Larval Parasitoids and Parasitism Rates of the Cereal Leafminer, Syringopais temperatella (Lederer, 1855) (Lepidoptera: Scythridae) in Cereal Fields of Northern Cyprus

Celalettin Gözüaçik1,*, Mustafa Güllü2, Ayda Konuksal3, Reşat Değirmenci3 and Ercan Akerzurumlu3

1Department of Plant Protection, Faculty of Agriculture, Iğdır University, 76 000, Iğdır, Turkey

2Department of Plant Protection, Faculty of Agriculture, Bingöl University, 12 000, Bingöl, Turkey

3Agricultural Research Institute, Lefkoşa, Turkish Republic of Northern Cyprus

ABSTRACT

The cereal leafminer, Syringopais temperatella Lederer (Lepidoptera: Scythridae) is an important pest in barley and wheat in Northern Cyprus. This study was carried out to identify the larval parasitoids and to determine the parasitism rate of S. temperatella. These studies were conducted in 42 cereal fields of 18 villages in Lefkoşa, Girne, Güzelyurt, Gazimağusa and İskele townships in 2012-2013 years, and 1567 and 862 larvae were collected in the two years, respectively. Larvae were kept inside boxes covered with nets in the laboratory at 25±1◦C and 65±5% r.h. Following pupation, adult moths and parasitoids were obtained and percentage of parasitized larvae was determined. At the end of the study, Bracon (Habrobracon) stabilis (Wesmael) (Braconidae) and Agathis gracilenta Tobias (Braconidae) species from Hymenoptera order were obtained. Bracon stabilis (93.4%) was determined as widespread and in higher level. A. gracilenta was identified for the first time as larval parasitoid of S. temperatella and also for Northern Cyprus and Cyprus Island. The average parasitism rate in cereal fields was 34.8-18.1% in Güzelyurt, 31.8-12.2% in İskele, 21.0-8.4% in Girne, 16.2-5.4% in Lefkoşa and, 9.5-1.8% in Gazimağusa townships in 2012-2013 years, respectively.

Article Information

Received 16 January 2017

Revised 18 May 2018

Accepted 25 October 2018

Available online 22 April 2020

Authors’ Contribution

CG, MG, AK, RD and EA collected and cultured the samples. CG analyzed the data and drafted the manuscript.

Key words

Cereal leaf miner, Syringopais temperatella, Larval parasitoids, Parasitism rates, Northern Cyprus.

DOI: https://dx.doi.org/10.17582/journal.pjz/20170116190155

* Corresponding author: cgozuacik46@gmail.com

0030-9923/2020/0004-1591 $ 9.00/0

Copyright 2020 Zoological Society of Pakistan

The cereal leafminer, Syringopais temperatella (Lederer, 1855) (Lepidoptera: Scythrididae), which is locally known as “Sirividhi” or “Sirvis”, is a serious insect pest of cereals in Cyprus (Georghiou and Shiakides, 1957; Vakis, 1975; Melifronides, 1977). Güllü et al. (2014) recorded the insect pests; S. temperatella and Mayetiola destructor (Say, 1817) (Diptera:Cecidomyiidae) in cereal fields in Northern Cyprus. Syringopais temperatella caused tremendous yield losses almost every year. The cereal leafminer was reported in wheat and barley fields in Iraq (Abu-Yaman and Jarjes, 1971; Ali et al., 2007), Turkey (Kaya, 1975; Güllü et al., 1993; Gözüaçık et al., 2008), Syria, Lebanon, Asia and the Mediterranean riparian countries (Daamen et al., 1989), Iran (Jemsi et al., 2002; Jemsi and Rajabi, 2003) and Jordan (Al-Zyoud, 2007). Damage done by larvae, prevents photosynthesis and desiccates the end portions of the leaves due to their feeding between epidermis, which lead to drying up of leaves. Bodenheimer (1930) reported that the damage due to cereal leaf minor increased from 30 to 90% owing to the absence of rainfall in Cyprus over the years. Dry winter and poor soils can increase the damage of larvae at changing rates from 30 to 100%. In Israel, the crop loss was recorded between 15 and 20% (Hüsseini, 1954). The pest reduced the yield by 40-60% in Turkey (Kaya, 1975). Later, Duran et al. (1979) estimated the reduction in the field to be around 22% in Turkey. In Iraq, the crop loss was found 10-20% (Abu-Yaman and Jarjes, 1971). In Jordan, the average grain yield reduction by cereal leafminer, S. temperatella was estimated at 36.1% for wheat and 50% for barley (Ghabeish et al., 2013).

