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Ecological engineering of ground cover vegetation promotes biocontrol services in peach orchards
Ecological Engineering 64 (2014) 62–65
Contents lists available at ScienceDirect
Ecological Engineering journal homepage: www.elsevier.com/locate/ecoleng
Short communication
Ecological engineering of ground cover vegetation promotes biocontrol services in peach orchards Nian-Feng Wan a,b,1 , Xiang-Yun Ji a,2 , Xiao-Jun Gu a,2 , Jie-Xian Jiang a,∗ , Ji-Hua Wu b,3 , Bo Li b,∗∗ a Eco-environment Protection Research Institute, Shanghai Academy of Agricultural Sciences, Shanghai Key Laboratory of Protected Horticultural Technology, Shanghai 201403, China b Coastal Ecosystems Research Station of the Yangtze River Estuary, Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, Institute of Biodiversity Science, Fudan University, Shanghai 200433, China
a r t i c l e
i n f o
Article history: Received 15 September 2013 Received in revised form 18 November 2013 Accepted 20 December 2013 Available online 21 January 2014 Keywords: Aphids Biocontrol services Ecological engineering Generalist arthropod predators Grapholitha molesta (Busck) Peach orchard Trifolium repens L.
a b s t r a c t We conducted a 2-year field experiment at two sites in eastern China, examining the effects of the ground cover by Trifolium repens L. on the biocontrol services in peach orchards. The results indicated that compared to those in control areas, the abundances of aphids and Grapholitha molesta decreased, respectively, by 31.4% and 33.3% in Shanghai and by 30.1% and 33.3% in Jiangsu, while the abundance of generalist arthropod predators increased by 116.7% in Shanghai and by 115.8% in Jiangsu in ground cover areas. Compared to that in control areas, the ratio of generalist predator abundance to aphid abundance and to G. molesta abundance increased, respectively, by 260.0% and 384.2% in Shanghai and by 213.3% and 253.1% in Jiangsu in ground cover areas. Our study revealed that the ecological engineering of ground cover by T. repens promoted biocontrol services in peach orchards. Crown Copyright © 2014 Published by Elsevier B.V. All rights reserved.
1. Introduction One of the goals of ecological engineering is to restore the ecosystems that have been substantially degraded by human activities (Mitsch, 2012). Ecological engineering of ground cover vegetation, as one of the most important ways for managing landscape biodiversity (Kolos and Banaszuk, 2013), has been widely adopted (Gray et al., 2012), and has the potential to enhance the abundance of natural enemies (Landis et al., 2000) and to decrease
∗ Corresponding author at: 1000#, Jinqi Road, Fengxian District, Shanghai 201403, China. Tel.: +86 021 62205462; fax: +86 021 62201112. ∗∗ Corresponding author at: 220#, Handan Road, Shanghai 200433, China. Tel.: +86 021 65642178; fax: +86 021 65642178. E-mail addresses: [email protected] (N.-F. Wan), [email protected] (X.-Y. Ji), [email protected] (X.-J. Gu), [email protected] (J.-X. Jiang), [email protected] (J.-H. Wu), [email protected] (B. Li). 1 Address 1: 1000#, Jinqi Road, Fengxian District, Shanghai 201403, China. Address 2: 220#, Handan Road, Shanghai 200433, China. Tel.: +86 021 62202767; fax: +86 021 62201112. 2 Address: 1000#, Jinqi Road, Fengxian District, Shanghai 201403, China. Tel.: +86 021 62205462; fax: +86 021 62201112. 3 Address: 220#, Handan Road, Shanghai 200433, China. Tel.: +86 021 65642178; fax: +86 021 65642178.
population densities of pests (Song et al., 2010). Previous studies have shown that ground cover in orchards enhances the abundance of natural enemies such as in pecan trees (Smith et al., 1996), pear trees (Song et al., 2010), apple trees (Wyss, 1996) and lemon trees (Silva et al., 2010). However, the biocontrol services involved in the populations of natural enemies have not been elaborated although there are some reports on the effects of ground cover on pests in peach orchards (Meagher and Meyer, 1990a,b). Several studies have reported that ground cover by Trifolium repens L. in peach orchards influences peach production (Meagher and Meyer, 1990a), the abundance of pests (Meagher and Meyer, 1990b), the temporal and spatial patterns of insects (Wan et al., 2011). However, the biocontrol services of ground cover by T. repens, which is a common practice in the management of peach orchards in China, have not been explored. China is the country that has the largest area of peach planting and the largest output of peach production, with annual peach cultivation area of 45.2 × 104 hm2 and annual peach yield of 4.6 × 109 kg. Ground cover vegetation in peach orchards was introduced into China in 1990s and then was gradually applied nationwide. Over recent years ground cover by T. repens has been considered as one of the most ideal approaches to enhancing soil fertility and peach quality in orchards (Wilson et al., 2010), and this
0925-8574/$ – see front matter. Crown Copyright © 2014 Published by Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.ecoleng.2013.12.033
N.-F. Wan et al. / Ecological Engineering 64 (2014) 62–65
