Maize intercropping reduces infestation of potato tuber moth, Phthorimaea operculella (Zeller) by the enhancement of natural enemies

Journal of Integrative Agriculture 2020, 19(2): 394–405 Available online at www.sciencedirect.com

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RESEARCH ARTICLE

Potato/Maize intercropping reduces infestation of potato tuber moth, Phthorimaea operculella (Zeller) by the enhancement of natural enemies ZHENG Ya-qiang1, ZHANG Li-min1, CHEN Bin1, YAN Nai-sheng1, GUI Fu-rong1, ZAN Qing-an1, DU Guang-zu1, HE Shu-qi1, LI Zheng-yue1, GAO Yu-lin3, XIAO Guan-li2 1

State Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Yunnan Agricultural University, Kunming 650201, P.R.China 2 College of Agriculture & Biology Technology, Yunnan Agricultural University, Kunming 650201, P.R.China 3 State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, P.R.China

Abstract The potato tuber moth (PTM), Phthorimaea operculella (Zeller), is one of the most economically significant insect pests for potato in both field and storage worldwide. To evaluate the infestation, reduction of potato yield and the control efficacy for PTM, field tests were conducted in two seasons by intercropping of potato as the host plant with maize as a non-host plant of PTM. Three intercropping patterns were tested, which were 2 rows of potatoes with either 2, 3, or 4 rows of maize (abbreviated 2P:2M, 2P:3M, and 2P:4M), and the monocropped potato as the control, 2 rows of potatoes, without maize, (abbreviated 2P:0M). Results showed that the population and infestation of PTM in the 2P:3M intercropping pattern was significantly lower than those in 2P:2M, 2P:4M and the monocropping pattern of 2P:0M, due to the enhancement of natural enemies. Cumulative mines and tunneling in potato leaves in 2P:3M intercropping were significantly lower than those in 2P:2M and 2P:4M patterns. The population of parasitoids and the parasitism rate of PTM in intercropping pattern of 2P:3M were significantly higher than that in intercropping pattern of 2P:2M, 2P:4M and monocropping pattern of 2P:0M. We conclude that the potato intercropped with maize reduced the adult and larva populations, and reduced the damage from PTM by enhancing the number of parasitoids and the level of parasitism. The greatest population density of parasitoids and parasitism rate were in the intercropping pattern of 2 rows of potatoes with 3 rows of maize. These data indicate that the host/non-host intercropping patterns can be used as a biological control tactic against PTM by enhancing the density of natural enemies in the agro-ecosystems. Keywords: potato tuber moth, Phthorimaea operculella (Zeller), intercrop, biological control, natural enemies, parasitoids

Received 6 November, 2018 Accepted 3 April, 2019 ZHENG Ya-qiang, Mobile: +86-15288338237, E-mail: [email protected]; Correspondence XIAO Guan-li, Mobile: +86-13888217416, E-mail: [email protected]; CHEN Bin, Mobile: +86-13708876067, E-mail: [email protected] © 2020 CAAS. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license (http:// creativecommons.org/licenses/by-nc-nd/4.0/). doi: 10.1016/S2095-3119(19)62699-7

1. Introduction The potato tuber moth (PTM), Phthorimaea operculella (Zeller) (Lepidoptera: Gelechiidae), is a cosmopolitan oligophagous pest insect of many Solanaceous crops, including potato (Xu 1985; Saour 2012), tobacco (Van

