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1.  From Augmentation to Conservation of Entomopathogenic Nematodes: Trophic Cascades, Habitat Manipulation and Enhanced Biological Control of Diaprepes abbreviatus Root Weevils in Florida Citrus Groves 
Journal of nematology  2008;40(2):73-84.
The use of entomopathogenic nematodes (EPN) for management of the root weevil, Diaprepes abbreviatus, in Florida citrus groves is considered a biological control success story and typically involves augmentation in which EPN are applied inundatively as biopesticides to quickly kill the pest. However, recent evidence indicates that efficacy of EPN applications in Florida citrus depends on soil type. They are very effective in the well drained coarse sands of the Central Ridge but often less so in poorly drained fine-textured soils of the Flatwoods. Moreover, groves on the Central Ridge can harbor rich communities of endemic EPN that might often suppress weevil populations below economic thresholds, whereas Flatwoods groves tend to have few endemic EPN and frequent weevil problems. Current research is examining the ecological dynamics of EPN in Florida citrus groves, the potential impact of EPN augmentation on soil food webs, especially endemic EPN, and whether habitat manipulation and inoculation strategies might be effective for conserving and enhancing EPN communities to achieve long-term control in problem areas. Conservation biological control could extend the usefulness of EPN in Florida citrus and be especially appropriate for groves with persistent weevil problems.
PMCID: PMC2586536  PMID: 19259523
biological control; citrus; conservation; Diaprepes abbreviatus; ecology; entomopathogenic nematode; Florida; food web; Heterorhabditis; management; manure; mulch; root weevil; soil; Steinernema; suppression; trophic cascades
2.  Augmenting Entomopathogenic Nematodes in Soil from a Florida CitrusOrchard: Non-Target Effects of a Trophic Cascade 
Journal of nematology  2007;39(2):203-210.
Laboratory experiments were conducted to study non-target effects of augmenting entomopathogenic nematode (EPN)communities in soil. When raw soil from a citrus orchard was augmented with either 2,000 Steinernema riobrave or S. diaprepesi, fewer EPN (P ≤ 0.05) survived if the soil had also been treated with 2,000 S. riobrave 7 d earlier (i.e., two augmentation events rather than one). EPN survival was unaffected by treatment (P ≤ 0.05) in soil that was air-dried to disrupt antagonist activity prior to the experiment. When S. diaprepesi, S. riobrave, Heterorhabditis zealandica or no EPN were added to raw soil and S. diaprepesi was added 5 d later, the survival of both S. diaprepesi and of total EPN was greater (P ≤ 0.05) in soil that received no pretreatment than in soilpre treated with S. riobrave. Pretreatment of soil with H. zealandica or S. diaprepesi had less or no affect on survival of S. diaprepesi or total EPN. When nematodes were recovered from soil and placed on water agar, the number of S. diaprepesi that were killed by endoparasitic and trapping nematophagous fungi was greater (P ≤ 0.05) if soil was pretreated with steinernematid species than if the soil was not pretreated or was pretreated with H. zealandica. The adverse effects of pretreating soil on EPN survival were density dependent within a range of pretreatment dosages (20–100 IJ/cm2 soil surface), and the treatment effects required more time to become evident at lower than at higher dosages. These experiments suggest that non-target effects of augmenting the EPN community in soil vary among EPN species and have the potential to temporarily reduce EPN numbers below the natural equilibrium density.
PMCID: PMC2586486  PMID: 19259489
Antagonism; nematophagous fungi; numerical response; post-application biology; predation; survival
3.  Food Web Responses to Augmenting the Entomopathogenic Nematodes in Bare and Animal Manure-Mulched Soil 
Journal of nematology  2007;39(2):176-189.
Factorial treatments of entomopathogenic nematodes (EPN) and composted, manure mulches were evaluated for two years in a central Florida citrus orchard to study the post-application biology of EPN used to manage the root weevil, Diaprepes abbreviatus. Mulch treatments were applied once each year to study the effects of altering the community of EPN competitors (free-living bactivorous nematodes) and antagonists (nematophagous fungi (NF), predaceous nematodes and some microarthro-pods). EPN were augmented once with Steinernema riobrave in 2004 and twice in 2005. Adding EPN to soil affected the prevalence of organisms at several trophic levels, but the effects were often ephemeral and sometimes inconsistent. EPN augmentation always increased the mortality of sentinel weevil larvae, the prevalence of free-living nematodes in sentinel cadavers and the prevalence of trapping NF. Subsequent to the insecticidal effects of EPN augmentation in 2004, but not 2005, EPN became temporarily less prevalent, and fewer sentinel weevil larvae died in EPN-augmented compared to non-augmented plots. Manure mulch had variable effects on endoparasitic NF, but consistently decreased the prevalence of trapping NF and increased the prevalence of EPN and the sentinel mortality. Both temporal and spatial abundance of NF were inversely related to the prevalence of Steinernema diaprepesi, whereas Heterorhabditis zealandica prevalence was positively correlated with NF over time. The number of weevil larvae killed by EPN was likely greatest in 2005, due in part to non-target effects of augmentation on the endemic EPN community in 2004 that occurred during a period of peak weevil recruitment into the soil.
