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Influence of Helicosporidium Spp. (Chlorophyta: Trebouxiophyceae) Infection on the Development and Survival of Three Noctuid

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Influence of Helicosporidium Spp. (Chlorophyta: Trebouxiophyceae) Infection on the Development and Survival of Three Noctuid BIOLOGICAL CONTROLÐMICROBIALS Influence of Helicosporidium spp. (Chlorophyta: Trebouxiophyceae) Infection on the Development and Survival of Three Noctuid Species 1 VERENA-ULRIKE BLA¨ SKE AND DRION G. BOUCIAS Department of Entomology and Nematology, University of Florida, Gainesville, FL 32611 Environ. Entomol. 33(1): 54Ð61 (2004) ABSTRACT A new Helicosporidium spp. isolate recently puriÞed from an aquatic weevil, Cyrtobagus salviniae Calder & Sands, was capable of infecting and reproducing in three heterologous noctuid hosts. Regardless of host species, oral treatment of Heliocoverpa zea (Boddie), Spodoptera exigua (Hu¨ bner), or Trichoplusia ni (Hu¨ bner) early instars with cyst preparations of Helicosporidium spp. resulted in Ϸ50% infection of the challenged larvae. The sex ratio did not differ between infected and control groups, suggesting the existence of a natural, nonsex-related resistance to the disease. Injection of Helicosporidium spp. into the hemocoels of late instars resulted in virtually 100% infection, indicating that resistance is related to the ingestion of the pathogen and therefore afÞliated with midgut-mediated barriers. The pathogenÕs development was not interrupted by metamorphosis; likewise, the infection did not necessarily interrupt the insectsÕ development. When treated as early instars, 50Ð90% of the infected larvae formed pupae, of which 20Ð30% emerged as adults. However, a high proportion of the infected adults (62Ð86%) had malformed wings, and their longevity was reduced compared with that of healthy adults. Infected S. exigua adults that seemed to be morphologically healthy were able to mate and produce viable offspring. The disease was detected in Þve of 12 groups of progeny produced by infected adults. However, the relative infection rate in the Þlial generation was low (2Ð5%). To our knowledge, this is the Þrst evidence for a vertical transmission of helicosporidial infection. KEY WORDS entomopathogenic algae, Helicosporidium, Heliocoverpa zea, Spodoptera exigua, Trichoplusia ni THE HELICOSPORIDIA ARE A UNIQUE, unclassiÞed group of analyses of several Helicosporidium spp. genes (rDNA, pathogens isolated from a small and diverse group of actin, ␤-tubulin, including 18S rDNA) all identiÞed invertebrates. These organisms were at one time con- this organism as a member of the green algae clade sidered to be either protozoa or fungi but have been (Chlorophyta). Moreover, nuclear phylogeny focused unclassiÞed since 1931 with only one named species, on Chlorophyta depicted Helicosporidium spp. as a Helicosporidium parasiticum Keilin. SigniÞcantly, He- close relative of Prototheca wickerhamii and Prototheca licosporidia have been reported to be pathogenic to zopfii within the class Trebouxiophyceae (Tartar et al. various invertebrate hosts, including insects, mites, 2002, 2003). cladocerans, and trematodes (Sayre and Clark 1978, In vivo studies have shown that the Helicosporidia Purrini 1984, Avery and Undeen 1987a, Pekkarinen are transmitted per os to both dipteran and lepidop- 1993). Recently, we have characterized two geneti- teran hosts (Kellen and Lindegren 1974, Fukuda et al. cally distinct Helicosporidium spp. isolates from the 1976, Boucias et al. 2001). Light microscopic exami- black ßy Simulium jonesi Stone & Snoddy (Diptera: nation of midgut preparations demonstrated that the Simuliidae) and from the weevil Cyrtobagus salviniae cyst stage binds to the peritrophic matrix and dehisces. Calder & Sands (Coleoptera: Curculionidae), found in Gainesville, FL (Boucias et al. 2001; Tartar et al. Upon activation, the pellicles rupture and release Þl- 2002, 2003). Microscopic examination has shown that amentous cells that penetrate the peritrophic matrix. these organisms possess a cell phenotype not found in Adhesion of intact cysts to the peritrophic matrix sug- any known protist. Microscopic observation of the gests that mechanical pressure expressed during de- vegetative growth of Helicosporidium spp. under in hiscence of the compressed cyst may mediate ingress vivo and in vitro conditions led Boucias et al. (2001) though the midgut barriers (peritrophic matrix and/or to associate this protist with green algae, particularly the microvillar membranes). Potentially, the Þlamen- the unicellular, nonphotosynthetic, and pathogenic tous cells penetrate the midgut columnar epithelium algae belonging to the genus Prototheca. Phylogenetic and differentiate into an intermediate stage that gains ingress through this tissue and enters the hemocoel. 1 Corresponding author, e-mail: [email protected]ß.edu. Within the hemocoel, vegetative cells replicate. 