Leafminer Parasitoid Research Articles

Host-size-dependent sex ratio theory and improving mass-reared parasitoid sex ratios

Although an effective parasitoid of agromyzid leafminers, Diglyphus isaea (Walker) (Hymenoptera: Eulophidae) is an expensive biological control agent in terms of production costs. In part, these costs arise from the production of male-biased offspring sex ratios. Here, we present a mass-rearing technique that will increase the proportion of females produced and reduce the need for frequent releases in biocontrol programs. By presenting female D. isaea groups of sequentially larger leafminer hosts to attack, we are able to generate progressively more female-biased sex ratios. After three days of providing increasingly larger hosts, we were able to reduce the sex ratios produced by individual females from 57% male to 36% male; sex ratios produced by groups of females dropped from 64% male to 45% male. Several attributes of D. isaea sex allocation allow us to manipulate sex allocation behavior. First, D. isaea is a solitary idiobiont; resources available to each offspring are present at the time of attack allowing the ovipositing female to accurately assess host quality. Host size positively affects both male and female wasps. Females laid more daughters in larger hosts and more sons in smaller hosts. We show that the observed relationship between host size and offspring sex ratio is due to maternal sex allocation decisions rather than differential mortality. Furthermore, assessment of the size threshold was relative to prior host encounters rather than an absolute assessment. Our simple memory model suggests that while females are influenced most strongly by recent encounters, females also base their assessment of the host-size threshold on prior host encounters.

Effect of temperature on life history of Cirrospilus vittatus (Hymenoptera: Eulophidae), an ectoparasitoid of Phyllocnistis citrella (Lepidoptera: Gracillariidae).

Cirrospilus vittatus is a generalist parasitoid detected on the invading Phyllocnistis citrella 1 yr after the introduction of this pest into Spain in 1993. In this study, the influence of temperature on parasitoid development, survival, and some selected life history parameters was determined. Development times shortened as the temperature increased from 15 to 30 degrees C, but increased between 30 and 35 degrees C. Larval development times varied the greatest over the range of temperatures, whereas egg development varied the least. The estimated upper and lower development thresholds were 38.2 and 8.2 degrees C, respectively, and the maximal developmental rate (8.75 d(-1)) occurred at 31.5 degrees C. The thermal constant was 275.1 +/- 4.6 degree-days. Cirrospilus vittatus appeared to be a synovigenic species. Mean fecundity at 25 degrees C was 39.17 eggs per female, and the oviposition rate fluctuated around five eggs per day. Superparasitism was quite common (42.8%), but fertility was high (85.6%). Immature C. vittatus survival was 58.1%. From these results, an intrinsic rate of increase of 0.126 females per female per day was estimated. Although under typical Mediterranean climatic conditions, development of C. vittatus could continue throughout the year, its reproductive fitness at 25 degrees C is lower than other leafminer parasitoids attacking P. citrella in Spain. These results could account for the progressive displacement observed in field populations occurring between C. vittatus and the predominant indigenous parasitoids of P. citrella, Cirrospilus sp. near lyncus.

Egg-pupal and larval-pupal parasitism in the parasitoid Gronotoma micromorpha (Hymenoptera: Eucoilidae).

I examined the effects of host age at oviposition, from 0 to 4 days (egg to mature larva), on emergence rate and developmental period of the leafminer parasitoid Gronotoma micromorpha (Perkins) (Hymenoptera: Eucoilidae) under laboratory conditions in the host Liriomyza trifolii (Burgess) (Diptera: Agromyzidae). No significant difference was found in the emergence rates of G. micromorpha among the host ages examined. However, the developmental period of G. micromorpha was significantly shorter when ovipositing into 3- or 4-d-old L. trifolii. The occurrence of thelytokous parthenogenesis in G. micromorpha was confirmed. The results show that G. micromorpha is an egg-pupal and larval-pupal parasitoid, utilizing a wide range of host stages in which oviposition can occur and progeny can complete development.