PMCID: PMC2586487  PMID: 19259487
Diaprepes abbreviatus; entomopathogenic nematodes; food webs; IPM; nematophagous fungi; post-application biology; survival; trophic cascades
4.  Bionomics of a Phoretic Association Between Paenibacillus sp. and the Entomopathogenic Nematode Steinernema diaprepesi 
Journal of Nematology  2005;37(1):18-25.
Spores of an unidentified bacterium were discovered adhering to cuticles of third-stage infective juvenile (IJ) Steinernema diaprepesi endemic in a central Florida citrus orchard. The spores were cup-shaped, 5 to 6 mm in length, and contained a central endospore. Based on 16S rDNA gene sequencing, the bacterium is closely related to the insect pathogens Paenibacillus popilliae and P. lentimorbus. However, unlike the latter bacteria, the Paenibacillus sp. is non-fastidious and grew readily on several standard media. The bacterium did not attach to cuticles of several entomopathogenic or plant-parasitic nematodes tested, suggesting host specificity to S. diaprepesi. Attachment of Paenibacillus sp. to the third-stage cuticle of S. diaprepesi differed from Paenibacillus spp. associated with heterorhabditid entomopathogenic nematodes, which attach to the IJ sheath (second-stage cuticle). The inability to detect endospores within the body of S. diaprepesi indicates that the bacterial association with the nematode is phoretic. The Paenibacillus sp. showed limited virulence to Diaprepes abbreviatus, requiring inoculation of larvae with 108 spores to achieve death of the insect and reproduction of the bacterium. The effect of the bacterium on the nematode population biology was studied in 25-cm-long vertical sand columns. A single D. abbreviatus larva was confined below 15-cm depth, and the soil surface was inoculated with either spore-free or spore-encumbered IJ nematodes. After 7 days, the proportion of IJ below 5-cm depth was seven-fold greater for spore-free IJ than for spore-encumbered nematodes. Mortality of D. abbreviatus larvae was 72% greater (P <= 0.01) for spore-free compared to spore-encumbered S. diaprepesi. More than 5 times as many progeny IJs (P <= 0.01) were produced by spore-free compared to spore-encumbered nematodes. These data suggest that the bacterium is a component of the D. abbreviatus food web with some potential to regulate a natural enemy of the insect.
PMCID: PMC2620948  PMID: 19262839
Antagonism; competition; Diaprepes abbreviatus; entomopathogenic nematode; Paenibacillus; phoresis; 16S rDNA; Steinernema diaprepesi; Xenorhabdus sp.
5.  Effects of Perennial Peanut (Arachis glabrata) Ground Cover on Nematode Communities in Citrus 
Journal of Nematology  2003;35(4):450-457.
The effects of perennial peanut (Arachis glabrata) ground cover on the nematode community in a citrus orchard were examined. Samples were taken from two different ground cover treatments (perennial peanut or bare ground) at each of three distances from the tree trunk. Richness, measured as total numbers of nematode genera per sample, and total numbers of nematodes were greatest in the perennial peanut treatment (P < 0.05). Abundance of many genera of bacterivores, fungivores, and omnivores were increased by the perennial peanut ground cover. Total numbers of plant parasites were greater in perennial peanut treatments on three of the five sampling dates (P < 0.05), mainly due to trends in numbers of Mesocriconema. Distance from a tree trunk and the interaction of ground cover treatments and proximity to a tree trunk were most influential for Belonolaimus and Hoplolaimus. Although differences among treatments were observed for nematode genera and trophic groups, ecological indices were not consistently sensitive to treatments. Among several ecological indices evaluated, richness was most often affected by ground cover treatment.
PMCID: PMC2620683  PMID: 19262779
Arachis glabrata; Belonolaimus; citrus; ecological indices; Hoplolaimus; Mesocriconema nematode community; perennial peanut; plant-parasitic nematodes
6.  Competition Between Entomopathogenic and Free-Living Bactivorous Nematodes in Larvae of the Weevil Diaprepes abbreviatus 
Journal of Nematology  2003;35(2):187-193.
