FIELD AND FORAGE CROPS Assessment of Fennel (: ) and Their Predators in Fennel Intercropped With Cotton With Colored Fibers

F. S. RAMALHO,1 F. S. FERNANDES, A.R.B. NASCIMENTO, J. L. NASCIMENTO JU´ NIOR, J. B. MALAQUIAS, AND C.A.D. SILVA

Biological Control Unit/Embrapa Algoda˜o, Av. Osvaldo Cruz, 1143 Campina Grande, Paraõ´ba, 58107-720, Brazil Downloaded from https://academic.oup.com/jee/article/105/1/113/845722 by guest on 28 September 2021

J. Econ. Entomol. 105(1): 113Ð119 (2012); DOI: http://dx.doi.org/10.1603/EC11219 ABSTRACT The fennel , Hyadaphis foeniculi (Passerini) (Hemiptera: Aphididae) is a major pest of fennel, Foeniculum vulgare Miller in northeast region of Brazil. We hypothesize that inter- cropping can be used as an alternative pest management strategy to reduce aphid yield loss in fennel. Thus, we investigated the severity of fennel plant damage in relation to infestation by the fennel aphid and predation by Cycloneda sanguinea (L.) (Coleoptera: Coccinellidae)(spotless lady beetle), green lacewing, Chrysoperla carnea (Stephens) (Neuroptera: Chrysopidae), and Scymnus spp. (Coleoptera: Coccinellidae) in sole fennel plots and plots of fennel intercropped with cotton with colored Þbers. The fennel aphid populations in nontreated plots were signiÞcantly larger in sole fennel plots than in intercropped plots. The highest densities of C. sanguinea, green lacewings and Scymnus spp., associated with the suppression of fennel aphid populations was found in fennel in the intercropping systems. Fennel aphids reduced the fennel seed yield by 80% in the sole fennel plots compared with Ϸ30% for all intercropping systems. The results obtained in this research are of practical signiÞcance for designing appropriate strategies for fennel aphid control in fennel-cotton intercropping systems. In summary, intercropping fennel with cotton with colored Þbers apparently promoted biocontrol of fennel aphid in fennel.

KEY WORDS fennel, Hyadaphis foeniculi, cotton with colored Þbers, damage, intercropping

The fennel aphid Hyadaphis foeniculi (Passerini) The severity of damage to fennel caused by the (Hemiptera: Aphididae) is the major pest of fennel aphid is unknown. Though if untreated, H. fennel (Foeniculum vulgare Miller) in northeastern foeniculi can probably cause a signiÞcant drop in yield, Brazil (Petersen and Romano 1999, Ferreira and reducing signiÞcantly the seed yield and essential oil Sousa-Silva 2004). It is a phloem-feeding and polypha- production. gous (Ferreira and Sousa-Silva 2004) species that can One alternative method to reduce the damage from attack fennel soon after the plant emerges and mainly aphids to fennel crop is the use of intercropping sys- during the ßower stage and can cause losses of the tems. Intercropping is an agronomic practice (Mon- ßowers and fruits (Abramson et al. 2006). tezano and Peil 2006), and when properly managed, it Hyadaphis foeniculi sucks sap from leaves and can signiÞcantly contribute to pest control (Sarker et mainly from ßowers and fruit and causes the umbels al. 2007). Intercropping systems represent a return to to shrivel and to desiccate (Ferreira and Sousa-Silva a more natural environment; they exhibit higher bio- 2004). Additionally, H. foeniculi can transmit viruses to logical diversity and, therefore, generally greater sta- plants. According to Blackman and Eastop (2000), it bility. Additionally, these systems bring beneÞts and vectors Ͼ12 types of viruses, including the mosaic economic returns to the farmer from northeastern potyvirus, yellow spot luteovirus and honeysuckle la- Brazil, reducing the risk of total crop failure because tent carlavirus. Furthermore, it excretes honeydew, of water stress, pest damage, or losses incurred as a which favors the development of Capnodium spp. result of ßuctuating market prices (Arau´ jo et al. 2008). fungi. This excretion can lead to the formation of sooty Intercropping systems also increases the farmersÕ net mold, consequently impairing umbel respiration and income (Zhang et al. 2007). fruit quality. When the population becomes too large Intercropping has been studied in various combi- or food is scarce, aphids produce winged phenothypes nations to assess its effects on the incidence of various and migrate to new ßowers (Blackman and Eastop insect species: intercropping cotton (Gossypium hir- 2000). sutum L.) with corn (Zea mays L.) with sorghum (Sorghum bicolor (L.) Moench) with beans (Vigna unguiulata (L.)) or sesame (Sesamum indicum L.) 1 Corresponding author, e-mail: [email protected]. (Gonzaga et al. 1991); cotton with alfalfa (Medicago