production model is gradually accepted by a large number of farmers and has been extensively applied in orchards’ management in China. However, whether the widespread adoption of ground cover by T. repens benefits the generalist predators and therefore potentially promotes associated ecosystem services such as the control of the most serious insect pests has not been explored. In the Yangtze River Delta of East China, we have found that the aphids which make leaves curl and the oriental fruit moth (Grapholitha molesta (Busck)) which makes peach shoots wither are the most serious insect pests. Meanwhile, spiders, ladybirds and lacewings were found to be the most key generalist arthropod predators in peach orchards (Wan et al., 2011). The widespread application of ground cover by T. repens may have contributed to an increase in populations of generalist natural enemies and promoted their associated biocontrol services. This study was therefore conducted to investigate whether adopting ground cover by T. repens induced an increase in populations of three groups of key generalist predators and led to a higher control efficiency of the generalist predators over the two key insect pests. 2. Materials and methods 2.1. Study sites Our study was conducted at two sites: one at Xinchang town, Pudong district, Shanghai of China (31.03◦ N, 121.41◦ E, elevation 4.3 m), and the other at Hudai town, Wuxi city, Jiangsu Province of China (31.34◦ N, 121.18◦ E, elevation 3.5 m). The two sites, at which the trees grow well and are vigorous, were both located in alluvial plain in the Yangtze River delta. Benzenehexachloride and dichlorodiphenyltrichloroethane residues were lower than detection limit (<0.004 mg kg−1 ) and the heavy metal contents were all below the Green Food Standard in China (As, Cu, Hg, Pb, Cr and Cd were 5.7–12.4, 26.4–46.1, 0.09–0.22, 22.8–32.6, 37.4–69.4 and 0.11–0.21 mg kg−1 in Xinchang, and 6.8–11.8, 22.3–43.7, 0.08–0.21, 20.7–30.3, 35.7–65.5 and 0.10–0.21 mg kg−1 in Hudai). Peach varieties grown in the orchards were “Xinfeng” honey peach in Xinchang and “Hujing” honey peach in Hudai, both of which are mid-season maturing varieties with 8–10 year-old trees, and arranged in a 4 × 4 m grid spacing. 2.2. Treatment and management The experiment was carried out in a randomized block design, and all treatments and controls were all replicated three times at both sites. Thirty peach trees (2–2.5 m high) at each replicate were sampled to calculate the abundance of insect pests and predators. Each experimental plot was 100 m wide and 52 m long, separated from adjacent plots by a 100 m long buffer belts. Treatment areas were covered with perennial plant Trifolium repens L., which was mowed twice a year to a height of about 10 cm. Control areas were bare ground, and every effort was made to keep them weed-free during the experimental period. Other managerial measures including pest management were the same for both the treatment and control plots in each orchard. Pest management in peach orchards mainly relies on physical and manual ways. To trap insect pests, we used plastic traps (-shaped section, 40 cm × 30 cm × 20 cm) for suspending sex pheromones. One Lyonetia prunifoliella Hubn and one Dichocrocis punctiferalis Guenee sex pheromone were installed with equidistance (10 m apart) in a line in the treated and control orchards. Traps were hung from tree branches at a height of 1.5 m above ground and lures were replaced every month. From the early April to late September, the pheromone traps were set in orchards. The statistics of pests
63
killed by attractants were surveyed and recorded every ten days. As lime sulfur are typical alternative to synthetic insecticides for the control of scale pests in orchards, 4–5 Baume lime sulfur were sprayed in dormant period in treated and control orchards. To prevent pathogens and pests from infesting peach, we trimmed the diseased and pest-infested peach branches with scissors in winter. Additionally, fruit bagging with yellow paper bags in June was adopted to avoid pest damage. 2.3. Sampling methods Within each replicate plot, 30 adjacent peach trees with checkerboard type distribution, similar to each other in height and vigor, were selected as permanent sampling points to monitor the population dynamics of peach aphids, G. molesta and the generalist arthropod predators (spiders, ladybirds and lacewings). On each sampling date, each tree was sampled from four directions (east, south, west, and north) at three levels each (upper, middle, and lower), i.e., each tree canopy was split into 12 resource units (Song et al., 2010). At each canopy level, we spent 3–5 min to collect arthropods and count the number of individuals of each species of the arthropods. The branch beating method was adopted to collect insect pests and predators from the peach tree canopy according to Simon et al. (2007). Insect pests and predators falling from the branches were collected, identified and counted immediately. Additionally, we took another few minutes to strip off the damaged young shoots in each twig to see if there were any G. molesta larvae. Sampling was done at appropriately 10-day intervals from late March to early October both in 2010 and 2011. 2.4. Data analysis Statistical analyses were performed with SPSS 16.0. Normal distribution and homocedasticity of all data were checked by the Kolmogorov–Smirnov test and Levene test, respectively. Threeway analysis of variance with general linear model in SPSS 16.0 was performed to analyze the above indices, so as to compare the interactive effects of sites, years and orchard types on the biocontrol service indices. If the values of the biocontrol service indices were not significantly affected by the years, we considered the two years’ data as a whole to compare the differences among means of treatments and controls with Tukey’s Honestly Significant Difference (HSD) test at 0.05 level. 3. Results The abundances of aphids, G. molesta and generalist arthropod predators were significantly affected by orchard type, but not by site and time. The interactive effects of two factors (site × time, site × orchard type, and time × orchard type) and three factors (site × time × orchard type) on the above abundances were not significant. The ratio of generalist arthropod predator to aphid abundance and the ratio of generalist arthropod predator to G. molesta abundance were significantly affected by the factor of orchard type but not by the factors site and time. Meanwhile, the interactive effects of two factors (site × time, site ×orchard type, and time × orchard type) and three factors also had no significant effect on the above ratios. The abundances of aphids and G. molesta were significantly lower but those of generalist arthropod predators were significantly higher in ground cover areas than in control areas at the two sites (Table 1). At both sites, irrespective of ground cover, the abundances of aphids, G. molesta and generalist arthropod predators increased during spring but were stabilized thereafter. Meanwhile,
