A general model for host plant selection in phytophagous insects

We develop a general theoretical framework for exploring the host plant selection behaviour of herbivorous insects. This model can be used to address a number of questions, including the evolution of specialists, generalists, preference hierarchies, and learning. We use our model to: (i) demonstrate the consequences of the extent to which the reproductive success of a foraging female is limited by the rate at which they find host plants (host limitation) or the number of eggs they carry (egg limitation); (ii) emphasize the different consequences of variation in behaviour before and after landing on (locating) a host (termed pre- and post-alighting, respectively); (iii) show that, in contrast to previous predictions, learning can be favoured in post-alighting behaviour--in particular, individuals can be selected to concentrate oviposition on an abundant low-quality host, whilst ignoring a rare higher-quality host; (iv) emphasize the importance of interactions between mechanisms in favouring specialization or learning.

Can mechanism help explain insect host choice?

Evolutionary theory predicts that herbivorous insects should lay eggs on plants in a way that reflects the suitability of each plant species for larval development. Empirical studies, however, often fail to find any relationship between an adult insect’s choice of host–plant and offspring fitness, and in such cases, it is generally assumed that other ‘missing’ factors (e.g. predation, host–plant abundance, learning and adult feeding sites) must be contributing to overall host suitability. Here, I consider an alternative theory – that a fitness cost inherent in the olfactory mechanism could constrain the evolution of insect host selection. I begin by reviewing current knowledge of odour processing in the insect antennal lobe with the aid of a simple schematic: the aim being to explain the workings of this mechanism to scientists who do not have prior knowledge in this field. I then use the schematic to explore how an insect’s perception of host and non-host odours is governed by a set of processing rules, or algorithm. Under the assumptions of this mechanistic view, the perception of every plant odour is interrelated, and seemingly bad host choices can still arise as part of an overall adaptive behavioural strategy. I discuss how an understanding of mechanism can improve the interpretation of theoretical and empirical studies in insect behaviour and evolution.

Understanding Heliothine (Lepidoptera: Heliothinae) pests: What is a host plant?

Heliothine moths (Lepidoptera: Heliothinae) include some of the world's most devastating pest species. Whereas the majority of nonpest heliothinae specialize on a single plant family, genus, or species, pest species are highly polyphagous, with populations often escalating in size as they move from one crop species to another. Here, we examine the current literature on heliothine host-selection behavior with the aim of providing a knowledge base for research scientists and pest managers. We review the host relations of pest heliothines, with a particular focus on Helicoverpa armigera (Hubner), the most economically damaging of all heliothine species. We then consider the important question of what constitutes a host plant in these moths, and some of the problems that arise when trying to determine host plant status from empirical studies on host use. The top six host plant families in the two main Australian pest species (H. armigera and Helicoverpa punctigera Wallengren) are the same and the top three (Asteraceae, Fabaceae, and Malvaceae) are ranked the same (in terms of the number of host species on which eggs or larvae have been identified), suggesting that these species may use similar cues to identify their hosts. In contrast, for the two key pest heliothines in the Americas, the Fabaceae contains approximate to 1/3 of hosts for both. For Helicoverpa zea (Boddie), the remaining hosts are more evenly distributed, with Solanaceae next, followed by Poaceae, Asteraceae, Malvaceae, and Rosaceae. For Heliothis virescens (F.), the next highest five families are Malvaceae, Asteraceae, Solanaceae, Convolvulaceae, and Scrophulariaceae. Again there is considerable overlap in host use at generic and even species level. H. armigera is the most widely distributed and recorded from 68 plant families worldwide, but only 14 families are recorded as a containing a host in all geographic areas. A few crop hosts are used throughout the range as expected, but in some cases there are anomalies, perhaps because host plant relation studies are not comparable. Studies on the attraction of heliothines to plant odors are examined in the context of our current understanding of insect olfaction, with the aim of better understanding the connection between odor perception and host choice. Finally, we discuss research into sustainable management of pest heliothines using knowledge of heliothine behavior and ecology. A coordinated international research effort is needed to advance our knowledge on host relations in widely distributed polyphagous species instead of the localized, piecemeal approaches to understanding these insects that has been the norm to date.

