Phyllocnistis citrella Stainton (Lepidoptera, Gracillaridae)
Evolution of Phyllocnistis citrella Stainton (Lepidoptera, Gracillaridae) and its parasitoids in the last five years in citrus orchards of the western Sicily (Italy)
INTRODUCTION
The citrus leafminer (CLM), Phyllocnistis citrella Stainton (Lepidoptera: Gracillariidae: Phyllocnistinae) is a phytophagous native from Southeast Asia. In Italy, the pest was first discovered during the autumn of 1994, in some citrus groves of Sardinia ( Benfatto, 1995; Ortu et al. 1995) and subsequently in Sicily in the summer of 1995 (Balzani et al., 1995; Longo and Siscaro, 1995; Liotta and Manzella, 1995) showing a rapid range expansion in other citrus-growing regions of Italy. Damage is caused by the larvae, producing serpentine mines on young and tender leaves and shoots. The larvae, contrarily to other miners, do not feed on the foliar parenchyma, but only from the juices that pour from it when the cuticle is separated (Garrido Vivas,1995). The pest attacks all citrus cultivars but it is an economic problem only on re-grafted plants (Caleca et al., 1995, 1997, 2000), and an aesthetic damage on ornamental citrus (Del Bene & Landi, 1999), on young plants in nurseries (Caleca,2000).
Biological control is a rational approach to reducing damage by citrus leafminer. Since the first occurrence of the citrus leafminer in Sicily, several indigenous natural enemies have been found as attacking the pest (Liotta et al., 1996). Several species of exotic parasitoids were introduced and released in citrus groves of Sicily (Siscaro et al. 1997; Mineo and Mineo, 1999). The most abundant species, in the last five years, are the exotic ectoparasitoids, C. phyllocnistoides Narayanan, and S. petiolatus (Girault) (Liotta et al., 2003). The aims of this study were to monitor the population dynamics, parasitism levels and mortality of P.citrella, from 2002 to 2006, in some unsprayed citrus orchards in western Sicily.
INTRODUCTION
The citrus leafminer (CLM), Phyllocnistis citrella Stainton (Lepidoptera: Gracillariidae: Phyllocnistinae) is a phytophagous native from Southeast Asia. In Italy, the pest was first discovered during the autumn of 1994, in some citrus groves of Sardinia ( Benfatto, 1995; Ortu et al. 1995) and subsequently in Sicily in the summer of 1995 (Balzani et al., 1995; Longo and Siscaro, 1995; Liotta and Manzella, 1995) showing a rapid range expansion in other citrus-growing regions of Italy. Damage is caused by the larvae, producing serpentine mines on young and tender leaves and shoots. The larvae, contrarily to other miners, do not feed on the foliar parenchyma, but only from the juices that pour from it when the cuticle is separated (Garrido Vivas,1995). The pest attacks all citrus cultivars but it is an economic problem only on re-grafted plants (Caleca et al., 1995, 1997, 2000), and an aesthetic damage on ornamental citrus (Del Bene & Landi, 1999), on young plants in nurseries (Caleca,2000).
Biological control is a rational approach to reducing damage by citrus leafminer. Since the first occurrence of the citrus leafminer in Sicily, several indigenous natural enemies have been found as attacking the pest (Liotta et al., 1996). Several species of exotic parasitoids were introduced and released in citrus groves of Sicily (Siscaro et al. 1997; Mineo and Mineo, 1999). The most abundant species, in the last five years, are the exotic ectoparasitoids, C. phyllocnistoides Narayanan, and S. petiolatus (Girault) (Liotta et al., 2003). The aims of this study were to monitor the population dynamics, parasitism levels and mortality of P.citrella, from 2002 to 2006, in some unsprayed citrus orchards in western Sicily.
Material and methods
This study was carried out during four consecutive years, from June 2002 to September 2006, in organic citrus orchards, located in areas of Trapani and Palermo (western Sicily, Italy). The orchards were planted to orange, and lemon. No insecticides were applied to the organic citrus orchards. At each location, 200 citrus tender leaves were randomly collected every 15 days, placed in plastic bags, and taken to the laboratory for examination under a stereomicroscope. Numbers of leaves sampled and total number of P. citrella (sum of live and dead larvae, pupae, pupal cases were recorded. Apparent percentage parasitism was calculated. Mortality was calculated by dividing the number of hosts with parasitoid eggs, larva or pupa plus number of hosts killed by a parasitoid or by a predator including the unknown mortality with total number of CLM(living and dead) (D.M. AMALIN, 2002).
