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Ooencyrtus pityocampae Mercet (Hymenoptera: Encyrtidae): a potential biocontrol agent of the seed bug, Leptoglossus occidentalis Heidemann (Heteroptera: Coreidae)

Abstract

Background

Western conifer seed bug, Leptoglossus occidentalis Heidemann (Hemiptera: Coreidae), is an invasive polyphagous pest of coniferous trees. It causes serious economic losses in pine kernel production. Biocontrol of L. occidentalis through the egg parasitoid Ooencyrtus pityocampae Mercet (Hymenoptera: Encyrtidae) seems to be sustainable solution to reduce economic losses of the pest. In this study, the biology of O. pityocampae was investigated on its natural host, L. occidentalis, under laboratory conditions.

Results

In this context, the effects of host age, female age, and temperature on parasitism rate, emergence rate, developmental time, and longevity were investigated. Female age had a great influence on the parasitism rate. Parasitism rates were 8.0, 17.0, and 37.3% in 1-, 3-, and 5-day-old females, respectively. There was no effect of host age or female age on emergence rates at the two different temperatures (25 and 30 °C). Emergence rate ranged from 74.0 to 88.3%. The longest developmental time (17.9 d) was obtained on 3-day-old hosts at 25 °C. The longevity, which was one of the important criteria of the parasitoid, was significantly affected by temperature.

Conclusion

The results of this study on the biology of O. pityocampae may contribute significantly to the biological control studies of L. occidentalis. This egg parasitoid can be mass-produced on lepidopteran hosts for field releases against L. occidentalis.

Background

The Western conifer seed bug, Leptoglossus occidentalis Heidemann (Heteroptera: Coreidae), is an important conifer pest that feeds on the seeds’ sap of coniferous trees, causing empty seeds. This pest is a North American origin. It was described in 1910 (Heidemann 1910). The pest is often found on pine trees (approximately 40 species) (Maltese et al. 2009) that feeds on young cones, sucking the sap from seeds containing protein and oil and causing empty seeds formation. Young cones fall prematurely due to the feeding. Regarding the economic damage of the species in Türkiye, the first detection was on Pinus pinea fields in İzmir-Bergama, causing economic losses in this region (Parlak 2017). For the control of harmful insects in forest areas, ecofriendly methods are preferred and one of them is biological control. Studies of the parasitoids of L. occidentalis are faunistic surveys. Ridge-O’Conner (2001) found the generalist adult parasitoid, Trichopoda pennipes (Fabricius 1781) (Diptera: Tachinidae), on the pest. Camponogara et al. (2003) reported the generalist egg parasitoid, Anastatus bifasciatus (Geoffroy) (Hymenoptera: Eupelmidae), on L. occidentalis egg masses. Bates and Borden (2004) reported another three egg parasitoids, Gryon pennsylvanicum Ashmead (Hymenoptera: Scelionidae), Anastatus pearsalli Ashmead (Hymenoptera: Eupelmidae), and Ooencyrtus spp. (Hymenoptera: Encyrtidae). Maltese et al. (2012) identified three egg parasitoids: Gryon pennsylvanicum Ashmead (Hymenoptera: Platygastridae), Ooencyrtus johnsoni Howard (Hymenoptera: Encyrtidae), and Anastatus pearsalli Ashmead (Hymenoptera: Eupelmidae). Oğuzoğlu ve Avcı (2020) reported two egg parasitoids: Anastatus bifasciatus (Geoffroy, 1785) (Hymenoptera: Eupelmidae) and Ooencyrtus telenomicida Vassiliev (Hymenoptera: Encyrtidae) on the L. occidentalis egg masses. Lesieur and Farinha (2021) recorded three egg parasitoids: Anastatus bifasciatus, Ooencyrtus pityocampae, and O. telenomicida. Ponce-Herrero et al. (2022) reported two native parasitoid species, Ooencyrtus pityocampae Mercet and O. obscurus Mercet (Hymenoptera: Encyrtidae), on the L. occidentalis eggs in Spain. As few biological studies have been carried out on the egg parasitoids of L. occidentalis, except of Binazzi et al. (2013), this study evaluated the effects of host and female ages on the potential of the parasitoid O. pityocampae at two different temperatures under laboratory conditions.