The functional significance of fruit exocarp on host selection and oviposition by Queensland fruit fly, Bactrocera tryoni (Froggatt) (Tephritidae: Diptera)

Queensland fruit fly is Australia's most serious insect pest of horticulture. The fly lays its eggs into fruit, where they hatch into maggots which destroy the fruit. Understanding egg laying behaviour, known as oviposition, is a critical but under-researched aspect of fruit fly biology. This thesis focused on three aspects of oviposition: the role of fruit peel as a physical barrier to oviposition; the quality of fruit for maggot development; and the structure and wear of the egg laying organ – the ovipositor. Results showed that flies selected fruit based on their suitability for offspring survival, not because of the softness or hardness of fruit peel. Previously reported use of holes or wounds in fruit peel by ovipositing females was determined to be a mechanism which saved the female time, not a mechanism to reduce ovipositor wear. The results offer insights into the evolution of host use by fruit flies and their sustainable management.

Biology and host range of Ophiomyia camarae Spencer (Diptera: Agromyzidae), a potential biocontrol agent for Lantana spp. (Verbenaceae) in Australia

The life history and host range of the herringbone leaf-mining fly Ophiomyia camarae, a potential biological control agent for Lantana spp., were investigated. Eggs were deposited singly on the underside of leaves. Although several eggs can be laid on a single leaf and a maximum of three individual mines were seen on a single leaf, only one pupa per leaf ever developed. The generation time (egg to adult) was about 38 days. Females (mean 14 days) lived longer than males (mean 9 days) and produced about 61 mines. Oviposition and larval development occurred on all five lantana phenotypes tested. Eleven plant species representing six families were tested to determine the host range. Oviposition and larval development occurred on only lantana and another nonnative plant Lippia alba (Verbenaceae), with both species supporting populations over several generations. A CLIMEX model showed that most of the coastal areas of eastern Australia south to 30°16' S (Coffs Harbour) would be suitable for O. camarae. O. camarae was approved for release in Australia in October 2007 and mines have been observed on plants at numerous field sites along the coast following releases.

The host range and biology of Cometaster pyrula; a biocontrol agent for Acacia nilotica subsp. indica in Australia

Prickly acacia, Acacia nilotica subsp. indica (Benth.) Brenan, a major weed of the Mitchell Grass Downs of northern Queensland, Australia, has been the target of biological control projects since the 1980s. The leaf-feeding caterpillar Cometaster pyrula (Hopffer) was collected from Acacia nilotica subsp. kraussiana (Benth.) Brenan during surveys in South Africa to find suitable biological control agents, recognised as a potential agent, and shipped into a quarantine facility in Australia. Cometaster pyrula has a life cycle of approximately 2 months during which time the larvae feed voraciously and reach 6 cm in length. Female moths oviposit a mean of 339 eggs. When presented with cut foliage of 77 plant species, unfed neonates survived for 7 days on only Acacia nilotica subsp. indica and Acacia nilotica subsp. kraussiana. When unfed neonates were placed on potted plants of 14 plant species, all larvae except those on Acacia nilotica subsp. indica and Acacia nilotica subsp. kraussiana died within 10 days of placement. Cometaster pyrula was considered to be highly host specific and safe to release in Australia. Permission to release C. pyrula in Australia was obtained and the insect was first released in north Queensland in October 2004. The ecoclimatic model CLIMEX indicated that coastal Queensland was climatically suitable for this insect but that inland areas were only marginally suitable.

