Within-field distribution of the damson-hop aphid Phorodon humuli (Schrank) (Hemiptera: Aphididae) and natural enemies on hops in Spain


Alicia Lorenzana

University of León, Dept. Agricultural Sciences and Engineering. Avda. Portugal 41, 24071 León, Spain

Alfonso Hermoso de Mendoza

IVIA, 46113 Moncada, Valencia, Spain

Victoria Seco

University of León, Dept. Agricultural Sciences and Engineering. Avda. Portugal 41, 24071 León, Spain

Piedad Campelo

University of León, Dept. Agricultural Sciences and Engineering. Avda. Portugal 41, 24071 León, Spain

Pedro A. Casquero

University of León, Dept. Agricultural Sciences and Engineering. Avda. Portugal 41, 24071 León, Spain



A field trial was performed in a hop yard throughout 2002, 2003 and 2004 in order to determine the within-field distribution of Phorodon humuli (Schrank) (Hemiptera: Aphididae) and its natural enemies. The distribution of P. humuli was directly affected by the position of the hop plants in the garden, with significantly higher concentrations of aphids (p=0.0122 in 2002 and p=0.0006 in 2003) observed along the edge. However, in 2004 the plants located on the marginal plots had similar populations to those on the more inner plots. This can be explained by a higher wind speed which made it more difficult to land on edge plants first. The hop aphid’s main natural enemy was Coccinella septempunctata (Coleoptera: Coccinellidae), whose population was greatest where the aphids were most abundant with a significantly greater number of eggs (p=0.0230) and adults (p=0.0245) in 2003. Lacewing eggs were also frequently observed, with a significantly higher population (p=0.0221 in 2003 and p=0.0046 in 2004) where the aphid numbers were high. The number of winged aphids was greatest towards the margins of the garden in 2003. It is argued that the spatial distribution of the hop aphid and its natural enemies could be used to plan a sampling program and to estimate the population densities of these insects for use in integrated pest management programs.

Additional key words: Humulus lupulus; spatial distribution; Coleoptera; Coccinelidae; winged aphids; integrated pest management.

Authors’ contributions: Conceived and designed the experiments, and analyzed the data: AL, AHM and PAC. Performed the experiments, and wrote the paper: AL and PC. Obtaining funding: VS. Coordinating the research project: AL, AHM and VS.

Citation: Lorenzana, A.; Hermoso de Mendoza, A.; Seco, V.; Campelo, P.; Casquero, P. A. (2017). Within-field distribution of the damson-hop aphid Phorodon humuli (Schrank) (Hemiptera: Aphididae) and natural enemies on hops in Spain. Spanish Journal of Agricultural Research, Volume 15, Issue 2, e1006.

Received:11 Jul 2016 Accepted:31 May 2017

Copyright © 2017 INIA. This is an open access article distributed under the terms of the Creative Commons Attribution (CC-by) Spain 3.0 License.

Funding: Junta de Castilla y León. Spain (Project Nº. LE57/O2); Fundación Chicarro-Canseco-Banciella (grant awarded to AL to work in the University of León).

Competing interests:The authors have declared that no competing interests exist.

Correspondence should be addressed to Alicia Lorenzana:





Material an methods






Spain is the sixth largest hop-producing country in the European Union (The Barth Report, Hops, 2014/2015 ). Most of the plantations are located in the Province of León and occupied 524 ha in 2013. These, together with 8 ha in La Rioja, 5 ha in Palencia and 2 ha in Navarra, account for all of the land cultivated for hops (Humulus lupulus L.) in Spain (MAPAMA, 2014). The most common cultivar in León is 'Nugget' (90.2%) compared with 'Columbus' (8.7%), 'Magnum' (0.7%), 'Perle' (0.1%) and 'Summit' and 'Millenium' under field tests (0.3%).