Plant-Derived Semiochemicals as Contact Host Location Stimuli for a Parasitoid of Leafminers

We elucidated the source of chemical cues in a system where the host is concealed and the parasitoid has no direct contact with the host larvae or its frass. Behavioral bioassays with Pholetesor bicolor, a larval parasitoid of the apple leafminer, Phyllonorycter pomonella, showed that the herbivore-damaged leaf epidermis (mine) elicited ovipositional probing of parasitoid females. Probing on larvae or frass was seldom observed. Hexane extracts of mines elicited the same ovipositional probing behavior while no response was observed with hexane extracts of larvae or frass or with methanol and diethyl ether extracts. In addition, gas chromatographic analyses showed qualitatively and quantitatively different profiles of these three components of the host-plant complex. By far the highest quantities and also the highest number of compounds was recovered from mine extracts. Identified compounds in the mine included six alkanes (n-C27 to n-C33) and squalene (C30H50). A synthetic blend of the seven compounds was slightly less active in biotests than the equivalent natural blend, as shown by a time delay in female response. We conclude that this leafminer parasitoid does not rely on host-derived kairomones but instead uses plant-derived semiochemicals for host location and ovipositional probing behavior.

Volumes of petroleum spray oil required for control of Phyllocnistis citrella Stainton (Lepidoptera: Gracillariidae) in mature citrus orchards

Studies on the relationship between volume of spray and suppression of citrus leafminer (Phyllocnistis citrella) oviposition by petroleum spray oil on 4 m‐high mature orange trees showed a negative exponential relationship between spray volume and the number of mines per leaf. Significant reductions in the number of mines per leaf compared to unsprayed trees was achieved at spray volumes of ≥ 3300 L/ha using oscillating boom and at ≥ 3200 L/ha using rotary atomiser sprayers. However, improvements in efficacy at volumes over 3200–3300 L/ha were not significant and so of little practical value. The optimal spray volumes for citrus leafminer control are therefore suggested to be 3000–3500 L/ha. No significant difference in effectiveness was found between the oscillating boom at 3300 L/ha and a rotary atomiser at 3200 L/ha. The effect of oil spray on the citrus leafminer parasitoid Semielacher petiolatus (Girault) (Hymenoptera: Eulophidae) was inconsistent. Improved droplet deposition and coalescence may enhance the coverage of new growths and increase the efficacy of oil spray for protection of plants from oviposition.

Effect of Reduced Insecticide and Fungicide Use on Parasitism of Leafminers ( Phyllonorycter spp.) (Lepidoptera: Gracillariidae) in Commercial Apple Orchards

Development of alternative controls (i.e., 2nd-level insect pest management [IPM] methods) for apple maggot | Rhagoletis pomonella (Walsh) ] that reduce pesticide use is in progress. The current project was undertaken to see if such controls would better conserve natural enemies of pest leafminers (Gracillariidae, Phyllonorycter spp.) when applied over a large physical scale, as compared with results in earlier studies with smaller plots. Second-level IPM in apple, Malus pumilla Miller, orchards may consist of substitution of either use of red sticky spheres in border rows or border-row pesticide applications for control of apple maggots rather than cover sprays of insecticides over entire orchard blocks. We previously established that 2nd-level IPM increased parasitism rates in tissue-feeding larvae of 2nd generation Phyllonorycter spp. under trap but not border-row spray management, when tested at the scale of 0.4-ha plots that were part of larger blocks under 1st-level IPM. We hypothesized that conservation of leafminer parasitoids would improve when 2nd-level IPM was applied to entire orchard blocks (1.6-3.6 ha) because conflicts with pesticides used in adjoining areas (drift into untreated areas and parasitoid movement into treated areas) would decrease. Results of our test did not support this hypothesis. We determined that benefits of 2nd-level IPM were the same in 1.6-3.6-ha blocks as in 0.4-ha plots. In both types of plots, parasitism increased only when trapping. not border sprays, was used to manage apple maggot, and benefits occurred only in the 2nd host generation. No carryover of benefit to the 3rd generation in the same year, or to the 1st generation of the following year, could be detected. Elimination of fungicide use (in disease-resistant blocks) increased leafminer parasitism. Although most parasitism was due to eulophid parasitoids, the proportion of total parasitism caused by braconids was greatest under 2nd-level IPM, suggesting that reduced pesticide use was especially beneficial to this parasitoid group. These findings suggest that 2nd-level IPM methods for apple maggot control have only a limited ability to conserve leafminer parasitoids. regardless of plot size. Furthermore, our findings suggest use of fungicides on apple orchards may be harmful to leafminer parasitoids.