0022-0493/12/0113Ð0119$04.00/0 ᭧ 2012 Entomological Society of America 114 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 105, no. 1 sativa L.) (Lin et al. 2003); cotton with corn (Fabia˜o 9) sole fennel (treated plot), and 10) sole fennel and Sousa 2007); cotton with wheat (Triticum aesti- (nontreated plot), with four replications. The treated vum L.) (Zhang et al. 2007); and cotton with wheat plots were sprayed periodically with thiamethoxam with alfalfa with sorghum (Phoofolo et al. 2010). Ac- insecticide at the rate of 0.6 g/lϪ1 at 1-wk intervals cording to Gonzaga et al. (1991), intercropping sig- beginning after the transplant of the fennel plants to niÞcantly alters the habitat for , favoring keep the plants aphid-free (full protection). The non- the development of populations and functioning of treated plots were not sprayed with any insecticide to natural enemies. allow for natural aphid infestation, along with their It has been suggested that the biotic, structural, and predators and parasitoids. microclimatic complexity of multispecies plant asso- The intercropped fennel-cotton experimental units ciations work synergistically to produce an “associa- consisted of rows of fennel between rows of naturally tional resistance” to pest attack (Tahvanainen and colored cotton (BRS SaÞra) (Fig. 1) with a row length

Root 1972). Root (1973) hypothesized two principal of 21 m. The sole fennel plots consisted of rows spaced Downloaded from https://academic.oup.com/jee/article/105/1/113/845722 by guest on 28 September 2021 ways that associational resistance may be achieved. 1.50 m apart with 0.50 m between the plants in each The Þrst, designated the “enemy hypothesis,” predicts row (Fig. 1). In the intercropped plots, cotton rows that the increased abundance of insect predators and were spaced 1.00 m apart with 0.20 m between the parasites in species-rich plant associations can better plants, whereas the spacing between the fennel and control herbivore populations (Pimentel 1961). cotton rows was 1.50 m (Fig. 1). The largest spacing Richer plant associations supposedly supply more fa- between the fennel and cotton rows avoids the fennel vorable conditions for predators and parasites, reduc- plants to shadow the cotton row. ing the probability that they will depart or go locally Species Samplings. The infestation by extinct. The second hypothesis, designated the “re- fennel aphids and the number of their natural enemies source concentration hypothesis” (Root 1973), con- in the sole fennel and intercropped plots were deter- cerns changes in the behavior of the herbivorous in- mined at intervals of seven days, sampling Þve plants sects themselves. per plot beginning 15 d after plant transplant and We hypothesize that intercropping fennel with nat- continuing until 30 d before the Þrst harvest (210 d). urally colored cotton can provide an alternative so- The number of fennel aphids and their predators was cioeconomic and ecological insect pest management recorded on leaves, branches, and umbels. strategy. These crops do not compete with each other Samples of the fennel aphid, H. foeniculi; eggs, lar- for nutrients, and naturally colored cotton is not host vae, pupae, and adults from three aphid predators of fennel aphids. In addition, this management strat- were collected from 15 fennel plants selected at ran- egy may create jobs and increase income for small dom in each plot (sole fennel and fennel-cotton in- farmers in northeast region of Brazil. The current tercrop). The fennel aphids and their