The hop aphid, Phorodon humuli (Schrank), is a major pest on hops in the northern hemisphere (Weihrauch & Moreth, 2005). P. humuli can inhibit growth and reduce the number of flowers, which constitute an essential raw material for brewing beer. Aphid contamination of hop cones also seriously reduces their economic value because of arbitrary commercial criteria related to the presence of aphids in cones (Lorenzana et al., 2010). P. humuli uses several common Prunus spp. as primary hosts (Eppler, 1986). The eggs hatch in early spring, and usually after two or three wingless generations winged emigrants appear and fly to hops, Humulus lupulus L., the sole secondary host (Blackman & Eastop, 1984). On hops, P. humuli does not produce winged morphs capable of re-infesting other hops (Campbell, 1985), so the pattern and intensity of aphid infestation within hop plantations largely reflects the colonization, accumulation and secondary flight behaviour of aphids migrating from Prunus spp. (Campbell & Ridout, 1999). In autumn, winged females (return migrants) and later winged males are produced. The return migrants produce wingless sexual females on primary hosts, which lay the overwintering eggs after mating (Campbell & Muir, 2005). Population development of this aphid has been studied in several countries. Specifically, within-field distribution have been studied by Campbell (1977) in England, Ilharco et al. (1979) in Portugal and Wright et al. (1990) in the USA but has not been studied in detail in Spain. A knowledge of the distribution of naturally-occurring enemies is fundamental to an integrated pest management system and this has not been studied here either. Campbell (1977) found that various features in plantations of hops such us bine density, bine height, plant position, hill type, string orientation and hop variety influenced the patterns of colonisation by migrant P. humuli and concluded that most of these probably reflected variation in local patterns of wind shelter within which aphids could manoeuvre and land (Campbell & Ridout, 1999). In addition, edge effects tend to be greatest where there are windbreaks, which are frequent in hop gardens in the UK. Field studies of aphid distributions have identified several forms of edge effects (Lewis, 1969), with the immigrants being observed first on the lea side of the edge of the crop (Dean & Luuring, 1970; Dean, 1973). By contrast, Ruggle & Holst (1995) studied a 60 m by 40 m area within a winter wheat field and concluded that aphids were concentrated in the centre of the field when population levels were high. Longley et al. (1997) studied the spatial and temporal distribution of aphids and parasitoids following insecticide application in winter wheat in the UK whilst Schotzko & Smith (1991) demonstrated that the host plant (winter wheat) itself may influence aphid distributions.

A quantitative knowledge of the distribution of arthropod pests and of their natural enemies is essential for an understanding of their interactions, as well as being a prerequisite for the development of reliable sampling plans for estimating and monitoring the pest and its natural enemy abundance (Onzo et al., 2005). A knowledge of spatial distribution of prey and predator is important in evaluating the system’s persistence and the potential of natural enemies to reduce prey density (Stavrinides & Skirvin, 2003). The spatial distribution of an insect can be employed in investigating population dispersal behavior, establishing a precise sampling scheme and for sequential sampling (Margolis et al., 1984), binomial sampling (Binns & Bostanian, 1990), the study of population dynamics (Jarosik et al., 2003), detecting pest levels that justify control measures (Arnaldo & Torres, 2005) and assessing crop loss (Hughes, 1996).

The aim of this research was to study the within-field distribution of P. humuli populations (apterous and winged aphids) and their natural enemies in hop plants.

Material and methodsTop

Location and methodology of sampling

The experimental site was in León, Spain, during 2002, 2003 and 2004. A garden planted with the hop cv. 'Nugget' (0.72 ha), consisting of 40 rows (3 m apart) each with 40 plants (1.5 m apart), was chosen for the study, situated at the University of León’s experimental farm maintained by the School of Agricultural Engineering. The garden was surrounded on the north by a road and on the south by arable crops (sugar beet in 2002 and 2004, and barley in 2003). The eastern boundary was a small area of mixed woodland and the western boundary was a small area of mixed vineyards and fruit trees. There were no edges or other structures to reduce the wind. The height of the wirework was 6 m with two strings per rootstock. Three hop bines were trained to each string.

Five plots for each treatment, “marginal plots” and “inner plots”, were established in the field. Each plot was made up of 18 plants in three adjacent rows of six plants per row. The area of each plot was 81 m² (9 m × 9 m). Three adjacent rows were left between both treatments (Fig. 1).

Figure 1. Diagram of sampling in the hop yard during 2002, 2003 and 2004.

Only the three central plants were sampled in each experimental plot of eighteen plants. Counts were taken in the following manner: a wooden frame measuring 20 cm by 30 cm was placed on the surface of one of the bines at heights of 2, 3.25, and 6 m from the ground. Within the area enclosed by this frame, counts were taken of the total number of leaves, the number of leaves with aphids, the total number of aphids and the average number of them per leaf attacked. The non-destructive sampling was carried out weekly, one week measuring aphid population on the left bine of the plant, and the following week on the right one.