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N.-F. Wan et al. / Ecological Engineering 64 (2014) 62–65
Table 1 Comparison of the abundances of aphids, Grapholitha molesta (Busck) and generalist arthropod predators in peach orchards with and without ground cover by Trifolium repens L. (abundance: individuals per 30 trees; means ± SE). Site
Orchard type
Aphid
Xinchang, Shanghai
Ground cover Bare ground Ground cover Bare ground
83.6 121.8 83.1 118.8
Hudai, Jiangsu
G. molesta ± ± ± ±
9.9b 13.7a 9.7b 14.3a
106.0 159.0 102.8 154.1
± ± ± ±
Generalist arthropod predators
14.2b 19.7a 13.0b 18.7a
318.8 147.1 304.9 141.3
± ± ± ±
22.2a 12.0b 25.4a 12.1b
Notes: Generalist arthropod predators mainly include spiders, ladybirds and lacewings; different letters in the same column indicate that the means are significantly different at P < 0.05 (HSD test) within groups of ground cover (treatment) and bare ground (control) in Xinchang and Hudai with consecutive two years (38 sample dates were considered as 38 replicates). Means of abundance were calculated from a total 30 trees per treatment or control in each replicate plot.
Peach orchard with ground cover (Xinchang, Shanghai) Peach orchard without ground cover (Xinchang, Shanghai) Peach orchard with ground cover (Hudai, Jiangsu) Peach orchard without ground cover (Hudai, Jiangsu)
400
Aphids per 30 trees
the abundance of predators was consistently higher but the abundances of aphids and G. molesta were consistently lower in ground cover areas than in control areas (Fig. 1). Ground cover by T. repens in peach orchards significantly increased the ratio of the abundance of generalist arthropod predators to that of aphids and the ratio of the abundance of generalist arthropod predators to that of G. molesta (Table 2). During the two year study at the two sites, the ratio of generalist arthropod predator to aphid abundance and the ratio of generalist arthropod predator to G. molesta abundance were consistently higher in ground cover areas than in control areas, providing evidence for the directly antagonist effect of the main predators on the populations of aphids and G. molesta (Fig. 2).
300
200
100
0 1
3
5
7
9
11 13 15
17 19
21 23 25
27 29 31 33 35 37
500
400
300
200
100
Generalist arthropod predator per 30 trees
Diversified planting in ecosystems has always been one of the focuses of ecological engineering (Montagna et al., 2012; Tropek et al., 2013), and many studies have documented that plant diversity in agro-ecosystems promotes the biocontrol services provided by the evidence that the natural enemy abundance increases and the pest abundance decreases (Andow, 1991). Our results indicated that when peach orchards were covered with T. repens the abundances of aphids and G. molesta decreased, respectively, by 31.4% and 33.3% in Xinchang, and by 30.1% and 33.3% in Hudai. Moreover, the abundance of generalist predators increased by 116.7% in Xinchang and by 115.8% in Hudai. Similar results were observed in other systems, for instance, the aphid abundance decreased and the abundance of the major predator of aphids, Chrysoperla rufilabris increased in response to ground cover in pecan orchards (Smith et al., 1996). Ground cover promoting biocontrol service is based on the principle that such ecological engineering creates a suitable ecological structure within the agricultural landscape to provide resources such as food for adult natural enemies, alternative prey or hosts, and shelter from adverse conditions (Landis et al., 2000). The benefits offered by ground cover might result from the dispersal and migration of predators from orchard floor plants to the trees, which augment the population densities of predators and promote the control efficacy of predators over insect pests on trees. In this study, we focused on certain predators overwintering in T. repens, and observed that the spiders migrated as well as the ladybirds, and that lacewings dispersed from T. repens to peach trees, which might explain the higher abundance of generalist predators in peach tree canopy. In addition, T. repens might provide a refuge and reservoir for predators to avoid the adverse effect of regular management in peach orchards, and other studies presented similar evidence that uncut strips of lucerne (Medicago sativa) offered refuges to a range of coccinellid and hemipteran predators (e.g., Hossain et al., 2000). Song et al. (2010) reported that peach orchards intercropped with aromatic plants could promote the biocontrol service,
Grapholitha molesta (Busck) per 30 trees
4. Discussion
0 1
3
5
7
9
11 13 15 17 19 21 23 25 27 29 31 33 35 37
600 500
400 300
200
100 0 1
3
5
7
9
11 13 15 17 19 21 23 25 27 29 31 33 35 37
Time order Fig. 1. Dynamics of the abundances of aphids, G. molesta and generalist arthropod predators in peach orchards with and without ground cover T. repens. Vertical bars denote SE. The number on the X-axis indicates the sampling times, i.e., the first 19 times (1–19) were conducted from late-March to early-October 2010; and the other 19 times (20–38) from late-March to early-October 2011.
