Life table parameters of Hippodami variagata (Col.: Coccinellidae) by feeding on Nasonovia ribisnigri

Document Type : Research Paper

Authors

1 Department of Entomology, Islamic Azad University, Shiraz, Shiraz, Iran

2 Department of Entomology, Shi. C., Islamic Azad University, Shiraz, Iran

10.22059/ijpps.2026.409877.1007104

Abstract

Nasonovia ribisnigri is one of the important pests of lettuce. Hippodamia variegata with worldwide distribution, feed on it in Iran. The development, reproduction and life table parameters of H. variegata were studied by feeding on N. ribisnigri at three constant temperatures (20, 25 and 30 ± 1°C). 100 eggs of ladybeetle were selected and maintained individually in Petri dishes. Newly emerged larvae were transferred to individual dishes, then development and mortality were assessed. After the emergence of adults, males and females were paired and transferred to new dishes. They were checked daily to record survival and fecundity until death. The data showed that the duration of total pre-adult stage of ladybeetle was found to decrease with increasing temperature from 22.38 days at 20°C to 12.62 days at 30°C. The oviposition period lasted 61.81, 50.06and 35.41days, with females laying an average of 1102.02, 1253.61 and 587.86 eggs at these three temperatures, respectively. The lowest mortality rate was observed 14% at 25°CThe highest intrinsic rate of increase (rm), finite rate of increase (λ) and net reproductive rate (R0) was recorded 0.2413, 1.239 (d–1) and 819.03 (offspring) at 25°C, respectively. But there were no significant differences in these parameters at 25 and 30 ± 1°C. Also, the shortest mean generation time (T) 25.44 (day) was observed at 30°C. According to these results, it seems that the 25-30 ±1°C were the optimum temperature for biological activities of H. variegata and this species has greater efficiency in biological control of lettuce aphid in these temperatures.

Keywords


Extended Abstract

Introduction

    The lettuce aphid Nasonovia ribisnigri Mosely (Hemiptera: Aphididae) is recognized globally as one of the most destructive pests of lettuce crops. By colonizing the inner leaves of lettuce heads—where contact insecticides penetrate poorly—this aphid can cause severe yield loss, sometimes reducing production by more than 40%. The pest has expanded widely in Europe, North America, and parts of Asia, including Iran, where it has become a recurring challenge in lettuce-producing regions. Given the limited effectiveness of chemical control, natural enemies play a critical role in managing N. ribisnigri populations within integrated pest management (IPM) programs.

Among the predators of N. ribisnigri, the variegated ladybeetle Hippodamia variegata Goeze (Coleoptera: Coccinellidae) has particular importance. This species is widely distributed throughout the Palearctic and has been reported from a variety of agroecosystems, including cereals, vegetables, and ornamentals. In Iran, H. variegata occurs abundantly and preys on several aphid species. Previous studies have examined various biological aspects of this predator, showing that temperature, prey availability, and host species significantly influence its development and fecundity. However, no detailed age-stage, two-sex life table analysis had been conducted to quantify its population growth potential when feeding specifically on the lettuce aphid N. ribisnigri.

This study aimed to evaluate the developmental duration, survival, reproduction, and life table parameters of H. variegata feeding on N. ribisnigri under three constant temperatures—20, 25, and 30 ± 1°C. Determining the optimal temperature range for predator performance is essential for predicting its biocontrol potential in lettuce fields, facilitating better planning of augmentative releases and compatible IPM strategies.

Materials and Methods

Colonies of N. ribisnigri were collected from lettuce fields around Shiraz and maintained on fresh lettuce leaves in ventilated acrylic cylinders under controlled conditions. A stock colony of H. variegata adults was also collected from the same fields and reared for one generation to ensure acclimation to laboratory conditions.