ZHENG Ya-qiang et al. Journal of Integrative Agriculture 2020, 19(2): 394–405

Vuuren et al. 1998; Zheng et al. 2008), tomato (Gilbora and Podoler 1994; Aryal and Jung 2019), eggplant (Xu 1985; Saour 2012), and other Solanaceous crops or weeds (Xu 1985; Varela and Bernays 1988; George et al. 2012). This pest likely originated in South America along with its main host of potato, Solanum tuberosum L. (Solanaceae) (Graft 1917; Xu 1985). It has been a key pest insect on potato in tropical and subtropical countries around the world (Rondon 2010; Saour 2012). The PTM larva damages potato leaves, stems and petioles in the field, which typically do not cause significant yield losses (Rondon 2010). However, it can damage tubers in both the field and storage conditions, and causes great reduction of potato quality, and the yield losses by 20–30% in southwestern Yunnan Province, China (Wang et al. 2002). In storage conditions, the PTM larva infestation may cause destructive damage to stored potato tubers (Radcliffe 1982; Sileshi and Teriessa 2001; Wang et al. 2002), which reduces their marketability and losses in storage may be up to 100%, especially in non-refrigerated systems (Finbarrg et al. 2010; Rondon 2010). Some approaches have been developed to control the PTM (Rondon 2010), including the application of chemical insecticides (Coll et al. 2000), semiochemicals (Arab et al. 2007), biological insecticides such as entomopathogenic fungi (Sabbour 2006; Sabbour and Abdel-Raheem 2015; Yuan et al. 2016, 2018), entomopathogenic nematodes (Sweelam et al. 2011; Hassani-Kakhki et al. 2012; Eivazian et al. 2018), entomopathogenic bacteria (Salama et al. 1995a, b; Sabbour 2006) and Granuloviruses (Kroschel et al. 1996a, b; Arthurs et al. 2008; Jukes et al. 2014), natural enemies (Salehi and Keller 2002; Saour 2004; Keasar and Steinberg 2008), integrated cultural practices (Coll et al. 2000; Clough et al. 2010; Ma and Xiao 2013) and plant resistance inducers, e.g., potassium phosphite (Mulugeta et al. 2018). Intercropping with a potential nonhost crop increases the parasitism of pests (Khan et al. 1997). Several natural enemies including parasitoids (e.g., Copidosoma koehleri Blanchard; Diadegma pulchripes (Kokujev); Temelucha decorate (Gravenhorst); Bracon gelechiae Ashmead) and predators (e.g., Coccinella septempunctata Linnaeus; Chrysoperla carnea Stephens; Orius albidipennis (Reuter)) play an important role in PTM control (Graf 1917; Abbas et al. 1993; Coll et al. 2000; Arab et al. 2007; Keasar and Sadeh 2007; Keasar and Steinberg 2008). For example, in one study, the parasitism rate reached 40% and predation was estimated at 79% in Israel (Coll et al. 2000), but less attention has been given to the mechanisms of intercropping in the control of PTM by enhancing the natural enemies. Intercropping is a multiple cropping practice that can produce a greater yield on a given piece of land by making use of resources or ecological processes (George and Jeruto 2010; Brooker et al. 2015;

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Dong et al. 2018). Intercropping of potato with other crops has been a popular planting strategy, which can increase land productivity (Chan et al. 1980; Saddam 2009; Huang et al. 2013) and yield (Su et al. 2007; Yang and Wu 2007; He et al. 2010; Xiao et al. 2011; Mu and Zhang 2012), control potato late blight (Sharaiha et al. 1989; Gui et al. 2004; He et al. 2010) and potato aphids (Ebwongu et al 2001), as well as the corn northern leaf blight (Ebwongu et al. 2001; Jiang et al. 2012). Specifically, the intercropping of potato with maize has been a major planting pattern and widely used in most potato planting areas (Ebwongu et al. 2001; Cao et al. 2003; Sljoqi and Van Emden 2003; Yang and Wu 2007; He et al. 2010). In the northwestern parts of China, such as in Yunnan, Guizhou, Sichuan, Gansu and Guangxi, it plays an important role in reduction of pest populations (Wang et al. 2004; Wu et al. 2003; Li C Y et al. 2009). The damage caused by pests decreased greatly in those potato cultivation areas using intercropping patterns in Yunnan Province (Li C Y et al. 2009). Field experiments were conducted in four potatoplanting systems for two successive seasons with the main objective of investigating the impact of intercropping on PTM and parasitoids, and the level of parasitism, in the different intercropping schemes, and to determine a better intercropping pattern for the integrated management of PTM. The aim of this study was to test the hypotheses that intercropping decreases the population of PTM by increasing the population of parasitoids and the parasitism rate.

2. Materials and methods 2.1. Intercropping patterns and field test This study was carried out for two successive seasons, during 2012 and 2013, in commercial potato planting areas in Banqiao District of Xuanwei City (26°05´52.3´´N, 104°04´27.5´´E, with an altitude of 1 967 m), Yunnan Province, China. Xuanwei City is the greatest potato planting area in Yunnan Province, with an annual average plant area of 63 529 ha in recent years (Sang et al. 2014). Three intercropping patterns were set up in the field with ratios of 2, 3, or 4 rows of maize intercropped with two rows of potatoes. They are indicated as 2P:2M (2 rows of potatoes with 2 rows of maize), 2P:3M (2 rows of potatoes with 3 rows of maize) and 2P:4M (2 rows of potatoes with 4 rows of maize), and 2P:0M (monocropped potato as the control, 2 rows of potatoes, without maize). The experiment was conducted in a randomized block design with three treatments and three replicates. Four plots were set up, each plot with a length of 20 m and width of 10 m, and twelve 200-m2 plots were set up in the two seasons in 2012–2013, respectively. Maize was planted with a row spacing of

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22 and 50 cm, potato was planted with a row spacing of 35 and 40 cm, in intercrop and monocrop patterns. The varieties of maize and potato were Huidan 4 and Xuanshu 2, respectively. Potatoes were planted on the 15th of March in 2012 and 16th of March in 2013, maize was planted on the 30th of March in 2012 and the 31st of March in 2013. Fertilizers, including carbamide, calcium superphosphate and potassium, were applied at amounts of 3.75, 10.00 and 2.5 g per maize plant, 3.1, 11.55 and 2.1 g per potato plant. Irrigation and mechanical weeding were conducted as required. No insecticides were used in the trials.