Beside the abiotic factors, biocontrol agents play a crucial role in suppressing the pest population. Among the biotic factors, parasitoids and predators (spiders etc.) are significant bio-agents in infested cereal fields with cereal leafminer. Some larval parasitoid species have been recorded on this insect pest in Turkey and Jordan (Kaya, 1975; Al-Zyoud, 2007; Yefremova et al., 2007; Gözüaçık et al., 2008; Pirhadi et al., 2008). More detailed surveys on the larval parasitoid species should be conducted. Therefore, this current study was conducted to survey larval parasitoid species of S. temperatella and its parasitism rates in cereal fields at five districts of Northern Cyprus during the years 2012-2013.

Materials and methods

The current study was conducted in 42 wheat, barley and oat fields of 18 villages in the districts of Lefkoşa (Nicosia), Gazimağusa (Famagusta), Girne (Kyrenia), Güzelyurt (Morphou) and İskele (Trikomo) of Turkish Republic of Northern Cyprus in the years 2012-2013. A total of 1587 and 865 leaves infested with the larvae of the cereal leafminer, S. temperatella were collected between March and April months in the years 2012 and 2013, respectively. Larvae were kept inside boxes covered with nets in the laboratory at 25±1°C, 65±5% RH, and 16L:8D photoperiod. They were controlled daily for emergence of moths and parasitoids. Following a completion of the emergence of the moths and parasitoids, parasitism rates of S. temperatella larvae was calculated as the number of parasitoids over the total count of parasitoids and moths. Specimens from the parasitoid species obtained in the survey were stored in 70% alcohol in small plastic tubes and sent to Prof. Dr. Ahmet Beyarslan (Bitlis Eren University, Faculty of Science and Literature, Department of Biology, Bitlis, Turkey) for identification.

Before two-way ANOVA, the data on parasitism rates were transformed by using Arcsin Transformation. The arcsin transformed data were exposed to two-way ANOVA at Randomized Block Design for testing year and districts fixed effects handled in the survey. Mean separation for district effect was performed using Duncan multiple comparison test at 1% significance level. To measure the effectiveness of two-way ANOVA, coefficient of determination (R2%) and adjusted coefficient of determination (Adjusted R2 %) were estimated. All the statistical evaluations were made through SPSS 20 software program.

Results and discussion

The survey of the larvae parasitoids of S. temperatella in cereal fields in Northern Cyprus revealed the presence of two braconid species; Bracon (Habrobracon) stabilis (Wesmael, 1838) and Agathis gracilenta Tobias, 1963. Bracon hebetor is the most common species. Whereas, A. gracilenta was identified for the first time as a larval parasitoid of S. temperatella in Northern Cyprus. In previous studies recorded the larvae parasitoid species; including Pnigalio pecticornis (Linnaeus, 1758) (Hym.: Ichneumonidae) (Kaya, 1975), Bracon stabilis Wesmael and Apanteles sp. (Hym.: Braconidae) (Gözüaçık et al., 2008) in Turkey; Anilastus sp. Förster (Hym.: Ichneumonidae) (Al-Zyoud, 2007) in Jordan; Diglyphus chabrias Walker and Necremnus tidius Walker (Yefremova et al., 2007) and Sympiesis euspilapterygis (Erdos) (Hym.: Eulophidae) in Iran (Pirhadi et al., 2008; Talebi et al., 2011).

