Neotrop Entomol DOI 10.1007/s13744-016-0383-0
PEST MANAGEMENT
Susceptibility of Five Sugar Beet Cultivars to the Black Bean Aphid, Aphis fabae Scopoli (Hemiptera: Aphididae) A GOLIZADEH, Z ABEDI, E BORZOUI, N GOLIKHAJEH, M JAFARY Dept of Plant Protection, Fac of Agricultural Science, Univ of Mohaghegh Ardabili, Ardabil, Iran
Keywords Aphid performance, host suitability, life table parameters, plant resistance Correspondence A Golizadeh, Dept of Plant Protection, Fac of Agricultural Science, Univ of Mohaghegh Ardabili, Ardabil, Iran; [email protected] Edited by Jorge B Torres – UFRPE Received 17 May 2015 and accepted 16 February 2016 * Sociedade Entomológica do Brasil 2016
Abstract The black bean aphid, Aphis fabae Scopoli (Hemiptera: Aphididae), is one of the important pests of sugar beet. The relative impact of resistance, including antibiosis and antixenosis of five sugar beet cultivars (Doroti, Perimer, Pershia, Rozier and 006) on A. fabae was studied under laboratory conditions using clip cages. The antibiosis test was based on life table parameters. Significant differences on developmental time, mean number of nymphs/aphid/day, fecundity, and adult longevity of A. fabae were found across tested sugar beet cultivars. In addition, there were significant differences among the sugar beet cultivars for population growth parameters such as the intrinsic rate of natural increase (rm), net reproductive rate (R0), finite rate of increase (λ), doubling time (DT), and mean generation time (T) of A. fabae. The highest and lowest (rm) values were observed on Pershia (0.449 nymphs/female/day) and Perimer (0.358 nymphs/female/day), respectively. No significant differences were found for the preference of the black bean aphid, and antixenosis had no effect on resistance against this aphid. As a result, our findings showed that the Pershia cultivar was a relatively susceptible host plant. Two cultivars (Perimer and Rozier) were relatively resistant to A. fabae, which could prove useful in the development of IPM programs for this aphid in sugar beet fields.
Introduction Black bean aphid, Aphis fabae Scopoli (Hemiptera, Aphididae), is a serious pest causing significant crop losses (Sadek et al 2013). This aphid has a host-alternating life cycle (Sandrock et al 2011), overwintering on spindle tree (Euonymus europaeus) as its winter host or to a lesser extent the snowball tree, Viburnum opulus and the Sweet Mockorange, Philadelphus coronarius (Dixon 1998), migrating in the spring to a wide variety of summer hosts, which include broad beans (Vicia faba), as well as several species of Chenopodiaceae such as sugar beet (Beta vulgaris) and goosefoot (Chenopodium sp.) as secondary hosts. After settling on the summer host plant, the spring migrant aphid gives birth to wingless females (generalist wingless virginoparae) that undergo several generations of
parthenogenetic viviparous reproduction (Muller et al 2001). Broad beans, sugar beet, and spinach (Spinacia oleracea) are economically important crops on which A. fabae causes considerable damage, either directly through feeding or by acting as a vector of multiple viral plant diseases (Ngumbi et al 2007). High population density on the secondary host plant causes the production of specialist winged virginoparae, which migrate to other summer host plants to start new colonies (Sadek et al 2013). The majority of sugar beet producers often apply synthetic aphicides to manage black bean aphid (FernandezQuintanilla et al 2002). The negative impacts of aphicides on natural enemies of aphids are extensively recognized (Hardin et al 1995, Torres et al 2003, Torres & Ruberson 2004). Continuous aphicide usage can produce undesirable environmental effects and has led to resistance of various
Golizadeh et al
aphid species (Foster et al 2007). Ioannidis (2000) reported that A. fabae from sugar beet in Greece showed 50-fold resistance to methamidophos, 8-fold resistance to pirimicarb, and 7-fold resistance to imidacloprid. Host plant resistance is an alternative method for pest management since it is both economically and environmentally acceptable (Karimi et al 2012). Plant species are different in terms of their suitability as hosts for different insect pests when their performance and preference are measured on these plants (Razmjou & Golizadeh 2010, Razmjou et al 2012). Antixenosis, antibiosis, and tolerance are three resistance mechanisms against insects in plants (Kogan & Ortman 1978, Mottaghinia et al 2011). For aphids, antixenosis and antibiosis can be effective in preventing their populations from reaching economic damage levels (Kennedy et al 1987). Variation in host plant quality is known to affect development, survivorship, reproduction and, hence, population growth of target herbivorous insects (Kim & Lee 2002, La Rossa et al 2013). Recently, Stout (2013) developed a new conceptual framework guiding host-plant resistance studies. This author proposed a dichotomous tolerance/resistance scheme that better reflects the strategies available to plants for reducing the impact of herbivores and better incorporates the known range of resistance mechanisms. The biological characteristics of aphids on host plants species and cultivars could be used as host plant susceptibility indices, and this information is needed to conduct successful pest management programs against aphids. The purpose of this study was to assess the response of black bean aphid A. fabae to sugar beet cultivars. Our findings suggest relatively low and high levels of resistance in the antibiosis experiment across the tested sugar beet cultivars.