The proportion of the infested tubers was finally evaluated by calculating the percentages of infested tubers occupied among the total number of tubers in each site. Number of PTM on the above-ground parts of potato The day before the tuber harvest, 5 potato plants from each site were collected and the above-ground parts were put into a 150-mesh nylon net bag for 10 sites for each intercropped and monocrpped pattern plots in fields. All collected above-ground parts of the potato plants were carried to the cloth for 2 months. The numbers of adult PTM that emerged

Sampling and count of the adult PTM Sampling was conducted by RYOBI Leaf Blower W/VAC suction sampler with a collection cone of 13.0 cm in diameter (Dietrick 1961; Timothy and Ronald 2001; Chen et al. 2011) in 10 random locations within each plot. The collection cone of the sampler was lowered to the potato plant for 5 s for sampling. Samplings were conducted once a week from March to June in 2012 and 2013. All collected insects from each sampling cone were transferred to the laboratory and stored at –10°C for identification. All the samplings were conducted from 10:00 a.m. in each sampling day, except it was postponed on rainy days. Number of PTM larvae on foliage A survey was conducted once a week from March to June in 2012 and 2013, with 20 potato plants at 10 sites randomly selected in each plot. The proportions of PTM-tunneled leaves with and without PTM larvae on each sampled plant were counted but no leaves were removed. Finally, larvae in all those leaves and stems were checked and counted by dissection. Number of PTM larvae in potato tubers The tubers damaged by larvae of PTM was evaluated 1–3 days before the tuber harvest. All tuber samples were collected from 10 sites, and 5 randomly selected plants per site in a plot. Tubers from each sample site were put into white nylon nets (100 mesh), carried to the laboratory and stored for 4 months from emergence at room conditions, covered with black cloth. Infested tubers were separated. Numbers of infested

visible tunneling damage, both with and without larvae.

laboratory and kept at room conditions covered with black

2.2. Sampling methods

Parasitism rate (%)=

and non-infested tubers in each site were counted with

from above-ground parts of potatoes were identified and recorded every day until the plant parts fully dried. The proportion of potato leaves infested by larval PTM feeding tunnels A spot sampling site survey was conducted. Fifty selected plants were marked and observed from 10 fixed sites in each plot. The numbers of leaves with mines and the total numbers of leaves on the sampled potato plants were counted. The proportion of infested leaves was estimated using the following formula: Leaf infestation proportion (%)= Number of infested leaves ×100 Total number of leaves on sampled potato

Species and number of parasitoids trapped by suction sampler in the field Two methods were applied to assess the species and number of parasitoids in the field. Firstly, parasitoids were trapped by suction sampler in the field following the method sampling adult PTM in this paper. Secondly, a total of 20 leaves with PTM larvae tunneling were randomly picked from 10 potato plants in each plot. For full observation and checking of parasitoids, every 2 sampled leaves were held in a dish (15 cm in diameter) at (25±2)°C, 16 h L:18 h D, 70% RH until adult PTM or parasitoids emerged. Emerged adult parasitoids were collected and identified under the stereoscopic microscope (He 2004). Cumulative rate of parasitism and contribution of each parasitoid species was estimated by the following formula:

The total number of parasitoids ×100 The total number of parasitoids+The total number of PTM

Species and number of parasitoids that emerged from potato tuber All the tubers from each sampling site were kept in net bags made from 150-mesh nylon with an insect collecting bottle placed at the top of the net bag. All bags were carried to the laboratory and kept at the room temperature of (25±3)°C covered with black cloth. Emerged adult parasitoids were examined and their numbers were recorded daily until the tubers fully dried.

(1)



(2)

Species and number of parasitoids that emerged from the above-ground parts of potato To accompany the numbers from the tubers, the number of PTM was determined for the above-ground parts of potato. Samples of potato tops were collected from 10 sites, 5 plants per site for each plot. Species of parasitoids were identified and their numbers were counted. The parasitism rate was calculated using the following formula:

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(3)

2.3. Data analysis and statistics The number of adult and larval PTM, the infestation of potato leaf by larval PTM, the population of parasitoids and the parasitism rate, were analyzed by “two-way” ANOVA (with year and sampling date as main effects) of repeated measures with post hoc LSD multiple comparison. All procedures for the data statistics were performed in the SPSS 11.0 software program for Windows.

3. Results 3.1. Population of the adult PTM The number of adult PTM was low between the 5th week and 19th week after the emergence of potato in the intercropping and monocropping potato fields (Fig. 1). With the growth of the potato plants, the populations gradually increased. The number of adult PTM was the highest on the 13th week after the emergence of potato in 2012, with mean numbers of 10.80, 8.70, 13.76 and 17.20 adult PTMs per sucker in 2P:2M, 2P:3M, 2P:4M and 2P:0M, respectively. In 2013, mean numbers of 8.15, 5.10, 10.59 and 14.21 adult PTMs per trap on the 13th week after the emergence of potato were found in 2P:2M, 2P:3M, 2P:4M and 2P:0M, respectively. After this peak population, as the season progressed, a rapid decrease of the population was observed in 2012, and the minimum number was found in the 15th week after the emergence of potato. In contrast with that in 2012, a gradual decrease was seen in 2013. The second maximum population was noted on the 18th week after emergence in 2012 and 2013, with mean numbers of 18.50, 13.20, 19.80, 23.20 adult PTMs per sucker in 2012 and 12.44, 9.27, 14.98, 16.19 in 2013, in 2P:2M, 2P:3M, 2P:4M and 2P:0M, respectively. The populations decreased at the end of season in late July. A multivariate test of repetitive measures ANOVA was performed in comparing the effect of intercropping pattern on the population of PTM. The results showed that the interaction between the intercropping pattern and time significantly affected the population of PTM (2012: F=213.65, P<0.01; 2013: F=189.54, P<0.01).