N.-F. Wan et al. / Ecological Engineering 64 (2014) 62–65
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Table 2 Comparison of the ratio of generalist arthropod predator abundance to aphid abundance and ratio of generalist arthropod predator abundance to G. molesta abundance in peach orchards with and without ground cover by T. repens (means ± SE). Site
Orchard type
Ratio of generalist arthropod predator abundance to aphid abundance
Xinchang, Shanghai
Ground cover Bare ground Ground cover Bare ground
6.12 1.70 5.42 1.73
Hudai, Jiangsu
± ± ± ±
0.69a 0.17b 0.54a 0.19b
Ratio of generalist arthropod predator abundance to G. molesta abundance 7.36 1.52 5.12 1.45
± ± ± ±
1.61a 0.18b 0.71a 0.20b
Notes: Generalist arthropod predators mainly include spiders, ladybirds and lacewings; different letters in the same column indicate that the means are significantly different at P < 0.05 (HSD test) within groups of ground cover (treatment) and bare ground (control) in Xinchang and Hudai with consecutive two years (38 sample dates were considered as 38 replicates). Means of abundance were calculated from a total 30 trees per treatment or control in each replicate plot.
Peach orchard with ground cover (Xinchang, Shanghai) Peach orchard without ground cover (Xinchang, Shanghai) Peach orchard with ground cover (Hudai, Jiangsu) Peach orchard without ground cover (Hudai, Jiangsu)
Ratio of generalist arthropod predators to aphids per 30 trees
20.0
However, a more comprehensive, long-term and large-scale assessment of the potential eco-engineering effects of ground cover vegetation in peach orchard ecosystem needs to be further studied. Acknowledgements
15.0
This study was funded by the grants from Shanghai Municipal Science and Technology Commission (12ZR1449100, 08dz1900401, 123919N0400), the National Natural Science Foundation of China, the Shanghai Rising-Star Program and the Key Project of Science and Technology for Agriculture of Shanghai from Shanghai Agriculture Committee.
10.0
5.0
0.0 1
3
5
7
9
11 13 15 17 19 21 23 25 27
29 31 33 35 37
References Ratio of generalist arthropod predators to G. molesta per 30 trees
30.0
20.0
10.0
0.0 1
3
5
7
9
11 13 15 17 19 21 23 25 27 29 31 33 35 37
Time order Fig. 2. Dynamics of the ratio of generalist arthropod predator abundance to aphid abundance and ratio of generalist arthropod predator abundance to G. molesta abundance in peach orchards with and without ground cover by T. repens. Vertical bars on each point denote SE. The numbers on the X-axis indicate the sampling times, i.e., the first 19 times (1–19) were conducted from late-March to early-October 2010; and the other 19 times (20–38) from late-March to early-October 2011.
indicated by the fact that the ratio of the abundance of natural enemies to that of insect pests was significantly higher in any of the aromatic plants than in control. Similar results were reported by Rieux et al. (1999) that ground cover resulted in a higher beneficial: phytophagous ratio in pear tree canopy. Our study indicated that compared to that in control, the ratio of generalist arthropod predator abundance to aphid abundance and that of generalist arthropod predator abundance to G. molesta abundance averagely increased, respectively, by 260.0% and 384.2% in Xinchang, and 213.3% and 253.1% in Hudai in ground cover areas. This study showed that the ecological engineering of ground cover vegetation ultimately promoted biocontrol services in peach orchards, indicated by the fact that the abundances of the generalist predators (ladybirds, lacewings and spiders) increased and the abundances of the key insect pest aphids and G. molesta decreased.
Andow, D.A., 1991. Vegetational diversity and arthropod population response. Annu. Rev. Entomol. 36, 561–568. Gray, D.M., Swanson, J., Dighton, J., 2012. The influence of contrasting ground cover vegetation on soil properties in the NJ pine barrens. Appl. Soil. Ecol. 60, 41–48. Hossain, Z., Gurr, G.M., Wratten, S.D., 2000. The potential to manipulate the numbers of insects in lucerne by strip cutting. Aust. J. Entomol. 39, 39–41. Kolos, A., Banaszuk, P., 2013. Mowing as a tool for wet meadows restoration: effect of long-term management on species richness and composition of sedgedominated wetland. Ecol. Eng. 55, 23–28. Landis, D.A., Wratten, S.D., Gurr, G.M., 2000. Habitat management to conserve natural enemies of arthropod pests in agriculture. Annu. Rev. Entomol. 45, 175–201. Meagher r., R.L., Meyer, J.R., 1990a. Effects of ground cover management on certain abiotic and biotic interactions in peach orchard ecosystems. Crop Prot. 9, 65–72. Meagher r., R.L., Meyer, J.R., 1990b. Influence of ground cover and herbicide treatments on Tetranychus urticae populations in peach orchards. Exp. Appl. Acarol. 9, 149–158. Mitsch, W.J., 2012. What is ecological engineering? Ecol. Eng. 45, 5–12. Montagna, M., Lozzia, C.G., Giorgi, A., Baumgärtner, J., 2012. Insect community structure and insect biodiversity conservation in an Alpine wetland subjected to an intermediate diversified management regime. Ecol. Eng. 47, 242–246. Rieux, R., Simonb, S., Defrance, H., 1999. Role of hedgerows and ground cover management on arthropod populations in pear orchards. Agric. Ecosyst. Environ. 