Predation by Anthocoris minki pistaciae Wagner (Hemiptera: Anthocoridae) on Agonoscena pistaciae Burckhardt and Lauterer (Hemiptera: Psyllidae) at different temperatures

Pistachio is globally valuable due to its nutritional value, economic significance, and important role in health (Kashaninejad and Tabil 2011). Kerman Province (in the southern part of Iran) is the largest pistachio-producing area in Iran (FAO 2016). The specific climatic conditions for the cultivation of pistachio (such as wilderness and dry areas with long and hot summers, cold winters, and low-quality soil, and salted water) have resulted in the spread of pests in pistachio orchards (Hosseinifard et al. 2008). Many phytophagous (herbivore) arthropod pests attack pistachio trees, causing considerable damages to the crop (Zohdi et al. 2015). Among these pests, the common pistachio psyllid (CPP), Agonoscena pistaciae Burckhardt and Lauterer (Psyllidae), is the most adverse pest which was first reported on pistachio trees in Iran by Kiriukhin (1946) (Mehrnejad 2001).

Both nymphs and adults of CPP suck the leaves’ sap and produce large amounts of dried and crystallized honeydew. Their damage to the plant leads to the fall of leaves, buds, and fruits which finally leads to yield reduction (Alizadeh et al. 2011). This pest produces several generations each year and is generally inhibited by applying chemical insecticides belonging to various classes multiple times per year (Hassani 2009). The use of insecticides failed to prevent the outbreak of this pest, and frequent use of these compounds has led to the development of pesticide resistance (CPP resistance occurs due to its high reproductive capacity and short life cycle) (Alizadeh et al. 2011). Due to such problems, integrated pest management (IPM) programs, especially biological control, are considered a suitable approach for controlling CPP (Mehrnejad 2001).

Some species of anthocorids including Anthocoris nemorum (L.), A. nemoralis (Fabricius), Orius vicinus (Ribaut), O. minutus (L.), and O. majusculus Reuter (Hemiptera: Anthocoridae) can effectively control psyllid species in infested pear orchards (Sigsgaard et al. 2006). Souliotis et al. (2002) reported A. nemoralis as a successful bio-control agent of CPP in Greece. Few studies have been found on its potential in pistachio orchards of Iran (Linnavuori and Hosseini 2000). Some aphid and psyllid species including Forda sp. (Hemiptera: Aphidoidea), Slavum sp. (Hemiptera: Aphidoidea), and Psyllopsis fraxini (L.) (Hemiptera: Psyllidae) have been recorded as preys of A. minki pistaciae (Falamarzi et al. 2009). Pourali et al. (2010) reported A. minki pistaciae as a well-known predator of A. pistaciae in pistachio orchards in Iran.

Anthocoris minki pistaciae is found from April to October in pistachio orchards in Kerman Province, Iran. Nowadays, the population of this predator in pistachio orchards (may be due to the use of large amounts of insecticides) is limited (Mehrnejad 2010; Yanik and Unlu 2011).

Among the known factors that influence the capacity of predators to consume prey is the temperature, as it affects the rate of growth, development, prey consumption, behavior, life cycles, population dynamics, and geographical distribution of insects (Islam and Chapman 2001). Rajabi (2004) reported that temperature increases boost metabolic interactions and then heighten the need for nutrition. So, before using biological control agents in new areas, it is necessary to know the thermal requirements of the agent (Pilkington and Hoddle 2006).

Previous studies showed benefits of using the age-stage, two-sex life table in food consumption of insect predators (Atlihan and Chi 2008).

The main purpose of this study was to investigate the influence of different temperatures on the predation rate of A. minki pistaciae when feeding on A. pistaciae as prey during immature and adult stages under laboratory conditions.

This is the first research conducted to investigate the age-stage, two-sex predation rate of A. minki pistaciae.

The net predation rates (C₀) of A. minki pistaciae at different temperatures are shown in Table 1. The (C₀) increased by increasing the temperature. At 30 °C, it was significantly higher than those at 17 and 26 °C. The C₀ was equal to the area under the curve of l_xk_x (Fig. 1).

Developmental stage	17 °C		26 °C		30 °C
	N	Mean ± SE*	N	Mean ± SE	N	Mean ± SE
Egg	15	0	15	0	15	0
1st nymphl instar	15	14.6 ± 0.46b	15	8.73 ± 0.27c	15	15.07 ± 0.21a
2nd nymphl instar	14	22.57 ± 0.44a	14	11.86 ± 0.54c	14	20.57 ± 0.4b
3rd nymphl instar	14	38.64 ± 0.69a	13	24.62 ± 0.29c	13	35.15 ± 0.27b
4th nymphl instar	14	63.36 ± 0.74a	13	39 ± 0.45c	13	56.85 ± 0.36b
5th nymphl instar	14	80.21 ± 4.96b**	13	91.69 ± 1.01a	13	79.38 ± 0.64b
Total nymphal stage	15	205.73 ± 14.34a	15	154.4 ± 14.63c	15	182.8 ± 16.64b
Adult male	5	803.4 ± 22.8b	4	839.75 ± 95.26b	4	994.75 ± 11.95a
Adult female	9	1086 ± 15.27c	9	1281.44 ± 31.63b	9	1435.89 ± 27.09a
Adult mean	14	985.07 ± 39.49c	13	1145.54 ± 67.99b	13	1300.15 ± 61.38a
Net predation rate (C0)	–	1125.32 ± 84.28b	–	1147.22 ± 127.5b	–	1309.13 ± 140.43a
Transformation rate (Qp)	–	36.45 ± 7.97b	–	39.05 ± 7.1b	–	54. 67 ± 10.67a