natural enemies study investigated the severity of fennel plant damage were counted visually over the entire plant. Samplings in relation to infestation by the fennel aphid, H. foe- were conducted in the morning when conditions were niculi and predation by natural enemies in sole fennel cooler and adults of predators were found to be less plots and plots of fennel intercropped with cotton active than the rest of the day. The choice of predator with colored Þbers. species for sampling was based on their abundance on the fennel crop. The damage caused directly by aphid infestation was estimated in each cropping system Materials and Methods separately based on the fennel seed yield (g per plant) Study Location and Cotton and Fennel Cultivars. obtained in treated plots compared with nontreated The 2-yr study was conducted at an experimental farm plots. The loss in yield because of aphids was thus located in Montadas, Paraiba, Brazil (latitude 7Њ10Ј15Љ, evaluated as follows: [yield (treated plot)] Ð [yield longitude 35Њ51Ј13Љ, elevation 634 m). A fennel (F. (nontreated plot)]/yield (treated plot*100). The vulgare) cultivar (Montadas) and a naturally colored number of fennel umbels infested by the aphid was cotton (G. hirsutum) cultivar (BRS SaÞra) were determined in 15 fennel plants. The umbels shriveled planted under dryland conditions. Field plots were and desiccated were considered infested by the fennel planted in the second week of March in 2007 and aphid. between the Þrst and the second weeks of April in Statistical Analysis. The numbers of fennel aphids 2008. Weed control was done by hoeing. and predators per plant were tested for normality Experimental Design Used. A randomized com- (Kolmogorov D normality test) and for homogeneity plete block design was used with 10 treatments: 1) two of variance (BartlettÕs test) and, where necessary, rows of fennel: one row of cotton (treated plot), 2) were converted into the square root of (x ϩ 0.5) or log two rows of fennel: one row of cotton (nontreated (x ϩ 1). plot), 3) three rows of fennel: one row of cotton The overall season means of the number of fennel (treated plot), 4) three rows of fennel: one row of aphids, Cycloneda sanguinea (L.) (Coleoptera: Coc- cotton (nontreated plot), 5) one row of fennel: two cinellidae) (spotless lady beetle), green lacewings and rows of cotton (treated plot), 6) one row of fennel: Scymnus spp., fennel seed yield and percentage of two rows of cotton (nontreated plot), 7) two rows of fennel umbels infested, were subjected to three-way fennel: three rows of cotton (treated plot), 8) two analysis of variance (ANOVA) [year, crop system, and rows of fennel: three rows of cotton (nontreated plot), aphid control (treated and nontreated plots)], using February 2012 RAMALHO ET AL.: ASSESSMENT OF FENNEL APHIDS 115

Table 1. Summarized model of three-way analysis of variance (ANOVA) for the effects of the year, cropping system, and control of aphids on the number of aphids per fennel plant for the fennel cultivar Montadas

Source Model df F ratio P Ͼ F Fennel aphid 22 19.28 0.0001 (n plantϪ1) Y 1 0.01 0.9148 Csa 4 5.56 0.0008 Acb 1 334.47 0.0001 Cs ϫ Ac 4 5.56 0.0007 Y ϫ Cs 4 0.05 0.9953 Y ϫ Ac 1 0.03 0.9722 Y ϫ Cs ϫ Ac 4 0.05 0.9950 Downloaded from https://academic.oup.com/jee/article/105/1/113/845722 by guest on 28 September 2021 Y, year; Cs, cropping systems; Ac, aphid control; F, fennel; C, cotton. a Sole fennel and fennel intercropped with cotton (2F:1C, 3F:1C, 1F:2C, and 2F:3C). b Plots treated or not treated with insecticide.