For life-table experiments, one hundred eggs of H. variegata (less than 6 hours old) were individually placed on lettuce leaf discs positioned on agar gel inside Petri dishes. Three constant temperature regimes (20, 25, and 30 ± 1°C), 70 ± 10% RH, and a photoperiod of 16:8 (L:D) were used. Newly hatched larvae were isolated individually to prevent cannibalism, and fed ad libitum with all developmental stages of N. ribisnigri. Larvae, pupae, and adults were checked every 12 hours to record survival and developmental duration.

After adult emergence, one male and one female (each <6 hours old) were paired in new Petri dishes and monitored daily. The pre-oviposition period (APOP and TPOP), oviposition period, fecundity, and adult longevity were recorded until all individuals died.

Life table parameters were calculated using the age-stage, two-sex life table approach (Chi & Liu 1985; Chi & Su 2006) with TWOSEX-MSChart software. Parameters estimated included intrinsic rate of increase (rm), finite rate of increase (λ), net reproductive rate (R0), and mean generation time (T). Variances and standard errors were computed via bootstrap resampling (10,000 iterations), and means were compared using Tukey’s test at the 5% significance level.

Results

 Development and Survival

    Temperature had a significant effect on all developmental stages. Egg development decreased from 5. 0 days at 20°C to 1. 6 days at 30°C. Larval development across four instars and pupal duration also shortened significantly with increasing temperature. Total pre-adult development required 22.38 days at 20°C, 15 days at 25°C, and only 12.62 days at 30°C.

Pre-adult mortality was lowest at 25°C (14%), moderate at 20°C (20%), and highest at 30°C (31%), indicating some detrimental effects of elevated temperature despite faster development.

 

Adult Reproduction and Longevity

    Temperature strongly influenced reproductive performance. The adult pre-oviposition period (APOP) was shortest at 30°C (1.77 days) and longest at 20°C (4.0 days). The total pre-oviposition period (TPOP) also decreased markedly with increasing temperature.

Fecundity exhibited a non-linear trend: the highest fecundity occurred at 25°C, where females laid 1253.61 ± 17.8 eggs, significantly more than at 20°C (1102.14 eggs) or 30°C (587.86 eggs). The oviposition period also decreased at higher temperatures, spanning 61.81 days at 20°C, 50.06 days at 25°C, and 35.41 days at 30°C.

Adult longevity declined sharply at high temperature. Females lived 68.0 days at 20°C but only 40.1 days at 30°C. Males showed similar trends but generally shorter lifespans.

(a)                 Life Table Parameters

Life table analysis revealed 25°C as the optimal temperature for population growth:

  • Intrinsic rate of increase (rm):
    • 1452 ± 0.0031 at 20°C
    • 2143 ± 0.0039 at 25°C (highest)
    • 2131 ± 0.0093 at 30°C
  • Finite rate of increase (λ):
    • 1564 ± 0.0035 at 20°C
    • 239 ± 0.0048 at 25°C
    • 2376 ± 0.0115 at 30°C
  • Net reproductive rate (R0):
    • 69 ± 67.7 offspring at 20°C
    • 03 ± 68.9 offspring at 25°C (highest)
    • 39 ± 89.1 offspring at 30°C
  • Mean generation time (T):
    • 94 ± 0.44 days at 20°C
    • 27 ± 0.31 days at 25°C
    • 50 ± 0.25 days at 30°C (shortest)

Although development was fastest at 30°C, fecundity and survival declined, causing overall population growth to peak at 25°C.

Conclusion

    This study demonstrates that temperature profoundly influences the biology and population dynamics of H. variegata feeding on the lettuce aphid N. ribisnigri. While higher temperatures accelerate development, very warm conditions (30°C) reduce fecundity and survival. The optimal temperature range for predator performance lies between 25 and 30°C, with 25°C providing the highest population growth potential, as reflected by maximal rm, λ, and R0 values.

