ARTÍCULO ORIGINAL

Relationship between damage on leaves caused by Liriomyza huidobrensis (Diptera, Agromizydae), adults trapped in sticky traps and parasitoids in a commercial crops of Cucurbita maxima var. zapallito (Cucurbitaceae)

 

Bertolaccini, I.¹; Curis, M. C.¹; Lutz, A.¹; Martinez, J. J.²; Favaro, J. C.¹ & Trod, A.¹

¹ Departamento de Producción Vegetal, Facultad de Ciencias Agrarias, Universidad Nacional del Litoral. Kreder 2805, (3080) Esperanza, provincia de Santa Fe. Email: isabelb@fca.unl.edu.ar
² CONICET. Dpto. Ciencias Biológicas. Facultad de Ciencias Exactas y Naturales. Universidad Nacional de La Pampa. Uruguay 151-L6300CLB. Santa Rosa, La Pampa.

Manuscrito recibido el 11 de febrero de 2019
y aceptado para su publicación el 25 de mayo de 2019.

---

ABSTRACT

Agromyzid leafminers cause damages in ornamental and horticultural crops. The objective of this study was to evaluate the number of adults of L. huidobrensis trapped in sticky traps in C. maxima var. zapallito and connect this with the total leaves, leaves damaged and parasitoids at different monitoring dates, and determine the correlation between the number of larvae and parasitoids, according to the number of galleries per leaf. Six traps were placed in a commercial plot, and they were replaced weekly. The total and damaged leaves were recorded weekly in 15 randomly picked plants. Damaged leaves were taken to laboratory where galleries per leaf were counted. Each leaf with a gallery was placed in a Petri dish until leafminer or parasitoid adults emerged. Liriomyza huidobrensis caused damage in in early crop stages. There was correspondence between adult population and damage and number of galleries per leaf with significant differences in the first monitoring date, which was not found with parasitoids.

Key words: Leafminer; Damage; Parasitoids; Summer squash.

ABSTRACT

Relación entre el daño en hojas causado por Liriomyza huidobrensis (Diptera, Agromizydae), los adultos atrapados en trampas pegajosas y los parasitoides en un cultivo comercial de Cucurbita maxima var. zapallito (Cucurbitaceae)

Los agromícidos causan daños en cultivos ornamentales y hortícolas. El objetivo de este estudio fue evaluar el número de adultos de L. huidobrensis en trampas pegajosas ubicadas en un cultivo de C. maxima var. zapallito, y relacionarlo con el total de hojas, hojas dañadas y parasitoides en diferentes fechas de monitoreo, y determinar la correlación entre el número de larvas y de parasitoides, de acuerdo a la cantidad de galerías por hojas. Seis trampas pegajosas fueron colocadas en un lote comercial y reemplazadas semanalmente. En 15 plantas seleccionadas al azar se registró el número total de hojas y el de hojas dañadas. Las hojas dañadas fueron llevadas a laboratorio donde se contó el número de galerías por hoja, y cada una fue colocada en cajas de Petri hasta la emergencia de los adultos del minador o del parasitoide. La población de adultos estuvo en correspondencia con el número de galerías por hoja con diferencias significativas en la primera fecha de monitoreo, pero no con los parasitoides.

Palabras clave: Minadores; Daños; Parasitoides; Zapallito.

---

 