Mean consumption capacity—mean number (± SE) of nymphs of Agonoscena pistaciae eaten by different stage/sex of Anthocoris minki pistaciae; C₀—the net predation rate; Q_p—the transformation rate from prey population to predator offspring at three different temperatures (17, 26, and 30 °C)

*The SEs were estimated using 10,000 bootstraps and compared by Tukey’s test (comparison of 95% CI)

**Within rows, values followed by the same letters do not significantly different.

^a,b,cRepresent quantities’ numbers. ^aShows the highest level of significance. ^cShows the lowest level of significance

The transformation rates from the prey population to predator offspring (Q_p) are shown in Table 1. The Q_p obtained a demographic estimation for the relationship between the reproduction rate and predation rate of the predator. A survey of the Q_p indicated that the highest and lowest values were obtained at 30 and 17 °C, respectively. This parameter increased significantly as temperature increased. In other words, A. minki pistaciae required 54.67 and 36.45 nymphs of CPP to produce a single egg at 30 and 17 °C, respectively.

At three temperatures, the predation rate estimated was higher in adult stage compared with the immature stage. Food consumption rate of the female was significant at the three temperatures (1086 ± 15.27, 1281.44 ± 31.63, and 1435.89 ± 22.09 nymphs) at 17, 26, and 30 °C, respectively. The results showed that the predation rate of females was higher than that of males. This difference could be due to the bigger size of females compared with the males, and the females need higher energy to lay eggs. Predation of adults gradually decreased with aging as well declined the number of eggs produced by females (Table 1).

The age-specific survival rate (l_x), the age-specific predation rate (k_x), and the age-stage-specific net consumption rate (q_x) at different temperatures were illustrated in Fig. 1. The age-stage-specific net predation rate (q_x) of the nymphs increased at first and then gradually decreased with the age-specific survival rate (l_x). The highest k_x and q_x were observed at 30 °C on the 20th day, at 26 °C on the 34th day, and at 17 °C on the 20th day. However, the highest age-stage-specific net predation rate of male and female adults was recorded at 30 °C (Fig. 1).

The age-stage-specific predation rate (c_xj) of A. minki pistaciae on the fourth instar nymphs of CPP is shown in Fig. 2. This parameter stated the trend in age-stage-specific predation rate, i.e., the mean number of psyllids eaten by nymphs and adults of the predator of age x and stage j. The daily consumption data for all individuals (males, females, and those died before reaching the adult stage) were used to calculate this item. The highest value for c_xj is observed at 30 °C.

Obtained results showed that the temperature was effective on mean consumption capacity of the nymphal stage, and it increased by increasing temperature, but due to a longer nymphal period at 17 °C the highest mean numbers of eaten prey at this temperature. Then, this quantity increased as temperature raised from 26 to 30 °C.

Weighting coefficient showed the effect of different stages of predator life in controlling the prey’s population quantitatively. If the weighting coefficient of adult females is one, the obtained weighting coefficients of adult males and fifth and fourth nymphal instars were 0.7, 0.7, and 0.5, respectively (Table 2).

The present study showed that the predation rate of adults of A. minki pistaciae is closely associated with temperature rise. This result is in accordance with the results of the studies of Simonsen et al. (2009) and Zhang et al. (2012).

Among the nymphal stages, the fifth instar showed the highest food consumption at the three temperatures. This result was similar to those of Yanik and Unlu (2010). They reported that the food consumption of pre-adults of A. minki feeding on Ephestia kuehniella Zell. (Lepidoptera: Pyralidae) was affected by temperature, and the corresponding value was 123.1, 94.1, and 99.4 eggs at 20, 25, and 30 °C, respectively. Obviously, this trend is similar to the results of immature stages in the present study.

At all temperatures tested, the prey consumption of adult females was more than that of males. Similar data has also been presented by Yanik and Unlu (2011) for A. minki feeding on A. pistaciae. Yanik and Unlu (2010) reported the highest prey consumption of females and males of A. minki fed with E. kuehniella egg was at 30 °C and 40% R.H. (309.7 and 108.8, respectively). The contradiction between these data and the obtained results could be due to the difference in the nutritional quality of the hosts and experimental conditions. Yanik and Unlu (2011) stated that 631 and 303.5 nymphs of A. pistaciae were consumed by females and males of A. minki at 25 ± 1 °C. In the present study, this item for females and males of A. minki pistaciae was higher compared to the results of Yanik and Unlu (2011). This difference was due to the age of prey used in the test. Yanik and Ugur (2004) reported that the females of A. nemoralis consumed totally 1936 eggs of E. kuehniella at 25 ± 1 °C. The difference than obtained results may be pertained to the difference in types of prey.

The present study demonstrated that temperature affected the predation capacity of A. minki pistaciae. According to the results, despite the fact that 30 °C decreased longevity, it was the best temperature for feeding adults of A. minki pistaciae under the laboratory conditions because at this temperature, the highest net predation rate (C₀) and the transformation rate from the prey population to predator offspring (Q_p) (1309.13 ± 140.3 and 54.67 ± 10.67 prey nymphs, respectively) were achieved. Moreover, the maximum mean prey consumption of adult insects (1300.15 ± 61.38 psyllid nymphs) was calculated at 30 °C.

With regard to the climate and high temperature of Kerman Province, the predation activity of the main predators of CPP including ladybirds and lacewings decreases as temperature increases (Zohdi 2016). On the contrary, the obtained results may suggest that A. minki pistaciae can increase the population density and cause greater efficiency (under laboratory conditions) at 30 °C than at other temperatures tested in this study.