These findings indicate that H. variegata has strong potential as a biological control agent against N. ribisnigri under warm spring and early summer conditions typical of many lettuce-growing regions in Iran. Adoption of temperature-aware release strategies and integration of this predator into IPM programs can substantially enhance the sustainable management of lettuce aphid populations.

Author Contributions

Conceptualization, Sh.D. and Sh.H.; methodology, Sh.D and Sh.H. and M.Gh.; Research & Investigation, Sh. D.; software, Sh.D.; writing—original draft preparation, Sh.D.; writing—review and editing, Sh.H. and M.Gh.; All authors have read and agreed to the published version of the manuscript. Sh.H. is supervisor and M. Gh. is advisor of the project. All authors contributed equally to the conceptualization of the article and writing of the original and subsequent drafts.

Data availability statement

Data generated or analyzed during this study are provided in full within the published article.

Ethical considerations

All research followed ethical guidelines to minimize harm to insects and avoid disruption of natural habitats. Sampling was limited to the minimum necessary, and no endangered or protected species were collected. All activities complied with relevant regulations, and data were recorded and reported with integrity.

Conflicts of Interest

The authors declare that they have no conflicts of interest

منابع

اصغری، ف.، سمیع، م. ا. و مهدیان، ک. (1391). برخی ویژگی­های زیستی کفشدوزک Hippodamia variegata با تغذیه از شته مومی کلم و تخم بید آرد. مجله کنترل بیولوژیک آفات و بیماری های گیاهی، شماره 1. 19-27.
باقری، س.، طاووسی، م. و دهقانی، ع. (1387). معرفی Nasonovia ribsnigri (Hem:Aphididae) بعنوان مهمترین شته کاهو در جنوب استان خوزستان و بررسی تاثیر تاریخ کاشت و ارقام کاهو روی جمعیت آن. خلاصه مقالات هجدهمین کنگره گیاه پزشکی ایران، همدان، ایران، صفحه 79-80.
جعفری، ر.، وفایی شوشتری، ر. (1388). تاثیر دماهای مختلف روی طول دوره های نشوونمایی کفشدوزک (Hippodamia variegata Goeze (Col., Coccinellidae با تغذیه از شته باقلا (Aphis fabae Scopoli (Hem., Aphididae. تحقیقات حشره شناسی، 4 (1): 289-296.
رضوانی، ع. (1380). کلید شناسایی شته های ایران. انتشارات سازمان تحقیقات، آموزش و ترویج کشاورزی، وزارت جهادکشاورزی.
سالاری، س.، خنامانی، م. و اسدی، م. (1401). ارزیابی امکان کاربردکفشدوزک Hippodamia variegata و رقم مقاوم گل رز در مدیریت شته رز Macrosiphum rosae. تحقیقات آفات گیاهی، 12(2): 61-76. https://doi.org/10.22124/iprj.2022.5795
طالبی،ع. ا.، جریانی، ر. و اللهیاری، ح. (1393). ویژگی‌هایی از زیست شناسی کفشدوزک Hippodamia variegata (Col.: Coccinellidae) روی سه گونه شته‌ی غلات. مجله پژوهشهای جانوری (مجله زیست شناسی ایران)، 27 (2): 260-269.
فارسی، ا.، کچیلی، ف.، مصدق، م.، راسخ، ا. و طاوسی، م. (1393). تغییرات فصلی و توزیع فضایی شته کاهو Nasonovia ribisnigri Mosely (Hem.: Aphididae)، در اهواز. فصلنامه تحقیقات آفات گیاهی، 4:1-12.
فارسی، ا.، کچیلی، ف.، مصدق، م.، راسخ، ا. و طاوسی، م. (1399). تاثیر دما بر ویژگی های زیستی و توان تغذیه ای Episyrphus balteatus شکارگر مهم شته کاهو Nasonovia ribisnigri. نامه انجمن حشره شناسی ایران، 40 (1): 83-93.
فرهادی، ر.، اللهیاری، ح.، راسخ، آ.، الداغی، م. و فرهودی، ف. (1390). مقایسه پارامترهای جدول زندگی کفشدوزک Hippodamia variegata (Col.: Coccinellidae) و شته سیاه باقلا Aphis fabae (Hem.: Aphididae).. مجله دانش گیاه­پزشکی ایران، 42 (2): 209-215.
مـلاشاهی، م.، صـحراگرد، ا. و حسیـنی، ر. (1383). تعیین پارامترهای جدول زندگی کفشدوزک Hippodamia variegata (Col.: Coccinellidae) در شرایط آزمایشگاهی. پژوهشنامه علوم کشاورزی. 1: 47-60.
مهاجری پاریزی، ع.، مددی، ح.، الهیاری، ح. و مهرنژاد، م.ر. (1391). پارامترهای جدول زندگی کفشدوزک Hippodamia variegata با تغذیه از شته‌های Aphis gossypii و Acyrthosiphon pisum. دانش گیاهپزشکی ایران، 43(1): 73-81.
نیکان چاپلو،‌ س. گلی زاده، علی. حسن پور، م. نوری قنبلانی، ق. ناصری، ب. و غفوری مقدم، م. (1392). زیست شناسی کفشدوزک شکارگر Hippodamia variegata با تغذیه از شته‌ی مومی کلم Brevicoryne brassicae روی شلغم و تربچه. همایش کنترل بیولوژیک در کشاورزی و منابع طبیعی، دانشگاه تهران، صفحات 77-76.
 