This study was carried out during four consecutive years, from June 2002 to September 2006, in organic citrus orchards, located in areas of Trapani and Palermo (western Sicily, Italy). The orchards were planted to orange, and lemon. No insecticides were applied to the organic citrus orchards. At each location, 200 citrus tender leaves were randomly collected every 15 days, placed in plastic bags, and taken to the laboratory for examination under a stereomicroscope. Numbers of leaves sampled and total number of P. citrella (sum of live and dead larvae, pupae, pupal cases were recorded. Apparent percentage parasitism was calculated. Mortality was calculated by dividing the number of hosts with parasitoid eggs, larva or pupa plus number of hosts killed by a parasitoid or by a predator including the unknown mortality with total number of CLM(living and dead) (D.M. AMALIN, 2002).
RESULTS
Population Dynamics
The seasonal trend of citrus leafminer population observed during the 4 years of study was similar. Population of P. citrella (Fig.1) began to increase in June-July, and reached its maximum in August, followed by a decline until the first moths of following year. There were no P. citrella individuals in April and May.The comparison of the years 2002 and 2003 revelead that population of P. citrella began to infest citrus orchard at the end of spring (late June), peaking at 2,92 immatures/leaf in late August 2002 and 1.42/leaf in late August 2003. By September, the CLM population decreased from 1, 29/leaf to 0, 01/leaf in January 2003, from 1, 01/leaf to 0, 01/leaf in March 2004.In the following years, from 2004-2006, the infestation were observed to increase earlier (early June) compared to previous years (late June), with exception of 2005 (early July).The highest values of infestation were observed in early August, reaching peaks of 1,09/leaf in 2004,2,26/leaf in 2005 and 2,03/leaf in 2006. By late August, P. citrella density began to decline from 0,97/leaf to 0,01/leaf in early March 2005 and from 1,79/leaf to 0,01/leaf in late March 2006.
Parasitism
In early July 2002, the percentage parasitism (Fig.2) of P. citrella began toincrease from 33,33 %, peaking on November at 48,15%. The maximum percentage parasitism in 2003 was 64,52% in December. In both years, parasitoids were not found from January to June, coinciding with absence of P. citrella infestation. In contrast, parasitism in January 2004 was recorded. Parasitism levels were recovered early in the year 2004(late June) compared to 2003 (July), reaching peak of 54,21% in December. In 2005, the maximum percentage parasitism was 70,83% in late January and 62,61% in late September. In the following year 2006, the highest percentage of parasitism, 61,51%, was observed in late August. These two years were characterized by the high values of parasitism from January to early March.
Mortality
There were differences in the mortality patterns from 2002 to2003 and 2004 to2006 (Fig3).
In 2002 and 2003, P. citrella mortality increased from June-July reaching peaks of 100% (2002) and 93,75% (2003) in late December. In both years, no mortality was observed from January to June.In the last three years (from 2004 to 2006), mortality was observed in the winter (from January to March), through the summer (June to September), and fall (mid September to December).Mortality peaks were recorded from January to February 2004 (100%), late January 2005 (95,12%) and late March 2006 (100%). CLM mortality due to natural enemis was high during the winter in comparison to the first years. In 2005, CLM mortality were recovered late (late July) compared to others years, probably because of low mean monthly temperature during the winter (5-6 C°) and spring (<20 C°).
Population Dynamics
The seasonal trend of citrus leafminer population observed during the 4 years of study was similar. Population of P. citrella (Fig.1) began to increase in June-July, and reached its maximum in August, followed by a decline until the first moths of following year. There were no P. citrella individuals in April and May.The comparison of the years 2002 and 2003 revelead that population of P. citrella began to infest citrus orchard at the end of spring (late June), peaking at 2,92 immatures/leaf in late August 2002 and 1.42/leaf in late August 2003. By September, the CLM population decreased from 1, 29/leaf to 0, 01/leaf in January 2003, from 1, 01/leaf to 0, 01/leaf in March 2004.In the following years, from 2004-2006, the infestation were observed to increase earlier (early June) compared to previous years (late June), with exception of 2005 (early July).The highest values of infestation were observed in early August, reaching peaks of 1,09/leaf in 2004,2,26/leaf in 2005 and 2,03/leaf in 2006. By late August, P. citrella density began to decline from 0,97/leaf to 0,01/leaf in early March 2005 and from 1,79/leaf to 0,01/leaf in late March 2006.