Table I.- The number of larvae and parasitism rates in cereal fields in 2012 in Northern Cyprus.

Table II.- The number of larvae and parasitism rates in cereal fields in 2013 in Northern Cyprus.

The number of larvae and parasitism rates in cereal fields where the studies were conducted in Northern Cyprus in the years 2012 and 2013 are given in Tables I and II, respectively. As also understood from Tables I and II, It was observed that the highest rates of parasitism 54.3% and 53.8% were recorded in barley fields of Akçay and Aydınköy (Güzelyurt) in 2012 and Ağırdağ (Girne) in 2013, respectively. No parasitoids were encountered at Güneşköy (Güzelyurt) and Boğaziçi (İskele) in the year 2012 and Boğaziçi and Güvercinlik (Gazimağusa) in the year 2013.

Parasitism rates (the arcsin transformed parasitism rates) in cereal fields of Northern Cyprus in the years 2012-2013 are given in Table III.

Table III illustrates the results of ANOVA performed for testing the effects of district and year factors on the arcsin transformed parasitism rates examined in the survey. Both coefficient of determination (R2 %) and adjusted coefficient of determination (Adjusted R2 %) reflected that nearly all of the variability in transformed parasitism rate was explained by district (P<0.01) and year (P<0.01) effects, which were found very significant in the survey. On the other hand, the result revealed that these two main effects were significant sources of variation.

Table III.- Results for the arcsin transformed parasitism rates (two-way ANOVA).

Table IV.- Average parasitism rates (the transformed rates) of Syringopais temperatella in cereal fields in Northern Cyprus during the year 2012-2013.

A, B, the difference between the averages of two years with different letter is significant at 1% level; a, b, c, the difference between the averages of two locations with different letter is significant at 1% level.

Average parasitism rates and their arcsin transformed rates on S. temperatella in cereal fields in Northern Cyprus in the years 2012-2013 are given in Table IV. The significantly difference between the years 2012 and 2013 was found for the transformed parasitism rate and the average transformed rate in the year 2012 was remarkably higher than that in the year 2013 (P<0.01). The highest values in the transformed parasitism rate were obtained from Güzelyurt and İskele districts, which were similar to each other, statistically, whereas the lowest transformed rate was recorded in Gazimağusa district, which was lower compared to Girne and Lefkoşa districts.

As shown in Table IV, the highest rates of parasitism were recorded in the year 2012 compared with that in the year 2013. Highest rates of parasitism were recorded at Güzelyurt (Morphou) district in both years (35.78 and 25.18%) while the lowest were at Gazimağusa (Famagusta) district (17.95 and 7.71%) (Table II). In Jordan, Al-Zyoud (2007) reported that parasitism rate was 49.0% created by Anilastus sp. In Turkey, the parasitism rate was determined to be 8-10% in the years 2005-2006 (Gözüaçık et al., 2008). It was seen that parasitism rates varied from year to year and from location to location. It is thought that every part of Güzelyurt and in some parts of Iskele districts have more trees, weeds and, polycultures on the basis of irrigation (citrus, potatoes, kolokas (Taro), artichokes etc.) causing to higher parasitism rate in comparison with Lefkoşa and Gazimağusa districts. Thus, semi-natural habitats provide natural enemies with prey and alternative hosts of pests having nutritional plant resources and together with shelter and overwintering sites (Médiène et al., 2011). Secondly, chemical insecticides used intensively by the cereal growers against S. temperatella might negatively affect the parasitoids population. For this reason, the chemical insecticides used against this pest should be of the least harmful or harmless class. In addition, the application of insecticides at the recommended doses and on time is of great importance.

Acknowledgement

We are grateful to Prof. Dr. Ahmet Beyarslan (Faculty of Science and Literature, Department of Biology, Bitlis Eren University, Bitlis, Turkey) for identifying the specimens.