Field and laboratory experiments were conducted to determine the degree to which free-living, bactivorous nematodes (FLBN) are able to competitively displace entomopathogenic nematodes (EPN) from insect cadavers. Two hundred larvae of the insect Diaprepes abbreviatus were buried at regular intervals during 2 years in experimental plots that were untreated or treated twice annually with Steinernema riobrave. Larvae were recovered after 7 days, and nematodes emerging from cadavers during the next 30 days were identified. The monthly prevalence of FLBN was directly related to that of S. riobrave (r = 0.38; P = 0.001) but was not related to the prevalence of the endemic EPN, S. diaprepesi, Heterorhabditis zealandica, H. indica, or H. bacteriophora (r = 0.02; P = 0.80). In a second experiment, treatment of small field plots with S. riobrave increased the prevalence of insect cadavers in which only FLBN were detected compared to untreated controls (30% vs. 14%; P = 0.052), and increased numbers of FLBN per buried insect by more than 10-fold. In the laboratory, sand microcosms containing one D. abbreviatus larva were treated with (i) the FLBN, Pellioditis sp.; (ii) S. riobrave; (iii) S. riobrave + Pellioditis; or (iv) neither nematode. Insect mortality was higher in the presence of both nematodes (57%) than when S. riobrave was alone (42%) (P = 0.01). An average of 59.2 Pellioditis sp. g-1 insect body weight emerged in the presence of S. riobrave, whereas 6.2 nematodes g-1 insect were recovered in the absence of the EPN (P = 0.01). Pellioditis sp. reduced the number of S. riobrave per cadaver by 84%; (P = 0.03), and per available insect by 82% (P = 0.001), compared to S. riobrave alone. Population size of S. diaprepesi was not affected by Pellioditis sp. in experiments of the same design. Faster development (P = 0.05) and nutrient appropriation within the insect cadaver by S. diaprepesi compared to S. riobrave may increase the fitness of the former species to compete with Pellioditis sp. The results of these studies demonstrate the potential of FLBN to regulate population densities of EPN and to dampen estimates of EPN-induced mortality of insect pests in the field.
PMCID: PMC2620622  PMID: 19265993
free-living nematodes; microbivorous nematodes; Pellioditis; Steinernema diaprepesi; Steinernema riobrave; Steinernematidae
7.  Incidence of Endemic Entomopathogenic Nematodes Following Application of Steinernema riobrave for Control of Diaprepes abbreviatus 
Journal of Nematology  2003;35(2):178-186.
Control of Diaprepes abbreviatus by endemic and exotic entomopathogenic nematodes (EPN) was monitored during 2000-2001 in two citrus orchards in central Florida (Bartow and Poinciana). Caged sentinel insect larvae were buried beneath citrus trees for 7 days at 1 to 2-month intervals from April to October each year. At Bartow, the survey occurred in experimental plots that were (i) not treated with commercial EPN, (ii) treated twice annually since 1998 with commercially formulated Steinernema riobrave, or (iii) treated twice annually with S. riobrave and liquid fertilization (15 times/year) occurred in place of dry fertilizer (3 times/year) used in the other treatments. Four endemic EPN species, in addition to S. riobrave, were recovered from the sandy soil at Bartow: S. diaprepesi, Heterorhabditis zealandica, H. indica, and H. bacteriophora. Mean insect mortality in control plots was 39.4% (range = 13% to 74%), with seasonal maxima in May to July each year. Endemic EPN were recovered from 55% (range = 22% to 81%) of the cadavers each month. Total numbers of endemic EPN recovered in all plots during 2 years were directly related to the numbers of adult weevils (D. abbreviatus and Pachnaeus litus) captured in modified Tedder's traps and inversely related to recovery of S. riobrave. Insect mortality was higher and cadavers containing endemic EPN were more numerous in untreated control plots than in S. riobrave-treated plots, except during months in which S. riobrave was applied. In treated plots, endemic EPN were recovered from cadavers at twice the rate of S. riobrave. Suppression of endemic EPN in plots treated with S. riobrave, combined with inferior persistence by the introduced species, may have attenuated the net efficacy of S. riobrave against D. abbreviatus. In contrast, H. indica was the only endemic nematode recovered from the sandy clay loam soil at Poinciana, where the average mortality of D. abbreviatus was 12% (range 3% to 20%) and incidence of H. indica did not exceed 8%. Results of these surveys suggest that the regional patterns in the abundance and damage to citrus caused by D. abbreviatus in Florida are regulated by endemic EPN and other soilborne enemies of the weevil.
