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FEEDING BEHAVIOR OF PREDATORY BUG NABIS FERUS (HETEROPTERA: NABIDAE)
TOWARD APHIDS
Elena I. Shatalova
Siberian Federal Scientific Centre ofAgrobiotechnologies of the Russian Academy of Sciences (SFSCA RAS),
Krasnoobsk, Russia Novosibirsk State Agrarian University, Novosibirsk, Russia
e-mail: [email protected]
This study investigated the feeding behavior of the generalist predator Nabis ferus (Heteroptera: Nabidae) toward various Aphididae species as prey in a laboratory setting. Data were obtained on the predatory behavior of N. ferus, including a ranking of the most preferred species for feed. Eight representatives of the Aphididae family were used as prey: Schizaphis graminum, Rhopalosiphum padi, Aphis fabae, Megoura viciae, Brevicoryne brassicae, Aphis pomi, Myzus cerasi and Aphis urticata. The average number of prey ranged from 11.2±1.18 in the case of bird cherry-oat aphid to 13.7±0.38 in case of the apple aphid. The consumption of M. viciae individuals was significantly lower, averaging 6.6±1.03 aphids per predator. These studies have implications for the biological control of phytophagous pests in agriculture. These findings highlight the potential of N. ferus as a sustainable and effective control agent to organic farming.
Keywords: Nabis ferus, predator, prey, entomophagous insect, biological control Submitted: 24.06.2024 Accepted: 30.08.2024
Population dynamics of phytophagous pests are significantly influenced by numerous, polyphagous, and eurytopic species within the genus Nabis, commonly found in natural and agricultural ecosystems. Nabis species feed on eggs, larvae, and even adults of various arthropods, including many significant pests such as the Colorado potato beetle, alfalfa weevil, cereal leaf beetle, various aphids, bugs, leafhoppers, thrips, mites, lepidopterans, and sawflies. They are crucial natural regulators of insect pest populations in agriculture and forestry (Bokina 2013, 2018; Esenbekova 2013; Cornelise et al. 2021; Shrestha et al. 2021; Smith et al. 2022).
In the Asian part of Russia, there are six species of the genus Nabis, belonging to two subgenera: Nabis Latr. and Himacerus Wolff. Five species from the genus Nabis predominantly inhabit herbaceous vegetation, including cereal agroecosystems. These species are N. ferus L., N. punctatus A. Costa, N. brevis Scholtz, N. limbatus Dahlbom, and N. flavomarginatus Scholtz. Several studies highlight the significant role of nabids in agroecosystems (Bokina 2013; Fernandez-Maldonado et al. 2017; Bokina 2018; Kim et al. 2019). For instance, species of the genus Himacerus, known as dendro-tamno-hortobionts, notably H. apterus Fabricus, exert a substantial impact on the population of tree and shrub consumers (Bokina 2013).
Despite the abundance of natural populations of the Nabidae family, they have not yet been widely applied in the
Material
Laboratory rearing of Nabis ferus. Nabis ferus was isolated in May 2023 from nature in Krasnoobsk (54.915278 N, 82.978686 E) and Poros (55.368912 N, 83.712526 E), Novosibirsk Province, Western Siberia, Russia, and
practice of biological plant protection. There are only a few studies dedicated to individual representatives of this group. Techniques for maintaining such predators as N. pseudoferus Remane and N. rugosus Linnaeus under laboratory conditions exist (Roth et al. 2008; Efe, Karaea 2013; Fernandez et al. 2020). Nabis pseudoferus is positioned as a promising agent for controlling the tomato leaf miner Tuta absoluta (Cabello et al. 2009; Mohammadpour et al. 2020). Currently, N. stenoferus Hsiao is considered as a biological control agent against phytophagous pests, which, due to its zoophytophagy, can damage flowering crops (Park et al. 2023). Nabis americoferus is also considered as a biological control agent against the dangerous strawberry pest Lygus lineolaris (Dumont et al. 2023).
One of the widely distributed species across the Eurasian continent is N. ferus, a zoophytophagous predator that ambushes its prey. To effectively use this bug for crop protection, it is necessary to find suitable environmental conditions (Park et al. 2023), including additional feed sources. Overall, the prey spectrum of Nabis ferus is insufficiently studied. Some studies report N. ferus feeding on cereal aphids, while information about the consumption of other Aphidoidea prey and other insects is sporadic (Puchkov 1980; Bokina 2013, 2018). A goal of this study was to determine the spectrum of potential prey for the adults of N. ferus for assessing its potential as a biological control agent to organic farming.
and methods
introduced into a laboratory culture. It is maintained in the Laboratory of the Biological Control of Phytophagous Pests and Phytopathogens at the Siberian Federal Scientific Centre of Agrobiotechnologies of the Russian Academy of Sciences
© Shatalova E. I., published by All-Russian Institute of Plant Protection (St. Petersburg).