INTRODUCTION

Most agromyzid species exhibit a high level of host specificity restricted to a genus or family, while others are polyphagous ⁽²⁾. Thus, Liriomyza species cause damage during both larval and adult stages. Larvae excavate galleries in leaf parenchyma leaving the epidermis intact ⁽²⁷⁾ on over 365 host plant species in 49 plant families, including ornamental, horticultural crops and weeds ^{(30, 31)}. According to Foba et al. (2015) ⁽⁴⁾ L. huidobrensis (Blanchard) attacks 20 different crops, with differences in geographic distribution, host preferences and other biological characteristics ^{(21, 27)}. In Argentina, it is one of the most polyphagous species, which attacks 9 wild species and 37 crops, and one of them is summer squash, Cucurbita maxima var. zapallito [(Carr.) Millan] ⁽²⁷⁾. Adult females cause lesions with their ovipositor to feed on epidermis exudates ⁽²⁵⁾. Damage decreases the photosynthesis capability, reduces nutrient assimilation, thus causing early leaves fall, and it also has the ability to transmit viruses and facilitate bacteria and fungi penetration ^{(23, 5)}.
Many leafminers are controlled by parasitoids under natural conditions. However, in certain areas, they are a serious pest because natural control is disrupted by insecticide use ^{(15, 16, 9, 20)}. The summer squash is a widespread crop in the area near the city of Santa Fe, and leafminer damage is very important. However, this pest has not been studied. The main objective of this study was to evaluate the number of adults of L. huidobrensis caught in sticky traps placed in a commercial plot of C. maxima var. zapallito, and the damage caused on total leaves. Also, the number of parasitoids was analyzed in relation to the number of galleries per leaf.

MATERIALS AND METHODS

Study site: The study was carried out on "summer squash" crops (cv. Franco, Basso Seed Company, Argentina) in a commercial plot near the city of Santa Fe (31º32 'S; 60º40' O) in the province of Santa Fe, Argentina). The seeding date was July 15th, 2014. The cultural practices were the usual ones for this crop, and only fungicides were applied in this plot -two sprays of sulfur and two of tebuconazole.
Sampling: The total number of leaves damaged by leafminers was recorded weekly in 15 plants randomly selected from 20 days after transplanting (to allow the pest to be installed) until harvest. The damaged leaves were collected and placed in Ziploc® plastic bags and taken to the Agricultural Zoological Laboratory, Facultad de Ciencias Agrarias (Universidad Nacional del Litoral), Santa Fe, Argentina. From each leaf, the number of galleries was counted, and each gallery (with a piece of leaf) was individually placed in a 5-cm-diameter Petri dish with wet cotton and filter paper on the bottom in order to maintain humidity. To capture adults, six 10x25-cm Süsbin® adhesive traps were placed in the crop plot at 50 cm from the ground, two on the north side and four inside the plot. The traps were replaced weekly and taken to laboratory, where the number of leafminer adults was counted using a 30x stereoscopic microscope.
Lab work: the leaves with galleries were taken to a climatic chamber (25 ± 5 ºC, 65 ± % RH, 14:10 L:D). The puparia were reviewed daily until adults of leafminers or endoparasitoids emerged, which were preserved in 1.5 ml Eppendorf® tubes with 70% ethanol until their identification, and labeled by date and plant number. Braconid parasitoids were identified following the key provided by van Achterberg and Salvo (1997) (1).
Data analysis: In order to measure the direct contribution of the independent variable (monitoring dates) and to explain the variability of dependent variables (number of larvae and parasitoids), a path analysis was performed. The correlations between damaged leaves, parasitoids and number of larvae according to number of galleries per leave were analyzed. Adults per sticky trap, total leaves, damaged leaves per plant, galleries per leaf, larvae and parasitoids (dependent variables) related to monitoring date (independent variable) were analyzed by ANOVA. Significant differences were determined by a Tukey test (α<0.01). Results were analyzed with InfoStat ⁽⁶⁾.

RESULTS AND DISCUSSION

Adults collected in sticky traps had a maximum peak in the first sampling (27.8), which showed significant differences with the remaining collecting dates (Table 1). Then, they began to decline until the last week of September, when adults captured did not exceed 8 individuals. At the end of the crop cycle, the average was 2 adults per trap. The presence of adults is related to climate conditions. Larraín and Muñoz (1997) ⁽¹⁰⁾ indicated that the optimal temperatures for L. huidobrensis population range between 14 to 21ºC. These results coincide with the records of maximum temperature mean during the monitoring months (24.0, 28.3, 29.2 and 30.3 ºC, for September, October, November and December, respectively), i.e., it was inversely proportional to the number of adults trapped. Salas et al. (1992) ⁽¹⁷⁾ and Niño et al. (2009) ⁽¹⁴⁾ report that rainfall is the climatic factor that most negatively influences the pest population density. In our trial, rainfall was (in mm) 89.41, 66.79, 105.92 and 125.99, for the months mentioned above, respectively, and is possibly related with the number of adults trapped.