PMCID: PMC2620623  PMID: 19265992
Abbott's formula; biological control; competition; entomopathogenic nematodes; Heterorhabditis; natural control; seasonality; Steinernema
8.  Tylenchulus semipenetrans Alters the Microbial Community in the Citrus Rhizosphere 
Journal of Nematology  2003;35(2):167-177.
Infection of citrus seedlings by Tylenchulus semipenetrans was shown to reduce subsequent infection of roots by Phytophthora nicotianae and to increase plant growth compared to plants infected by only the fungus. Hypothetical mechanisms by which the nematode suppresses fungal development include nutrient competition, direct antibiosis, or alteration of the microbial community in the rhizosphere to favor microorganisms antagonistic to P. nicotianae. A test of the last hypothesis was conducted via surveys of five sites in each of three citrus orchards infested with both organisms. A total of 180 2-cm-long fibrous root segments, half with a female T. semipenetrans egg mass on the root surface and half without, were obtained from each orchard site. The samples were macerated in water, and fungi and bacteria in the suspensions were isolated, quantified, and identified. No differences were detected in the numbers of microorganism species isolated from nematode-infected and uninfected root segments. However, nematode-infected root segments had significantly more propagules of bacteria at all orchard sites. Bacillus megaterium and Burkholderia cepacia were the dominant bacterial species recovered. Bacteria belonging to the genera Arthrobacter and Stenotrophomonas were encountered less frequently. The fungus community was dominated by Fusarium solani, but Trichoderma, Verticillum, Phythophthora, and Penicillium spp. also were recovered. All isolated bacteria equally inhibited the growth of P. nicotianae in vitro. Experiments using selected bacteria, T. semipenetrans, and P. nicotianae, alone or in combination, were conducted in both the laboratory and greenhouse. Root and stem fresh weights of P. nicotianae-infected plants treated with T. semipenetrans, B. cepacia, or B. megaterium were greater than for plants treated only with the fungus. Phytophthora nicotianae protein in roots of fungus-infected plants was reduced by nematodes (P ≤ 0.001), either alone or in combination with either bacterium. However, treatment with bacteria did not affect P. nicotianae development in roots. The results suggest different mechanisms by which T. semipenetrans, B. cepacia, and B. megaterium may mitigate virulence of P. nicotianae.
PMCID: PMC2620617  PMID: 19265991
Bacillus megaterium; Burkholderia cepacia; interaction; nematode; Phytophthora nicotianae; rhizosphere microorganisms; Tylenchulus semipenetrans
9.  Infection of Citrus Roots by Tylenchulus semipenetrans Reduces Root Infection by Phytophthora nicotianae 
Journal of Nematology  2002;34(4):384-389.
Bioassays and whole-plant experiments were conducted to investigate the interaction between Tylenchulus semipenetrans and Phytophthora nicotianae. Both organisms are parasites of the citrus fibrous root cortex. Nematode-infected and non-infected root segments were excised from naturally infected field roots and placed on water agar in close proximity to agar plugs of P. nicotianae and then transferred to a Phytophthora-selective medium. At 10 and 12 days, 50% fewer nematode-infected segments were infected by P. nicotianae than non-infected segments. In whole-plant experiments in glass test tubes, sour orange seedlings were inoculated with two densities (8,000 or 80,000 eggs and second-stage juveniles) of T. semipenetrans, and after establishment of infection were inoculated with two densities (9,000 and 90,000 zoospores) of P. nicotianae. In the first experiment, fungal protein was 53% to 65% lower in the roots infected by both organisms than in roots infected by the fungus only. Compared to plants infected only by P. nicotianae, shoot weights were 33% to 50% greater (P ≤ 0.05) in plants infected by both parasites, regardless of inoculum density. Fibrous and tap root weights were 5% to 23% and 19% to 34% greater (P ≤ 0.05), respectively, in nematode-fungus combination treatments compared to the fungus alone. A second experiment was conducted, where plants were infected by the fungus, the nematode, both organisms, or neither organism. The soil mixture pH for 50% of the plants was adjusted from 4.5 to 7.0 to favor nematode infection. A higher rate of nematode infection of plants growing at pH 7.0 compared to pH 4.5 resulted in greater suppression of fungal development and greater inhibition of fungal damage to the plant. Compared to plants infected only by P. nicotianae, shoot and root weights were 37% and 33% greater (P ≤ 0.05), respectively, in plants infected by both parasites. These experiments have revealed antagonism between T. semipenetrans and P. nicotianae in citrus.
PMCID: PMC2620587  PMID: 19265961
citrus; competition; interspecific interactions; Phytophthora nicotianae; Tylenchulus semipenetrans
10.  Eggs of Tylenchulus semipenetrans Inhibit Growth of Phytophthora nicotianae and Fusarium solani in vitro 
Journal of Nematology  2002;34(3):267-272.