73, 119–127. Silva, E.B., Franco, J.C., Vasconcelos, T., Branco, M., 2010. Effect of ground cover vegetation on the abundance and diversity of beneficial arthropods in citrus orchards. Bull. Entomol. Res. 100, 489–499. Simon, S., Defrance, H., Sauphanor, B., 2007. Effect of codling moth management on orchard arthropods. Agric. Ecosyst. Environ. 122, 340–348. Smith, M.W., Arnold, D.C., Eikenbary, R.D., Rice, N.R., Shiferaw, A., Cheary, B.S., Carroll, B.L., 1996. Influence of ground cover on beneficial arthropods in pecan. Biol. Control 6, 164–176. Song, B.Z., Wu, H.Y., Kong, Y., Zhang, J., Du, Y.L., Hu, J.H., 2010. Effects of intercropping with aromatic plants on the diversity and structure of an arthropod community in a pear orchard. BioControl 55, 741–751. Tropek, R., Hejda, M., Kadlec, T., Spitzer, L., 2013. Local and landscape factors affecting communities of plants and diurnal Lepidoptera in black coal spoil heaps: implications for restoration management. Ecol. Eng. 57, 252–260. Wan, N.F., Ji, X.Y., Jiang, J.X., Dan, J.G., 2011. Effects of ground cover on the niches of main insect pests and their natural enemies in peach orchard. Chin. J. Ecol. 30, 30–39. Wilson, A.R., Nzokou, P., Cregg, B., 2010. Ground covers in fraser fir (Abies fraseri [Pursh] Poir.) production systems: effects on soil fertility, tree morphology and foliar nutrient status. Eur. J. Hortic. Sci. 75, 269–277. Wyss, E., 1996. The effects of artificial weed strips on diversity and abundance of the arthropod fauna in a Swiss experimental apple orchard. Agric. Ecosyst. Environ. 60, 47–59.
Contents lists available at ScienceDirect
Ecological Engineering journal homepage: www.elsevier.com/locate/ecoleng
Short communication
Ecological engineering of ground cover vegetation promotes biocontrol services in peach orchards Nian-Feng Wan a,b,1 , Xiang-Yun Ji a,2 , Xiao-Jun Gu a,2 , Jie-Xian Jiang a,∗ , Ji-Hua Wu b,3 , Bo Li b,∗∗ a Eco-environment Protection Research Institute, Shanghai Academy of Agricultural Sciences, Shanghai Key Laboratory of Protected Horticultural Technology, Shanghai 201403, China b Coastal Ecosystems Research Station of the Yangtze River Estuary, Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, Institute of Biodiversity Science, Fudan University, Shanghai 200433, China
a r t i c l e
i n f o
Article history: Received 15 September 2013 Received in revised form 18 November 2013 Accepted 20 December 2013 Available online 21 January 2014 Keywords: Aphids Biocontrol services Ecological engineering Generalist arthropod predators Grapholitha molesta (Busck) Peach orchard Trifolium repens L.
a b s t r a c t We conducted a 2-year field experiment at two sites in eastern China, examining the effects of the ground cover by Trifolium repens L. on the biocontrol services in peach orchards. The results indicated that compared to those in control areas, the abundances of aphids and Grapholitha molesta decreased, respectively, by 31.4% and 33.3% in Shanghai and by 30.1% and 33.3% in Jiangsu, while the abundance of generalist arthropod predators increased by 116.7% in Shanghai and by 115.8% in Jiangsu in ground cover areas. Compared to that in control areas, the ratio of generalist predator abundance to aphid abundance and to G. molesta abundance increased, respectively, by 260.0% and 384.2% in Shanghai and by 213.3% and 253.1% in Jiangsu in ground cover areas. Our study revealed that the ecological engineering of ground cover by T. repens promoted biocontrol services in peach orchards. Crown Copyright © 2014 Published by Elsevier B.V. All rights reserved.
1. Introduction One of the goals of ecological engineering is to restore the ecosystems that have been substantially degraded by human activities (Mitsch, 2012). Ecological engineering of ground cover vegetation, as one of the most important ways for managing landscape biodiversity (Kolos and Banaszuk, 2013), has been widely adopted (Gray et al., 2012), and has the potential to enhance the abundance of natural enemies (Landis et al., 2000) and to decrease
∗ Corresponding author at: 1000#, Jinqi Road, Fengxian District, Shanghai 201403, China. Tel.: +86 021 62205462; fax: +86 021 62201112. ∗∗ Corresponding author at: 220#, Handan Road, Shanghai 200433, China. Tel.: +86 021 65642178; fax: +86 021 65642178. E-mail addresses: [email protected] (N.-F. Wan), [email protected] (X.-Y. Ji), [email protected] (X.-J. Gu), [email protected] (J.-X. Jiang), [email protected] (J.-H. Wu), [email protected] (B. Li). 1 Address 1: 1000#, Jinqi Road, Fengxian District, Shanghai 201403, China. Address 2: 220#, Handan Road, Shanghai 200433, China. Tel.: +86 021 62202767; fax: +86 021 62201112. 2 Address: 1000#, Jinqi Road, Fengxian District, Shanghai 201403, China. Tel.: +86 021 62205462; fax: +86 021 62201112. 3 Address: 220#, Handan Road, Shanghai 200433, China. Tel.: +86 021 65642178; fax: +86 021 65642178.