The population density of P. humuli has habitually been expressed as the number of aphids per leaf, although other parameters can be used, such as the number of aphids per dm² of leaf (Campbell, 1978), or per m² of plant (Hermoso de Mendoza et al., 2001, for Aphis gossypii on clementines). This study expresses aphid population density by number of aphids per m² of hop bine in a two-dimensional approach, by extrapolating the frame area (6 dm2). For each treatment, the mean was calculated first for the three plants in each plot and then for its five repetitions.

Within-field distribution of aphids and natural enemies

Within-field distribution of P. humuli was studied, and the mean number of aphids per m² of hop bine surface for each replicate in the “marginal plots” and “inner plots” was calculated. The weekly sampling in 2002 began on 21 June and terminated on 6 September, and included just apterae. In 2003, it began on 30 May and finished on 29 August, and included both apterous and alate forms. In 2004, it began on 25 June and terminated on 3 September, and included just apterae. We started sampling when plants had reached their full height (6 m) in 2002 and 2004, whereas sampling begun before in 2003 in order to record the alatae aphid, although this was not the aim of this study.

In the same way, the distribution and frequency of the natural enemies (ladybird beetles (egg clutches, larvae and adults) and lacewings eggs) was studied in 2003 and 2004, giving the number of natural enemies per m² of hop bine.

In 2003, within-field distribution for winged aphids was studied in the same way as for total aphids.

Meteorological data were recorded with a local weather station located about 200 m from the hop plot in order to analyse the relationship between them and the distribution of aphids.

Statistical analysis

The field data were transformed using the square-root transformation (X + 0.5)½, where X is the original data. This transformation is appropriate for insect data especially when zeroes are present (Steel & Torrie, 1986). These square-root values were used in the analysis of variance.

Analysis of variance was performed using the general linear models (GLM) procedure. Analyses for aphid and natural enemy density for each week and for their total number between marginal and inner plots were carried out. Mean comparisons were performed using the LSD test to examine differences (p<0.05). Linear regressions were performed between aphids and beetles on the marginal and on the inner plots. All analyses were performed using SAS software version 9.1.2 (SAS Institute Inc., 2004).


Natural enemies

Coccinelids and eggs of Neuroptera were the most abundant natural enemies found on leaves during 2003 and 2004. Coccinella septempunctata was the most common species in 2003 (>20 records) and this species was as frequent as the other coccinelid species in 2004 (<20 records), i.e. Propylea quatuordecempunctata (Linnaeus, 1758), Adalia decempunctata (Linnaeus, 1758) and Adalia bipiunctata (Linnaeus, 1758). A large number of lacewing eggs (>20 records in 2003 and 10-20 records in 2004) and Aeolothrips sp. (<5 records in 2003 and <20 records in 2004) were also registered while parasitized aphids were found only in 2003 (10-20 records) (Lorenzana et al., 2013).

Within-field distribution of aphids and natural enemies

In 2002, the marginal plots contained the highest characteristic population peaks of mid July and early September (Fig. 2). The final cumulative aphid density was significantly greater in the marginal plots than on the inner plots (F=3.30; DF=1; p=0.0122) (Fig. 3). In 2003, the peak aphid population on the marginal plots was also significantly greater than those on the inner plots (20 June) (F=18.14; DF=1; p=0.0237) and also in the following week (F=24.86; DF=1; p=0.0155) (Fig. 4). In 2003, the final cumulative aphid density was significantly greater in the marginal plots than in the inner plots, as in 2002 (F=34.74; DF=1; p=0.0006) (Fig. 3). Unlike the previous two years, the highest population peaks of mid July and early September in 2004 are reached on the inner plots (Fig. 5). The final cumulative aphid density in the two treatments was not significantly different (Fig. 3).

Figure 2. Within-field distribution of P. humuli (aphids on the marginal plots and aphids on the inner plots) on hops in 2002.

Figure 3. Within-field distribution of P. humuli on hops in 2002, 2003 and 2004. Columns represent the final cumulative aphid density on the marginal plots and on the inner plots. Different letters above the histogram bars indicate significant differences between groups (p‹0.05, Tukey’s test).

Figure 4. Within-field distribution of P. humuli (aphids on the marginal plots and aphids on the inner plots) and ladybirds beetles (beetles on the marginal plots and beetles on the inner plots) on hops in 2003. Mean comparisons significantly different between sides for aphids (at the same date) are shown with capital letters (p‹0.05)

Figure 5. Within-field distribution of P. humuli (aphids on the marginal plots and aphids on the inner plots) and ladybird beetles (beetles on the marginal plots and beetles on the inner plots) on hops in 2004.