In previous greenhouse and laboratory studies, citrus seedlings infested with the citrus nematode Tylenchulus semipenetrans and later inoculated with the fungus Phylophthora nicotianae grew larger and contained less fungal protein in root tissues than plants infected by only the fungus, demonstrating antagonism of the nematode to the fungus. In this study, we determined whether eggs of the citrus nematode T. semipenetrans and root-knot nematode Meloidogyne arenaria affected mycelial growth of P. nicotianae and Fusarium solani in vitro. Approximately 35,000 live or heat-killed (60°C, 10 minutes) eggs of each nematode species were surface-sterilized with cupric sulfate, mercuric chloride, and streptomycin sulfate and placed in 5-pl drops onto the center of nutrient agar plates. Nutrient agar plugs from actively growing colonies of P. nicotianae or F. solani were placed on top of the eggs for 48 hours after which fungal colony growth was determined. Live citrus nematode eggs suppressed mycelial growth of P. nicotianae and F. solani (P ≤ 0.05) compared to heat-killed eggs and water controls. Reaction of the fungi to heat-killed eggs was variable. Root-knot nematode eggs had no effect on either P. nicotianae or F. solani mycelial growth. The experiment demonstrated a species-specific, direct effect of the eggs of the citrus nematode on P, nicotianae and F. solani.
PMCID: PMC2620562  PMID: 19265943
antagonistic interaction; citrus; competition; eggs; Fusarium solani; Meloidogyne arenaria; Phytophthora nicotianae; Tylenchulus semipentrans
11.  Hydraulic Lift Increases Herbivory by Diaprepes abbreviatus Larvae and Persistence of Steinernema riobrave in Dry Soil 
Journal of Nematology  2001;33(2-3):142-146.
Citrus seedlings were grown in double pots that separated the root systems into discrete lower and upper zones to test the hypothesis that hydraulic lift affects persistence and efficacy of entomopathogenic nematodes. Three treatments were established: (i) both pots were irrigated at water potential ≤ -15 kPa (no drought); (ii) only the bottom pot was irrigated (partial drought); (iii) neither pot was irrigated (complete drought). Steinernema riobrave infective juveniles (IJ) were added to the soil in the top pots of all treatments. During 27 days, the water potential in soil in the top pots of both the partial and complete drought treatments declined to ca. -160 kPa. A greater number of nematodes (P ≤ 0.01) persisted in soil as motile IJ under conditions of partial drought (143/pot) than under no drought (6.1/pot) or complete drought (4.4/pot). A second experiment was initiated with the same treatments as the first, except that only half of the 20 replicates in each moisture regime were inoculated with nematodes. After 15 days, all top pots were irrigated and two larvae of the insect Diaprepes abbreviatus were added to all of the top pots in each treatment. Irrigation regimes were reinstituted until water potential in the top pots under partial and complete drought had again declined to ca. -150 kPa and the experiment was terminated. In the absence of nematodes, the damage to tap roots caused by D. abbreviatus feeding under partial drought and complete drought was 80% and 32%, respectively, of that under no drought. Numbers of motile IJ in soil were greater under conditions of partial drought (736/pot) than under complete drought (2.0/pot) or no drought (7.2/pot). Survival of D. abbreviatus and insect damage to roots were reduced by the presence of S. riobrave to a greater extent under partial drought as compared to other treatments. Hydraulic lift from the lower to the upper rhizosphere appears to have modulated the effect of dry soil conditions on feeding behavior of D. abbreviatus and created favorable conditions for persistence and efficacy of the entomopathogenic nematode.
PMCID: PMC2638139  PMID: 19266011
biological control; citrus; Diaprepes abbreviatus; drought; hydraulic lift; soil moisture; Steinernema riobrave; water potential
12.  Nematode Community Composition under Various Irrigation Schemes in a Citrus Soil Ecosystem 
Journal of Nematology  1998;30(2):170-178.
Interest in the sustainability of farming practices has increased in response to environmental problems associated with conventional agricultural management often adopted for the production of herbaceous crops, ornamentals, and fruit crops. Availability of measures of the status of the soil ecosystem is of immediate importance, particularly for environmental assessment and monitoring programs. This study investigated the effects of various irrigation regimes (an example of an agricultural management practice) on the structure of the nematode fauna in a citrus orchard in the sandy ridge area of Central Florida. Ecological measures such as community structure indices, diversity indices, and maturity indices were assessed and related to irrigation intensity. Maturity index was an effective measure in distinguishing differences between irrigation regimes, whereas other indices of community structure were not. Of various nematode genera and trophic groups, only omnivores and the omnivore genera. Aporcelaimellus and Eudorylaimus responded to irrigation treatments.