REFERENCES
Asghari, F., Samih, M. A. & Mahdian, K. (2012). Some Biological Characteristics of Hippodamia variegata (Goeze) Reared on Brevicoryne brassicae L. and Eggs of Ephestia kuehniella Zeller. Biological Control of Pests and Plant Diseases, 1(1), 19-27. doi: 10.22059/jbioc.2012.32071 (In Persian).
Bagheri, S., Tavosi, M. & Dehghani, A. (2008). Introduction of Nasonovia ribisnigri (Mosely) (Hom.: Aphididae) as the most important lettuce aphid in south of Khuzestan province and study on the effect of cultivation date and lettuce cultivars on its population. Proceedings of 18th Iranian Plant Protection Congress, Hamedan, Iran, 79-80.
Chi H. (2021). TWOSEX-MSChart: A Computer Program for the Age Stage, Two-Sex Life Table Analysis. National Chung Hsing University; Taichung, Taiwan (accessed on 8 March 2021). Available online: https://lifetablechi.com/software/.
Chi, H. and Su, H. Y. (2006). Age–stage, two–sex life tables of Aphidius gifuensis (Ashmead) (Hymenoptera: Braconidae) and its host Myzus persicae (Sulzer) (Homoptera: Aphididae) with mathematical proof of the relationship between female fecundity and the net reproductive rate. Environmental Entomology, 35: 10-21.
Chi, H., and Liu, H. (1985). Two new methods for the study of insect population ecology Bulletin of the Institute of Zoology, Academia Sinica 24: 225-240.
Della Porta, B. (2021). Biological Control and Population Dynamics of Aphids (Hemiptera:Aphididae) and Their Natural Enemies in Protected and Open Field Agroecosystems. M. Sc. Thesis, School of Life Sciences, La Trobe University, Victoria, Australia.
Diaz, B. M., Muñiz, M., Barrios, L., & Fereres, A. (2007). Temperature thresholds and thermal requirements for development of Nasonovia ribisnigri (Hemiptera: Aphididae). Environmental Entomology, 36(4), 681–688. https://doi.org/10.1603/0046-225x(2007)36[681:ttatrf]2.0.co;2
Dou, S., Liu, B., Liu, Y., Zhang, J., & Lu, Y. (2023). Intraguild predation of Hippodamia variegata on aphid mummies in cotton field. Insects, 14(1), 81. https://doi.org/10.3390/insects14010081
Farhadi, R., Allahyari, H., Rasekh, A., Aldaghi, M. & Farhoudi, F. (2011). Comparative Study of Life Table Parameters of Hippodamia variegata (Col.: Coccinellidae) vs. Aphis fabae (Hem.: Aphididae). Iranian Journal of Plant Protection Science, 42(2), 209-215. doi: 10.22059/ijpps.2012.24328
Farsi, A., Kocheili, F., Mossadegh, M. S., Rasekh, A. & Tavoosi, M. (2014). Natural enemies of the currant lettuce aphid, Nasonovia ribisnigri (Mosely) (Hemiptera: Aphididae) and their population fluctuations in Ahvaz, Iran. Journal of Crop Protection, 3(4): 487-497.
Farsi, A., Kocheili, F., Mossadegh, M. S., Rasekh, A. & Tavoosi, M. (2015). Seasonal dynamics and spatial distribution of the lettuce aphid, Nasonovia ribisnigri Mosely (Hem.: Aphididae) in Ahvaz Plant Pest Research, 4(4), 1-12. (in Persian).