Material and Methods Plant material Seeds of five sugar beet (B. vulgaris) cultivars—Doroti, Perimer, Pershia, Rozier, and 006—were obtained from Seed and Plant Breeding Research Institute, Karaj, Iran. These cultivars are commonly grown in sugar beet growing plantations in Iran and were selected based on visual observation in the fields of region because some cultivars were severely infested but some cultivars seemed to be attacked at low density by the black bean aphid. The plants were obtained by sowing in plastic pots (30 cm in diameter and 30 cm in height) filled with a suitable mixture of soil (2:1:1 field soil, sand, and rotten dung, respectively). Each pot contained at least three seeds but when the seedlings were emerged, the plants were thinned and only one plant remained in each pot. The plant grown was carried out at 25 ± 5°C, 60 ± 10% RH, and an approximate photoperiod of 16:8 h (L:D).
When the sugar beet seedlings reached 4–6 leaf stage, they were transferred and placed in a growth chamber under conditions of 25 ± 1°C, 60 ± 5% RH, and a photoperiod of 16:8 h (L:D) in order to conduct the experiments. Before using the leaves in the experiments, they were checked and cleaned of aphids and other pests if required (Razmjou & Golizadeh 2010). Aphids The aphid colony originated from sugar beet fields in Ardabil County, Iran, in July 2014. Colonies were established on broad bean seedlings (local variety) in framed plastic cages inside a growth chamber under the same conditions used to grown the sugar beet plants. The aphid population was reared for at least 1 month before experiments were initiated. Newly emerged adult apterous aphids were used at the beginning of each experiment. Every 2 weeks, 10–15 aphids were transferred from an infested plant to a young plant to maintain the colony. Newly emerged apterous adult aphids were used at the start of the experiments (Mohamadi et al 2012). Antibiosis experiment Experiments were conducted in a growth chamber under conditions of 25 ± 1°C, 60 ± 5% RH, and a photoperiod of 16:8 h (L:D) using clip cages (6-cm diameter and 1.5-cm high). All aphids used in the experiments were apterous viviparous adults of roughly similar size. Developmental time and survival rate In order to assess the developmental time, adult apterous aphids were randomly selected from the stock culture and placed on the lower leaf surface, each confined inside a clip cage (6-cm diameter and 1.5-cm high) to prevent escape and parasitism. They were then allowed to produce nymphs for 24 h. The adults and all nymphs except one were removed from the leaf cage. The remaining nymph was daily monitored to assess developmental performance of the aphid on each cultivar. Forty nymphs were monitored on each cultivar. Nymph developmental time and their survival rate were recorded. Adult fecundity, longevity, and life table On each cultivar, newly emerged apterous adults were taken from the previous experiment. We selected and transferred only one newly emerged adult to a new leaf clip cage. They were left for 24 h and then all aphids were removed maintaining only one nymph per plant. The number of nymphs produced by the apterous aphid was recorded, and the offspring were discarded daily until death of the adult. The experiment was arranged in the complete randomized design. In this way, we evaluated the fecundity of 25 adult
Susceptibility of sugar beets to Aphis fabae
aphids per each cultivar. The developmental time, immature survival rate, and adult fecundity were used to calculation of life table parameters. A complete life table (Carey 1993) was calculated including life expectation (ex) (the mean number of remaining days of life at age x). Antixenosis experiment The five sugar beet cultivars were randomly planted in round plastic pots (50-cm diameter × 15-cm deep), which were filled with suitable field soil and maintained in the growth chamber at 25 ± 1°C, 60 ± 5% RH, and a photoperiod of 16:8 h (L:D). These plants were used in the experiment when reached 3–4 leaf developmental stage. The plastic pots were surrounded with clear cylindrical plastics covered with muslin (50 meshes) for ventilation. For each replicate, 120 viviparous apterous adults were randomly selected from the colony and released in the center of each plastic on the soil surface and allowed to choose the plants. The number of aphids on each plant was counted and recorded after 24, 48, and 72 h. This experiment was conducted with three replications.