Characterising insect plant host relationships facilitates understanding multiple host use

Weed biocontrol relies on host specificity testing, usually carried out under quarantine conditions to predict the future host range of candidate control agents. The predictive power of host testing can be scrutinised directly with Aconophora compressa, previously released against the weed Lantana camara L. (lantana) because its ecology in its new range (Australia) is known and includes the unanticipated use of several host species. Glasshouse based predictions of field host use from experiments designed a posteriori can therefore be compared against known field host use. Adult survival, reproductive output and egg maturation were quantified. Adult survival did not differ statistically across the four verbenaceous hosts used in Australia. Oviposition was significantly highest on fiddlewood (Citharexylum spinosum L.), followed by lantana, on which oviposition was significantly higher than on two varieties of Duranta erecta (‘‘geisha girl’’ and ‘‘Sheena’s gold’’; all Verbenaceae). Oviposition rates across Duranta varieties were not significantly different from each other but were significantly higher than on the two non-verbenaceous hosts (Jacaranda mimosifolia D. Don: Bignoneaceae (jacaranda) and Myoporum acuminatum R. Br.: Myoporaceae (Myoporum)). Production of adult A. compressa was modelled across the hosts tested. The only major discrepancy between model output and their relative abundance across hosts in the field was that densities on lantana in the field were much lower than predicted by the model. The adults may, therefore, not locate lantana under field conditions and/or adults may find lantana but leave after laying relatively few eggs. Fiddlewood is the only primary host plant of A. compressa in Australia, whereas lantana and the others are used secondarily or incidentally. The distinction between primary, secondary and incidental hosts of a herbivore species helps to predict the intensity and regularity of host use by that herbivore. Populations of the primary host plants of a released biological control agent are most likely to be consistently impacted by the herbivore, whereas secondary and incidental host plant species are unlikely to be impacted consistently. As a consequence, potential biocontrol agents should be released only against hosts to which they have been shown to be primarily adapted.

Life history and host range of Alagoasa extrema (Coleoptera: Chrysomelidae: Alticinae), a potential biological control agent of Lantana spp. (Verbenaceae) in Australia

The life history and host range of the lantana beetle, Alagoasa extrema, a potential biocontrol agent for Lantana spp. were investigated in a quarantine unit at the Alan Fletcher Research Station, Brisbane, Australia. Adults feed on leaves and females lay batches of about 17 eggs on the soil surface around the stems of plants. The eggs take 16 days to hatch and newly emerged larvae move up the stem to feed on young leaves. Larvae feed for about 23 days and there are three instars. There is a prepupal non-feeding stage that lasts about 12 days and the pupal stage, which occurs in a cocoon in the soil, lasts 16 days. Teneral adults remain in the cocoon for 3 days to harden prior to emergence. Males live for about 151 days while females live for about 127 days. The pre-oviposition period is 19 days. In no-choice larval feeding trials, nine plant species, representing three families, supported development to adult. Three species, Aloysia triphylla, Citharexylum spinosum and Pandorea pandorana were able to support at least two successive generations. These results confirm those reported in South Africa and suggest that A. extrema is not sufficiently specific for release in Australia. Furthermore, it is not recommended for release in any other country which is considering biological control of lantana.

Multiple host use by a sap-sucking membracid: population consequences of nymphal development on primary and secondary host plant species

Aconophora compressa is a gregarious, sap-sucking insect that uses multiple host plant species. Nymphal host plant species (and variety) significantly affected nymphal survival, nymphal development rate and the subsequent size and fecundity of adults, with fiddlewood ( Citharexylum spinosum ) being significantly best in all respects. Nymphs that developed on a relatively poor host ( Duranta erecta var “geisha girl”) and which were moved to fiddlewood as adults laid significantly fewer eggs (mean ± SE = 836 ± 130) than those that developed solely on fiddlewood (1,329 ± 105). Adults on geisha girl, regardless of having been reared as nymphs on fiddlewood or geisha girl, laid significantly fewer eggs (342 ± 83 and 317 ± 74, respectively) than adults on fiddlewood. A simple model that incorporates host plant related survival, development rate and fecundity suggests that the population dynamics of A. compressa are governed mainly by fiddlewood, the primary host. The results have general implications for understanding the population dynamics of herbivores that use multiple host plant species, and also for the way in which weed biological control host testing methods should be conducted.