With regard to the natural enemies, in 2003, the final cumulative ladybird beetle (egg, larva and adult) and lacewing egg density was greatest on the marginal plots (Fig. 6). Beetle adults (F=1.12; DF=1; p=0.0245) and eggs (F=8.42; DF=1; p=0.0230), as well as lacewing eggs (F=6.16; DF=1; p=0.0221) were significantly more abundant in the marginal plots (Fig. 6) whereas, in 2004, the final cumulative ladybird beetle (egg, larva and adult) density was somewhat higher on the inner plots as was the number of lacewing eggs (F=14; DF=1; p=0.0046) (Fig. 6). Statistical analysis for each week over both years indicated that there were no significant differences between the natural predator populations between the marginal and inner plots, except for 3 September, 2004, when lacewing eggs were significantly more abundant in the marginal than in the inner plots (F=11.89; DF=1; p=0.0040) (Figs. 4–5).

Figure 6. Within-field distribution of natural enemies of P. humuli on hops in 2003 and 2004: beetles adults, beetles larvae, beetles eggs and lacewing eggs. Columns represent the final cumulative natural enemy density on the marginal plots and on the inner plots. Different letters above the histogram bars indicate significant differences between groups (p‹0.05, Tukey’s test).

Regression analyses showed a positive correlation between aphids and ladybird beetles in the marginal plots in both 2003 and 2004 (y = 0.0451x + 0.6655 and R2 = 0.958 in 2003; y = 0.0518x + 0.5054 and R2 = 0.846 in 2004) and in the inner plots (y = 0.06x + 0.6459 and R2 = 0.961 in 2003; y = 0.1145x + 0.1401 and R2 = 0.89 in 2004).

With regard to within-field distribution of winged aphids in 2003, they were most abundant in the marginal plots since the beginning of sampling (30 May) until the last alatae aphid was found (18 July), apart from on the 4 July when one alatae aphid was found in the inner plots. The final cumulative winged aphid density (spring migration) was significantly greater in the marginal plots than in the inner plots in 2003 (F=4.13; DF=1; p=0.0446) (Fig. 7).

During the period May-July (spring migration from Prunus spp.) the prevailing wind direction was between 200º and 340º, with a greater number of days between 200º and 250º (south-west). It was registered a greater number of days with rain and wind in 2004 than in 2002 and 2003 in the same period. Wind speed did not exceed 36 km/h between May and July in 2002 and 2003, whereas wind speed exceeded 36 km/h on ten days and 50 km/h on two days in 2004. In the same period, there was seven days with storms in 2002, five days with storms in 2003 and twelve days with storms in 2004.

Figure 7. Within-field distribution of winged aphids on hops in 2003. Columns represent the final cumulative winged aphid density (spring migration) on the marginal plots and on the inner plots. Different letters above the histogram bars indicate significant differences between groups (p‹0.05, Tukey’s test).


Within-field distribution of hop aphids and their natural enemies

The results obtained in 2002 and 2003 are similar to those obtained for hop aphids in other countries. Thus, Campbell (1977) in England, Ilharco et al. (1979) in Portugal and Wright et al. (1990) in the USA stated that the position of the plots relative to the margin influenced distribution of P. humuli, with more aphids to be found on the plants at the edge and on those plants close to them. If, in addition, there are wind breaks, these would have had a marked effect on the settling of the alatae, causing significant greater colonization within the more marginal rows. The fewer aphids in the marginal plots than the inner plots in 2004 might have been caused by the wind, which could have made it difficult for them to settle on the plants. When wind speed is low, aphids tend to accumulate around the edges of the plantation (as happened in the previous years); in this way, aphids could direct their flight in the slower moving air on the lea side of the hedge. Wind speed was not upon 36 km/h between the spring migration of P. humuli in 2002 and 2003, so aphids could fly even against the wind to land in the shelter of the plants. However, wind speed was higher in 2004, so aphids had difficulty in settling on any plants. This was confirmed by Campbell (1977) in his trials in hop gardens in England. Furthermore, the greater number of days with rain, wind and storms during the spring migration of aphids in 2004 damaged mainly the plants around the edge, making them in an unfavorable habitat for the aphids.