3.2. Number of larval mines on potato plants in different planting patterns Adult PTM usually lay eggs on the potato leaf or tubers

2P:2M Mean number of potato tuber moth per sucker

Number of parasitoids  ×100 Number of parasitoids+Number of PTM

throughout the growing season. With a preference for the potato leaf, the larvae mine into the leaf when eggs hatch, and leave punctures causing irregular mine tunnels upon leaving the epidermis. Larval feeding tunnels in leaves rapidly increased in number with the onset of the PTM infestation both in 2012 and 2013. The cumulative number of tunnels per plant increased to the maximum of 5.54±0.39, 4.13±0.35, 7.26±0.25, 7.23±0.36 per plant at final sampling in 2012, and 3.70±0.32, 2.75±0.15, 4.90±0.25, 6.82±0.23 per plant in 2013 for 2P:2M, 2P:3M, 2P:4M and 2P:0M, respectively (Fig. 2). Results of the interaction between the two seasons and intercropping showed that the tunnel numbers in the two seasons were significantly higher in the monocropped potato than those in intercropped potato in 2012 (F=16.02, P<0.01) and 2013 (F=13.54, P<0.01). The tunnel numbers in the 2P:3M intercropping were significantly lower than those in the 2P:2M (2012: F=68.58, P<0.01; 2013: F=59.65, P<0.01) and 2P:4M (2012: F=57.43, P<0.01; 2013:

Mean number of potato tuber moth per sucker

Parasitism rate (%)=

25.0

2P:4M

2P:3M

2P:0M

2012

20.0 15.0 10.0 5.0 0.0 25.0

2013

20.0 15.0 10.0 5.0 0.0

5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 Weeks after the emergence of potato

Fig. 1 Mean number of Phthorimaea operculella (PTM) adult trapped per sucker from different planting patterns in 2012 and 2013. 2P:2M, 2 rows of potatoes intercropped with 2 rows of maize; 2P:3M, 2 rows of potatoes intercropped with 3 rows of maize; 2P:4M, 2 rows of potatoes intercropped with 4 rows of maize; 2P:0M, monocropped potato as the control, 2 rows of potatoes, without maize. Bars indicate SE.

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F=54.35, P<0.01). There was a significant interaction between intercropping pattern and season analyzed by the multivariate test of repetitive measures ANOVA (2012: F=152.57, P<0.01; 2013: F =147.28, P<0.01).

3.3. Density of PTM adults from above-ground parts of potato Numbers of PTM adult emerging from the above-ground parts of potato were different in the monocropping and intercropping patterns. The cumulative number of PTM

2P:2M

3P:2M

4P:2M

0P:2M

Mean number of mines per potato plant

8.0 7.0

2012

6.0 5.0 4.0 3.0 2.0 1.0

Mean number of mines per potato plants

0.0 8.0 7.0 6.0 5.0 4.0 3.0 2.0 1.0 0.0

2013

adults in 2012 was significantly lower than that in 2013, but it was significantly higher in 2P:0M than in the 2P:2M, 2P:3M, 2P:4M potato intercropping system both in 2012 and 2013 (Table 1). Moreover, statistical results from the multivariate test of repetitive measures ANOVA indicated that the number of PTM adults from the above-ground parts of potato was significantly affected by the interaction between the intercropping pattern and time (2012: F=46.58, P<0.01; 2013: F=35.74, P<0.01) .

3.4. Number of PTM larvae that emerged from the potato tubers after harvest The number of PTM larvae that emerged from tubers at harvest was significantly higher in monocropping than in intercropping systems. Amongst intercropping patterns, the density of PTM in 2P:3M was significantly lower than in 2P:2M and 2P:4M (Fig. 3). The number of PTM per 100 potatoes was 89.43±12.25, 65.35±17.65, 102.65±19.76 and 123.39±14.47 in 2012 and 15.85±1.59, 12.25±3.67, 37.87±2.65, 45.64±2.65 in 2013, respectively, in the 2P:2M, 2P:3M, 2P:4M and 2P:0M (F=6.51, P<0.05 in 2012; F=4.89, P<0.05 in 2013). The cumulative numbers of PTM in the harvested potato tubers were significantly higher in the 2P:0M than in the 2P:2M, 2P:3M, 2P:4M potato intercropping systems (F=61.43, P<0.01 in 2012; F=57.65, P<0.01 in 2013).

