quinquenervia (Cav.) Blake (Myrtales: Myrtaceae: Leptospermoideae)

Abstract Invasion of south Florida wetlands by the Australian paperbark tree, Melaleuca quinquenervia (Cav.) S.T. Blake (melaleuca), has caused adverse economic and environmental impacts. The tree’s biological attributes and favorable ambient biophysical conditions combine to complicate efforts to restore and maintain south Florida ecosystems. Management requires an integrated strategy that deploys multiple biological control agents to forestall reinvasion and to supplement other control methods, thereby lessening recruitment and regeneration after removal of existing trees. This biological control program began during 1997 when an Australian weevil, Oxyops vitiosa (Pascoe), was released. A second Australian insect, the melaleuca psyllid (Boreioglycaspis melaleucae Moore), first introduced during 2002, has also widely established. After inoculation of the psyllid in a field study, only 40% of seedlings survived herbivory treatments compared with 95% survival in controls. The resultant defoliation also reduced growth of the surviving seedlings. A weevil-induced decline at a site comprised mainly of coppicing stumps had slowed after a 70% reduction. Psyllids colonized the site, and 37% of the remaining coppices succumbed within 10 mo. The realized ecological host range of B. melaleucae was restricted to M. quinquenervia; 18 other nontarget plant species predicted to be suboptimal or nonhosts during laboratory host range testing were unaffected when interspersed with psyllid-infested melaleuca trees in a common garden study. Evaluations are ongoing, but B. melaleucae is clearly reducing seedling recruitment and stump regrowth without adversely impacting other plant species. Manifestation of impacts on mature trees will require more time, but initial indications suggest that the psyllid will be an effective supplement to the weevil.

Genetic Variation in Melaleuca quinquenervia Affects the Biocontrol Agent Oxyops vitiosa1

Abstract Melaleuca was first imported into the United States during 1886, and introduction records suggest that at least six sources have contributed to extant populations in Florida. Allozyme analyses found substantial genetic variation within and among populations, contributing to geographic structuring of melaleuca in southern Florida. The presence and distribution of two chemical phenotypes (chemotypes) contributed to this variation. Performance of the melaleuca snout beetle imported as a biological control agent differed dramatically in laboratory studies depending on which chemotype it was fed, with larval survivorship and growth substantially greater on an (E)-nerolidol chemotype. We are currently investigating whether these differences can be detected in the field. Nomenclature: Melaleuca, Melaleuca quinquenervia (Cav.) Blake; melaleuca snout beetle, Oxyops vitiosa Pascoe. Additional index words: Allozyme analysis, biological control, chemotype, herbivory, invasion history, insect–plant interactions.

Host range validation, molecular identification and release and establishment of a Chinese biotype of the Asian leaf beetle Lilioceris cheni (Coleoptera: Chrysomelidae: Criocerinae) for control of Dioscorea bulbifera L. in the southern United States

Abstract Dioscorea bulbifera, an Asian vine, is invasive in the southeastern USA. It rarely flowers but propagates from potato-like bulbils formed in leaf axils, which persist into the subsequent growing season. Lilioceris cheni Gressitt and Kimoto, a foliage-feeding beetle (Coleoptera: Chrysomelidae: Criocerinae) from Nepal, had been tested, proven to be a specialist and approved for release as a biological control agent. Regulatory delays, however, resulted in the demise of quarantine-held colonies, and acquisition of new Nepalese stock proved untenable. Searches then undertaken in southern China resulted in the collection of over 300 similar beetles. Two Chinese Lilioceris species were identified: one confirmed to be L. cheni and the other identified as Lilioceris egena (Weise). Mitochondrial analysis revealed an exact DNA match between some Chinese and one of the two Nepalese c oxidase subunit I haplotypes and all Chinese L. cheni haplotypes clustered as a single species but the comingling of the two species aroused concerns over possible hybridisation. These concerns were allayed by nuclear D2 analysis showing the absence of dual parental sequences. Nonetheless, diligence was exercised to ensure that the Chinese strains were safe to release. Abridged host testing using critical test species verified specificity. Caged releases during autumn 2011 documented the ability of adult beetles to overwinter in south Florida despite a prolonged lack of foliage. Open releases the following year produced vigorous populations that caused extensive defoliation. Preliminary observations indicate that L. cheni now contributes to the control of D. bulbifera and the bulbil-feeding L. egena should complement these effects if its host range proves appropriate.

Selection for Resistance in Invasive Plants

Abstract Although evolution has been neglected in invasive species work, evolutionary theory can be used to guide invasive species management, and research on exotic species can be used to test evolutionary theory. One substantial challenge in invasive plant management is the evolution of resistance to herbicides, biological control, and other treatments. We show how the tools of quantitative genetics and selection analysis can be used to investigate the potential for evolution of resistance, which can aid in the management of invasive plant populations. We also illustrate how invasive species research can be used to test theory, such as the evolution of increased competitive ability hypothesis. We outline the methods to investigate this theory and recommend including evolutionary considerations in invasive species management. Additional index words: Biological control, genetics, herbivory, natural enemies, Melaleuca quinquenervia MLAQU. Abbreviation: EICA, evolution of increased competitive ability.

Release and distribution of Lilioceris cheni (Coleoptera: Chrysomelidae), a biological control agent of air potato (Dioscorea bulbifera: Dioscoreaceae), in Florida

ABSTRACT From 2012 to 2015, 429,668 Lilioceris cheni Gressit and Kimoto (Coleoptera: Chrysomelidae) were released in Florida for biological control of air potato Dioscorea bulbifera L. (Dioscoreaceae). In the fall of 2015, a state-wide survey was conducted at 113 randomly selected air potato infestations in order to determine the spatial distribution of L. cheni. Damage due to L. cheni was found at 86% of locations and was low in the Florida panhandle where air potato was relatively uncommon and fewer beetles had been released, and in far south Florida, despite high numbers of beetle releases. On average, beetles travelled 9.5 km from the nearest release site to survey sites from the date of release to the time of the survey, with a maximum distance of nearly 67 km. The rate of spread was estimated at 8.2 km/year under the assumption that beetles present at survey sites migrated or were moved from the nearest release site. Air potato vines produced fewer aerial tubers, the vegetative propagule of air potato, as foliar damage due to L. cheni increased. The results suggest that future research efforts should focus on determining the biotic and abiotic factors that may be limiting establishment in some areas of Florida.