Table 1. L. huidobrensis adults, total leaves and leaves damaged (number per plant) (Mean ± SD) by monitoring date.
Tabla 1. Nº de adultos de L. huidobrensis, Nº de hojas totales, número de hojas dañadas (número por planta (Media ± DS) por fecha de monitoreo.

¹ Mean values within a column followed by the same letter are not significantly different, according to Tukey test (α=<0.01).
¹ Valores medios en una columna seguidos por la misma letra no son significativamente diferentes. Test de Tukey (α=<0.01).

The adults captured in sticky traps and the average number of damaged leaves corresponded, 1.67 on the fi rst monitoring date (Table 1) (9.64% of total leaves per plants), and 0.47, in the last observation (2.57% of total leaves per plant). These results could be due to the greater female pest crop colonization ⁽¹¹⁾. Plants damaged early in the season, or with 25% or more of the leaves mined late in the season, will suffer signifi cant loss of photosynthate production that extends the time required for crop completion ⁽²⁶⁾. The greatest damage was in lower leaves, which coincides with Mujica and Cisneros (2001) ⁽¹²⁾ and with López et al. (2010) ⁽¹¹⁾. Our results showed an association between L. huidobrensis population and crop development, in line with López et al. (2010) ⁽¹¹⁾ in potatoes, and Salvo and Valladares (1995) ⁽¹⁸⁾ in beans, for the same species. Population density remains high during early crop stages, and declines during crop senescence ⁽²⁹⁾.
The number of galleries per leaf are related to the number of adults captured in sticky traps (Table 1 and 2), with significant differences, coincident with seedling crops to flowering beginnings. On 16th September the highest average was recorded (5.62 ± 4.69), possibly due to the lag between the adults captured in traps and larvae inside the leaves (Table 2), and because L. huidobrensis distribution was available throughout the season ⁽²²⁾. The number of galleries declined at the end of the crop cycle, with significant differences on 14th and 21th October (0.06 ± 0.24) (13, 11) because females appear to be able to select those plants that provide a higher performance for their offsprings ⁽²⁸⁾.

Table 2. Galleries, L. huidobrensis larvae and parasitoids (number per leaf) in C. maxima var. zapallito (Mean ± SD) according to monitoring dates.
Tabla 2. Número de galerías, de larvas de L. huidobrensis y de parasitoides, por hoja, en C. maxima var. zapallito (Media ± DS) por fecha de monitoreo.

¹ Mean values within a column followed by the same letter are not significantly different. Tukey test (α=<0.01). *n= Total leaves per plant.
¹ Valores medios en una columna seguidos por la misma letra no son significativamente diferentes. Test de Tukey (α=<0.01). *n= Nº total de hojas por planta.