Statement of conflict of interest

The authors declare no conflict of interest.

References

Abu Yaman, I.K. and Jarjes, S.J., 1971. Z. angew. Ent., 67: 266-272.

Ali, A.A., Mohammad, J.K. and Hussain, H.M., 2007. Al-Anbar J. agric. Sci., 5: 330-336.

Al-Zyoud, F.A., 2007. Bull. Facul. Agric. Cairo Univ., 58: 164-172.

Bodenheimer, F.S., 1930. Die Schädlings Fauna Palästinas. Monograpgin zur angewandten Entomologie, Paul Parey, Berlin, pp. 10.

Daamen, R.A., Wijnandsand, F.G. and Vliet, G., 1989. J. Phytopathol., 125: 305-319. https://doi.org/10.1111/j.1439-0434.1989.tb01075.x

Duran, M., Altınayar, G., Koyuncu, N. and Dörtbudak, Y., 1979. Bitki Koruma Bült., 19: 1-15.

Georghiou, G.P. and Shiakides, T., 1957. Host plants of the cereal leafminer Syringopais temperatella Led. in Cyprus. Department of Agriculture Cyprus. Tech. Bull., pp. 1-3.

Ghabeish, I., Al-Zyoud, F. and Hassawi, D., 2013. Rev. Colomb. Entomol., 40: 176-181.

Gözüaçık, C., Erdoğan, Ö.Ç. and Beyarslan, A., 2008. Phytoparasitica, 36: 489-490. https://doi.org/10.1007/BF03020295

Güllü, M., Gözüaçık, C., Hekimhan, H., Fidan, H., Konuksal, A., Değirmenci, R. and Akerzurumlu, E., 2014. The investigations on determination of some harmful insect species and their distributions and situations of damage in the cereal fields in Northern Cyprus. Abstracts of the Fifth Plant Protection Congress of Turkey, 3–5 February 2014, Antalya, pp. 5.

Güllü, M., Şimşek, N. and Kişmir, A., 1993. Pl. Protec. Res. Annu., 28-29: 1-4.

Hüsseini, S.Y., 1954. FAO Pl. Protec. Bull., 2: 22-23.

Jemsi, G. and Rajabi, G., 2003. Appl. Ent. Phytopathol., 70: 13-15.

Jemsi, G., Shojai, M., Radjabi, G. and Ostovan H., 2002. J. agric. Sci., 8: 1-21.

Kaya, A.O., 1975. Tech. Bull., 24: 40.

Médiène, S., Valantin-Morison, M., Sarthou, J.P., de Tourdonnet, S., Gosme, M., Bertrand, M., Roger-Estrade, J., Aubertot, J.N., Rusch, A., Motisi, N., Pelosi, C. and Doré, T., 2011. Agron. Sustain. Develop., 31: 491-514. https://doi.org/10.1007/s13593-011-0009-1

Melifronides, I.D., 1977. PANS, 23: 268-271. https://doi.org/10.1080/09670877709412449

Pirhadi, A, Radjabi, G., Ebrahimi, E., Ostovan, H., Shekarian-Moghaddam, B., Mohiseni, A. A., Mozaffarian, F. and Ghavami, S., 2008. Natural enemies of cereal leafminer Syringopais temperatella Led. (Lep., Elachistidae) in Lorestan Province. Proceedings of the 18th Iranian Plant Protection Congress, Buali Sina University, Hamedan, Iran, 24-27 August 2008, pp. 71.

Talebi, A.A., Khoramabadi, A.M. and Rakhshani, E., 2011. J. Sp. Lists Distrib., 7: 708-719. https://doi.org/10.15560/11008

Vakis, N.J., 1975. J. econ. Ent., 68: 491-494.

Yefremova, Z., Ebrahimi, E. and Yegorenkova, E., 2007. Entomofauna, 28: 321-356.