and percentage of infested umbels showed that the densities of aphids (Table 1), C. sanguinea (Table 2), green lacewings (Table 2), Scymnus spp. (Table 2), fennel seed yield (Table 3), and percentage of infested umbels (Table 4) per plant did not differ between years. Thus, the analyses were conducted using the pooled data. There were no interactions among the year, crop- ping system and aphid control (Table 1), year and aphid control (Table 1), or year and cropping system (Table 1) for fennel aphid numbers per plant. How- ever, there was an interaction between the cropping system and aphid control (Table 1) for aphid numbers per plant. Irrespective of the crop system, the number of fennel aphids found on a plant varied with the control of the aphids. There was no signiÞcant differ- ence in the fennel aphid densities among the Þve cropping systems for the treated plots (Fig. 2A); how- ever, the fennel aphid populations in nontreated plots were signiÞcantly larger in sole fennel plots than in intercropping plots (Fig. 2B). In the nontreated plots, the average numbers of fennel aphids in sole fennel plots were 1.78, 1.72, 1.66, and 1.67 times higher than in intercropping systems (Fig. 1) consisting of two Fig. 1. Layout of experimental units in the fennel-cotton intercropping system and monoculture. In the sole fennel Table 2. Summarized model of two-way analysis of variance crop, the row spacing is 1.50 m apart. The sole crop is not (ANOVA) for the effects of year and cropping systems on the arranged in strips. In contrast, the intercropping system is number of C. sanguinea, C. carnea, and Scymnus spp. found per arranged in strips (rows of fennel alternating with rows of fennel plant in nontreated plots cotton). Between the fennel and cotton rows, the spacing is 1.50 m apart. The cotton rows were spaced 1.00 m apart. F ϭ Source Model df F ratio P Ͼ F Fennel ( ) and C ϭ cotton ( ). C. sanguinea (n plantϪ1) 12 46.10 0.0001 Y 1 2.84 0.1037 Cs 4 131.77 0.0001 PROC GLM of SAS (SAS Institute 2006) and the Y ϫ Cs 4 1.50 0.1058 averages were compared using the StudentÐNewmanÐ C. carnea (n plantϪ1) 12 13.35 0.0001 Keuls test (P ϭ 0.05). Y 1 1.21 0.2812 Csa 4 26.54 0.0001 Y ϫ Cs 4 0.25 0.9063 Ϫ Results Scymnus spp. (n plant 1) 12 10.04 0.0001 Y 1 0.44 0.5106 Considering the year-to-year data, analyses of the sea- Cs 4 26.40 0.0001 son-long averages for the numbers of fennel aphids, C. Y ϫ Cs 4 0.56 0.6931 sanguinea, green lacewings, Chrysoperla carnea (Ste- Y, year; Cs, cropping systems; Ac, aphid control; F, fennel; C, cotton. phens) (Neuroptera: Chrysopidae), Scymnus spp. a Sole fennel and fennel intercropped with cotton (2F:1C. 3F:1C, (Coleoptera: Coccinellidae), and fennel seed yield 1F:2C, and 2F:3C). 116 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 105, no. 1

Table 3. Summarized model of three-way analysis of variance (ANOVA) for the effects of the year, cropping system, and control of aphids on the fennel yield for the fennel cultivar Montadas on 2007 and 2008 seasons