Parasitism
In early July 2002, the percentage parasitism (Fig.2) of P. citrella began toincrease from 33,33 %, peaking on November at 48,15%. The maximum percentage parasitism in 2003 was 64,52% in December. In both years, parasitoids were not found from January to June, coinciding with absence of P. citrella infestation. In contrast, parasitism in January 2004 was recorded. Parasitism levels were recovered early in the year 2004(late June) compared to 2003 (July), reaching peak of 54,21% in December. In 2005, the maximum percentage parasitism was 70,83% in late January and 62,61% in late September. In the following year 2006, the highest percentage of parasitism, 61,51%, was observed in late August. These two years were characterized by the high values of parasitism from January to early March.
Mortality
There were differences in the mortality patterns from 2002 to2003 and 2004 to2006 (Fig3).
In 2002 and 2003, P. citrella mortality increased from June-July reaching peaks of 100% (2002) and 93,75% (2003) in late December. In both years, no mortality was observed from January to June.In the last three years (from 2004 to 2006), mortality was observed in the winter (from January to March), through the summer (June to September), and fall (mid September to December).Mortality peaks were recorded from January to February 2004 (100%), late January 2005 (95,12%) and late March 2006 (100%). CLM mortality due to natural enemis was high during the winter in comparison to the first years. In 2005, CLM mortality were recovered late (late July) compared to others years, probably because of low mean monthly temperature during the winter (5-6 C°) and spring (<20 C°).
Conclusion
After the introduction of Citrostichus phyllocnistoides in 1999 (Mineo and Mineo, 1999) and the accidental introduction of Semielacher petiolatus in 1998,the citrus leafminer population density decreased compared with the previous years. Ours study confirm that C. phyllocnistoides is predominant parasitoid and one of the main factor responsible for the decline in leafminer population. But other factors such as predators contributed significantly to the overall management of P. citrella in the field as shown by the mortality estimates for five years.
Ours study show that the period without CLM individuals become shorter from year to year and concentrated in two moths April and May, probably due to variation in climatic conditions among years.
Reference
Amalin D.M., Peña J.E., Duncan R.E., Browning H.W. and Mcsorley R. 2002.Natural mortality factors acting on citrus leafminer,Phyllocnistis citrella, in lime orchards in South Florida. BioControl 47: 327–347.
Balzani M., Guarasci F., Pecorelli L. (1995)-Segnalazioni in Sicilia della minatrice serpentina degli agrumi - Informatore Agrario, LI (32): 81.
Benfatto D. 1995 – La minatrice serpentine degli agrumi: un nuovo fitofagi presente in Italia – L’Informatore Agrario 4/94: 79-80.
Caleca V. 2000:Assessment of damage due to Phyllocnistis citrella Stainton in citrus nurseries in Sicily; growth delay, esthetical damage and economic injury levels. Proc. XXI International Congress of Entomology, Brazil, August 20-26/2000:666.
Caleca V., Lo Verde G., Blando S. & Lo Verde V. 1998: New data on the parasitism of citrus leafminer(Phyllocnistis citrella Stainton, Lepidoptera Gracillaridae)in Sicily.Boll.Zool.Agr.Bachic.(Ser.II)30(2):213-222.
Caleca V., Lo Verde G. (1997)-Sul controllo Naturale di Phyllocnistis citrella Stainton (Lepidoptera: Gracillariidae) esercitato da parassitoidi. Phytpphaga, volume VII, 65-75.
Caleca V., Lo Verde G., Tsolakis H. T. (1995)-La minatrice serpentina Phyllocnistis citrella Stainton (Lepidoptera: Gracillariidae Phyllocnistinae): un nuovo fitofago degli agrumi siciliani. Sviluppo agricolo, anno XXIX, n. 9/10, settembre/ottobre 1995, 37-48.
Garrido Vivas A., 1995 – Phyllocnistis citrella Stainton, biological aspects and natural enemies found in Spain – IOBC WPRS Bull., 18 (5): 1 – 14.
Liotta G., Agrò A. And Lo Genco A., 2003. Activity of indigenous and exotics parasitoids of P. citrella Stainton in Western Sicily. IOBC wprs Bulletin Vol. 26 (6), pp. 23-25.
Liotta G., Peri E., Salerno G., Di Cristina D., Manzella S. (1996)-Nemici naturali della minatrice serpentina degli agrumi. L’informatore Agrario, LII (8), 123-124.
Liotta G., Manzella S. (1995)-Indicazioni preliminari per la difesa dalla minatrice serpentina. L’informatore agrario, LI (42): 61-62.
Longo S., Siscaro G. (1995a)-La minatrice serpentina degli agrumi (Phyllocnistis citrella Stainton). Nota divulgativa. Ist. difesa piante, Univ. Reggio C., Ist. ent. agr., Univ. Catania.
Mineo G., Mineo N. (1999a)-Introduzione di Citrostichus phyllocnistoides (Narayanan) in Sicilia e suo allevamento simultaneo con Semielacher petiolatus (Girault) (Hym. Eulophidae).-Boll. Zool. agr. Bachic., Ser. II, 31 (2): 197-206.