Cat's claw creeper leaf-mining jewel beetle Hylaeogena jureceki Obenberger (Coleoptera: Buprestidae), a host-specific biological control agent for Dolichandra unguis-cati (Bignoniaceae) in Australia

Cat's claw creeper, Dolichandra unguis-cati (L.) L.G. Lohman (syn: Macfadyena unguis-cati (L.) A.H. Gentry) (Bignoniaceae), a major environmental weed in Queensland and New South Wales, is a Weed of National Significance and an approved target for biological control. A leaf-mining jewel beetle, Hylaeogena jureceki Obenberger (Coleoptera: Buprestidae), first collected in 2002 from D. unguis-cati in Brazil and Argentina, was imported from South Africa into a quarantine facility in Brisbane in 2009 for host-specificity testing. H. jureceki adults chew holes in leaves and lay eggs on leaf margins and the emerging larvae mine within the leaves of D. unguis-cati. The generation time (egg to adult) of H. jureceki under quarantine conditions was 55.4 ± 0.2 days. Host-specificity trials conducted in Australia on 38 plant species from 11 families supplement and support South African studies which indicated that H. jureceki is highly host-specific and does not pose a risk to any non-target plant species in Australia. In no-choice tests, adults survived significantly longer (>32 weeks) on D. unguis-cati than on non-target test plant species (<3 weeks). Oviposition occurred on D. unguis-cati and one non-target test plant species, Citharexylum spinosum (Verbenaceae), but no larval development occurred on the latter species. In choice tests involving D. unguis-cati, C. spinosum and Avicennia marina (Avicenniaceae), feeding and oviposition were evident only on D. unguis-cati. The insect was approved for field release in Australia in May 2012.

Life cycle and host range of Phycitasp. rejected for biological control of prickly acacia in Australia

Prickly acacia (Vachellia nilotica subsp. indica), a native of the Indian subcontinent, is a serious weed of the grazing areas of northern Australia and is a target for classical biological control. Native range surveys in India identified a leaf webber, Phycita sp. (Lepidoptera: Pyralidae) as a prospective biological control agent for prickly acacia. In this study, we report the life cycle and host-specificity test results Phycita sp. and highlight the contradictory results between the no-choice tests in India and Australia and the field host range in India. In no-choice tests in India and Australia, Phycita sp. completed development on two of 11 and 16 of 27 non-target test plant species, respectively. Although Phycita sp. fed and completed development on two non-target test plant species (Vachellia planifrons and V. leucophloea) in no-choice tests in India, there was no evidence of the insect on the two non-target test plant species in the field. Our contention is that oviposition behaviour could be the key mechanism in host selection of Phycita sp., resulting in its incidence only on prickly acacia in India. This is supported by paired oviposition choice tests involving three test plant species (Acacia baileyana, A. mearnsii and A. deanei) in quarantine in Australia, where eggs were laid only on prickly acacia. However, in paired oviposition choice trials, only few eggs were laid, making the results unreliable. Although oviposition choice tests suggest that prickly acacia is the most preferred and natural host, difficulties in conducting choice oviposition tests with fully grown trees under quarantine conditions in Australia and the logistic difficulties of conducting open-field tests with fully grown native Australian plants in India have led to rejection of Phycita sp. as a potential biological control agent for prickly acacia in Australia.

In-vitro effect of fungicides on hyphal growth and sporogenesis of Lagenidium sp. isolated from Penaeus monodon larvae and Scylla serrata eggs

The sensitivity of Lagenidium, isolated from Penaeus monodon, Scylla serrata , to 34 antimycotics was determined. Effects on the development of vesicles, zoospores and mycelial growth were evaluated. Although mycoidal levels of the chemicals tested will be ideal for lethal treatment on control of the fungus, the high dose required may be lethal to the host, thus the use of mycostatic concentrations is more practical. Treatments of rearing water containing larvae, adult shrimps or crabs should be done only after preliminary tolerance experiments using at least the mycostatic dose prove to be safe for the hosts. Mycocidal doses can be used for determining disinfection doses of equipment and facilities used in rearing procedures as well as for destroying batches of infected larvae.