population densities of pests (Song et al., 2010). Previous studies have shown that ground cover in orchards enhances the abundance of natural enemies such as in pecan trees (Smith et al., 1996), pear trees (Song et al., 2010), apple trees (Wyss, 1996) and lemon trees (Silva et al., 2010). However, the biocontrol services involved in the populations of natural enemies have not been elaborated although there are some reports on the effects of ground cover on pests in peach orchards (Meagher and Meyer, 1990a,b). Several studies have reported that ground cover by Trifolium repens L. in peach orchards influences peach production (Meagher and Meyer, 1990a), the abundance of pests (Meagher and Meyer, 1990b), the temporal and spatial patterns of insects (Wan et al., 2011). However, the biocontrol services of ground cover by T. repens, which is a common practice in the management of peach orchards in China, have not been explored. China is the country that has the largest area of peach planting and the largest output of peach production, with annual peach cultivation area of 45.2 × 104 hm2 and annual peach yield of 4.6 × 109 kg. Ground cover vegetation in peach orchards was introduced into China in 1990s and then was gradually applied nationwide. Over recent years ground cover by T. repens has been considered as one of the most ideal approaches to enhancing soil fertility and peach quality in orchards (Wilson et al., 2010), and this
0925-8574/$ – see front matter. Crown Copyright © 2014 Published by Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.ecoleng.2013.12.033
N.-F. Wan et al. / Ecological Engineering 64 (2014) 62–65
production model is gradually accepted by a large number of farmers and has been extensively applied in orchards’ management in China. However, whether the widespread adoption of ground cover by T. repens benefits the generalist predators and therefore potentially promotes associated ecosystem services such as the control of the most serious insect pests has not been explored. In the Yangtze River Delta of East China, we have found that the aphids which make leaves curl and the oriental fruit moth (Grapholitha molesta (Busck)) which makes peach shoots wither are the most serious insect pests. Meanwhile, spiders, ladybirds and lacewings were found to be the most key generalist arthropod predators in peach orchards (Wan et al., 2011). The widespread application of ground cover by T. repens may have contributed to an increase in populations of generalist natural enemies and promoted their associated biocontrol services. This study was therefore conducted to investigate whether adopting ground cover by T. repens induced an increase in populations of three groups of key generalist predators and led to a higher control efficiency of the generalist predators over the two key insect pests. 2. Materials and methods 2.1. Study sites Our study was conducted at two sites: one at Xinchang town, Pudong district, Shanghai of China (31.03◦ N, 121.41◦ E, elevation 4.3 m), and the other at Hudai town, Wuxi city, Jiangsu Province of China (31.34◦ N, 121.18◦ E, elevation 3.5 m). The two sites, at which the trees grow well and are vigorous, were both located in alluvial plain in the Yangtze River delta. Benzenehexachloride and dichlorodiphenyltrichloroethane residues were lower than detection limit (<0.004 mg kg−1 ) and the heavy metal contents were all below the Green Food Standard in China (As, Cu, Hg, Pb, Cr and Cd were 5.7–12.4, 26.4–46.1, 0.09–0.22, 22.8–32.6, 37.4–69.4 and 0.11–0.21 mg kg−1 in Xinchang, and 6.8–11.8, 22.3–43.7, 0.08–0.21, 20.7–30.3, 35.7–65.5 and 0.10–0.21 mg kg−1 in Hudai). Peach varieties grown in the orchards were “Xinfeng” honey peach in Xinchang and “Hujing” honey peach in Hudai, both of which are mid-season maturing varieties with 8–10 year-old trees, and arranged in a 4 × 4 m grid spacing. 2.2. Treatment and management The experiment was carried out in a randomized block design, and all treatments and controls were all replicated three times at both sites. Thirty peach trees (2–2.5 m high) at each replicate were sampled to calculate the abundance of insect pests and predators. Each experimental plot was 100 m wide and 52 m long, separated from adjacent plots by a 100 m long buffer belts. Treatment areas were covered with perennial plant Trifolium repens L., which was mowed twice a year to a height of about 10 cm. Control areas were bare ground, and every effort was made to keep them weed-free during the experimental period. Other managerial measures including pest management were the same for both the treatment and control plots in each orchard. Pest management in peach orchards mainly relies on physical and manual ways. To trap insect pests, we used plastic traps (-shaped section, 40 cm × 30 cm × 20 cm) for suspending sex pheromones. One Lyonetia prunifoliella Hubn and one Dichocrocis punctiferalis Guenee sex pheromone were installed with equidistance (10 m apart) in a line in the treated and control orchards. Traps were hung from tree branches at a height of 1.5 m above ground and lures were replaced every month. From the early April to late September, the pheromone traps were set in orchards. The statistics of pests
63