Source Model df F ratio P Ͼ F Fennel yield 22 12.57 0.0001 (g plantϪ1) Y 1 0.43 0.5125 Csa 4 14.45 0.0001 Acb 1 117.36 0.0001 Cs ϫ Ac 4 6.94 0.0001 Y ϫ Cs 4 0.01 0.9471 Y ϫ Ac 1 0.02 0.9389 Y ϫ Cs ϫ Ac 4 0.01 0.9472 Downloaded from https://academic.oup.com/jee/article/105/1/113/845722 by guest on 28 September 2021 Y, year; Cs, cropping systems; Ac, aphid control; F, fennel; C, cotton. a Sole fennel and fennel intercropped with cotton (2F:1C, 3F:1C, 1F:2C, and 2F:3C). b Plots treated or not treated with insecticide. rows of fennel with one row of cotton, three rows of fennel with one row of cotton, one row of fennel with two rows of cotton, and two rows of fennel with three rows of cotton, respectively (Fig. 2B). No signiÞcant difference was observed among the four intercrop- ping systems for fennel aphids per plant (Fig. 2B). There was no signiÞcant interaction found between years and cropping systems for the numbers of spotless ladybird beetles, green lacewings, or Scymnus spp. (Table 2). However, there were signiÞcant differ- ences observed for spotless ladybird beetles, green Fig. 2. Mean (ϮSD) of aphids per fennel plant cultivar lacewings, and Scymnus spp. among the sole fennel Montadas in nontreated plots (A) and treated plots (B) of ϭ system versus intercropping systems (Table 5), for sole fennel and fennel intercropped with cotton (FCs xAc nontreated fennel plots (Table 2). In the nontreated 5.56; df ϭ 4, 57; P ϭ 0.0007). Means with common lower case plots, the numbers of C. sanguinea in the intercropping letter within each group of bars or with common upper case systems (Fig. 1) consisting of two rows of fennel with letter between the two groups of bars are not signiÞcantly ϭ one row of cotton, three rows of fennel with one row different using the StudentÐNewmanÐKeuls test (P 0.05). of cotton, one row of fennel with two rows of cotton, and two rows of fennel with three rows of cotton were than in the sole fennel plots (Table 5). In nontreated 1.98, 1.84, 1.94, and 1.96 times higher than in the sole plots, Scymnus spp. were 2.96, 2.57, 2.00, and 2.80 times fennel plots, respectively (Table 5). In the nontreated more abundant in the intercropping systems (Fig. 1) fennel plots, green lacewings were 1.85, 1.98, 2.08, and comprised of two rows of fennel with one row of 2.09 times more abundant in the intercropping systems cotton, three rows of fennel with one row of cotton, (Fig. 1) comprised of two rows of fennel with one row one row of fennel with two rows of cotton, and two of cotton, three rows of fennel with one row of cotton, rows of fennel with three rows of cotton, respectively, one row of fennel with two rows of cotton, and two than in the sole fennel plots (Table 5). rows of fennel with three rows of cotton, respectively, There was a signiÞcant interaction between crop- ping systems and the control of fennel aphids for

Table 4. Summarized model of three-way analysis of variance ANOVA) for the effects of the year, cropping system and control Table 5. Number (mean ؎ SE) of C. sanguine, C. carnea, and) of aphids on the percentage of fennel umbels infested by aphids Scymnus spp. per plant for the fennel cultivar Montadas grown in five cropping systems (sole fennel and fennel intercropped with Source Models df F ratio P Ͼ F cotton)

Fennel yield 22 19.39 0.0001 Cropping Scymnus Ϫ1 C. sanguine C. carnea (g plant ) Y 1 0.01 0.9907 system spp. Csa 4 2.87 0.0311 Acb 1 117.36 0.0001 2F:1C 19.92 Ϯ 2.82a 8.80 Ϯ 1.43a 7.43 Ϯ 0.98a Cs ϫ Ac 4 5.94 0.0005 3F:1C 18.50 Ϯ 1.99a 9.39 Ϯ 1.29a 6.46 Ϯ 1.10a Y ϫ Cs 4 0.02 0.9992 1F:2C 19.46 Ϯ 2.77a 9.88 Ϯ 2.60a 5.02 Ϯ 1.20a Y ϫ Ac 1 0.01 0.9173 2F:3C 19.63 Ϯ 2.42a 9.91 Ϯ 1.41a 7.02 Ϯ 1.88a Y ϫ Cs ϫ Ac 4 0.07 0.9904 Sole fennel 10.04 Ϯ 1.88b 4.75 Ϯ 1.10b 2.51 Ϯ 1.01b

Y, year; Cs, cropping systems; Ac, aphid control; F, fennel; C, cotton. Cropping systems: 2F:1C, 3F:1C, 1F:2C, and 2F:3C. (F, fennel; C, a Sole fennel and fennel intercropped with cotton (2F:1C, 3F:1C, cotton.) 1F:2C, and 2F:3C). Means with the same lowercase letter within columns do not differ b Plots treated or not treated with insecticide. signiÞcantly based on the StudentÐNewmanÐKeuls test (P ϭ 0.05). February 2012 RAMALHO ET AL.: ASSESSMENT OF FENNEL APHIDS 117