0046-225X/04/0054Ð0061$04.00/0 ᭧ 2004 Entomological Society of America February 2004 BLA¨ SKE AND BOUCIAS:EFFECT OF HELICOSPORIDIA ON INSECT DEVELOPMENT 55 Within 10Ð14 d, infected insects contain massive num- After 4Ð7 h, larvae that consumed the droplets were bers of mature cysts in the cream-colored hemolymph. weighed and transferred to single 1-oz cups with ar- Importantly, both the black ßy and the weevil iso- tiÞcial insect diet. Treated larvae were incubated at lates have been shown to infect and to replicate in constant conditions (27 Ϯ 1ЊC, 70 Ϯ 5% RH, photo- insect hosts that can be readily maintained under period of 12:12 [L:D] h) and checked for mortality laboratory conditions. Currently, the original hosts daily. To determine infection rates, control and test from which these algae were isolated are not available larvae were bled by needle puncture within 3Ð8 d for detailed pathogenÐhost laboratory studies. In this after oral treatment (larval weight Ն100 mg), and the study, we examined the impact of infection with the presence of Helicosporidium spp. in the hemolymph of Helicosporidium spp. weevil isolate on the survival and test larvae was recorded using differential interfer- development (selected Þtness parameters) of differ- ence contrast (DIC) optics (Leica DM R, Leica Mi- ent noctuid species. The infection data gathered with crosystems Wetzlar GmbH, Wetzlar, Germany). In- per os challenge assays were compared with bioassays sects diagnosed as not infected were checked again involving the hemocoelic injection of helicosporidial 1Ð3 d after pupation. cells. Then, a series of mating experiments examined For injection treatments, 5 ␮l of aqueous cyst sus- 1) the ability of this transstadial disease to affect the pension was injected into the hemocoels of late Þfth reproductive Þtness of both female and male adults, (S. exigua and T. ni) or sixth instars (H. zea)ata and 2) whether this pathogenic alga can be vertically concentration of 2 ϫ 105 cysts per larva. Control in- transmitted from infected Spodoptera exigua (Hu¨ b- sects were injected with sterile water. Larvae were ner) (Lepidoptera: Noctuidae) adults to Þlial gener- weighed, transferred to single 1-oz cups containing ations. artiÞcial diet, and incubated at constant conditions (27 Ϯ 1ЊC, 70 Ϯ 5% RH, photoperiod of 12:12 [L:D] h). Five to eight days after injection, the presence of Materials and Methods cysts in the hemolymph was recorded as described for Preparation of Helicosporidium. The Helicospo- the oral infection experiments. By this time, all larvae ridium spp. used in this study originated from an in- except for three had pupated. fected aquatic weevil, C. salviniae, collected in Aus- In all experiments, pupae were weighed and sexed, tralia and maintained under quarantine in Gainesville, and insect development and mortality were followed FL. Cysts were propagated in orally infected Helio- throughout adult emergence. Three to Þve replicates coverpa zea (Boddie) (Lepidoptera: Noctuidae) lar- with differing numbers of larvae (n ϭ 7Ð28) were vae and puriÞed from homogenates of late instars and conducted for each control and treatment. pupae by high-speed centrifugation (16,000 ϫ g, 30 Mating Experiments. To examine the effect of He- min) on a 20Ð80% linear gradient of Ludox HS40 licosporidium spp. infection on adult fecundity and to (PerkinElmer Life Sciences, Boston, MA). The band elucidate the ability of the pathogen to be vertically containing the cysts was collected, diluted in sterile transmitted to F1 progeny, a series of mating experi- water, and subjected to several cycles of low-speed ments were conducted with infected and control S. centrifugation (4,000 ϫ g, 10 min) to remove residual exigua adults that were obtained from injection treat- gradient material. After suspension in a cryopro- ments. One female and one male were transferred into tectant (10% dimethyl sulfoxide plus 10% glycerol), a 16-oz paper cup. A piece of tissue towel along the cysts were counted using a hemacytometer and ali- edge served as egg-laying substrate and a Kimwipe quots containing 1 ϫ 108 cysts/ml were stored at (Kimberly-Clark Corporation, Roswell, GA) soaked in Ϫ70ЊC. Before each experiment, cyst preparations a 10% sucrose solution in a small petri dish (60 mm in were thawed quickly, washed twice in sterile water diameter) provided nutrient to the adults. Each cup (2,000 ϫ g, 10 min), and resuspended either in 0.1% was held in a separate plastic box to prevent phero- aqueous Nile Blue A or in sterile water. mone interference between different mating trials. Insects and Infection Experiments. Larvae of H. zea Insects were incubated at constant conditions (27 Ϯ and eggs of S. exigua and Trichoplusia ni (Hu¨ bner) 1ЊC, 70 Ϯ 5% RH, photoperiod of 12:12 [L:D] h). (Lepidoptera: Noctuidae) were obtained from estab- When eggs were laid, pieces of artiÞcial diet were lished colonies at the Center
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