Similar within-field distributions have been reported for other aphid species such as Aphis gossypii in Capsicum annuum (Rahman et al., 2010), where aphid populations formed larger patches towards the edge of the chilli fields than in the centre, and Rhopalosiphum padi in cereal crops (Parry et al., 2006) where the highest aphid densities were found on the field edge where the wind played a significant role in the distribution of individuals.

Edge effects may be due to a number of factors. The most important may be the effect field edges have on the deposition of small insects; this could enhance aphid immigration within the margins (Winder et al., 1999). Small flying insects such as aphids generally accumulate on the lea side of wind breaks (Lewis, 1966, 1969, 1970; Lewis & Stephenson, 1966). Evans & Allen-Williams (1993) argued that the edge of any crop ecosystem is where herbivores, including aphids, first locate abundant food sources, using either visual or olfactory cues. Dean & Luuring (1970) concluded that aggregation was higher at field margins because more airborn aphids become established there.

Site-specific management (i.e., targeted insecticide applications) is appropriate for insects that aggregate during their initial colonization; targeted applications can direct control, improve cropping economics, reduce exposure to animals and the environment, and provide refuge to natural enemies (Weisz et al., 1995, 1996). Site specific management is currently recommended for the green peach aphid, Myzus persicae (Sulzer), along potato field edges in the USA (Suranyi et al., 1999, Carroll et al., 2009) and for the grain aphid, Sitobion avenae F. in the UK (Winder et al., 1999). However, Nault et al. (2004) suggest that the soybean aphid (Aphis glycines Matsumura), pea aphid (Acyrthosiphon pisum (Harris)), corn leaf aphid (Rhopalosiphum maidis (Fitch)) and yellow clover aphid (Therioaphis trifolii (Monell)) all disperse randomly in snap bean, Phaseolus vulgaris L., in the USA. Differences in alatae spring colonization may be due to the overwintering potential of the aphid species and proximity to secondary hosts in the spring (Hodgson et al., 2005). Landing behavior appears to vary among aphid species and cropping systems; therefore, a single management tactic is not appropriate for all aphids. The colonization behavior of P. humuli provides a window of opportunity for targeting aerial sprays of insecticides to field margins to control early colonizing aphids in hop gardens. This would provide direct benefits through lower production and application costs and a reduction in worker and environmental exposure. Reductions in the dry weight of the crop associated with large numbers of aphids could also be avoided (a yield loss of 44% was observed when the population rose to 4400 P. humuli/m² in late June in Spain) (Lorenzana, 2006). The effectiveness of targeted applications would dependent upon availability of timely information on local P. humuli presence and movement into hop field, taking into account that, if there were strong winds at that time, the aphids could not land at the edges of the plots.

Naturally enemy populations may be positively related to landscapes with many field margins (Landis et al., 2000; Sutherland & Samu, 2000). Lady beetles appear to be able to effectively reduce hop aphid populations because they coincide spatially and temporally. These two-dimensional distributions of P. humuli and predatory lady beetles may also be helpful in developing accurate sampling techniques for forecasting the presence of P. humuli and its interaction with natural enemies.

In relation to within-field distribution of winged aphids, it has never been closely studied in Spain. As was to be expected, the total number of winged aphids was significantly greater on the marginal than on the inner plots.

In conclusion, it is important to emphasize that the position of plants within the yard influences the distribution of P. humuli, with more aphids occurring on the edges than inside. The number of winged aphids was also higher along the margins. The initial distribution of the aphid along field borders may make it possible to reduce insecticide usage by directing initial control efforts on field borders. However, in years with high winds, in fields without windbreaks, the aphid population may be similar within hop fields as in the marginal plots. The total number of ladybird beetles (eggs, larvae and adults) was greatest where the aphid population was most abundant. These results clearly indicate that the ladybird beetle population is an important factor to consider within an integrated management program for hop aphids, although some increase in the natural build-up of these natural enemies would be necessary in order to exploit them for control purposes.


We thank Colin Campbell, Florian Weihrauch, David James, José Antonio Magadán, Blanca Ramírez, Nicolás Pérez, Alfonso Pérez and Juan Luis Gutiérrez for their help.


Arnaldo PS, Torres LM, 2005. Spatial distribution and sampling of Thaumetopoea pityocampa (Lep., Thaumetopoeidea) populations of Pinus pinaster Ait. In Monntesinho, N. Portugal. Forest Ecol Manag 210: 1-7.