In our study the parasitoids were only found on three sampling dates (Table 2). The parasitoid species was Phaedrotoma scabriventris (Nixon) (=Opius scabriventris) (Hymenoptera, Braconidae), a solitary, koinobiont, and larva-pupal endoparasitoid. Females lay their eggs directly inside the second-third stage of larval bodies and the larvae develop inside. The parasitized leafminer larvae still consume the tissue of plant leaves until their pupation ⁽¹³⁾. The highest parasitized larvae percentage was recorded on 23rd September (72.0%), followed by 7th October (59.0%). According to Videla et al. (2006) ⁽²⁸⁾ higher mortality rates by P. scabriventris were found on those crops where the leafminer was larger. Different authors found variable parasitoidism percentages according to natural enemy species, host and crop ⁽³⁾. Salvo and Valladares (1995) ⁽¹⁸⁾ found 51.6% of L. huidobrensis larvae attacked by P. scabriventris in beans, whereas Cure and Cantor (2003) ⁽⁴⁾ mentioned that, after blooming, parasitoidism by Diglyphus begini (Ashmead) (Hymenoptera, Eulophidae), reached 90.0% in Gypsophila paniculata L. (Caryophyllaceae), and decreased (70.0%) at the crop cycle end, without insecticides to control pest. In our study, parasitoid population was not abundant, probably because the host larvae were not large enough to allow parasitoid reproduction.
The path analysis showed a significant correlation between the number of parasitoid and leafminer larvae, as a function of the number of galleries per leaf (Fig. 1 a, b). For parasitoids (r=0.30; P 0.001) the analysis indicates a little relation to leave galleries, while for larvae (r=0.59; P 0.001), although low, the value indicates a better fit. Parasitoids did not exercise a dense-dependent control on L. huidobrensis, unlike the results found by Ehler (1992) ⁽⁷⁾, and Salvo and Valladares (1995) ⁽¹⁸⁾. The regional biodiversity clearly provides a rich community of indigenous parasitoids that contribute to the control of the native Liriomyza species, despite the difficulties in quantifying the effects of indigenous parasitoids (often due to patterns of pesticide use), and they should be treated as a resource and protect them as much as possible ⁽²⁴⁾. Therefore, it is necessary to continue studies especially referring to biology, natural mortality factors, alternative hosts, monitoring, among others, which will allow for achieving a rational management of Liriomyza sp. in horticultural crops in the province of Santa Fe, Argentina.

Figure 1. Correlation between number oof L. huidobrensis larvae (a) and parasitoids (P. scabriventris) (b), according to the number of galleries per leaf in C. maxima var. zapallito.
Figura 1. Correlación entre el número de larvas de L. huidobrensis (a) y de parasitoides (P. scabriventris) (b), de acuerdo al número de galerías por hoja en C. maxima var. zapallito.

CONCLUSIONS

Liriomyza huidobrensis causes damage in commercial plots of summer squashes in early stages of development, near the city of Santa Fe, Argentina, with 25% or more of the leaves mined. Adults collected in sticky traps had a maximum peak in the first sampling (27.8) with significant differences with the remaining collecting dates. On 16th September the highest average number of galleries (5.62 ± 4.69) was recorded, which declined at the end of the crop cycle. Adult population showed correspondence with damage and number of galleries per leaf, with significant differences in the first monitoring date. The relation between Phaedrotoma scabriventris and leave galleries was low, but the relation value for larvae indicates a better fit, both there of which are not significant.

ACKNOWLEDGEMENTS

The authors are thankful for the financial support provided by Universidad Nacional del Litoral (Argentina).

DISCLOSURE

The authors report no conflicts of interest in this study.

REFERENCES

1. ACHTERBERG, C. VAN AND SALVO, A. 1997. Reared Opiinae (Hymenoptera: Braconidae) from Argentina Leiden, 71: 189-214.         [ Links ]

2. BARRANCO VEGA, P. 2003. Dípteros de interés agronómico. Agromícidos plaga de cultivos hortícolas intensivos. Bol. S.E.A., 33: 293-307.         [ Links ]

3. BJORKSTEN, T.A.; ROBINSON, M. AND LA SALLE, J. 2005. Species composition and population dynamics of leafmining flies and their parasitoids in Victoria. Australian Journal of Entomology, 44: 186-191.         [ Links ]

4. CURE, J.R. AND CANTOR, F. 2003. Atividade predadora e parasítica de Diglyphus begini (Ashm.) (Hymenoptera: Eulophidae) sobre Liriomyza huidobrensis (Blanch.) (Diptera: Agromyzidae) em cultivos de Gypsophila paniculata L. Neotropical Entomology, 32(1): 085-089.         [ Links ]

5. DE FREITAS BUENO, A.; ZECHMANN, B.; HOBACK, W.W.; OLIVEIRA DE FREITAS BUENO, R.C. AND FERNÁNDES, O.A. 2007. Mosca-minadora (Liriomyza trifolii) na cultura da batata (Solanum tuberosum): observações de campo e respostas fotossintéticas da planta à injuria. Ciência Rural, 37(6): 1510-1517.         [ Links ]