Leaf Vibrations and Air Movements in a Leafminer–Parasitoid System

Abstract This paper analyzes the vibratory environment of the leafminerPhyllonorycter malella(Ger.) (Lep. Gracillariidae) and its parasitoidSympiesis sericeicornisNees (Hym. Eulophidae). Previous studies established that both the host and the parasitoid not only produce but also use leaf vibrations: the former in order to escape ovipositor stings, the latter as a physical cue in the foraging process. First we characterize vibration patterns produced by simulated wind and rain and discuss the influence of these background vibrations on the host–parasitoid interaction. Second, we present a method of producing leaf vibration patterns of high repeatability. This technique allows us to characterize the influence of the leaf as modifier of vibratory signals. We discuss howS. sericeicorniscould use such spatially variable vibratory information for between-mine foraging. Finally, a combined laser Doppler vibrometry–laser Doppler anemometry study revealed that leaf vibrations induce air movements in their immediate surroundings with characteristic temporal and spatial structures. We discuss if and how host-related information contained in the air particle displacement can be used by parasitoids.

Vibration–mediated interactions in a host–parasitoid system

The aim of this paper was to obtain behavioral evidence of vibration mediated interactions between the apple tentiform leafminer Phyllonorycter malella (Ger.) (Lepidoptera, Gracillariidae) and its parasitoid Sympiesis sericeicornis Nees (Hymenoptera, Eulophidae). The experimental set–up allowed the simultaneous recording on video film of both the parasitoids and the hosts behavior, thus enabling us to contrast their respective responses to the leaf vibrations produced by the other party. We analysed the one step transition probabilties from one behavioral state to the following. Active larval movements had a marked influence on the parasitoid's behavior, while feeding and still had no detectable effect. We found no evidence for vibrotaxis on the part of the parasitoid. While parasitoid searching behavior on the leaf surface did not seem to alter the leafminers behavior, ovipositor insertions triggered a characteristic avoidance response. The described interactions are discussed in the context of the ‘princess and monster’ model developed in search and game theory.

Arthropod pest and natural enemy abundance under second-level versus first-level integrated pest management practices in apple orchards: a 4-year study

The authors conceive of second-level integrated pest management (IPM) in apple orchards as involving integration of multiple management tactics across all classes of pests. From 1991–1994, a second-level IPM pilot project was carried out in six commercial Massachusetts apple orchard blocks (2–4 ha) in which pest and natural enemy populations and injuries to fruit were compared with those in adjacent blocks receiving first-level IPM practices (considered to be integration of tactics within a single class of pests). The approach to second-level IPM was use of chemically based tactics for arthropod, disease and weed control during the first part of the growing season (up to mid-June for arthropods) and thereafter use of only biologically based tactics (cultural, behavioral and biological control methods). This article deals with findings on arthropod management. As expected, total injury to fruit by insects causing damage before mid-June did not differ between second-level (4.7%) and first-level (4.8%) IPM blocks. Total injury to fruit by insects active after mid-June averaged about the same (0.5%) in both types of blocks in 1991 and 1992, but in 1993 and 1994 it averaged more in second-level blocks (4.8%) than first-level blocks (1.9%). This was particularly true for Grapholitha prunivora Walker and leafrollers and less so for Cydia pomonella (L.) and Rhagoletis pomonella (Walsh). Among foliar pest arthropods and their natural enemies, populations of aphids and aphid predators and populations of spider mites and mite predators averaged about the same in both types of blocks. Populations of leafminers averaged lower and parasitoids of leafminers averaged greater in second-level blocks. Populations of leafhoppers averaged greater in second-level blocks. Pesticide use against fruit-damaging insects averaged 37% less in second-level than in first-level blocks, but against foliar-damaging arthropods, it was not less. Some refinements of second-level IPM tactics for arthropod control are needed before second-level IPM practices can be recommended broadly to commercial growers in New England as an economical and reliable alternative to first-level IPM.