Binns MR, Bostania NJ, 1990. Robustness in empirically based binomial decision rules of integrated pest management. J Econ Entomol 83: 420-427.

Blackman RL, Eastop VF, 1984. Aphids on the world’s crops. Willey, Chichester, UK. 466 pp.

Campbell CAM, 1977. Distribution of damson-hop aphid (Phorodon humuli) migrants on hops in relation to hop variety and wind shelter. Ann Appl Biol 87: 315-325.

Campbell CAM, 1978. Regulation of the damson-hop aphid (Phorodon humuli (Schrank.)) on hops (Humulus lupulus L.) by predators. J Hortic Sci 53(3): 235-242.

Campbell CAM, 1985. Has the damson-hop aphid an alatae alienicolous morph? Agr Ecosyst Environ 12: 171-180.

Campbell CAM, Ridout MS, 1999. Effects of plant spacing and interplanting with oilseed rape on colonisation of dwarf hops by the damson-hop aphid, Phorodon humuli. Entomol Exp Appl 99: 211-216.

Campbell CAM, Muir RC, 2005. Flight activity of the damson-hop aphid, Phorodon humuli. Ann Appl Biol 147: 109-118.

Carrol MW, Radcliffe EB, MacRae IV, Ragsdale DW, Olson KD, 2009. Border treatment to reduce insecticide use in seed potato production: biological, economic, and managerial analysis. Am J Potato Res 86: 31-37.

Dean GJ, 1973. Aphid colonisation of spring cereals. Ann Appl Biol 75: 183-193.

Dean GJ, Luuring BB, 1970. Distribution of aphids in cereal crops. Ann Appl Biol 66: 485-496.

Eppler A, 1986. Untersuchungen zur Wirstwahl von Phorodon humuli Schr. I. Besiedelte Pflanzenarten. Anzeiger für Schädlingskunde, Pflanzenschutz, Umweltschutz 59: 1-8.

Evans KA, Allen-Williams LJ, 1993. Distant olfactory response of the cabbage seed weevil, Ceutorhynchus assimilis, to oilseed rape odour in the field. Physiol Entomol 18: 251-256.

Hermoso de Mendoza A, Belliure B, Carbonell EA, Real V, 2001. Economic thresholds for Aphis gossypii (Hemiptera: Aphididae) on Citrus clementina. J Econ Entomol 94 (2): 439-444.

Hodgson EW, Koch RL, Ragsdale DW, 2005. Pan trapping for soybean aphid (Homoptera: Aphididae) in Minessota soybean fields. J Entomol Sci 40 (4): 409-419.

Hughes G, 1996. Incorporating spatial pattern of harmful organisms into crop loss models. Crop Protect 15: 407-421.

Ilharco FA, Pinto J, Vieira JJ, 1979. O piolho do lúpulo na regiao da Bragança. Serviços Regionais de Agricultura. Direcçao Regional de Trás-os-Montes, Protecçao a Produçao Agrícola, Vila Real, Portugal. 38 pp.

Jarosik V, Honek A, Dixon AFG, 2003. Natural enemy ravine revisited: the importance of sample size for determining population growth. Ecol Entomol 28: 85-91.

Landis DA, Wratten SD, Gurr GM, 2000. Habitat management to conserve natural enemies of arthropod pests in agriculture. Ann Rev Entomol 45: 175-201.

Lewis T, 1966. An analysis of compounds of wind affecting the accumulation of flying insects near artificial windbreaks. Ann Appl Biol 58: 365-370.

Lewis T, 1969. The distribution of flying insects near a low hedgerow. J Appl Ecol 6: 443-452.

Lewis T, 1970. Patterns of distribution of insects near a windbreak of tall trees. Ann Appl Biol 65: 213-220.

Lewis T, Stephenson JW, 1966. The permeability of artificial windbreaks and the distribution of flying insects in the leeward sheltered zone. Ann Appl Biol 58: 355-363.

Longley M, Jepson PC, Izquierdo J, Sotherton N, 1997. Temporal and spatial changes in aphid and parasitoid populations following applications of deltamethrin in winter wheat. Entomol Exp Appl 83: 41-52.

Lorenzana A, 2006. Determinación de los umbrales de tratamiento del pulgón del lúpulo Phorodon humuli (Schrank, 1801) y estudio de la evolución poblacional en la provincia de León. Doctoral thesis. Univ. de León, Spain.

