Nonpreference Among Gerbera Cultivars by the Leafminer Liriomyza trifolii (Agromyzidae: Diptera)

Significance to the Nursery industry

Gerbera daisies are the third most preferred cut flowers in the world, and increasing in demand in the United States. The lack of cost-effective options to control the complex of primary and secondary pests, however, impedes development of a sustainable production system. Anecdotal evidence indicated variable infestation among gerbera cultivars by the primary pest leafminer, Liriomyza trifolii. A range in susceptibility among 60 cultivars was observed, suggesting that early and heavily infested plants could serve as early indicator plants, while those that were initially less preferred may provide some benefit in an IPM program. Gerberas ‘Jaguar Pink’, ‘Jaguar Rose Deep’, ‘Jaguar Salmon Pastel’, and ‘Revolution Spring Pastel’ were the least damaged initially. All cultivars evaluated, however, eventually became equally damaged when in the presence of high populations of leafminers for five weeks.

Introduction

The primary pests affecting greenhouse gerberas are serpentine leafminers, Liriomyza trifolii (Burgess) (Diptera: Agromyzidae), which have a wide distribution and attack more than 400 species (14) of plants including vegetables and ornamentals. The larvae feed on the palisade mesophyll (13) and decrease photosynthesis and yield, directly affecting the marketable produce. Rigorous and extended use of pesticides has rendered leafminers resistant to almost all chemistries (7). Leafminers are also protected from chemicals by being concealed within the leaves in their larval stages. Successful biocontrol has been achieved using augmentative releases of parasitoids. This has, however, been effective in areas only where disruptive use of chemicals have been avoided (8).

The influx of secondary pests like mites, thrips, whiteflies, aphids, and pathogens causing powdery mildew through the season necessitate pesticide sprays, which in turn, kill the leafminer parasitoids. Insecticide toxicology assays demonstrated that many of the commonly used pesticides (against secondary pests) cause high mortality in beneficial arthropods (leafminer parasitoid Diglyphus isaea (Walker) and the predatory mite Neoseiulus californicus (McGregor)) and hence disrupt effective pest management (1). While pesticides are not effective against leafminers, they certainly are detrimental to the effective buildup of natural enemy populations. Host plant resistance could avoid the pest, reducing the need for chemical intervention.

Host plant resistance studies in vegetables have identified effective mechanisms against leafminers. The narrow leaf architecture in celery (15), trichomes and acyl sugars (within the trichomes) in wild tomatoes (5), and jasmonic acid sprays in celery (3) have all successfully reduced leafminer damage/host feeding. However, similar studies in ornamentals or cut flowers are lacking. Resistance could be an innate function of the plant through the chemical contents within the leaf (3), or a function of the toughness of leaf as found to deter lace bugs (10). Even partial resistance could supplement biological control and work synergistically to control leafminer pests (17).

In this unique system, while pesticides work against secondary pests, they disrupt biological control of the primary pest. IPM can provide an effective solution for gerberas. Finding a successful host plant resistance mechanism would assist in designing an IPM protocol. A successful IPM program would control leafminers, the primary pest, through host plant resistance, natural enemies, or a combination of both, and utilize pesticides compatible with biological control to manage the secondary pests and pathogens.

Materials and Methods

Plant material. Seeds of 60 gerbera cultivars (Gerbera jamesonii, Ball® horticultural company, West Chicago, IL, see Table 1) were germinated in a commercial facility (Speeding® Inc., Blairsville, GA). Seeds were planted in cell packs (128 cells/tray) filled with Fafard super fine germinating mix (Agawam, MA) and, after being watered lightly, kept in the germination chamber at 23.9C (75F) and 80–100% relative humidity until complete germination was achieved a week later. When plants were well rooted after 7 wks, they were transplanted into larger cell packs (36 cells/tray) and housed in a greenhouse on the UGA-Griffin campus.

Table 1. Gerbera cultivars evaluated for leafminer L. trifolii preference.

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Greenhouse choice study. Sixty gerbera cultivars were evaluated for leafminer feeding or oviposition, and subsequent development in a greenhouse choice study. A randomized complete block design with 10 replications for each of the 60 cultivars was employed in the experiment. Each plant was an experimental unit. All the plants were exposed to high leafminer pressure for 72 hr at a commercial greenhouse and then returned to the UGA-Griffin campus facility. High leafminer pressure was maintained by 2 biweekly introductions, each an excess of 500 L. trifolii captured from other greenhouses on the UGA-Griffin Campus and grower greenhouses in Thomaston, GA. Data collection began 48 hr after relocation to UGA-Griffin campus. Data included the numbers of stings (puncture marks caused by egg laying or feeding by the leafminer) and the number of mines (silver patterns characterized by the lack of chlorophyll due to the feeding and development of the leafminer larva within the leaf) found in a 15 cm² area of each of 3 upper leaves on the plant (non-destructive sampling). Data were collected weekly on each of the 600 experimental units from May 11 to June 15, 2011. Age of larvae was not assessed during the study.