3.5. Cumulative proportion of foliage infestation in different planting patterns 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 Weeks after the emergence of potato

Fig. 2 Mean number of larval mines on the potato leaves in different planting patterns in 2012–2013. 2P:2M, 2 rows of potatoes intercropped with 2 rows of maize; 2P:3M, 2 rows of potatoes intercropped with 3 rows of maize; 2P:4M, 2 rows of potatoes intercropped with 4 rows of maize; 2P:0M, monocropped potato as control, 2 rows of potatoes, without maize. Bars indicate SE.

Potato leaf infestation by PTM in the field was characterized by foliage mines. Feeding mines on potato leaves appeared in the 7th week after the emergence of potato, and the cumulative proportion of foliage infestation increased with the growth of potato (Fig. 4). The cumulative proportions of foliage infestation peaked on the 19th week after the emergence of potato in 2012 and 2013, at (13.23±1.33), (8.21±1.15), (19.45±0.65) and (21.35±0.65)% in 2012, and (10.80±0.76), (6.89±0.56), (14.00±0.36) and (16.35±0.35)%

Table 1 Density of Phthorimaea operculella adults from above-ground parts of potato (mean±SE) Plant system1) 2P:2M 2P:3M 2P:4M 2P:0M 1)

Density of P. operculella adults (individuals per aboveground parts of potato) In the year of 2012 In the year of 2013 Variance analysis 5.54±0.39 Bb 15.85±1.59 Ab F=15.34, P<0.01 4.13±0.35 Bb 12.25±3.67 Ab F=16.43, P<0.01 7.26±0.25 Ba 37.87±2.65 Aa F=42.16, P<0.01 7.23±0.36 Ba 45.64±2.65 Aa F=46.78, P<0.01 F=7.87, P<0.01 F=25.43, P<0.01

2P:2M, 2 rows of potatoes intercropped with 2 rows of maize; 2P:3M, 2 rows of potatoes intercropped with 3 rows of maize; 2P:4M, 2 rows of potatoes intercropped with 4 rows of maize; 2P:0M, monocropped potato as the control, 2 rows of potatoes, without maize. The capital letter in the same row means the significant difference at 1% level, and the lowercase letter in the same line means the significant difference at 1% level.

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B 2012

60.0 50.0

Mean number of PTM emerged from 100 potato tubers

Mean number of PTM emerged from 100 potato plants

A

40.0 30.0 20.0 10.0

C

D

2013

60.0 50.0

Mean number of PTM emerged from 100 potato tubers

Mean number of PTM emerged from 100 potato plants

120.0 90.0 60.0 30.0 0.0

0.0

40.0 30.0 20.0 10.0 0.0

2012

150.0

2P:2M

2P:3M 2P:4M Potato:Maize

2P:0M

150.0

2013

120.0 90.0 60.0 30.0 0.0

2P:2M

2P:3M 2P:4M Potato:Maize

2P:0M

Fig. 3 Mean number of Phthorimaea operculella (PTM) adults that emerged from the above-ground parts (A and C) of potato and tubers (B and D) under different planting systems in 2012 and 2013. 2P:2M, 2 rows of potatoes intercropped with 2 rows of maize; 2P:3M, 2 rows of potatoes intercropped with 3 rows of maize; 2P:4M, 2 rows of potatoes intercropped with 4 rows of maize; 2P:0M, monocropped potato as the control, 2 rows of potatoes, without maize. Bars indicate SE.

Cumulative proportion of leaf infestation (%)

Cumulative proportion of leaf infestation (%)

2P:2M 25.0

2P:4M

2P:3M

2P:0M

2012

20.0 15.0 10.0 5.0 0.0 25.0 20.0

2013

in 2013 in the 2P:2M, 2P:3M, 2P:4M intercropping, and 2P:0M, respectively. The cumulative proportion of foliage infestation was significantly higher in the monocropped potato system than that in intercropped potato systems both in 2012 (F=22.36, P<0.01) and 2013 (F=27.45, P<0.01). The proportion of foliage infestation followed a rank of 2P:0M, 2P:4M, 2P:2M, and 2P:3M, with the lowest proportion of foliage infestation in the 2P:3M planting pattern. The multivariate test of repetitive measures ANOVA (2012: F=29.43, P<0.01; 2013: F=34.16, P<0.01) showed that the interaction between the intercropping pattern and time showed a statistically significant effect on the infestation of potato leaves by the larval PTM.

15.0

3.6. Species and number of parasitoids trapped by suction sampler in the field

10.0 5.0 0.0

5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 Weeks after the emergence of potato

Fig. 4 Cumulative proportion of potato leaves infested by larval feeding in 2012–2013. 2P:2M, 2 rows of potatoes intercropped with 2 rows of maize; 2P:3M, 2 rows of potatoes intercropped with 3 rows of maize; 2P:4M, 2 rows of potatoes intercropped with 4 rows of maize; 2P:0M, monocropped potato as the control, 2 rows of potatoes, without maize. Bars indicate SE.