Farsi, A., Kocheili, F., Mossadegh, M. S., Rasekh, A. & Tavoosi, M. (2020). Effect of temperature on biological characteristics and feeding capacity of Episyrphus balteatus (Diptera: Syrphidae) as important predator of the currant lettuce aphid, Nasonovia ribisnigri (Hemiptera: Aphididae). Journal of Entomological Society of Iran, 40 (1): 83-93.
Hosseini, A., Hosseini, M., Rohani, A., & Lawson, S. (2023). Modeling reproductive fitness of predator, Hippodamia variegata (Coleoptera: Coccinellidae) using support vector machine (SVM) on three nitrogen treatments. Neural Computing and Applications. https://doi.org/10.1007/s00521-023-09020-y
Huang, Y., Gu, X., Peng, X., Tao, M., Chen, G. & Zhang, X. (2020). Effect of short-term high-temperatures on the growth, development and reproduction in the fruit fly, Bactrocera tau (Diptera: Tephritidae). Scientific Report, 10, 6418. https://doi.org/10.1038/s41598-020-63502-w
Jafari, R. & Vafaei Shoushtari, R. (2010). Effect of different temperatures on life developmental stages  of Hippodamia variegata Goeze (Col., Coccinellidae), feeding  on Aphis fabae Scopoli (Hem., Aphididae). IAU Entomological Research Journal, 4 (1): 289-296.
Khattawi, S., Kayahan, A., & Karaca, İ. (2022). Functional and numerical response of Hippodamia variegata (Goeze) (Coleoptera: Coccinellidae) on Macrosiphum rosae (L.) (Hemiptera: Aphididae). International Journal of Agriculture, Environment and Food Sciences, 6(2), 311-318. https://doi.org/10.31015/jaefs.2022.2.15
Kontodimas, D. C. & Stathas, G. J. (2005). Phenology, fecundity and life table parameters of the predator Hipopodamia variegata reared on Dysaphis crataegi. Biocontrol, 50: 223-233.
Liu, H.-L., Yong, Y.-P., Wu, X.-L., Chen, Z.-T., Wei, S.-J., Cai, P., & Pu, D.-Q. (2025). Chromosome-level genome assembly of the Adonis ladybird Hippodamia variegata. Scientific Data, 12, 558. https://doi.org/10.1038/s41597-025-04882-4
Mackenzie, J. R. (1986). Improved insect pest management of crisp head lettuce grown in S. W. British Columbia. M.Sc. Thesis, Simon Fraser University, 150 pp.
McDougall, S. (2012). The delivery of IPM for the lettuce industry. Project Number: VG07076, Horticulture Australia Ltd.
Mohajeri parizi, E., Madadi, H., Alahyari, H. & Mehrnejad, M. R. (2012). A Comparison of Life History Parameters of Hippodamia variegata Feeding on either Aphis gossypii Glover or Acyrthosiphon pisum. Iranian Journal of Plant Protection Science, 43(1), 73-81.
Mollashahi, M., Sahragard, A. & Hossaini, R. (2004). Determination of life table parameters of lady beetle, Hippodamia variegata (Col: Coccinellidae) under laboratory conditions. Journal of Agricultural Science, 1: 47-60.