Penetrometer study. From the results of the greenhouse experiments, 15 cultivars were selected from among 4 categories: high number of stings and mines (cultivar #2, 53, 28, 39), medium number of stings and high number of mines (cultivar #40, 49, 35), high number of stings and low number of mines (cultivar #16, 56), low number of stings and mines (cultivar #5, 7, 30, 50, 55, 57). L. trifolii oviposition is exclusively through the dorsal side of the leaf while other leafminer species use a combination of dorsal and ventral side or exclusively one side also (2, 11, 12). Using a penetrometer force gauge (Chatillon DFX-010-NIST Digital Force Gauge), the force required (in newtons) to penetrate the dorsal side of the leaf was assessed. Ten observations each from 3 similarly aged leaves for each cultivar were taken, equaling 30 observations for each cultivar. Each leaf was placed on a stage attached to the force gauge and the pointed portion of the instrument was lowered according to prescribed operating procedures between leaf veins and observations recorded.

Statistical analyses. Data were subjected to analysis of variance (ANOVA) using the general linear model procedure (SAS Institute 2003, Cary, NC). Means in both studies were separated using Tukey's HSD test at α = 0.05. Data from the penetrometer study were further subjected to a correlation analysis using PROC CORR (SAS Institute 2003, Cary, NC) to determine if leaf damage had a correlation with leaf toughness or lack thereof.

Results and Discussion

Greenhouse choice study. Even though mines in several plants were absent during the first week, all plants in the study sustained oviposition or feeding punctures at that point (Tables 2 and 3). Numbers of punctures and mines varied by cultivar, but were not always consistent from week to week. Trends were identified indicating differential susceptibility among cultivars. While no cultivars were immune to L. trifolii, ‘Gerbera Jaguar Pink’ (cultivar #5), ‘Gerbera Jaguar Rose Deep’ (cultivar #7), ‘Gerbera Jaguar Salmon Pastel’ (cultivar #9) and ‘Gerbera Revolution Spring Pastels’ (cultivar #57), consistently showed less damage (Table 4). Sustained exposure to high populations of leafminers rendered plants equally damaged by the sixth week when there were no more significant differences in cultivar damage (F values range= 1.33–3.75, df = 59, 599, p values range = < 0.0001–0.059, Tables 2, 3).

Table 2. Mean ± SE number of L. trifolii oviposition and feeding leaf punctures per gerbera plant by cultivar.

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Table 3. Mean ± SE number of L. trifolii mines per gerbera plant by cultivar (n = 10)

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Table 4. Gerbera cultivars highly preferred by the leafminer L. tri-folii with > 80% of highest damage on at least 2 observation dates.

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While cultivar groups of ‘Gerbera Jaguar’ and ‘Gerbera Revolution’ showed potential for lower leafminer preferences, the non-preference did not extend to all color variants in the group. ‘Gerbera Jaguar Rose Deep’ (cultivar #7) was among cultivars that had least damage while ‘Gerbera Jaguar Fire Dark Eye’ (cultivar #2) sustained consistently high damage. While ‘Gerbera Revolution Spring Pastel’ (cultivar #57) showed lower damage, ‘Gerbera Revolution Yellow’ (cultivar #59) and ‘Gerbera Mega Revolution Yellow’ (cultivar #49) sustained heavier leafminer damage.

The mine damage values for the cultivar lines averaged across the six observation dates (Table 5) (f = 4.21; df = 5, 169; p value = 0.0010) identified the cultivar lines ‘Gerbera Revolution’ and ‘Gerbera Festival Mini’ as having significantly less mine damage overall. Cultivar lines ‘Gerbera Jaguar’, ‘Gerbera Royal’, ‘Gerbera Festival’, and ‘Gerbera Mega Revolution’ had significantly higher damages and were not significantly different among them.

Table 5. Mean ± SE of L. trifolii mines on cultivar lines across six observation dates.

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Penetrometer study. Cultivars showed significant differences in the force required to penetrate the dorsal surface of the leaves (f = 13.68; df = 14, 449; p value < 0.0001) (Fig. 1). However, the force required to penetrate the surface was not consistent with the preference or non-preference of leafminer damage from the correlation analysis (R = 0.0032; P = 0.4948). Data from leafminer non-preferred cultivars like ‘Gerbera Revolution Scarlet Dark Eye’ (cultivar #56), ‘Gerbera Festival White Shade’ (cultivar #30), and leafminer preferred ‘Gerbera Festival Spider Salmon Eye’ (cultivar #40) corresponded with the force required to penetrate the surface. A higher force to penetrate the surface in non-preferred cultivars and, less force required to penetrate the surface in highly preferred ones.