Five species of parasitoids were found in both the monocropped and intercropped potato fields in the two successive seasons: Temelucha sp., C. chlorideae, Sympiesis sp., Apanteles sp., B. lasus Walker (Fig. 5). The cumulative density of all natural enemies trapped by suction sampler was 2.82±0.61, 4.53±0.87, 1.51±0.33, 0.95±0.21 parasitoids per suction sampler in 2012, and 4.16±0.92, 5.84±1.33, 2.08±0.45, 1.75±0.49 in 2013, respectively, in 2P:2M, 2P:3M, 2P:4M and 2P:0M. From the 5th week to the

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4.50 4.00 3.50 3.00 2.50 2.00 1.50 1.00 0.50 0.00

2P:3M

2012

2P:4M

2012

2P:0M

2012

5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 Weeks after the emergence of potato

Mean number of parasitoids per sucker

2012

Mean number of parasitoids per sucker

2P:2M

Sympiesis sp.

Mean number of parasitoids per sucker

4.50 4.00 3.50 3.00 2.50 2.00 1.50 1.00 0.50 0.00 4.50 4.00 3.50 3.00 2.50 2.00 1.50 1.00 0.50 0.00 4.50 4.00 3.50 3.00 2.50 2.00 1.50 1.00 0.50 0.00

Campoletis chlorideae

Mean number of parasitoids per sucker

Mean number of parasitoids per sucker

Mean number of parasitoids per sucker

Mean number of parasitoids per sucker

Mean number of parasitoids per sucker

Temelucha sp.

4.50 4.00 3.50 3.00 2.50 2.00 1.50 1.00 0.50 0.00 4.50 4.00 3.50 3.00 2.50 2.00 1.50 1.00 0.50 0.00 4.50 4.00 3.50 3.00 2.50 2.00 1.50 1.00 0.50 0.00 4.50 4.00 3.50 3.00 2.50 2.00 1.50 1.00 0.50 0.00

Apanteles sp. 2P:2M

2P:3M

2P:4M

2P:0M

Brachymeria lasus

2013

2013

2013

2013

5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 Weeks after the emergence of potato

Fig. 5 Mean number of parasitoids on potato plants under different planting patterns in 2012 and 2013. 2P:2M, 2 rows of potatoes intercropped with 2 rows of maize; 2P:3M, 2 rows of potatoes intercropped with 3 rows of maize; 2P:4M, 2 rows of potatoes intercropped with 4 rows of maize; 2P:0M, monocropped potato as the control, 2 rows of potatoes, without maize. Bars indicate SE.

19th week after the emergence of potato, C. chlorideae was the predominant species, at a rate of 34.43% in 2012 and 38.14% in 2013. The tests of within-subjects effects indicated that no significant variation was found for the cumulative density of all natural enemies captured by suction sampler in 2012 (F=3.46, P>0.05) and 2013 (F=2.69, P>0.05). However, the effect of the interaction between the treatment and time by the multivariate test of repetitive measures ANOVA was significant (2012: F=47.87, P<0.01; 2013: F=36.45, P<0.01).

3.7. Species and number of natural enemies that emerged from potato leaves Parasitoids that emerged from the larvae of PTM collected from experimental fields were identified as Temelucha sp., Campoletis chlorideae, Sympiesis sp., Apanteles sp., and

Brachymeria lasus Walker. Total numbers of parasitoids were 3.44±0.72, 4.38±0.82, 2.24±0.50 and 0.99±0.23 wasps from 100 leaves in 2P:2M, 2P:3M and 2P:4M intercropping and 2P:0M, which differed significantly (F=15.65, P<0.01). The densities of the key parasitoids of B. lasus from the sampled 100 potato leaves in intercropped patterns were higher than that in the monoculture pattern (F=26.15, P<0.01). The overall parasitoid densities were 5.66±1.06, 8.58±1.60, 2.39±0.44 and 1.79±0.38 per 100 leaves in 2013, and the density was significantly lower in the monocropped potato pattern than those in the intercropped patterns in 2013 (F=67.25, P<0.01). The test of within-subject effects indicated that there was no significant variation in the number of natural enemies that emerged from potato leaves in 2012 (F=3.58, P>0.05) and 2013 (F=1.54, P>0.05). However, a significant interaction