killed by attractants were surveyed and recorded every ten days. As lime sulfur are typical alternative to synthetic insecticides for the control of scale pests in orchards, 4–5 Baume lime sulfur were sprayed in dormant period in treated and control orchards. To prevent pathogens and pests from infesting peach, we trimmed the diseased and pest-infested peach branches with scissors in winter. Additionally, fruit bagging with yellow paper bags in June was adopted to avoid pest damage. 2.3. Sampling methods Within each replicate plot, 30 adjacent peach trees with checkerboard type distribution, similar to each other in height and vigor, were selected as permanent sampling points to monitor the population dynamics of peach aphids, G. molesta and the generalist arthropod predators (spiders, ladybirds and lacewings). On each sampling date, each tree was sampled from four directions (east, south, west, and north) at three levels each (upper, middle, and lower), i.e., each tree canopy was split into 12 resource units (Song et al., 2010). At each canopy level, we spent 3–5 min to collect arthropods and count the number of individuals of each species of the arthropods. The branch beating method was adopted to collect insect pests and predators from the peach tree canopy according to Simon et al. (2007). Insect pests and predators falling from the branches were collected, identified and counted immediately. Additionally, we took another few minutes to strip off the damaged young shoots in each twig to see if there were any G. molesta larvae. Sampling was done at appropriately 10-day intervals from late March to early October both in 2010 and 2011. 2.4. Data analysis Statistical analyses were performed with SPSS 16.0. Normal distribution and homocedasticity of all data were checked by the Kolmogorov–Smirnov test and Levene test, respectively. Threeway analysis of variance with general linear model in SPSS 16.0 was performed to analyze the above indices, so as to compare the interactive effects of sites, years and orchard types on the biocontrol service indices. If the values of the biocontrol service indices were not significantly affected by the years, we considered the two years’ data as a whole to compare the differences among means of treatments and controls with Tukey’s Honestly Significant Difference (HSD) test at 0.05 level. 3. Results The abundances of aphids, G. molesta and generalist arthropod predators were significantly affected by orchard type, but not by site and time. The interactive effects of two factors (site × time, site × orchard type, and time × orchard type) and three factors (site × time × orchard type) on the above abundances were not significant. The ratio of generalist arthropod predator to aphid abundance and the ratio of generalist arthropod predator to G. molesta abundance were significantly affected by the factor of orchard type but not by the factors site and time. Meanwhile, the interactive effects of two factors (site × time, site ×orchard type, and time × orchard type) and three factors also had no significant effect on the above ratios. The abundances of aphids and G. molesta were significantly lower but those of generalist arthropod predators were significantly higher in ground cover areas than in control areas at the two sites (Table 1). At both sites, irrespective of ground cover, the abundances of aphids, G. molesta and generalist arthropod predators increased during spring but were stabilized thereafter. Meanwhile,
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N.-F. Wan et al. / Ecological Engineering 64 (2014) 62–65
Table 1 Comparison of the abundances of aphids, Grapholitha molesta (Busck) and generalist arthropod predators in peach orchards with and without ground cover by Trifolium repens L. (abundance: individuals per 30 trees; means ± SE). Site
Orchard type
Aphid
Xinchang, Shanghai
Ground cover Bare ground Ground cover Bare ground
83.6 121.8 83.1 118.8
Hudai, Jiangsu
G. molesta ± ± ± ±
9.9b 13.7a 9.7b 14.3a
106.0 159.0 102.8 154.1
± ± ± ±
Generalist arthropod predators
14.2b 19.7a 13.0b 18.7a
318.8 147.1 304.9 141.3
± ± ± ±
22.2a 12.0b 25.4a 12.1b
Notes: Generalist arthropod predators mainly include spiders, ladybirds and lacewings; different letters in the same column indicate that the means are significantly different at P < 0.05 (HSD test) within groups of ground cover (treatment) and bare ground (control) in Xinchang and Hudai with consecutive two years (38 sample dates were considered as 38 replicates). Means of abundance were calculated from a total 30 trees per treatment or control in each replicate plot.
Peach orchard with ground cover (Xinchang, Shanghai) Peach orchard without ground cover (Xinchang, Shanghai) Peach orchard with ground cover (Hudai, Jiangsu) Peach orchard without ground cover (Hudai, Jiangsu)
400
Aphids per 30 trees
the abundance of predators was consistently higher but the abundances of aphids and G. molesta were consistently lower in ground cover areas than in control areas (Fig. 1). Ground cover by T. repens in peach orchards significantly increased the ratio of the abundance of generalist arthropod predators to that of aphids and the ratio of the abundance of generalist arthropod predators to that of G. molesta (Table 2). During the two year study at the two sites, the ratio of generalist arthropod predator to aphid abundance and the ratio of generalist arthropod predator to G. molesta abundance were consistently higher in ground cover areas than in control areas, providing evidence for the directly antagonist effect of the main predators on the populations of aphids and G. molesta (Fig. 2).
