Gary S. Taylor

Psyllid communication: acoustic diversity, mate recognition and phylogenetic signal

Acoustic signals play an important role in mate selection and speciation in diverse groups of insects. We report reciprocal acoustic mate signalling, often as highly synchronised duetting, for several species of psyllid (Hemiptera:Psylloidea). We reveal that considerable acoustic diversity is present in Australian psyllids belonging to the family Triozidae. The acoustic signals are species and gender specific. Our acoustic analysis and observations suggest that acoustic signals are important in both species recognition and mate selection in psyllids. We found a significant level of phylogenetic signal in the acoustic data when we compared divergence in genetic data (obtained from mitochondrial DNA sequences of the small subunit rRNA) with divergence in acoustic signals in two groups of Australian psyllids. Phylogenetic reconstruction based on DNA sequence data supports the monophyly of the Eucalyptus-feeding genus Schedotrioza Tuthill & Taylor, 1955, whereas a diverse but little known group on Casuarinaceae hosts appears to be paraphyletic. These two psyllid groups also differ in amounts of geographical and ecological sympatry. We found a significant positive correlation between acoustic distance and genetic distance using pairwise comparisons for all taxa, but the trends within the two groups differ due to a negative association between acoustic and genetic divergence among the sympatric taxa. Phylogenetic information in acoustic data may be greatest in recently speciating and allopatric groups because of increased acoustic divergence in sympatric taxa and greater acoustic convergence in more distantly related species. Additional keywords: acoustic communication, Allocasuarina, Casuarinaceae, Eucalyptus, Psylloidea, speciation, substrate vibration, Triozidae.

‘Osmotic pump‘ feeding by coreids

Species of Coreidae (Heteroptera) cause ‘water soaked’ lesions in their food plants. Such insects typically feed from parenchyma in and surrounding vascular tissues and also cause acropetal wilting and necrosis of small diameter shoots. Feeding by Mictis profana (Fabr.) in South Australia on the shoots of Acacia iteaphylla F. Muell. ex Benth. was found to cause a local, concurrent increase in both water content and free amino acid concentration, consistent with phloem unloading. Coreids, unlike other groups of phytophagous Heteroptera, secrete a salivary sucrase (α‐D‐glucohydrolase, EC 3.2.1.48) as probably the sole salivary carbohydrase, and tissues attacked by M. profana showed more sucrose hydrolysing activity than unattacked. The salivary enzyme is postulated to cause unloading of solutes into the apoplast due to the osmotic effects of conversion of endogenous sucrose to glucose and fructose, allowing the insect to suck the leaked contents of many cells from a single locus. The term ‘osmotic pump feeding’ is proposed for such a process. In demonstrations of its feasibility, infiltration of shoots with mixtures of glucose and fructose stoichiometrically equivalent to isosmotic sucrose increased the amounts of tissue sap and amino acid that could be sucked from the tissues; similarly, invertase and 1 M sugars forced into the extracellular space of stem sections increased the amino acids offloaded into the bathing solutions.

Revision of Fergusonina Malloch gall flies (Diptera:Fergusoninidae) from Melaleuca (Myrtaceae)

Flies of the monogeneric Australasian family Fergusoninidae (Diptera) and nematodes of the genus Fergusobia Currie (Tylenchida : Neotylenchidae) together form galls on various Myrtaceae, in the only recorded mutualism between flies and nematodes. New species of Fergusonina Malloch gall-forming flies are here described from the broad-leaved Melaleuca leucadendra species-complex (Myrtaceae), which includes M. quinquenervia (Cav.) S. T. Blake, an invasive weed outside its natural range. The putatively monophyletic Fergusonina turneri species-group is defined to accommodate: F. turneri, sp. nov.; F. burrowsi, sp. nov.; F. centeri, sp. nov.; F. goolsbyi, sp. nov.; F. makinsoni, sp. nov.; F. purcelli, sp. nov.; and F. schefferae, sp. nov. Partial descriptions are provided for further unnamed species from the M. leucadendra species-complex, and for an additional unassigned species from a narrow-leaved Melaleuca. The fly–nematode associations are species-specific and appear to have a high degree of host specificity within the Myrtaceae. Information on the mutualist nematodes and host plant associations are presented, together with two keys to species of Fergusonina: one based on adult characters, and one (for field workers) based on larva, puparium and gall characters and host and nematode associations.

Phylogenetic Relationships, Species Limits, and Host Specificity of Gall-Forming Fergusonina Flies (Diptera: Fergusoninidae) Feeding on Melaleuca (Myrtaceae)

Abstract Phylogenetic analysis of recently described gall-forming Fergusonina Malloch flies was performed using DNA sequence data from the mitochondrial cytochrome oxidase I gene. Fifty-three flies reared from nine species of Melaleuca L. were sequenced. Species boundaries delimited by mitochondrial data confirm recent morphological investigation with one exception. Fergusonina turneri Taylor, believed to feed on both Melaleuca quinquenervia (Cav.) S. T. Blake and Melaleuca fluviatilis Barlow, seems to be comprised of two cryptic species, each specialized on one of the two hosts. Because F. turneri is under consideration as a potential biological control agent for invasive M. quinquenervia in the Florida Everglades, understanding cryptic variation and the degree of dietary specialization of this species is critical.