This is an open access article distributed under the terms of the Creative Commons Attribution License 4.0
(http://creativecommons.org/licenses/by/4.0/).
(SFSCA RAS). The rearing of this entomophagous bug is conducted in 40*40*40 cm cages on wheat sprouts infested with the wheat aphid, Schizaphis graminum Rond. The culturing regime is day:night 18:6, relative humidity 50-60 %, and temperature 25 °C. Nabis ferus adults, kept without food for one day before the experiment, was used for experiments.
Feed sources. Various representatives of the Aphididae family were used as prey. The wheat aphid (Schizaphis graminum Rond.), the bird cherry-oat aphid (Rhopalosiphum padi L.), the black bean aphid (Aphis fabae Scopoli), the vetch aphid (Megoura viciae Buckton), and the cabbage aphid (Brevicoryne brassicae L.) are reared year-round in the Laboratory of Biological Control of Phytophagous Pests and Phytopathogens at SFSCA RAS on suitable species of host plants: wheat, fodder beans, and white cabbage. The apple aphid (Aphis pomi De Geer), the cherry aphid (Myzus cerasi Fabricius), and the nettle aphid (Aphis urticata J.F. Gmelin) were collected from natural and agricultural habitats.
Experimental design. In Petri dishes (0 9 cm) with moistened filter paper, a plant leaf with 15 insect prey individuals for each replication was placed, followed by the introduction of one Nabisferus adults regardless of sex. Control treatments without the predator were used to account for the
effects of transplantation, natural mortality, and to calculate Abbott's corrected mortality. After 24 hours, the numbers of dead and surviving phytophagous insects were recorded. All treatments in the trial were replicated using the same number of different individuals of N. ferus (n = 15 insects/day) for each day. After assessing the mortalities of the insects on each counting day, the insects and Petri dishes corresponding to that day were removed from the experiment.
Statistical analysis. The numbers of dead prey in each treatment were analyzed after verifying normal distribution of the data using QQ-plots, and differences between treatments were determined using the Kruskal-Wallis test followed by Dwass-Steel-Critchlow-Fligner (DSCF) test for multiple comparisons (Jamovi for Windows 2.3.28.0, Jamovi Computer Software, https://www.jamovi.org/). Descriptive statistics and graphs were produced using LibreOffice 7.6. Differences were considered statistically significant at p < 0.05.
Percent mortality of aphids was determined according to Abbott (Abbott, 1925):
X - the percent living in the control, Y - the percent living in the threated plat.
Results and Discussion
The study found significant differences between the number of individuals consumed by the entomophagous bug between Megoura viciae and five species of aphids: S. graminum (p=0.032), A. fabae (p< 0.001), A. pomi (p< 0.001), M. cerasi (p= 0.028), A. urticata (p< 0.001), where the average number of prey ranged from 11.2±1.18 in the case of bird cherry-oat aphid to 13.7±0.38 with the apple aphid (Fig. 1). The consumption of Megoura viciae individuals was significantly lower, averaging 6.6±1.03 aphids per predator. The amount of prey also differs significantly between A. pomi and M. cerasi (p=0.035) (Fig. 1).
Aphis urticata Myzus cerasi Aphis pomi Brevicoryne brassicae Megoura viciae Aphis fabae Rhopalosiphum padi Schizaphis graminum
Abbott's corrected mortality ranged from 88.8 ± 2.7 %% in the case of the black bean aphid to 70.5 ± 5.8 %% in the case of the cabbage aphid (Fig. 2). Abbott's corrected mortality for the vetch aphid was significantly lower compared to the other treatments, amounting to 31.1 ± 9.1 %>. When calculating Abbott's corrected mortality considering the natural mortality of aphids, significantly different data were obtained between M. viciae and three variants: S. graminum (p < 0.001), Rh. padi (p < 0.001), A. fabae (p=0.004) and M. cerasi and two variants: S. graminum (p < 0.001), Rh. padi (p = 0.008), in pair S. graminum - B. brassicae (p=0.025).