Table 6. Fennel yield (g plant؊1) (mean ؎ SE) for the fennel Discussion cultivar Montadas grown in five cropping systems (sole fennel and fennel intercropped with cotton) as a function of aphid control Our research investigated the severity of plant dam- ؊1 ؍ ؍ ؍ (FCsxAc 6, 94; df 4, 57; P 0.0001) and losses (% plant ) age related to infestation by the fennel aphid, H. foe- ;122.13 ؍ mean ؎ SE) of fennel yield caused by the fennel aphid (F) .niculi, as well as its predation by C. sanguinea, C (0.0001 ؍ P ;19 ,4 ؍ df carnea, and Scymnus spp. in sole fennel plots and plots Aphid control Fennel of fennel intercropped with cotton with colored Þ- Cropping Treated plot Nontreated plot yield loss bers. The results showed that fennel aphid populations system Ϫ1 (g plantϪ1) (g plantϪ1) (% plant ) were smaller in the plots with fennel-cotton inter- 2F:1C 82.22 Ϯ 15.82aA 59.32 Ϯ 14.12aB 27.85b cropping than in sole fennel plots (Fig. 2A). 3F:1C 81.20 Ϯ 17.18aA 58.15 Ϯ 15.72aB 28.39b The highest densities of C. sanguinea, green lace- 1F:2C 80.88 Ϯ 19.17aA 57.81 Ϯ 14.10aB 28.52b wings, and Scymnus spp. associated with the sup- 2F:3C 83.90 Ϯ 18.49a 62.38 Ϯ 14.90aB 25.65b