Demography of the Leafminer ParasitoidGanaspidium utilisBeardsley (Hymenoptera: Eucoilidae) at Different Temperatures

Abstract Demographic parameters, reproductive pattern, and heterogeneity for the leafminer parasitoid Ganaspidium utilis Beardsley (Hymenoptera: Eucoilidae) were determined in the laboratory at 16, 27, and 32°C using Liriomyza trifolii (Burgess) with “Henderson” bush lima beans as the host. Development and progeny production did not occur at 16°C. Mean developmental time was significantly shorter (13.2 days) at 32°C than at 27°C (18.4 days). Preadult cumulative survival rates at 27°C (62%) and 32°C (43%) were significantly different. Male and female longevities were similar. Adult G. utilis lived a maximum of 23 days at 16°C, 13 days at 27°C, and 8 days at 32°C. Total mean lifetime progeny production per female G. utilis ranged from 68.50 progeny at 32°C to 115.10 progeny at 27°C. Heaviest progeny production occurred during Days 2 and 3 of a female's life at 32 and 27°C, respectively. Of the total progeny produced, the female percentage ranged from 47 at 27°C to 49 at 32°C. Mean generation time was 15 days at 32°C and 21 days at 27°C. Intrinsic rate of increase varied from 0.19 at 27°C to 0.23 at 32°C. In the stable age distribution, egg percentage was highest (56–58) followed by larval stage (36–37), whereas pupal and adult stages each only represented 3 to 4. Age-by-parity relations demonstrated that timing and magnitude of reproduction were influenced by temperature.

Flexible patch time allocation by the leafminer parasitoid, Opius dimidiatus

Abstract. The ability to use flexible decision rules can be an advantage to parasitoid females searching for patchily‐distributed hosts. In a series of laboratory experiments the hypothesis that Opius dimidiatus, a solitary parasitoid of the chrysanthemum leafminer (Liriomyza trifolii), adjusts the time she allocates to searching for her larval hosts in response to both patch qualities and experiences with hosts was tested by varying such patch parameters as area, presence of host mines and density of host mines, and by allowing ovipositions and encounters with parasitized hosts. Though leaf area was not a factor, the presence of host mines in a leaf did increase the time a female O.dimidiatus spent searching, over time spent on unmined leaves. When host mine density was increased, females responded by increasing their search period in a density‐dependent manner, suggesting a perception of patch quality. Ovipositions in hosts caused females to reset their‘giving‐up time’(GUT), or increase search intensity, by adding an amount of search time that increased with each successive oviposition. Conversely, encounters with parasitized (unsuitable) hosts incremented the GUT, but by an amount that decreased with each successive encounter.

Variation in Susceptibility to Insecticides in the Leafminer Parasitoid Ganaspidium utilis (Hymenoptera: Eucoilidae)

Five populations of a parasitoid of agromyzid leafminers, Ganaspidium utilis Beardsley, were tested for susceptibility to five insecticide . Four field populations were significantly less susceptible than a laboratory population that had not been exposed to insecticides for 20 generations. Compared with the laboratory population, maximum resistance ratios at LC 50 were 3 for methomyl, 2 for oxamyl, 3 for fenvalerate, 12 for permethrin, and 9 for malathion. The most toxic insecticide was malathion, followed by methomyl. oxamyl, permethrin, and fenvalerate. LC 5O s,vere lower than concentrations similar to the recommended field rates for all populations for methomyl, oxamyl, and malathion, but LC 50 s for some populations were higher than the recommended field rates for permethrin and fenvalerate.

Intraspecific size variation in polyphagous parasitoids (Hym.: Parasitica), of leaf miners and its relation to host size

Wing and body lengths of polyphagous parasitoids of leafminers are analyzed in order to understand the relationship between host and parasitoid sizes. A distinct positive relationship was observed: within each parasitoid species, smaller individuals were reared from smaller hosts. There was no difference between idio-and koinobionts in sexual dimorphism, with females being significantly larger than males in both groups.

The influence of humidity on emergence inDacnusa sibiricaTelenga (Hymenoptera: Braconidae)

The effects of four humidities (33, 55, 76 and 93% relative humidity) and four ages (0–1, 2–3, 4–5, 6–7 days) of parasitized Chromatomyia syngenesiae puparia on adult emergence in the leafminer parasitoid Dacnusa sibirica were examined in the laboratory. Parasitized puparia harvested at 0–1 days were susceptible to low humidities resulting in a significantly reduced parasitoid emergence. Aging of the puparia appeared to protect the developing parasitoid from low humidities. Increasing humidity produced a corresponding increase in the longevity of the adult parasitoid.