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There were two peaks of parasitism throughout the potato growing seasons in both 2012 and 2013. The first density peak was in the 12th week after the emergence of potato and the parasitism rates were 7.17, 11.17, 3.87 and 1.91% in 2012, respectively. The parasitism rates were 5.24, 9.28, 2.69 and 1.06% in the 2P:2M, 2P:3M, 2P:4M, 2P:0M, respectively, at the 12th week after the emergence of potato in 2013. With the development of crops and PTM, as well as the parasitoids in all plant systems, the parasitism rates in the 2P:3M and 2P:2M reached the second peak in the 15th week and they were 13.13 and 9.10%, respectively. However, the second peak of the parasitism rate reached 4.80 and 2.68% in the 2P:4M and 2P:0M at the 16th week after the emergence of potato. Therefore, the 2nd peak of the parasitism rate in 2P:3M and 2P:2M appeared 1 week before those in the 2P:4M and 2P:0M. The dynamics of the parasitism rate was the same in 2013. The general percentages of parasitism were higher in intercropped fields than in monocropped fields during both 2012 and 2013 (Fig. 6). In 2012, the overall percentages of parasitism during the whole growing season of potato were (5.88±0.50) and (8.64±1.21)% in 2P:2M and 2P:3M intercropping fields, but they were (3.42±0.89)and (1.61±0.25)% in 2P:4M and monocropped potato fields, respectively. The parasitism in 2P:2M and 2P:3M intercropping systems in 2013 were (2.46±0.43)% and (7.10±1.76)%, they were (4.97±0.86) and (1.67±0.32)% in 2P:4M intercropped and in monocropped potato fields. All in all, the percentage of parasitism in the 2P:3M intercropping system was significantly higher than those in the other intercropped and 2P:0M in 2012 and 2013 (F=43.65, P<0.01 in 2012; F=31.29, P<0.01 in 2013).

3.9. Species and number of parasitoids that emerged from the above-ground parts of potato Four species of parasitoids, C. chlorideae, Sympiesis sp., Apanteles sp., B. lasus Walker, emerged from the potato tops from different planting systems in 2012 and 2013. The cumulative average densities of C. chlorideae, Sympiesis sp., Apanteles sp., and B. lasus were 13.43±2.18, 15.37±3.35, 9.65±1.58, and 7.76±1.45 per 100 plants in 2012 and 13.65±3.25, 18.21±4.29, 10.75±3.32, and 8.21±2.56 in 2013, respectively. From this, we can see that C. chlorideae and B. lasus were the most abundant species,

2P:3M

2P:4M

2P:0M

16.00 14.00 General parasitism (%)

3.8. The overall percent of parasitism

2P:2M 2012

12.00 10.00 8.00 6.00 4.00 2.00 0.00 16.00

General parasitism (%)

between the intercrop planting and time was found in 2012 (F=95.52, P<0.01) and 2013 (F=81.34, P<0.01) by multivariate test of repetitive measures ANOVA. All these results showed that the parasitism was significantly affected by the intercropping pattern.

14.00

2013

12.00 10.00 8.00 6.00 4.00 2.00 0.00

5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 Weeks ater the emergence of potato

Fig. 6 General parasitism rate of Phthorimaea operculella (Zeller) in potato leaves under different planting patterns in 2012 and 2013. 2P:2M, 2 rows of potatoes intercropped with 2 rows of maize; 2P:3M, 2 rows of potatoes intercropped with 3 rows of maize; 2P:4M, 2 rows of potatoes intercropped with 4 rows of maize; 2P:0M, monocropped potato as the control, 2 rows of potatoes, without maize. Bars indicate SE.

amounting to 62.4 and 27.3% of the parasitoids in 2012, and 63.1 and 27.9% in 2013, respectively.

3.10. Species and numbers of natural enemies of PTM from the tubers No predators or parasitoids were found in the stored potato tubers harvested from the field, except for the entomopathogenic fungi including Beauveria bassiana (Bals.) Vuill and Nomuraea rileyi (Farl.) Samson. Moreover, no significant differences were found between infection rates of the PTM larvae by entomopathogenic fungi during the storage of the harvested potato tubers from different planting patterns. The percentages of infection of PTM larvae by entomopathogenic fungi were (4.59±0.15), (4.75±0.27), (3.25±0.31), and (3.46±0.35)% for B. bassiana and (0.43±0.04), (0.35±0.06), 0, and (0.46±0.12)% for the N. rileyi in 2012. The rates were lower in 2013, amounting to (3.25±0.12), (3.42±0.31), (2.46±0.22), and (2.39±0.16)% infection by B. bassiana and (0.21±0.02), (0.26±0.03),

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(0.12±0.04), and (0.32±0.17)% by N. rileyi for 2P:2M, 2P:3M, 2P:4M, and 2P:0M, respectively.