Methods

Rearing of Leptoglossus occidentalis

Leptoglossus occidentalis was collected from Pinus spp. fields around Bursa-Orhaneli province (39.751435° Lat-29.050089° Long and 996 m), in Türkiye. The collected adults were transferred to the biological control laboratory of Ankara University, Faculty of Agriculture, Department of Plant Protection. Adults were placed in the insect rearing box and kept under the climatic room (25 ± 1 °C, RH 65 ± 5% and L:D 16:8 h photoperiod). Pine nut seeds were provided for adults feeding, and Pinus sylvestris branches were placed in the box for females laying eggs. Moistened cotton with a solution honey water (10%) was placed inside a Petri dish to provide water and carbohydrates to the adults. In order to prevent adults from getting stressed, three Petri dishes with soil were also placed inside the rearing box.

Rearing of Ooencyrtus pityocampae

Eggs of the pine moth were collected from İzmir-Torbalı (38.178319° Lat-27.393717° Long and (94–227 m) province. Collected parasitized egg batches of pine processionary moth were transferred to a rearing room under controlled conditions of (25 ± 1 °C, RH 65 ± 5% and L:D 16:8 h photoperiod). The scales of the egg batches were removed and placed individually in test glass tubes closed by cotton and kept at the rearing room. The tubes were checked daily and the emerged parasitoids were separated, after they were identified under a stereomicroscope. Parasitoids O. pityocampae were placed into tubes separately and fed on honey water (10%) and maintained at a rearing room at (25 ± 1 °C, RH 65 ± 5% and L:D 16:8 h photoperiod). Daily collected L. occidentalis eggs were offered to the parasitoid, and their progeny were allowed to emerge. After their emergency, adult parasitoids were used in the experiments for the establishment of parasitoid cultures. Parasitoids were reared for over 10 generations on eggs of L. occidentalis.

Experimental procedures

To investigate the effect of female age, host egg age, and temperature, a 3 (1, 3, or 5 days old) × 2 (1 or 3 days) × 2 (25 or 30 °C) factorial design with 15 replicates was tested. In this experiment, 20 unparasitized L. occidentalis eggs (either 1 or 3 days old) were exposed in a test tube (1 × 7 cm) to one female of O. pityocampae (1, 3, or 5 days old) for 24-h parasitism at the two temperatures. The tested tubes were covered by cotton. Test tubes were checked daily until adult parasitoids emerged. Nymphs that hatched from unparasitized eggs were removed, and parasitism rate was calculated as a percentage. Number of the newly emerged O. pityocampae individuals was recorded daily. Emergence rate was calculated. To determine the longevity, honey water (10%) was given to adult parasitoids for feeding.

Statistical analysis

Parasitism rate, emergence rate, developmental time, and adult longevity were analyzed using a general linear model (GLM). Percentage data were normalized using an arcsine transformation (Zar 1999). The means were compared with Tukey’s test at a significance level of α = 0.05 (McKenzie and Goldman 2005; Minitab Release 14 2004; SAS Institute 2003).

Results

Statistical results are summarized in Tables 1, 2, 4, and 6. Only females’ age had an effect on the parasitism rate (Table 1) (F2 = 128.51, P < 0.001). The parasitism rate increased with the increase in the female age. The percentage of parasitism by O. pityocampae was nonsignificantly affected by host age (F1 = 2.17, P = 0.143) and temperature (F1 = 0.95, P = 0.332). The parasitism rate was the highest at the parasitoid age of 5 days (37. 3%). Parasitism rates were 8.0 and 17.0% in 1- and 3-day-old females, respectively. All observed factors and interactions were nonsignificant on the emergence rate (Table 2). All of the emergence rates ranged from 74.0 to 88.3% (Table 3). There was a significant interaction between the host age and temperature (F1 = 12.01, P = 0.001) on the developmental time of O. pityocampae (Table 4). The longest developmental time (17.9 days) was obtained from the 3-day-old L. occidentalis eggs at 25 °C, whereas the shortest development time (13.4) was obtained from the 1-day-old L. occidentalis eggs at 30 °C (Table 5). There was a significant two-way interaction between the female age and temperature on the longevity (F2 = 4.09, P = 0.018) (Table 6). The longest longevity (34.8 days) was obtained from the 5-day-old female at 25 °C, while the shortest one (21.0 days) was obtained from the 5-day-old female at 30 °C (Table 7).