6. DI RIENZO, J.A.; CASANOVES, F.; BALZARINI, M.G.; GONZÁLEZ, L.; TABLADA, M. AND ROBLEDO, C.W. 2008. InfoStat, versión 2008, Grupo InfoStat, FCA, Universidad Nacional de Córdoba, Argentina.         [ Links ]

7. EHLER, L.E. 1992. Guild analysis in biological control. Environmental Entomology, 21(1): 26-40.         [ Links ]

8. FOBA, C.N.; SALIFU, D.; LAGAT, Z.O.; GITONGA. L.M.; AKUTSE, K.S. AND FIABOE, K.K.M. 2015. Species composition, distribution, and seasonal abundance of Liriomyza leafminers (Diptera: Agromyzidae) under different vegetable production systems and agroecological zones in Kenya. Environmental Entomology, 44(2): 1-10.         [ Links ]

9. KEIU, C.B. AND PARRELLA, M.P. 1990. Characterization of insecticide resistance in two colonies of Liriomyza trifolii (Diptera: Agromyzidae). Journal of Economic Entomology, 83(1): 18-26.         [ Links ]

10. LARRAÍN, P. AND MUÑOZ, C. 1997. Abundancia estacional, hospederos alternativos y parasitismo de Liriomyza huidobrensis (Blanchard) (Diptera: Agromyzidae) en cultivos de papa de la IV Región de Chile. Agricultura Técnica, (4): 290-296.         [ Links ]

11. LÓPEZ, R.; CARMONA, D.; VINCINI, A.M.; MONTERUBBIANESI, G. AND CALDIZ, D. 2010. Population dynamics and damage caused by the leafminer Liriomyza huidobrensis Blanchard (Diptera: Agromyzidae), on seven potato processing varieties grown in temperate environment. Neotropical Entomology, 39(1): 108-114. http://dx.doi.org/10.1590/S1519-566X2010000100015.         [ Links ]

12. MUJICA, N. AND CISNEROS, F. 2001. Biología de la mosca minadora Liriomyza huidobrensis. Módulo 1: investigación biológica. Manual de capacitación, Lima. 7 p.         [ Links ]

13. MUJICA, N.; VALENCIA, C.; CARHUAPOMA, P. AND KROSCHEL, J. 2016. Phaedrotoma scabriventris (Nixon, 1955). In: Kroschel, J.; Mujica, N.; Carhuapoma, P. & Sporleder, M. (Eds.). Pest distribution and risk atlas for Africa. Potential global and regional distribution and abundance of agricultural and horticultural pests and associated biocontrol agents under current and future climates. Lima (Perú). International Potato Center (CIP), 257- 268. Doi: 10.4160/9789290604761-20.         [ Links ]

14. NIÑO, L.; PRIETO, L.; SANTIAGO, V. AND ACEVEDO, E. 2009. Fluctuación poblacional de la mosca minadora (Liriomyza huidobrensis Blanchard) en cultivos de papa de Pueblo Llano, Estado Mérida, Venezuela. Entomotrópica, 24(2): 65-70.         [ Links ]

15. OATMAN, E.R. AND KENNEDY, G.G. 1976. Methomyl induced outbreak of Liriomyza sativae on tomato. Journal of Economic Entomology, 69 (5): 667-668. https://doi.org/10.1093/jee/69.5.667.         [ Links ]

16. PARRELLA, M.P.; KEIL, C.B. AND MORSE, J.G. 1984. Insecticide resistance in Liriomyza trifolii. California agriculture, 22-23.         [ Links ]

17. SALAS, J.; ÁLVAREZ, C.; PARRA, A. AND MENDOZA, O. 1992. Manejo integrado de insectos plagas en el cultivo de la papa en el Estado Lara, Venezuela. FONAIAP. PRACIPA. Asociación de Horticultores del Estado Lara. 66 p.         [ Links ]

18. SALVO, A. AND VALLADARES, G. 1995. Complejo parasítico (Hymenoptera: Parasitica) de Liriomyza huidobrensis (Diptera: Agromyzidae) en haba. AgrisScientia, XII: 39-47.         [ Links ]