Evidence of host specificity and congruence between phylogenies of bitterling and freshwater mussels

Evidence of host specificity and congruence between phylogenies of bitterling and freshwater mussels. Zoological Studies 45(3): 428-434. Bitterling (Cyprinidae: Acheilognathinae) are freshwater fishes with a unique spawning relationship with freshwater mussels on whose gills they lay their eggs. During the breeding season of bitterling fishes, we collected 843 mussels belonging to 16 species from Lake Qinglan, central China and examined their gill chambers for the presence of bitterling larvae. Three species of bitterling larvae were identified; Acheilognathus tonkinensis, Ach. cf. meridianus, and Ach. barbatulus, in 3 species of mussel: Unio douglasiae, Lamprotula caveata, and L. tortuosa, suggesting host specialization. Using our own and other published data, we compared the respective phylogenies of bitterling and mussels, but failed to show clear congruence. However, broad specializations are evident, with Acheilognathus and Tanakia showing preferences for mussels with a relatively simple gill structure (Ableminae), and Rhodeus spp. showing preferences for mussels of the Anodontinae and Unioninae, which have more-complex gill structures.

An integrated transcriptomics and proteomics analysis of the secretome of the helminth pathogen Fasciola hepatica: Proteins associated with invasion and infection of the mammalian host

To infect their mammalian hosts, Fasciola hepatica larvae must penetrate and traverse the intestinal wall of the duodenum, move through the peritoneum, and penetrate the liver. After migrating through and feeding on the liver, causing extensive tissue damage, the parasites move to their final niche in the bile ducts where they mature and produce eggs. Here we integrated a transcriptomics and proteomics approach to profile Fasciola secretory proteins that are involved in host-pathogen interactions and to correlate changes in their expression with the migration of the parasite. Prediction of F. hepatica secretory proteins from 14,031 expressed sequence tags (ESTs) available from the Wellcome Trust Sanger Centre using the semiautomated EST2Secretome pipeline showed that the major components of adult parasite secretions are proteolytic enzymes including cathepsin L, cathepsin B, and asparaginyl endopeptidase cysteine proteases as well as novel trypsin-like serine proteases and carboxypeptidases. Proteomics analysis of proteins secreted by infective larvae, immature flukes, and adult F. hepatica showed that these proteases are developmentally regulated and correlate with the passage of the parasite through host tissues and its encounters with different host macromolecules. Proteases such as FhCL3 and cathepsin B have specific functions in larvae activation and intestinal wall penetration, whereas FhCL1, FhCL2, and FhCL5 are required for liver penetration and tissue and blood feeding. Besides proteases, the parasites secrete an array of antioxidants that are also highly regulated according to their migration through host tissues. However, whereas the proteases of F. hepatica are secreted into the parasite gut via a classical endoplasmic reticulum/Golgi pathway, we speculate that the antioxidants, which all lack a signal sequence, are released via a non-classical trans-tegumental pathway.

Development of the vitellaria of the liver fluke, Fasciola hepatica in the rat host

The development of the vitellaria of Fasciola hepatica within the liver of its rat host was studied by means of whole-mount stained preparations and transmission electron microscopy, together with light and electron immunocytochemistry using an antibody to vitelline protein B, an eggshell precursor protein synthesized by F. hepatica. No vitelline cells could be identified in flukes recovered from the liver parenchyma, by any of the methods used. In contrast, follicles were present in flukes at the earliest time of recovery from the bile duct, namely, 5 weeks 3 days post-infection. The vitellaria in these flukes formed a row of small follicles on either side of the body. Development of the follicles was rapid: by 6 weeks 3 days, the vitellaria resembled those in the adult fluke and eggs were present in the uterus. Immunolabelling was confined to the shell protein globules in the vitelline cells, confirming the packaging of the eggshell protein within the shell globule clusters.