Table 1 Results of the GLM analysis of the parasitism rate of Ooencyrtus pityocampae
Table 2 Results of the GLM analysis of the emergence rate of Ooencyrtus pityocampae
Table 3 Results of the GLM analysis of the emergence rate of Ooencyrtus pityocampae
Table 4 Results of the GLM analysis of the development time of Ooencyrtus pityocampae
Table 5 Development time of Ooencyrtus pityocampae
Table 6 Results of the GLM analysis of the longevity of Ooencyrtus pityocampae
Table 7 Longevity of Ooencyrtus pityocampae

Discussion

The western conifer seed bug, L. occidentalis, is an economically damaging pest of stone pines (İpekdal et al. 2019). The habitat of the L. occidentalis is the forest areas; therefore, the use of insecticides for its control is extremely inconvenient. Biological control can be a key method for managing pests’ populations in long-lived crops such as forestry plantations (Fischbein and Corley 2015). In this study, some biological characteristics of the synovigenic egg parasitoid O. pityocampae were determined on its natural host, L. occidentalis, at two different temperatures. Results of the parasitism rate showed that female age of O. pityocampae was important for successful parasitism and had an effect on the parasitism rate. Highest parasitism rate (37.3%) was recorded in 5-day-old female parasitoids. The result was also supported by other researchers (Tunca et al. 2019). The effect of female age can vary depending on the parasitoid biological characteristics, such as synovigenic or pro-ovigenic.

All emergence rates were found above 74%. The emergence rate of O. pityocampae on the host Philosamia ricini Donovan (Lepidoptera: Saturniidae) differed according to the female age and host number. It ranged from 59.3 to 87.2% (Tunca et al. 2016). Tunca et al. (2019) reported that the emergence rate of O. pityocampae on the host Halyomorpha halys Stål (Hemiptera: Pentatomidae) differed according to the host age and time of exposure.

The developmental time of the O. pityocampae was affected by temperature and host age. A shorter developmental time was obtained in one-day-old L. occidentalis eggs at 30 °C. The development of parasitoids was affected by the change of host species from which they developed (Jones et al. 2015) and temperature (Jerbi-Elayed et al 2021). Tunca et al. (2016) reported that the development time of O. pityocampae was influenced by the interaction of four factors (parasitoid age, parasitoid number, host number, and host egg age) on the host P. ricini. All of the developmental times ranged from 19.5 to 22.6 days. Also, three-way interactions among the host density, host age, and time of exposure on the H. halys were obtained. Developmental times ranged from 17.1 to 18.3 days (Tunca et al. 2019).

In the present study, it was found that the temperature significantly reduced the life span. In parasitoids, host species affects longevity; the life span of O. pityocampae was 46 days on P. ricini and 44 days on H. halys (Tunca et al. 2016 and Tunca et al. 2019).

Conclusion

The present study showed that the egg parasitoid O. pityocampae can be a potential biocontrol agent against L. occidentalis in pine trees, but further studies are needed.

Availability of data and materials

The datasets used and analyzed during this study are available from the corresponding author upon reasonable request.

References

  • Bates SL, Borden JH (2004) Parasitoids of Leptoglossus occidentalis Heidemann (Heteroptera: Coreidae) in British Columbia. J Entomol Soc Br Columb 101:143–144

    Google Scholar 

  • Binazzi F, Benassai D, Sabbatini Peverieri G, Roversi PF (2013) Effects of Leptoglossus occidentalis Heidemann (Heteroptera Coreidae) egg age on the indigenous parasitoid Ooencyrtus pityocampae Mercet (Hymenoptera: Encyrtidae). REDIA XCVI:79–84

    Google Scholar 

  • Camponogara P, Festi M, Battisti A (2003) La cimice dei semi americana: unospite indesiderato delle conifere. Vita Camp 2003:7–8

    Google Scholar 

  • Fischbein D, Corley JC (2015) Classical biological control of an invasive forest pest: a world perspective of the management of Sirex noctilio using the parasitoid Ibalia leucospoides (Hymenoptera: Ibaliidae). Bull Entomol Res 105(1):1–12. https://doi.org/10.1017/S0007485314000418

    Article  CAS  PubMed  Google Scholar 

  • Heidemann O (1910) New species of Leptoglossus from North America Hemiptera: Coreidae). Proc Entomol Soc Wash 12:191–197

    Google Scholar 

  • İpekdal K, Oğuzoğlu Ş, Oskay F, Aksu Y, Doğmuş Lehtijarvi HT, Lehtijarvi A H, Aday Kaya, AG, Can T, Özçankaya M, Avcı M. (2019) Western Conifer Seed Bug Leptoglossus occidentalis Heidemann (1910) (Hemiptera: Coreidae) Current Situation in the World and Turkey. General Directorate of Forestry, Ankara, Turkey

  • Jerbi-Elayed M, Foray V, Tougeron K, Grissa-Lebdi K, Hance T (2021) Developmental temperature affects life-history traits and heat tolerance in the aphid parasitoid Aphidius colemani. Insects 12:852. https://doi.org/10.3390/insects12100852