Morales, I., Diaz, B. M., Mendoza, A. H. D., Nebreda, M. & Fereres, A. (2013). The development of an economic threshold for Nasonovia ribisnigri (Hemiptera: Aphididae) on lettuce in central Spain. Journal of Economic Entomology, 106(2), 891-898.
Nikan-Chaploo, S., Golizadeh, A., Hasanpour, M., Noori Ghanbalani, Gh., Naseri, B. & Ghafoorimoghadam, M. (2003). Biology of Hippodamia variegata feeding on the cabbage aphid Brevicoryne brassicae on Turnip and radish. Proceedings of Conference of Biological Control in Agriculture and natural Resources, Tehran University, pp.76-77.
Obrycki, J. J. & Orr, C. J. (1990). Suitability of 3 prey species for Nearctic populations of Coccinella septempunctata, Hippodamia variegata, and Propylea quatuordecimpunctata (Coleoptera: Coccinellidae). Journal of Economic Entomology, 83: 1292-1297.
Palumbo, J. C. (1999). Preliminary examination of the population dynamics and control of the lettuce aphid on romaine. Report no.AZ1143, Series P-118 , http://ag.arizona.edu/pubs/crops/az1143.
Rezvani, A. (2001). Identify key of aphids in Iran. Agriculture Research, Education and Extension Organization, Tehran, Iran (In Persian)
Salari, A. , Khanamani, M. & Asadi, M. (2022). Assessing compatibility of Hippodamia variegata and resistant rose cultivar in the management of Macrosiphum rosae. Plant Pest Research, 12(2), 61-76. https://doi.org/10.22124/iprj.2022.5795
Talebi, A.A., Jaryani, R. & Allahyari, H. (2014). Some biological characteristics of Hippodamia variegata (Col.: Coccinellidae) rearing on three species of Wheat Aphids. Journal of Animal Research (Iranian Journal of Biology), 27(2), 260-269.
Tao, Y. D., Liu, Y., Wan, X. S., Xu, J., Fu, D. Y., & Zhang, J. Z. (2023). High and low temperatures differentially affect survival, reproduction, and gene transcription in male and female moths of Spodoptera frugiperda. Insects, 14(12), 958. https://doi.org/10.3390/insects14120958.
Wang, Y.H., Liu, B.S., Fu, H.Z. & Gu, L.N. (1984) Studies on the habits and bionomics of Adonia variegata Goze (Col:Coccinellidae). Insect Knowledg.Kunchung-Zhiski, China Cotton, 21(1): 19-22.
Wang, Y., Zhang, Y., Zhang, T., Li, Z., Liu, T., & Lu, Y. (2025). Behavioral and electrophysiological responses of Hippodamia variegata to plant volatiles. PLoS ONE, 20(6), e0327160. https://doi.org/10.1371/journal.pone.0327160
Yang, Q., Liu, J., Wyckhuys, K. A. G., Yang, Y., & Lu, Y. (2022). Impact of Heat Stress on the Predatory Ladybugs Hippodamia variegata and Propylaea quatuordecimpunctata. Insects, 13(3), 306. https://doi.org/10.3390/insects13030306
Yu, J. Z., Chi, H. and Chen, B. H. (2013). Comparison of the life tables and predation rates of Harmonia dimidiata (F.) (Coleoptera: Coccinellidae) fed on Aphis gossypii Glover (Hemiptera: Aphididae) at different temperatures. Biological Control, 64: 1-9.