Molecular evidence of hybridization in Florida’s sheoak (Casuarina spp.) invasion

The presence of hybrids in plant invasions can indicate a potential for rapid adaptation and an added level of complexity in management of the invasion. Three Casuarina tree species, Casuarina glauca, Casuarina cunninghamiana and Casuarina equisetifolia, native to Australia, are naturalized in Florida, USA. Many Florida Casuarina trees are considered unidentifiable, presumably due to interspecific hybridization. We collected tissue from over 500 trees from Australia and Florida and genotyped these using amplified fragment length polymorphisms. Our goal was to determine the exact identity of the Florida species, including any putative hybrid combinations. In Australia, we found high assignment values to the three parental species, and no evidence of hybridization. In Florida, we found many trees with strong assignment to any one of the three species, as well as 49 trees with assignment values intermediate to C. glauca and C. equisetifolia, suggesting hybridization between these species. One population of 10 trees had assignment values intermediate to C. cunninghamiana and C. glauca, suggesting additional hybridization. For 69 of these putative hybrid and parental types, we sequenced a low‐copy intron of nuclear G3pdh, and these sequences indicated that some Florida trees contain heterozygotic combinations of C. glauca and C. equisetifolia haplotypes. The presence of novel hybrids in the Florida invasion may enhance evolution of invasive traits in these species. Novel Casuarina hybrids in Florida have no coevolutionary history with any insects or diseases, which may be problematic for biological control efforts.

First record of Fergusonina (Diptera: Fergusoninidae) and associated Fergusobia (Tylenchida: Neotylenchidae) forming galls on Metrosideros (Myrtaceae) from New Zealand.

Abstract A new species of fly, Fergusonina metrosiderosi Taylor sp.n. (Diptera: Fergusoninidae) [and its associated nematode, Fergusobia pohutukawa Davies sp.n. (Tylenchida: Neotylenchidae)], is described from unilocular basal shoot‐bud galls on Pohutukawa (New Zealand Christmas Tree), Metrosideros excelsa Banks ex Gaertn. (Myrtaceae). The fly is characterized by the short, sclerotized postabdomen of the female, distinctly grey wings, reduction in length of the reclinate orbital, postocellar and vertical setae, undifferentiation of the ocellar setae, supernumerary setation of the genae, and three pairs of scutellar setae rather than two. The dorsal shield is restricted to a few raised sclerotized spicules on the first to third thoracic segments of the larva and epidermis of the puparium. The nematode is characterized by the combinations of arcuate shape, small ‘a’ ratio, swollen cuticle, small cephalic region with elevated circum‐oral area with a flat tip, coarse annulation and relatively slender conical tail of the parthenogenetic female, and coarse annulation, long bursa and angular spicule with short, broad, offset manubrium of the male. Fergusonina metrosiderosi sp.n. and Fergusobia pohutukawa sp.n. represent the first record of the fly‐nematode association from the host genus Metrosideros, and the first record from New Zealand. Aspects of the biology and biogeography of the fly‐nematode association are discussed.

Composition and variability of the saliva of coreids in relation to phytoxicoses and other aspects of the salivary physiology of phytophagous Heteroptera

In the saciform, principal salivary glands of Mictis profana (Fabr.) (Coreidae: Heteroptera, Pentatomorpha), the contents of all lobes other than the posterior form gels consistent with their contributing to the solidifying saliva (stylet sheath); the posterior lobe secretes most if not all of a sucrose‐hydrolysing enzyme that occurs in the nongelling (watery) saliva. Evidence for the occurrence of such an enzyme in the saliva of other coreids is presented. That in M. profana has a pH optimum near neutral and a substrate specificity consistent with sucrase (sucrose α ‐D‐glucohydrolase, EC 3.2.1.48) as distinct from plant invertase (β ‐D‐fruccofuranosidase, EC 3.2.1.26). Apart from some maltose‐hydrolysing activity in the salivary glands, also consistent with sucrase, no other carbohydrases and neither proteinase nor lipase were detected. Phosphatases were found in gland extracts but not in secreted saliva. The saliva contains catechol oxidase (EC 1.10.3.1) from the accessory gland and ducts. Topical application of pilocarpine caused individual M. profana to secrete up to 58 μl watery saliva which showed continuous and independent variation of sucrase activity (up to ca 0.012 Units/μl) and pH (6–8), although high sucrase content tended to coincide with high pH. Total protein varied up to 10 μg/μl, and free amino acids up to 1.8 μg/μl leucine eq. Of the many proteins and/or protein subunits separable by electrophoresis of gland contents and saliva, four had sucrase activity, the most mobile with MW ca 66000. TLC indicated inter alia phenyl alanine and tyrosine, but no DOPA nor other diphenolic substrates of the catechol oxidase in the watery saliva. The soluble components of the saliva, which also has marked surfactant properties, are discussed in relation to the feeding process of coreids and the characteristic lesions they produce in their food plants.