pression of fennel aphid populations was found in Downloaded from https://academic.oup.com/jee/article/105/1/113/845722 by guest on 28 September 2021 Sole fennel 74.20 Ϯ 15.16aA 15.24 Ϯ 8.83bB 79.46a the intercropping systems (Table 5). This could be Cropping systems: 2F:1C, 3F:1C, 1F:2C, and 2F:3C. (F, fennel; C, because of two factors: 1) fennel-cotton intercrop- cotton.) ping preserved and augmented more C. sanguinea, Means with the same lowercase letter within columns and means green lacewings, and Scymnus spp. than those in sole with a common uppercase letter within rows do not differ signiÞcantly based on the StudentÐNewmanÐKeuls test (P ϭ 0.05). fennel plots (Table 5); and 2) changes in the light regime in the intercropped plots that probably pre- vented H. foeniculi from Þnding its host. These results were consistent with the Þndings of fennel seed yield (Table 3). This indicates that irre- previous studies on cotton-wheat intercropping spective of the crop system, the fennel seed yield per (Zhao et al. 1987, Wang et al. 1993, Parajulee et al. plant varied with control of the aphids. There was no 1997, Velders et al. 2002, Ma et al. 2006). The results signiÞcant difference in fennel seed yield among the of this study further showed that intercropping affects Þve cropping systems for the treated plots (Table 6); the population dynamics of insect herbivores in agri- however, fennel seed yields were signiÞcantly higher cultural and natural communities (Risch et al. 1983, in the intercropping plots than in sole fennel plots for Bach and Tabashnik 1990, Ma et al. 2006). Specialist nontreated plots (Table 6). The percentages of losses arthropod herbivores display lower population den- in fennel seed yield were higher in the sole fennel sities in diverse habitats than in simple habitats plots than in the four intercropping systems (Table 6). (Andow 1991) because of the preservation and aug- There was a signiÞcant interaction between crop- mentation of existing predators in the agroecosystems ping systems and the control of fennel aphids for (Robinson et al. 1972, Xing et al. 1991). DiversiÞcation percentage of umbels infested by aphids (Table 4). of plants within the crop area may favor natural en- This indicates that irrespective of the crop system, the emies by providing protection from environmental percentage of umbels infested by aphids per plant factors and alternative food sources such as nectar, varied with control of the aphids. There was no sig- pollen and honeydew (Landis et al. 2000, Gurr et al. niÞcant difference in percentage of umbels infested 2003). The relay intercropping provides a predator by aphids among the Þve cropping systems for the reservoir that is in place before the arrival of key pests treated plots (Table 7). The percentages of umbels of the primary crop (Vandermeer 1989). infested by aphids were signiÞcantly higher in the High aphid densities can have a negative impact on intercropping plots than in sole fennel plots for non- cotton yield and can result in economic losses (Fer- treated plots (Table 7). reira and Sousa-Silva 2004). Our results showed that fennel aphids reduced the fennel seed yield by 80% in the sole fennel plots compared with 26, 29, 28, and 28% in the intercropping systems consisting of two rows of ؎ ؊1 Table 7. Umbels infested (% plant ) (mean SE) by fennel fennel with three rows of cotton, one row of fennel aphids for the fennel cultivar Montadas grown in five cropping systems (sole fennel and fennel intercropped with cotton) as a with two rows of cotton, three rows of fennel with one ؍ ؍ function of aphid control (FCs x Ac 5.94; df 4, 57; P < 0.0005) row of cotton, and two rows of fennel with one row of cotton, respectively (Table 6). Li (2001) reported Aphid control Cropping wheat-cotton relay intercropping being able to Treated plot Nontreated plot control the cotton aphid, Aphis gossypii Glover system Ϫ1 Ϫ1 (% plant ) (% plant ) (Hemiptera: Aphididae) as well as cotton-rape inter- 2F:1C 9.59 Ϯ 2.38aA 71.38 Ϯ 15.98aB cropping that reduced insect damage. 3F:1C 6.92 Ϯ 1.94aA 77.11 Ϯ 11.89aB The presence of the spotless ladybird beetle, green 1F:2C 7.67 Ϯ 1.89aA 76.56 Ϯ 12.12aB 2F:3C 6.94 Ϯ 1.61aA 68.60 Ϯ 13.19aB lacewing and Scymnus spp. predators in the plots con- Sole fennel 7.82 Ϯ 1.18aA 97.01 Ϯ 10.12bB tributed to the regulation of aphid populations, as indicated by the relatively low abundance of fennel Cropping systems: 2F:1C, 3F:1C, 1F:2C, and 2F:3C. (F, fennel; C, aphids in the plots of fennel intercropped with cotton cotton.) in comparison with the sole fennel plots (Fig. 2A). Means with the same lowercase letter within columns and means with a common uppercase letter within rows do not differ signiÞcantly According to Dreistadt and Flint (1996) and Kaplan based on the StudentÐNewmanÐKeuls test (P ϭ 0.05). and Eubanks (2002), the beneÞcial impact of gener- 118 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 105, no. 1 alist predators appears to be consistent across a wide References Cited range of cotton-management systems, although the Abramson, C. I., P. A. Wanderley, M.J.A. Wanderley, A.J.S. effectiveness of predators may be inßuenced by the Mina´, and O. B. de Souza. 2006. Effect of essential oil relative abundance of aphids (Costamagna and Landis from citronella and alfazema on fennel aphids Hyadaphis 2007) and by the spatial distribution of aphid popu- foeniculi (Passerini) (Hemiptera: Aphididae) and its lations (Desneux et al. 2006). The difference in fennel predator Cycloneda sanguinea L. (Coleoptera: Coccinel- aphid densities in sole fennel plots and intercropping lidae). Am. J. Environ. Sci. 3: 9Ð10. systems comprised of fennel and cotton is because of Andow, D. A. 1991. Yield loss to arthropods in vegetation- beneÞcial activities of predators and increased re- ally diverse agroecosystems. Environ. Entomol. 20: 1228Ð 1235. source concentration on fennel aphid behavior is di- Arau´ jo, A. C., N.E.B.M. Beltra˜o, M. S. Morais, J.L.O. Arau´ jo, rectly supported by the low abundance of fennel and J.L.X.L. Cunha. 2008. Indicadores agroeconoˆmicos aphids observed in fennel-cotton intercropping na avaliacao do consorcio algodao herbaceo-amendoim. ¸ ˜ ´ ˜ ´ Downloaded from https://academic.oup.com/jee/article/105/1/113/845722 by guest on 28 September 2021 plots (Fig. 2A). According to Ma et al. (2006), the Cieˆn. Agrote´c. 32: 1467Ð1472. highest density of natural enemies and low cotton Bach, C. E., and B. E. Tabashnik. 1990. 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