Sexual Differences in Insecticide Susceptibility and Synergism with Piperonyl Butoxide in the Leafminer Parasitoid Diglyphus begini (Hymenoptera: Eulophidae)

Susceptibility of males and females of the Liriomyza leafminer parasitoid Diglyphus begini (Ashmead) to methomyl, oxamyl, fenvalerate, and permethrin was Compared with laboratory bioassays. For each insecticide and five populations tested, males were more susceptible than females. Differences in LC50s between the sexes ranged from 1.3- to 15.7-fold and were greater in resistant Compared with susceptible populations. Tibia length was significantly less for male than female D. begini. Size differences ranged from 1.1- to 1.2-fold. Piperonyl butoxide synergized oxamyl and fenvalerate in males and females, suggesting that oxidative detoxification was important in both sexes. The addition of piperonyl butoxide to oxamyl affected both sexes similarly. The synergistic effect of piperonyl butoxide with fenvalerate was significantly greater for females than males, suggesting greater oxidative detoxification of fenvalerate in females than males.

Production of Ganaspidium utilis (Hymenoptera: Eucoilidae) for biological control of Liriomyza spp. (Diptera: Agromyzidae)

Abstract A method for rearing the Liriomyza leafminer parasitoid Ganaspidium utilis Beardsley (Hymenoptera: Eucoilidae) is described. ‘Henderson’ bush lima beans, Phaseolus limensis var. limenanus L. H. Bailey, were planted in vermiculite in six 20 × 14 × 35.5-cm2 plastic bags. After 10 to 11 days the plants were exposed to 500 to 600 adult Liriomyza trifolii (Burgess) (Diptera: Agromyzidae) for 24 h and then placed in a holding cage for 4 days at 22°C. Plants containing second instar L. trifolii were exposed to G. utilis for 48 h. Emergence of parasitoids occurred 24 to 33 days after exposure. The number of G. utilis emerging per bag of beans was 403 ± 29 ( X ± SEM ; n = 15) ; 51% of these were females. Recurring cost of production of 5000 parasitoids per day was estimated at $36 for G. utilis compared with $97 for another leafminer parasitoid, Diglyphus begini Ashmead (Hymenoptera: Eulophidae).

Role of volatile infochemicals in foraging behavior of the leafminer parasitoidDacnusa sibirica (Diptera: Agromyzidae)

Previous investigations suggested that the leafminer parasitoid Dacnusa sibirica Telenga does not use a volatile hostrelated infochemical in foraging for hosts. Parasitoids landed with equal frequencies on an uninfested tomato plant and on a tomato plant infested with larvae of the leafminer Liriomyza bryoniae (Kalt.) (Hendrikse et al., 1980). In contrast, we found that volatile infochemicals emitted by uninfested and leafminer-infested tomato plants differently affected the parasitoid 's foraging behavior in a windtunnel. This was obvious from the proportion of wasps flying upwind but not from the proportion of wasps landing on the leaves. Latency time on an uninfested tomato leaflet and proportion of latency time devoted to preflight antennal behavior were influenced by the presence of upwind infested or uninfested tomato leaves. However, these parameters were not affected by odors in the absence of visual plant stimuli. Our data provide a new view on foraging behavior of Dacnusa sibirica.

Oil Treatments for Leafminer and Associated Parasitoids on Snap Beans, 1990

Abstract Four oils and a insecticide-oil treatment were applied on 22 Oct with a prototype electrostatic sprayer (Terronics, Inc., Elwood, Ind.). Beans were planted 31 Aug in double rows on beds with 40 inch centers at the Bruce Church of Arizona, Inc. farm located near Poston, Ariz. Two rows of each variety were planted side by side in the 4 row block. Beans, especially the 04' variety, were heavily infested with leafminers and much defoliation and leaf drop had occurred with the lower leaves prior to the 16 Oct treatment. Plants were very heavily infested with sweetpotato whiteflies, Bemisia tabaci (Gennedius). Plots were 25 ft long by one bed wide and treatments were replicated 4 times in a randomzied complete block design. Plots were sampled on 19 Oct for leafminer parasitoids. Parasitoid complex was comprised of mostly Diglyphus spp., Chrysocharis spp., as well as other similar parasitoids. Other parasitoids also included about 1% Opius and 3% Chrysonotomyia. Three samples were taken per plot. Samples consisted of placing a 8.5 inch × 17 inch × 1.5 inch deep styrofoam food tray between bed rows, shaking the foliage, and counting the parasitic wasps on the trays. Leafminer samples were obtained by leaving 3 trays/plot between rows from 3-8 DAT. Leafminer pupae that had emerged from leaves and collected in trays were counted.