Lorenzana A, Hermoso de Mendoza A, Seco MV, Casquero PA, 2010. Population development of Phorodon humuli and predators (Orius spp.) within hop cones: Influence of aphid density on hop quality. Crop Prot 29: 832-837.

Lorenzana A, Hermoso de Mendoza A, Seco MV, Casquero PA, 2013. Population dynamics and integrated control of the damson-hop aphid Phorodon humuli (Schrank) on hops in Spain. Span J Agric Res 11 (2): 505-517.

MAPAMA, 2014. Avance anuario estadística 2014. Ministerio de Agricultura y Pesca, Alimentación y Medio Ambiente, Gobierno de España. [20 May, 2016].

Margolis DC, Lanpert EP, Kennedy GC, 1984. Sampling program for two spotted spider mite (Acari:Tetranychidae) in peanut. J Econ Entomol 77: 1024-1028.

Nault BA, Shah DA, Dillard HR, McFaul AC, 2004. Seasonal and spatial dynamics of alate aphid dispersal in snap bean fields in proximity to alfalfa and implications for virus management. Environ Entomol 33: 1593-1601.

Onzo A, Hanna R, Sabelis MW, Yaninek JS, 2005. Temporal and spatial dynamics of an exotic predatory mite and its herbivorous mite prey on cassava in Benin, West Africa. Environ Entomol 34: 866-874.

Parry HR, Evans AJ, Morgan D, 2006. Aphid population response to agricultural landscape change: A spatially explicit, individual-based model. Ecol Model 199: 451-463.

Rahman T, Nor Mohd Roff M, Bin Abd Ghani I, 2010. Within-field distribution of Aphis gossypii and aphidophagous lady beetles in chili, Capsicum annuum. Entomol Exp Appl 137: 211-219.

Ruggle P, Holst N, 1995. Spatial variation of Sitobion avenae (F.) (Hom.: Aphididae) and its primary parasitoids (Hym.: Aphididae, Aphelinidae). Acta Jutlandica 70: 227-233.

SAS Institute, 2004. SAS® 9.1.2. Qualification Tools User’s Guide. SAS Institute, Cary, NC, USA. 218 pp.

Schotzko DJ, Smith CM, 1991. Effects of host plant on the between-plant spatial distribution of the Russian wheat aphid (Homoptera: Aphididae). J Econ Entomol 84: 1725-1734.

Stavrinides MC, Skirvin DJ, 2003. The effect of chrysanthemum leaf trichome density and prey spatial distribution on predation of Tetranychus urticae (Acari: Tetranychidae) by Phytoseiulus persimilis (Acari: Phytoseiidae). Bull Entomol Res 93: 343-350.

Steel RGD, Torrie JH, 1986. Bioestadística: Principios y procedimientos. McGraw Hill, México DF. 622 pp.

Suranyi R, Radcliffe T, Ragsdale D, MacRae IV, Lockhart B, 1999. Aphid alert: A research/outreach initiave addressing potato virus problems in the northern Midwest. In: Radcliffe’s IPM World Textbook; Radcliffe EB, Hutchison WD, Cancelado RD (eds.). University of Minnesota, St. Paul, MN, USA. [21 December, 2015].

Sutherland K, Samu F, 2000. Effects of agricultural diversification on the abundance, distribution, and pest control potential of spiders: a review. Entomol Exp Appl 95: 1-13.

Weihrauch F, Moreth L, 2005. Behaviour and population development of Phorodon humuli (Schrank) (Homoptera: Aphididae) on two hop cultivars of different susceptibility. J Ins Behav 18: 693-705.

Weisz R, Fleischer S, Smilowitz Z, 1995. Map generation in high value horticultural integrated pest management appropriate methods for site-specific pest management of Colorado potato beetle (Coleoptera: Chrysomelidae). J Econ Entomol 88: 1650-1657.

Weisz R, Fleischer S, Smilowitz Z, 1996. Site-specific integrated pest management for high- value crops: impact on potato pest management. J Econ Entomol 88: 501-509.

Winder L, Perry JN, Holland JM, 1999. The spatial and temporal distribution of the grain aphid Sitobion avenae in winter wheat. Entomol Exp Appl 93: 277-290.

Wright LC, Cone WW, Menzies GW, Wildman TE, 1990. Numerical and binomial sequential sampling plans for the hop aphid (Homoptera: Aphididae) on hop leaves. J Econ Entomol 8 (4): 1388-1394.