    Article  PubMed  PubMed Central  Google Scholar 

  • Jones TS, Bilton AR, Mak L, Sait SM (2015) Host switching in a generalist parasitoid: contrasting transient and transgenerational costs associated with novel and original host species. Ecol Evol 5(2):459–465. https://doi.org/10.1002/ece3.1333

    Article  PubMed  PubMed Central  Google Scholar 

  • Lesieur V, Farinha AO (2021) Responses of native egg parasitoids to the invasive seed bug Leptoglossus occidentalis. Agric for Entomol 23:323–333

    Article  Google Scholar 

  • Maltese M, Caleca V, Guerrieri E, Strong WB (2012) Parasitoids of Leptoglossus occidentalis Heidemann (Heteroptera: Coreidae) recovered in western North America and first record of its egg parasitoid Gryon pennsylvanicum (Ashmead) (Hymenoptera: Platygastridae) in California. Pan-Pac Entomol 188:347–355. https://doi.org/10.3956/2012-23.1

    Article  Google Scholar 

  • Maltese M, Caleca V, Carapezza A (2009) Primi reperti in Sicilia su diffusione e biologia di Leptoglossus occidentalis Heidemann (Heteroptera: Coreidae), cimice americana dei semi delle conifere. In: Atti del Terzo Congresso Nazionale di Selvicoltura. Taormina (ME), 16–19 ottobre 2008. Accademia Italiana di Scienze Forestali, Firenze, pp 1413–1418

  • McKenzie JD, Goldman R (2005) The student guide to Minitab release 14. Pearson Education, Boston

    Google Scholar 

  • MINITAB Release 14 (2004) Statistical software for windows

  • Oğuzoğlu Ş, Avcı M (2020) Türkiye’de Leptoglossus occidentalis Heidemann, 1910 (Hemiptera: Coreidae) üzerine biyolojik gözlemler, parazitoitleri ve yayılışına katkılar. Ormanc Araşt Derg 7(1):9–21

    Article  Google Scholar 

  • Parlak S (2017) An invasive species: Leptoglossus occidentalis (Heidemann) how does it affect f orestry a ctivities? Kastamonu Univ J For Fac 17(3):531–542

    Google Scholar 

  • Ponce-Herrero L, Farinha AO, Fernández VP, Alonso JAP, Santos FMA (2022) Native egg parasitoids on Leptoglossus occidentalis Heidemann (Hemiptera: Coreidae) in Spain: potential biological control agents? J App Entomol 146(5):525–538

    Article  Google Scholar 

  • Ridge-O’Conner GE (2001) Distribution of the western conifer seed bug, Leptoglossus occidentalis Heidemann (Heteroptera: Coreidae) in Connecticut and parasitism by a tachinid fly, Trichopoda pennipes (F.) (Diptera: Tachinidae). Proc Entomol Soc Wash 103:364–366

    Google Scholar 

  • SAS Institute (2003) SAS/STAT version 8.2. SAS Institute, Cary

    Google Scholar 

  • Tunca H, Colombel EA, Ben Soussan T, Galio F, Tabone E (2016) Optimal biological parameters for rearing Ooencyrtus pityocampae on the new laboratory host Philosamia ricini. J App Entomol 140(7):527–535. https://doi.org/10.1111/jen.12282

    Article  CAS  Google Scholar 

  • Tunca H, Venard M, Colombel EA, Capelli M, Tabone E (2019) Life history traits of Ooencyrtus pityocampae (Hymenoptera: Encyrtidae) reared on Halyomorpha halys eggs (hemiptera: Pentatomidae). Entomol Gen 39(2):93–101. https://doi.org/10.1127/entomologia/2019/0761

    Article  Google Scholar 

  • Zar JH (1999) Biostatistical analysis, 4th edn. Prentice-Hall, Upper Sadle River

    Google Scholar 

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Acknowledgements

All authors acknowledged the Bursa General Directorate of Forestry, for their support in providing necessary facilities for the study.

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HTC contributed to investigations, writing, editing, and data analysis; ET, BC, ÖT, and AE helped in supervisions, methodology, and writing review. DÇ contributed to the rearing of insects. All authors have read and approved the final manuscript.

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Correspondence to Hilal Tunca Cosic.

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Tunca Cosic, H., Tabone, E., Çaycı, D. et al. Ooencyrtus pityocampae Mercet (Hymenoptera: Encyrtidae): a potential biocontrol agent of the seed bug, Leptoglossus occidentalis Heidemann (Heteroptera: Coreidae). Egypt J Biol Pest Control 32, 117 (2022). https://doi.org/10.1186/s41938-022-00615-6

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Keywords

  • Leptoglossus occidentalis
  • Ooencyrtus pityocampae
  • Biological control