300
200
100
0 1
3
5
7
9
11 13 15
17 19
21 23 25
27 29 31 33 35 37
500
400
300
200
100
Generalist arthropod predator per 30 trees
Diversified planting in ecosystems has always been one of the focuses of ecological engineering (Montagna et al., 2012; Tropek et al., 2013), and many studies have documented that plant diversity in agro-ecosystems promotes the biocontrol services provided by the evidence that the natural enemy abundance increases and the pest abundance decreases (Andow, 1991). Our results indicated that when peach orchards were covered with T. repens the abundances of aphids and G. molesta decreased, respectively, by 31.4% and 33.3% in Xinchang, and by 30.1% and 33.3% in Hudai. Moreover, the abundance of generalist predators increased by 116.7% in Xinchang and by 115.8% in Hudai. Similar results were observed in other systems, for instance, the aphid abundance decreased and the abundance of the major predator of aphids, Chrysoperla rufilabris increased in response to ground cover in pecan orchards (Smith et al., 1996). Ground cover promoting biocontrol service is based on the principle that such ecological engineering creates a suitable ecological structure within the agricultural landscape to provide resources such as food for adult natural enemies, alternative prey or hosts, and shelter from adverse conditions (Landis et al., 2000). The benefits offered by ground cover might result from the dispersal and migration of predators from orchard floor plants to the trees, which augment the population densities of predators and promote the control efficacy of predators over insect pests on trees. In this study, we focused on certain predators overwintering in T. repens, and observed that the spiders migrated as well as the ladybirds, and that lacewings dispersed from T. repens to peach trees, which might explain the higher abundance of generalist predators in peach tree canopy. In addition, T. repens might provide a refuge and reservoir for predators to avoid the adverse effect of regular management in peach orchards, and other studies presented similar evidence that uncut strips of lucerne (Medicago sativa) offered refuges to a range of coccinellid and hemipteran predators (e.g., Hossain et al., 2000). Song et al. (2010) reported that peach orchards intercropped with aromatic plants could promote the biocontrol service,
Grapholitha molesta (Busck) per 30 trees
4. Discussion
0 1
3
5
7
9
11 13 15 17 19 21 23 25 27 29 31 33 35 37
600 500
400 300
200
100 0 1
3
5
7
9
11 13 15 17 19 21 23 25 27 29 31 33 35 37
Time order Fig. 1. Dynamics of the abundances of aphids, G. molesta and generalist arthropod predators in peach orchards with and without ground cover T. repens. Vertical bars denote SE. The number on the X-axis indicates the sampling times, i.e., the first 19 times (1–19) were conducted from late-March to early-October 2010; and the other 19 times (20–38) from late-March to early-October 2011.
N.-F. Wan et al. / Ecological Engineering 64 (2014) 62–65
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Table 2 Comparison of the ratio of generalist arthropod predator abundance to aphid abundance and ratio of generalist arthropod predator abundance to G. molesta abundance in peach orchards with and without ground cover by T. repens (means ± SE). Site
Orchard type
Ratio of generalist arthropod predator abundance to aphid abundance
Xinchang, Shanghai
Ground cover Bare ground Ground cover Bare ground
6.12 1.70 5.42 1.73
Hudai, Jiangsu
± ± ± ±
0.69a 0.17b 0.54a 0.19b
Ratio of generalist arthropod predator abundance to G. molesta abundance 7.36 1.52 5.12 1.45
± ± ± ±
1.61a 0.18b 0.71a 0.20b
Notes: Generalist arthropod predators mainly include spiders, ladybirds and lacewings; different letters in the same column indicate that the means are significantly different at P < 0.05 (HSD test) within groups of ground cover (treatment) and bare ground (control) in Xinchang and Hudai with consecutive two years (38 sample dates were considered as 38 replicates). Means of abundance were calculated from a total 30 trees per treatment or control in each replicate plot.
Peach orchard with ground cover (Xinchang, Shanghai) Peach orchard without ground cover (Xinchang, Shanghai) Peach orchard with ground cover (Hudai, Jiangsu) Peach orchard without ground cover (Hudai, Jiangsu)
Ratio of generalist arthropod predators to aphids per 30 trees
20.0
However, a more comprehensive, long-term and large-scale assessment of the potential eco-engineering effects of ground cover vegetation in peach orchard ecosystem needs to be further studied. Acknowledgements
15.0
This study was funded by the grants from Shanghai Municipal Science and Technology Commission (12ZR1449100, 08dz1900401, 123919N0400), the National Natural Science Foundation of China, the Shanghai Rising-Star Program and the Key Project of Science and Technology for Agriculture of Shanghai from Shanghai Agriculture Committee.
10.0
5.0
0.0 1
3
5
7
9
11 13 15 17 19 21 23 25 27
29 31 33 35 37
References Ratio of generalist arthropod predators to G. molesta per 30 trees
30.0
20.0
10.0
0.0 1
3
5
7
9
11 13 15 17 19 21 23 25 27 29 31 33 35 37
Time order Fig. 2. Dynamics of the ratio of generalist arthropod predator abundance to aphid abundance and ratio of generalist arthropod predator abundance to G. molesta abundance in peach orchards with and without ground cover by T. repens. Vertical bars on each point denote SE. The numbers on the X-axis indicate the sampling times, i.e., the first 19 times (1–19) were conducted from late-March to early-October 2010; and the other 19 times (20–38) from late-March to early-October 2011.
indicated by the fact that the ratio of the abundance of natural enemies to that of insect pests was significantly higher in any of the aromatic plants than in control. Similar results were reported by Rieux et al. (1999) that ground cover resulted in a higher beneficial: phytophagous ratio in pear tree canopy. Our study indicated that compared to that in control, the ratio of generalist arthropod predator abundance to aphid abundance and that of generalist arthropod predator abundance to G. molesta abundance averagely increased, respectively, by 260.0% and 384.2% in Xinchang, and 213.3% and 253.1% in Hudai in ground cover areas. This study showed that the ecological engineering of ground cover vegetation ultimately promoted biocontrol services in peach orchards, indicated by the fact that the abundances of the generalist predators (ladybirds, lacewings and spiders) increased and the abundances of the key insect pest aphids and G. molesta decreased.
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