4. Discussion The present study found a significant suppression on the populations of PTM in potato/maize intercropping systems compared with potato monocropping. The populations of both the adult and larva PTM were lower in all intercropping systems than in the monocropping system. Our results are consistent with many studies on insect pest control by using intercropping (Altieri 2002; Li Z Y et al. 2009). The lowest population of PTM among the 3 intercropping systems was in the intercropping system of 2P:3M. However, no significant differences were found among the population densities in the 2M:2P, 2M:4P and monocropping systems. Potato is one of the favorite hosts for PTM (Rondon 2010), but maize is not a host plant. The results indicated that the PTM response was not proportional to host quantity, and the best pattern was the intercropping of 2 rows of potato intercropped with 3 rows of maize, and the results may provide a theoretical base for the control of PTM for potato growers. Moreover, the cumulative proportion of potato leaves infested by larval feeding increased at the 19th week. This was probably caused by adult PTM migrating from the surrounding potato fields, which were planted earlier than our experimental field, because the experiment site happened to be located in the main potato planting area in Yunnan Province. Parasitoids are the main natural enemies of PTM in the potato planting regions (Graf 1917; Abbas et al. 1993; Coll et al. 2000). We found 5 species of parasitoids of PTM in both potato intercropping and monocropping systems. The dynamics of parasitoids and parasitism were the same in the intercropped and monocropped systems, and were all low at the early growth stage of the potato and maize. With the development of the crops and the PTM in the field, the dynamics increased. However, the number and parasitism rate in the 2M:3P increased more rapidly than that in other intercropping patterns from the 6th to 12th weeks. Perhaps this was caused by the parasitism in this system and yet it is worth studying the biology of the key parasitoids in subsequent research. With the development of the crops and the parasitoids, the maximum populations and parasitism rates appeared in the 12th week after the emergence of potato, and they were significantly higher in the 2P:3M and 2P:2M than those in 2P:4M and 2P:0M. This increase was perhaps caused by the appearance of the blooming of maize, which may provide an alternative food resource for the parasitoids. This finding is consistent with Chen et al. (2011) who found there are more abundant natural enemies in in polycultures than monocultures, as

more pollen and nectar resources are available in the complex systems (Altieri and Letourneau 1982; Li Z Y et al. 2009). Similar results that intercropping increase parasitism of pests were also found by Khan et al. (1997). Overall, the population density and the parasitism level of PTM in intercropping systems were significantly higher than in the monocropping system. Our results support the “Enemies Hypothesis” by Hasse and Litsinger (1981) and Russell (1989) who elaborate higher levels of parasitism occur in intercropping than in monoculture systems, and has proven true in other field studies as well (Root 1973; Russell 1989; Khan et al. 1997; Chen et al. 2011). However, we did not observe any parasitoids or predators of PTM except for entomopathogenic fungi from stored tubers in the laboratory after harvest. It is not surprising to see that PTM larvae on potato leaves are more accessible to parasitoids than larvae in potato tubers buried in the soil. Larval feeding by mining potato leaves in the intercropping systems were significantly lower than that in the monocropped system, and this result is consistent with the potato growers’ observations that the incidence and infestation of PTM was significantly decreased with the increase of intercropping practices of potato with maize. Moreover, the intercropping of potato with maize can increase the income with a good control efficacy on the pests (Li C Y et al. 2009). The infested aboveground exposed tuber is a major source of infestation in storage (Sileshi and Teriessa 2001). In this study, some PTM adults were found emerging from the aboveground potato parts at the storage stage, indicating that PTM adults have been in the aboveground parts of potato before the harvest of potato (Rondon 2010). Most potato growers in Yunnan Province usually cut the aboveground potato parts at harvest, and many of them cover the harvested tubers in sacks in the field using the aboveground potato parts for sheltering from sunlight. However, this probably facilitates infestation when such potatoes are stored, and it is very important and necessary to clarify this suspicion by further study. In the intercropping systems, it was not necessary to cover the harvested tubers in the field because of the sun sheltering from the maize, and this decreased the risk of the source of pests in stored tubers transferred from the aboveground potato parts in the field. Most studies have highlighted the importance of biodiversity in crop pest control, such as agrobiodiversity conservation, sustainable agriculture development, and agroecosystem stability enhancement (Risch et al. 1983; Altieri 1999; Li et al. 2007). However, intercropping is a common practice as a means of increasing food output per unit land that has been applied in China since ancient times. This form of biodiversity enhancement seems to reduce pest problems (Altieri and Letourneau 1982; Li Z Y et al. 2009; Philpott 2013). Intercropping of 3 rows of maize

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with 2 rows of potatoes has shown the highest efficacy for reducing PTM infestation. In Yunnan Province, the most popular intercropping system adopted by potato growers is potato and maize (Cao et al. 2003; Gui et al. 2005; Xiao and Zheng 2005; Li C Y et al. 2009). This practice seems beneficial for farmers in reducing damage to their potato by controlling insect pests, but the effect of maize on pests remains to be evaluated.

5. Conclusion Potato intercropped with maize can reduce the population and the damage of PTM by enhancing the number of parasitoids and parasitism rate. An intercropping pattern of 2 rows of potatoes with 3 rows of maize was the best intercropping pattern for PTM control. The host/non-host intercropping patterns could be a promising biological control tactic against insect pest by enhancing the natural enemies in the cropping system.

Acknowledgements We are grateful to Prof. Narayan Sarjerao Talekar (International Agriculture Center, National Chung Hsing University, Taiwan, China), Prof. Gurr Fres Geoff (Institute of Applied Ecology, Fujian Agriculture and Forestry University, China) and Prof. Zhang Lizhen (China Agricultural University) for their critical review of the manuscript. This research was supported by the National Key Research and Development Program of China (2018YFD0200703 and 2018YFD0200802) and the National Natural Science Foundation of China (3176059 and 31660537). We are grateful to the staff of Xuanwei Plant Protection and Plant Inspection Station, Yunnan Province, China for their kind cooperation, especially for providing the test field and field management.

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