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However, leafminer preferred cultivars like ‘Gerbera Festival Semi DB Yellow’ (cultivar #39), ‘Gerbera Festival Mini Yellow’ (cultivar #35), and non-preferred cultivars like ‘Gerbera Royal Semi DB Pink Dark Eye’ (cultivar #16) and ‘Gerbera Jaguar Rose Deep’ (cultivar #7) inversely corresponded with the force required to penetrate the leaf surface. Preferred cultivars in this situation required higher force to penetrate, while non-preferred cultivars required less force to penetrate. Hence in general, the preference or non-preference of leafminer attack did not align with the force required to penetrate the dorsal surface of leaf.

Anecdotal evidence that yellow cultivars attract more leafminers than other colors is consistent with the fact that yellow sticky cards are best in attracting leafminers (16) and an effective tool in sampling (6, 9). Our experiment was conducted on plants without flowers to assess foliar-based potential for avoidance or antibiosis. Observations of the different cultivars in our study showed very little variation within the spectrum of being pubescent or glabrous, though the texture seemed to have some difference, and hence the investigation into leaf toughness as a factor to deter leafminer oviposition and resultant damage.

Punctures and mines did not correspond in this study. Punctures are a function of either feeding behavior or oviposition, and feeding frequency has been shown to ‘not predict’ leafminer preference or damage (4). Punctures can hence only be an indicator of leafminer preference while the best measure of resistance is a lower number of mines. There was no consistent preference by leafminers for yellow cultivars. While there were some yellow cultivars that were among the most damaged, all yellow cultivars were not heavily damaged. There were pink and orange cultivars that sustained heavier damage than certain yellow cultivars, but no yellow cultivars ranked very low in number of punctures and mines (Tables 5, 6). Also, innate mechanisms might be expected to be a trait of a certain cultivar group. With 10–12 cultivars coming under the same general cultivar group, we expected that they would be armed with the same defense mechanism and hence remain together in being preferred by leafminers or sustaining damage. The results however didn't agree with that. For example, while ‘Gerbera Jaguar Rose Deep’ (cultivar #7) and ‘Gerbera Jaguar Pink’ (cultivar #5) showed low levels of damage, ‘Gerbera Jaguar Fire Dark Eye’ (cultivar #2) sustained heavy leafminer damage. ‘Gerbera Jaguar’ (cultivars #5, 7, and 9) and ‘Gerbera Revolution’ (cultivar #57) were two cultivar groups where at least a few of them showed reduced leafminer damage (Table 6).

Table 6. Gerbera cultivars least preferred by the leafminer L. trifolii with < 20% of highest damage on at least 2 observation dates.

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While more cultivars in the Gerbera Jaguar line consistently showed low mine damage on individual observation dates (Table 6), cultivar lines (including all cultivars in the cultivar group) ‘Gerbera Revolution’ and ‘Gerbera Festival Mini’ showed less mine damage across the duration of the experiment (Table 5). There might be some innate quality in these lines that could help in resistance breeding in gerberas.

Leaf toughness was not a predictor of leafminer preference. Color variants of the cultivar group ‘Gerbera Revolution’ varied in the force required to penetrate the dorsal leaf surface and did not correspond with leafminer preferences from the greenhouse choice study. ‘Gerbera Revolution Scarlet Dark Eye’ (cultivar #56) required high force to penetrate the surface, and was one of the cultivars with lower number of mines developing in spite of high number of stings. ‘Gerbera Revolution Red Shade Dark Eye’ (cultivar #53) was among the cultivars that sustained high leafminer damage, but the force required to penetrate the surface was intermediate but higher than that required to penetrate ‘Gerbera Revolution Pastel range Dark Eye’ (cultivar #55), which sustained low leafminer damage.

Related species like G. ambigua (Cass.) Schultz. Bip., G. crocea (L.) Kuntze, G. linnaei Cass., G. serrata (Thunb.) Druce, G. tomentosa DC, G. viridifolia (DC.) Sch. Bip., and G. wrightii Harv. might provide sources of resistant germplasm. Alternatively jasmonic acid sprays that were successful in celery (3) could be explored. The search for an effective host plant resistance mechanism will have to continue for the reason that it can tremendously help the IPM program that will then result. The leafminer L. trifolii has been a successful cosmopolitan pest and will continue to drive pest management in gerbera production for years to come. Our answer to that would depend on finding successful components that could be weaved into an integrated program to control the suite of pests in this system.