PMCID: PMC2620287  PMID: 19274207
bioindicator; citrus; community structure; diversity; Florida; irrigation regime; maturity index; nematode; soil ecology; sustainable systems
13.  Population Changes of Tylenchulus semipenetrans Under Localized Versus Uniform Drought in the Citrus Root Zone 
Journal of Nematology  1996;28(3):360-368.
Population development of Tylenchulus semipenetrans in dry soil was investigated in a greenhouse study. Citrus seedlings were grown in sandy soil in vertical tubes with upper and lower sections. Nematode population densities in the upper tubes were measured at 16, 23, and 37 days, post-treatment. Three treatments consisted of i) irrigating both tubes when soil water potential reached -1 5 kPa (non-drought), ii) irrigating only the bottom tube (local drought), and iii) no irrigation (uniform drought). Soil water potential in the upper tubes did not differ under local and uniform drought during the first 16 days post-treatment, when it approached - 125 kPa. Thereafter, the water potential of soil under uniform drought continued to decrease, while that under local drought stabilized at approximately -150 kPa. Treatments had no consistent effects on female T. semipenetrans counts from soil or roots. However, after 37 days, numbers of eggs, juvenile, and male nematodes per gram of root under local drought were more than 2.4-fold greater than those under non-drought or uniform drought. Numbers of juvenile and male nematodes in soil were 6.5 times higher under local drought than under non-drought after 37 days. Nematodes did not survive in soil under uniform drought. Most of the eggs recovered on each date, from roots under local and non-drought, hatched within 35 days. Sixteen days of uniform drought reduced cumulative egg hatch to 51%, and almost no eggs hatched after 23 and 37 days of uniform drought. Thus, the response of T. semipenetrans to dry soil is fundamentally different, depending on whether all or part of the rhizosphere experiences drought. These data and field observations suggest that hydraulic lift via the root xylem may prolong the activity of some nematodes and possibly other rhizosphere-inhabiting organisms in dry soil.
PMCID: PMC2619702  PMID: 19277154
carbohydrate; citrus; citrus nematode; ecology; drought; hydraulic lift; soil moisture; survival; Tylenchulus semipenetrans
14.  Spatial Patterns of Belonolaimus spp. Among and Within Citrus Orchards on Florida's Central Ridge 
Journal of Nematology  1996;28(3):352-359.
A survey was initiated to determine the incidence of Belonolaimus spp. (sting nematodes) in citrus orchards in the central ridge region of Florida, following widespread damage by these nematodes to young trees replanted after freezing weather in 1989-90. Sting nematodes were detected in 50% of 210 samples and in 64% of 84 orchards surveyed. More orchards in Polk County were infested with sting nematodes (82%) than in counties to the north (36%) or south (48%). Principal component analysis of morphometric data separated six of seven sting nematode populations in northeastern Polk County from six populations in adjacent regions. Stylet:tail ratio for nematodes in northeastern Polk County tend to be > 1.0 and were ≪ 1.0 for all other populations. Patchiness of nematodes within an orchard was associated with stunted trees (23% smaller), reduced root mass density (25% lower), and low fruit yield (57% reduction). Soil texture did not vary among trees of different size in the orchard, but soil water potential between irrigation events was highest beneath small trees with low root mass density. Results of the survey indicate that the incidence of sting nematodes in orchards on the central ridge is much higher than previously estimated and that sting nematodes can cause substantial damage in replanted orchards. Further research is needed to evaluate the significance of sting nematode population variability and its relationship to citrus crop loss in Florida.
PMCID: PMC2619698  PMID: 19277153
Belonolaimus longicaudatus; citrus; crop loss assessment; ecology; nematode; nematode survey; soil moisture; spatial distribution; spatial pattern; sting nematode
15.  Spatial Patterns of Entomopathogenic Nematodes in Microcosms: Implications for Laboratory Experiments 
Journal of Nematology  1996;28(2):252-258.
Laboratory microcosms were used to: i) measure the effects of soil moisture on survival of Steinernema riobravis and ii) investigate the suitability of using microcosms to study motility and survival of these nematodes. Nematodes recovered from soil contained in petri dishes declined by more than 95% during 7 days, whereas nematodes recovered from the inner surfaces of dishes increased 35-fold. After 7 days in dishes, >20 times as many nematodes were recovered from dish surfaces than from soil. Nematodes exhibited a negative geotropism; greater numbers of nematodes were recovered from the lid surfaces than from the surfaces of dishes. Survivorship of nematodes in soil in plastic centrifuge tubes was somewhat greater than in petri dishes, and fewer nematodes ascended above the soil line in tubes than dishes. Downward migration of nematodes was inversely related to soil column diameter, possibly due to relatively unimpeded movement along container surfaces. An assay was developed by which nematodes were rinsed from the inner surfaces of centrifuge tubes into the soil. The resulting slurry was then processed on Baermann trays to recover motile nematodes. Nematode survival in soil in centrifuge tubes was higher at soil moistures between 2-4% than at lower (0.5-1.0%) and higher (4.0-12.0%) moisture levels. Survival of S. riobravis may be enhanced by quiescence induced by moisture deficits.