Ortu S. (1997) – Osservazioni sulle infestazioni di Phyllocnistis citrella in Sardegna. Informatore Fitopatologico, 4,3-9.
Siscaro G., Barbagallo S., Longo S., Patti I. (1997)-Prime acquisizioni sul controllo biologico e integrato della minatrice serpentina degli agrumi in Italia - Informatore fitopatologico 7-8/1997: 19-26
After the introduction of Citrostichus phyllocnistoides in 1999 (Mineo and Mineo, 1999) and the accidental introduction of Semielacher petiolatus in 1998,the citrus leafminer population density decreased compared with the previous years. Ours study confirm that C. phyllocnistoides is predominant parasitoid and one of the main factor responsible for the decline in leafminer population. But other factors such as predators contributed significantly to the overall management of P. citrella in the field as shown by the mortality estimates for five years.
Ours study show that the period without CLM individuals become shorter from year to year and concentrated in two moths April and May, probably due to variation in climatic conditions among years.
Reference
Amalin D.M., Peña J.E., Duncan R.E., Browning H.W. and Mcsorley R. 2002.Natural mortality factors acting on citrus leafminer,Phyllocnistis citrella, in lime orchards in South Florida. BioControl 47: 327–347.
Balzani M., Guarasci F., Pecorelli L. (1995)-Segnalazioni in Sicilia della minatrice serpentina degli agrumi - Informatore Agrario, LI (32): 81.
Benfatto D. 1995 – La minatrice serpentine degli agrumi: un nuovo fitofagi presente in Italia – L’Informatore Agrario 4/94: 79-80.
Caleca V. 2000:Assessment of damage due to Phyllocnistis citrella Stainton in citrus nurseries in Sicily; growth delay, esthetical damage and economic injury levels. Proc. XXI International Congress of Entomology, Brazil, August 20-26/2000:666.
Caleca V., Lo Verde G., Blando S. & Lo Verde V. 1998: New data on the parasitism of citrus leafminer(Phyllocnistis citrella Stainton, Lepidoptera Gracillaridae)in Sicily.Boll.Zool.Agr.Bachic.(Ser.II)30(2):213-222.
Caleca V., Lo Verde G. (1997)-Sul controllo Naturale di Phyllocnistis citrella Stainton (Lepidoptera: Gracillariidae) esercitato da parassitoidi. Phytpphaga, volume VII, 65-75.
Caleca V., Lo Verde G., Tsolakis H. T. (1995)-La minatrice serpentina Phyllocnistis citrella Stainton (Lepidoptera: Gracillariidae Phyllocnistinae): un nuovo fitofago degli agrumi siciliani. Sviluppo agricolo, anno XXIX, n. 9/10, settembre/ottobre 1995, 37-48.
Garrido Vivas A., 1995 – Phyllocnistis citrella Stainton, biological aspects and natural enemies found in Spain – IOBC WPRS Bull., 18 (5): 1 – 14.
Liotta G., Agrò A. And Lo Genco A., 2003. Activity of indigenous and exotics parasitoids of P. citrella Stainton in Western Sicily. IOBC wprs Bulletin Vol. 26 (6), pp. 23-25.
Liotta G., Peri E., Salerno G., Di Cristina D., Manzella S. (1996)-Nemici naturali della minatrice serpentina degli agrumi. L’informatore Agrario, LII (8), 123-124.
Liotta G., Manzella S. (1995)-Indicazioni preliminari per la difesa dalla minatrice serpentina. L’informatore agrario, LI (42): 61-62.
Longo S., Siscaro G. (1995a)-La minatrice serpentina degli agrumi (Phyllocnistis citrella Stainton). Nota divulgativa. Ist. difesa piante, Univ. Reggio C., Ist. ent. agr., Univ. Catania.
Mineo G., Mineo N. (1999a)-Introduzione di Citrostichus phyllocnistoides (Narayanan) in Sicilia e suo allevamento simultaneo con Semielacher petiolatus (Girault) (Hym. Eulophidae).-Boll. Zool. agr. Bachic., Ser. II, 31 (2): 197-206.
Ortu S. (1997) – Osservazioni sulle infestazioni di Phyllocnistis citrella in Sardegna. Informatore Fitopatologico, 4,3-9.
Siscaro G., Barbagallo S., Longo S., Patti I. (1997)-Prime acquisizioni sul controllo biologico e integrato della minatrice serpentina degli agrumi in Italia - Informatore fitopatologico 7-8/1997: 19-26