Ecology and management of sheoak (Casuarina spp.), an invader of coastal Florida, U.S.A.

Abstract The Casuarina spp. are invasive plants in Florida that threaten biological diversity and beach integrity of coastal habitats. The trees include three species and their hybrids that aggressively invade riverine and coastal areas. Of the three species, C. equisetifolia and C. glauca are highly salt tolerant and widespread in coastal areas. The third species, C. cunninghamiana, invades riverine habitats. These species pose dangers to both the environment and public safety. The environmental damage includes interfering with nesting by endangered sea turtles, American crocodiles, and the rare swallow-tailed kite. Additionally, allelochemical leachates reduce germination and establishment of native vegetation. Casuarina-infested beaches are more prone to sand loss and erosion. Moreover, with shallow roots and tall canopies, they are among the first trees to fall in high winds and as such restrict evacuation efforts during hurricanes. Control of these species is mostly with herbicides, requiring repeated applications and monitoring. One of the most cost-effective means of controlling these invasive species would be with classical biological control. Australian surveys for potential biological control agents began in 2004, resulting in the discovery of several promising candidates. These include seed-feeding torymid wasps, defoliating caterpillars and weevils, leaf tip gall-formers from cecidomyiid midges, and sap-feeding psyllids. Continued work is needed to determine the suitability of these species for biological control. Despite conflicts of interest expressed by some homeowners and the agricultural industry who value the trees for shade and windbreaks, there are good prospects for safe and effective biological control of these invasive species.

Nutritional enhancement of leaves by a psyllid through senescence-like processes : insect manipulation or plant defence?

Some herbivores can modify the physiology of plant modules to meet their nutritional requirements. Induction of premature leaf senescence could benefit herbivores since it is associated with the mobilisation of nutrients. We compared the effects of nymphal feeding by Cardiaspina near densitexta on Eucalyptus moluccana with endogenous processes associated with senescence to assess the relative merits of an insect manipulation or plant defence interpretation of responses. Evidence supporting insect manipulation included increased size of fourth and fifth instar nymphs (in the latter the effect was restricted to forewing pad length of females) on leaves supporting high numbers of conspecifics and feeding preventing leaf necrosis. Intra-specific competition negated greater performance at very high densities. High and very high abundances of nymphs were associated with increased concentrations of amino acid N but only very high abundances of nymphs tended to be associated with increased concentrations of six essential amino acids. Contrary to the insect manipulation interpretation, feeding by very high abundances of nymphs was associated with significant reductions in chlorophyll, carotenoids and anthocyanins. Evidence supporting plant defence included the severity of chlorosis increasing with the abundance of nymphs. Leaf reddening did not develop because ambient conditions associated with photoinhibition (high irradiance and low temperature) were not experienced by leaves with chlorotic lesions. Leaf reddening (from anthocyanins) alone is not expected to adversely affect nymphal survival; only leaf necrosis would kill nymphs. For senescence-inducing psyllids, nutritional enhancement does not fit neatly into either an insect manipulation or plant defence interpretation.

Codivergence of the primary bacterial endosymbiont of psyllids versus host switches and replacement of their secondary bacterial endosymbionts.

Coevolution between insects and bacterial endosymbionts contributes to the success of many insect lineages. For the first time, we tested for phylogenetic codivergence across multiple taxonomic scales, from within genera to superfamily between 36 psyllid species of seven recognised families (Hemiptera: Psylloidea), their exclusive primary endosymbiont Carsonella and more diverse secondary endosymbionts (S-endosymbionts). Within Aphalaridae, we found that Carsonella and S-endosymbionts were fixed in one Glycaspis and 12 Cardiaspina populations. The dominant S-endosymbiont was Arsenophonus, while Sodalis was detected in one Cardiaspina species. We demonstrated vertical transmission for Carsonella and Arsenophonus in three Cardiaspina species. We found strong support for strict cospeciation and validated the informative content of Carsonella as extended host genome for inference of psyllid relationships. However, S-endosymbiont and host phylogenies were incongruent, and displayed signs of host switching and endosymbiont replacement. The high incidence of Arsenophonus in psyllids and other plant sap-feeding Hemiptera may be due to repeated host switching within this group. In two psyllid lineages, Arsenophonus and Sodalis genes exhibited accelerated evolutionary rates and AT-biases characteristic of long-term host associations. Together with strict vertical transmission and 100% prevalence within host populations, our results suggest an obligate, and not facultative, symbiosis between psyllids and some S-endosymbionts.