PMCID: PMC2619690  PMID: 19277142
entomopathogenic nematode; spatial distribution; soil moisture; Steinernema riobravis; survival
16.  Estimating Sample Size and Persistence of Entomogenous Nematodes in Sandy Soils and Their Efficacy Against the Larvae of Diaprepes abbreviatus in Florida 
Journal of Nematology  1996;28(1):56-67.
In two studies to estimate sampling requirements for entomogenous nematodes in the field, highest persistence of Heterorhabditis bacteriophora after application occurred beneath the canopies of mature citrus trees. Nematode persistence declined with distance from the center-line of the tree row toward the row-middles. Immediately after nematode application to soil, 32 samples (15 cm deep, 2.5-cm diameter) beneath a single tree were required to derive 95% confidence intervals that were within 40% of mean nematode population density. The estimated probability of measuring the mean density within 40%, using 32 samples, declined to 88% at 2 days post-application and to 76% at 7 days. The persistence in soil of Steinernema carpocapsae, S. riobravis, and two formulations containing H. bacteriophora and their efficacy against the larvae of Diaprepes abbreviatus were compared in a grove of 4-year-old citrus trees. Within 6 days, the recovered population densities of all nematodes declined to <5% of levels on day 0. The recovery of H. bacteriophora during the first 2 weeks was lower than that of the other two species. Steinemema riobravis and both formulations of H. bacteriophora reduced recovery of D. abbreviatus by more than 90% and 50%, respectively. Steinernema carpocapsae did not affect population levels of the insect.
PMCID: PMC2619672  PMID: 19277346
control; Diaprepes abbreviatus; efficacy; entomopathogenic nematode; Heterorhabditis bacteriophora; sampling; Steinernema riobravis; survival
17.  Sampling Citrus Fibrous Roots and Tylenchulus semipenetrans 
Journal of Nematology  1994;26(4):442-451.
Sampling precision was investigated for Tylenchulus semipenetrans juveniles and males in soil and females from roots and for citrus fibrous root mass density. For the case of two composite samples of 15 cores each, counts of juvenile and male nematodes were estimated to be within 40% of μ, at P < 0.06 (α) in orchards where x̄ > 1,500 nematodes/100 cm³ soil. A similar level of α was estimated for measurements of fibrous root mass density, but at a precision level of 25% of μ. Densities of female nematodes were estimated with less precision than juveniles and males. Precision estimates from a general sample plan derived from Taylor's Power Law were in good agreement with estimates from individual orchards. Two aspects involved in deriving sampling plans for management advisory purposes were investigated. A minimum of five to six preliminary samples were required to appreciably reduce bias toward underestimation of σ. The use of a Student's t value rather than a standard normal deviate in formulae to estimate sample size increased the estimates by an average of three units. Cases in which the use of z rather than Student's t is appropriate for these formulae are discussed.
PMCID: PMC2619518  PMID: 19279914
citrus nematode; sampling; Taylor's Power Law; Tylenchulus semipenetrans
18.  Damage Potential and Reproduction of Belonolaimus longicaudatus and Hoplolaimus galeatus on Alyceclover 
Journal of Nematology  1992;24(3):438-441.
Alyceclover (Alysicarpus spp.) is an annual, high-quality leguminous forage, suitable for production under tropical and subtropical climates where the husbandry of conventional leguminous forages, Trifolium spp., is uneconomical. The damage potential and reproduction of Belonolairaus longicaudatus and Hoplolaimus galeatus on alyceclover were studied under greenhouse conditions, using sand and sandy clay loam soil materials, respectively. Both nematode species reproduced on alyceclover, but only B. longicaudatus was pathogenic. Symptoms of B. longicaudatus damage were suppression of shoot yield, limited root system, stunting, incipient wilting, and occasional seedling mortality. In one experiment, the threshold-damage density was three nematodes/100 cm³ sand, whereas in the other experiment it was zero nematodes.