Leafminer and Leafminer Parasitoid Incidence on Selected Weeds in South Florida

The leafininer Liriomyza trifolii Burgess (Diptera: Agromyzidae) is a serious pest of celery in Florida. L. sativae (Blanchard), a morphologically similar species which has many hosts in common with L. trifolii, was once considered a pest of Florida celery but no longer affects this crop (Leibee 1984). Both species are attacked by the same parasitoid complex (Johnson & Hara 1987). L. sativae and L. trifolii occur on many weed hosts in south Florida (Stegmaier 1981); two of those named as hosts of the former, and not of the latter, were castor bean, Ricinus communis L., and sicklepod, Cassia tora L., (Stegmaier 1981). Both occur in the Everglades agricultural area (EAA) of south Florida where the majority of Florida's celery is grown. These weeds, serving as hosts of L. sativae, could act as potential reservoirs for parasitoids which could possibly enhance the biological control of L. tifolii in celery. Dayflower, Commelina diffusa Burm., a weed common in the EAA, was reported as containing significantly more chalcidoid leafminer parasitoids than other weeds sampled (Genung 1981). The only leafminer known to attack dayflower, L. commelinae (Frost), may have parasitoids in common with L. trifolii. In February of 1984 a study was initiated at Everglades Research and Education Center (EREC), Belle Glade, to determine the leafminer species occurring on castor bean, sicklepod, and dayflower and the parasitoids attacking the leafminers on these host plants. The weeds were planted at EREC at two sites, each consisting of three plots per weed species. Plots were 3 m by 3 m and consisted of five rows. Castor bean and sicklepod were thinned to 10 plants per row and dayflower, a prostrate plant grown from transplants, was allowed to cover the entire plot. Sampling was conducted once per week for eight weeks from late May until the third week in July. Three leaves of castor bean and three trifoliates of sicklepod were excised from 10 randomly selected plants per plot. Dayflower was sampled by collecting all foliage from 10 randomly selected 18 cm x 18 cm areas within a plot. Foliage was taken to the laboratory where it was held on wire screen in closed 4-liter cardboard containers. Adult larval parasitoids and leafminer puparia were collected after the foliage had dried. Puparia were held in glass vials until all adult leafminers and larval-pupal parasitoids had emerged. Representative specimens of parasitoid species were identified by E. E. Grissell, A. S. Menke, and M. E. Schauff, Systematic Entomology Laboratory, USDA, Washington, D.C., R. A. Wharton, Department of Entomology, Texas A&M University, College Station, Texas, and C. M. Yoshimoto, Canadian Forestry Service, Department of Environment, Ottawa, Ontario, Canada. Adult leafminer identifications were made by the senior author. No leafminers or parasitoids were reared from sicklepod foliage. Only two active (= those containing living leafminer larvae) mines were found on this weed and neither larva survived to pupation. Four active mines were collected from dayflower and from these were reared an adult L. commelinae and a cynipid pupal parasitoid.

Foraging behaviour of a leafminer parasitoid in the field

Abstract. 1. The searching behaviour of the parasitoid Sympiesis sericeicornis Nees (Hymenoptera, Eulophidae) is analysed under field conditions.2. Females were tracked when flying around the canopy of apple trees infested with the tentiform leafminer Phyllonorycter cydoniella (D. & S.)(Lepidoptera, Gracillariidae) and their behaviour studied at the level of a single mine and at the level of several mines on the same leaf (patch level).3. The presence of mines is detected during flight. The foraging behaviour at the patch level is efficient: the female is able to distinguish the suitable from the unsuitable hosts and handle the suitable hosts first. Not all mines are visited before departure from the leaf and those left unvisited are exclusively mines without suitable hosts. The patch leaving rule is discussed.4. An ethogram of the behaviour on the mine is constructed. Selected behavioural categories are analysed for different combinations of mine content and outcome of the visit to the mine. The assessment of the mine content is done in a differential way, quickly and without mistakes.5. The results are discussed in the context of two environmental factors, wind speed and temperature, which reduce the available time for searching. They are also related to the growing percentage of unsuitable hosts during each host generation. Tentiform mines remain attractive for a long period of time, even after parasitism or emergence of the adult, and their examination reduces the rate of host discovery.