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Figure 1. Box-plot of daily prey consumption by adults of Nabis ferus depending on aphid species (n=15) with maximum, minimum and median. *Boxes followed by the same letter within a column are not significantly different at p < 0.001 (x2 = 36; df =7). DSCF multiple comparisons were used as a post hoc test for the Kruskal-Wallis test Рисунок 1. Суточное потребление жертв имаго Nabis ferus в зависимости от вида тли (n=15) с обозначением
максимума, минимума и медианы. *Одинаковыми буквами в основании столбцов диаграммы обозначены статистически не различающиеся значения при p < 0.001 (x2 = 36; df =7). DSCF тест использовался в качестве
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Figure 2. Abbott corrected mortality (mean % ± SE) of Nabis ferus. *Bars followed by the same letter within a column are not significantly different at p < 0.001 (x2 = 35.96; df =7). DSCF multiple comparisons were used as a post hoc test for the Kruskal-Wallis test Рисунок 2. Биологическая эффективность (среднее значение % ± SE) Nabis ferus. *Одинаковыми буквами в основании столбцов диаграммы обозначены статистически не различающиеся значения при p < 0.001 (x2 = 35.96; df =7). DSCF тест использовался в качестве апостериорного анализа для теста Краскела-Уоллиса
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Studying the trophic relationships of potential agents of biological plant protection will determine the possibility of their mass rearing and application in various agroecosystems. The complex feeding relationships of polyphagous predators complicate the prediction of their contribution to pest suppression. Alternative prey may distract predators from attacking target phytophagous pests, thereby weakening pest control measures. At the same time, a diverse array of insect species can provide feed that supports larger communities of predators during the absence of the "optimal" prey for its targeted work (Campos et al. 2020; Park et al. 2023).
The study established that N. ferus attacked significantly fewer vetch aphids compared to S. graminum, A. fabae, A. pomi, M. cerasi, and A. urticata. This selectivity may be related to the physiological characteristics of M. viciae and to the interactions in the phytophagous pest-plant system: allelochemical interactions, impact of host plants on the physiology of aphid (Shih et al. 2023). Another reason for the lower consumption of the vetch aphid by the bug could be its morphometric indicators, as this species is larger relative
to other tested species (Ivanovskaya, 1977). Also, the vetch aphid M. viciae may exhibit earlier defensive behavior under the influence of alarm pheromones, escaping attack through thanatosis and active movement on the plant (Kunert et al. 2008; Bruno et al. 2018). The influence of aphid endosymbionts (for example Buchnera, Spiroplasma, Wolbachia) on unspecialized entomophagous insects also cannot be ruled out. Insect symbionts can directly affect the host's interactions with natural enemies, but also indirectly through changes in plant physiology and the emission of herbivore-induced plant volatiles. (Vorburger 2018).
When calculating Abbott's corrected mortality that adjusts for control mortality, and accordingly natural mortality in the population, the same trend was maintained. There were no significant differences between S. graminum, Rh. padi, A. fabae, A. pomi, and A. urticata. However, predator efficiency was significantly lower for M. viciae, B. brassicae and M. cerasi. Thus, the entomophagous bug N. ferus demonstrated its ability to feed on a fairly wide range of species in the family Aphididae.
Conclusion
The results of this study extend our knowledge of additional feed sources of N. ferus used for plant protection.
Acknowledgements
The work was performed with the financial support of the Russian Science Foundation № 23-26-00073.
References
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https://doi.org/10.31993/2308-6459-2024-107-2-16593
Краткое сообщение
ПИЩЕВОЕ ПОВЕДЕНИЕ ХИЩНОГО КЛОПА NABIS FERUS (HETEROPTERA: NABIDAE)
В ОТНОШЕНИИ ТЛЕЙ Е.И. Шаталова
1 Сибирский федеральный научный центр агробиотехнологий Российской академии наук (СФНЦА РАН),
Краснообск, Россия
2 Новосибирский государственный аграрный университет, Новосибирск, Россия
* ответственный за переписку, e-mail: [email protected]
В данной работе изучено пищевое поведение хищного клопа Nabis ferus L. (Heteroptera: Nabidae) по отношению к различным видам Aphididae в качестве добычи в лабораторных условиях. Получены данные о хищном поведении N. ferus, включая выделение наиболее предпочитаемых видов для питания. В качестве добычи использовались восемь представителей семейства Aphididae: Schizaphis graminum, Rhopalosiphum padi, Aphis fabae, Megoura viciae, Brevicoryne brassicae, Aphis pomi, Myzus cerasi и Aphis urticata. Среднее количество добычи варьировало от 11.2±1.18 в случае R. padi и до 13.7±0.38 для A. pomi. Потребление особей M. viciae было значительно ниже, в среднем составляло 6.6±1.03 тли на хищника. Результаты имеют практическое значение для биологического контроля фитофагов в сельском хозяйстве.
Ключевые слова: Nabis ferus, хищник, добыча, энтомофаг, биологический контроль Поступила в редакцию: 24.06.2024 Принята к печати: 30.08.2024
© Шаталова Е.И. Статья открытого доступа, публикуемая Всероссийским институтом защиты растений (Санкт-Петербург) и распространяемая на условиях Creative Commons Attribution License 4.0 (http://creativecommons.org/licenses/by/4.0/).