PMCID: PMC2619285  PMID: 19283020
Alysicarpus spp.; damage threshold; lance nematode; leguminous forage; nematode; sting nematode; susceptible host; tolerant host
19.  Leaching Soluble Salts Increases Population Densities of Tylenchulus semipenetrans 
Journal of Nematology  1992;24(1):103-108.
The effect of salinity on population densities of Tylenchulus semipenetrans was measured on 3-month-old salt-tolerant Rangpur lime growing on either loamy sand, sand, or organic mix and on 4-month-old salt-sensitive Sweet lime in organic mix. Salinity treatments were initiated by watering daily with 25 mol/m³ NaCl + 3.3 mol/m³ CaCl₂ for 3 days and every other day with 50 mol/m³ NaC1 + 6.6 mol/m³ CaC1₂ for one week, with no salt (NS) treatments as controls. Salinity was discontinued in one treatment (DS) by leaching with tap water prior to inoculation with nematodes, whereas the continuous salinity (CS) treatment remained unchanged. Overall, in Rangpur lime organic soil supported the highest population densities of T. semipenetrans, followed by loamy sand and sand. The DS treatment resulted in the highest (P ≤ 0.05) mean population densities of T. semipenetrans in the three soil types. Similarly, the DS treatment in Sweet lime resulted in the highest (P ≤ 0.05) nematode populations. The DS treatment predisposed citrus to nematode infection through accumulated salt stress, whereas leaching soluble salt in soil solution offered nematodes a suitable nonosmotic habitat. Nematode females under the DS treatment also had the highest (P ≤ 0.05) fecundity.
PMCID: PMC2619237  PMID: 19283210
Citrus limettioides; citrus nematode; citrus reticulata; electrical conductivity; nematode; Rangpur lime; salinity; soil type; Sweet lime; pH; Tylenchulus semipenetrans
20.  Application of Taylor's Power Law to Sample Statistics of Tylenchulus semipenetrans in Florida Citrus 
Journal of Nematology  1989;21(4S):707-711.
Taylor's Power Law was fit to Tylenchulus semipenetrans population data obtained from individual trees in a survey of 50 Florida citrus orchards (geographic survey) and to data from individual trees within a single orchard collected at regular intervals for 2 years (temporal survey). No significant differences were detected between slope or intercept values when log variance was regressed against log mean for the geographic and temporal data sets. The geographic survey was divided into two subsets of data according to the perceived size of patches of T. semipenetrans. Subsets consisted of orchards which appeared to have numerous small patches of trees infected by the nematode (small patch) and orchards in which most of the trees were infected (large patch). The slope value for the orchards with smaller patches of nematodes was different (P ≤ 0.05) from that from large-patch orchards. Assuming mean nematode levels of 1,000 juveniles and males/100cm³ soil, sample sizes (predicted standard error to mean ratio = 0.20) estimated from the relationships of variances to means were 12 trees in the geographic survey and 11 trees in the temporal. Omission of the small-patch data from the geographic survey resulted in a 17% reduction in optimum sample size. Sample size in sporadically infested orchards was estimated to be 69 trees. A data transformation of x0.23 was calculated from parameters of Taylor's Power Law fit to the survey data.
PMCID: PMC2618982  PMID: 19287677
citrus; citrus nematode; population distribution; sampling; Taylor's Power Law; Tylenchulus semipenetrans
21.  Effect of Fenamiphos Placement on Tylenchulus semipenetrans and Yield in a Florida Citrus Orchard 
Journal of Nematology  1989;21(4S):703-706.
Grapefruit trees on sour orange rootstock on the east coast of Florida were treated with 22.3 kg a.i./ha fenamiphos (broadcast equivalent) in 1.52-m bands extending from the dripline to beneath the canopy, in 1.52-m bands extending from the dripline toward the row middle, or left as untreated controls. During the course of the experiment, mean density of feeder roots and Tylenchulus semipenetrans in control plots was 3.8 and 5.8 times greater, respectively, in samples from beneath tree canopies than from 90 cm beyond the dripline on the top of beds. Population densities of T. semipenetrans in each zone (under canopy vs. row middle) were smallest when treatment occurred in that zone. Nematode levels beneath the canopy were 11% of control levels 19 weeks following treatment when fenamiphos was applied beneath the canopy and 52% of controls when treated at the dripline. The number of female T. semipenetrans per gram root weight was also reduced under the canopy by the under-canopy treatment. Fruit yield 5 months following nematicide application was not affected by treatment. Percentage change in yield between that harvest and a harvest 16 months after treatment was + 17% in the under-canopy treatment, - 1% in the dripline treatment, and - 17% in the untreated controls.
PMCID: PMC2618980  PMID: 19287676
chemical control; citrus; citrus nematode; fenamiphos; Tylenchulus semipenetrans

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