19. SALVO, A. & VALLADARES, G. 1998. Taxonomic composition of hymenopteran parasitoid assemblages from Agromyzidae leaf-miners sampled in central Argentina. Studies on Neotropical Fauna and Environment, 33: 116-123.         [ Links ]

20. SARYAZDI, G.A.; HEJAZI, M.J.; RASHIDI, M-R. AND FERGUSON, S. 2014. Incidence and characterization of resistance to Fenpropathrin in some Liriomyza sativae (Diptera: Agromyzidae) populations in Iran. Journal of Economic Entomology, 107 (5): 1908-1915. doi: org/10.1603/EC14181.         [ Links ]

21. SCHEFFER, S.J. AND LEWIS, M.L. 2001. Two nuclear genes confirm mitochondrial evidence of two cryptic species within Liriomyza huidobrensis (Diptera: Agromyzidae). Annals of the Entomological Society of America, 94(5): 648-653.         [ Links ]

22. SINGH, O.L. AND SINGH, CHJ. 2013. Population dynamics and seasonal incidence of Liriomyza huidobrensis (Blanchard) (Diptera: Agromyzidae) on onion vegetable in Manipur. International Journal of Advancements in Research & Technology, 2(9): 89-95.         [ Links ]

23. SPENCER, K.A. AND STEGNAUER, C.E. 1973. The Agromyzidae of Florida, with supplement of species from the Caribbean. In: Arthropods of Florida and Neighboring Land Areas. Vol. 7. 205 p.         [ Links ]

24. TONG-XIAN, L.; LE, K.; HEINZ, K.M. AND TRUMBLE, J. 2009. Review Biological control of Liriomyza leafminers: progress and perspective CAB Reviews: Perspectives in Agriculture. Veterinary Science, Nutrition and Natural Resources. Nº 004. 16 p.

25. TROUVE; C.; MARTÍNEZ, M.; PHALIP, M. AND MARTIN, C. 1991. Un nouveau ravager en Europe, la mouche mineuse sud-américaine. Phytoma-Defense des Vegetaux, 429: 42-46.         [ Links ]

26. TRUMBLE, J.T.; TING, I.P. AND BATES, L. 1985. Analysis of physiological, growth, and yield responses of celery to Liriomyza trifolii. Entomologia Experimentalis et Applicata, 38: 15-21.         [ Links ]

27. VALLADARES, G.; SALVO, A. AND SAINI, E. 2011. Moscas minadoras del girasol y sus enemigos naturales. RIA, 37(2): 180-188.         [ Links ]

28. VIDELA, M.; VALLADARES, G. AND SALVO, A. 2006. A tritrophic analysis of host preference and performance in a polyphagous leafminer. Entomologia Experimentalis et Applicata, 121:105-114.         [ Links ]

29. VINCINI, A.M. AND CARMONA, D.M. 2006. Insectos. Producción, cosecha y almacenamiento de papa en la Argentina. En; Caldiz, D. O. (Ed.) BASF Argentina (Buenos Aires) p. 165-169.         [ Links ]

30. WEINTRAUB, P.G.; SCHEFFER, S.J.; VISSER, D.; VALLADARES, G.; SOARES CORREA, A.; SHEPARD, B.M.; RAUF, A.; MURPHY, S.T.; MUJICA, N.; MAC VEAN, C.; KROSCHEL, J.; KISHINEVSKY, M.; JOSHI, R.C.; JOHANSEN, N.S.; HALLET, R.H.; CIVILEK, H.S.; CHEN, B. AND METZLER, H.B. 2017. The invasive Liriomyza huidobrensis (Diptera: Agromyzidae): Understanding its pest status and management globally. Journal of Insect Science, 17(1): 1-27. doi: 10.1093/jisesa/iew121.         [ Links ]

31. ZHANG, S.; ZHANG, Z. AND KANG, L. 2012. Transcriptome response analysis of Arabidopsis thaliana to leafminer (Liriomyza huidobrensis). BMC Plant Biology, 12:234. doi: 10.1186/1471-2229-12-234.         [ Links ]