developmental times (7.4 days), whereas the shortest times were found on Pershia cultivar (6.3 days) (Table 1). The adult longevity of A. fabae was also different on the sugar beet cultivars (F = 21.97; df = 4, 124; p < 0.0001). The shortest and longest longevity were observed on Perimer (4.9 days) and Pershia (9.2 days), respectively (Table 1). The fecundity of A. fabae differed significantly among the tested sugar beet cultivars (F = 7.84; df = 4, 124; p < 0.0001). Aphid fecundity was lowest on Rozier and highest on Pershia, respectively (Table 1). In addition, the mean number of nymphs produced per female per day of A. fabae was significantly affected by cultivars studied (F = 17.36; df = 4, 124; p < 0.0001). Those females reared on the Pershia cultivar produced the highest mean number of nymphs per day, whereas those reared on the Perimer cultivar produced the lowest mean number of nymphs per day (Table 1). The age-specific fecundity rate (mx) and age-specific survival rate (lx) of A. fabae on different cultivars is shown in Fig 1. The lx of aphid started to drop earlier on Rozier and Perimer in comparing with Pershia. The width of the mx peak, i.e., the fecundity period, was narrower on Rozier and Perimer than on Pershia.
Statistical analysis Nymphal survival rate Daily recorded survival rate and fecundity were integrated into a life table format (Carey 1993) and were used to calculate net reproductive rate (R0), mean generation time (T), intrinsic rate of increase (rm), doubling time (DT), and finite rate of increase (λ). Jackknife pseudo-values computed for life table parameters on five cultivars were analyzed by ANOVA (SAS Institute 2002) (Meyer et al 1986, Maia et al 2000). Additionally, developmental time, mean numbers of offspring per aphid per day, longevity, and fecundity data were analyzed by ANOVA with mean separation at 5% level of significance by Tukey’s test. Nymphal survival rates recorded from five sugar beet cultivars were used to build survival curves through the Kaplan-Meier method, and comparisons were made by log rank test using the SPSS v. 16.0 statistical program (SPSS Inc 2007). Data from antixenosis experiment were analyzed under the null hypothesis in which an equal number of aphids present per plant (20:20:20:20:20% ratio; no selection behavior). These analyses were performed using chi-square test (α = 0.05).
Results Developmental time, adult fecundity, and longevity The developmental time of viviparous apterae (mean number of days from birth to first reproduction) was different (F = 4.61; df = 4, 180; p = 0.0018) among cultivars. On Rozier cultivar, aphids were generally found to have the longest
The survival rate throughout the nymphal stage ranged from 67.5 to 90.0% with the lower and greater survival rate observed on Rozier and Pershia cultivars, respectively (Table 1). However, this survival rates generated similar curves of survival among the cultivars (Kaplan-Meier method, log rank test; χ2 = 0.75; df = 4; p = 0.944) (Fig 1). The life expectancy of newly born nymphs was estimated to be 13.82, 12.30, 10.78, 9.22, and 9.10 days on Pershia, 006, Doroti, Perimer, and Rozier, respectively. Life table parameters Population growth parameters of viviparous apterous A. fabae were significantly affected by studied cultivars (F = 30.25; df = 4, 124; p < 0.001). The cohorts reared on Pershia had the highest R0 value, and those on Perimer and Rozier had the the lowest R0 value, whereas on Doroti and 006, R0 showed intermediate values (Table 2). In addition, the intrinsic rate of increase (rm) of viviparous apterae of A. fabae was found to be significantly different (F = 4.93; df = 4, 124; p = 0.001) depending on the sugar beet cultivars on which they were reared. The rm values ranged from 0.358 to 0.449 nymphs per female per day (Table 2). The lowest rm value resulted from rearing the aphid on Perimer and the highest value on Pershia. The variations in finite rate of increase (λ) were similar to the intrinsic rate of increase, and the former parameter was significantly influenced by different cultivars (F = 5.52; df = 4, 124; p = 0.0004) (Table 2). The
Golizadeh et al Table 1 Survival rate of nymphs, developmental time, mean number of nymphs per aphid per day, fecundity, and adult longevity of Aphis fabae reared on five sugar beet cultivars. Cultivar
Developmental data (mean ± SE) Adult longevity (d)
Nymphal survival rate % (n)
Developmental time (d)
Mean number of nymphs/aphid/ day
Total number of offspring/ female
Doroti
75.0 ± 6.85p
7.3 ± 0.01a
1.9 ± 0.08b
35.8 ± 1.26ab
5.8 ± 0.32c
Perimer Pershia
70.0 ± 7.25p 90.0 ± 4.74p
7.3 ± 0.02a 6.3 ± 0.01b
1.3 ± 0.14c 2.8 ± 0.14a
33.7 ± 6.21bc 48.7 ± 2.84a
4.9 ± 0.42c 9.2 ± 0.37a
Rozier
67.5 ± 7.41p
7.4 ± 0.03a
1.7 ± 0.17bc
22.5 ± 2.21c
5.2 ± 0.48c
006
82.5 ± 6.01p
7.0 ± 0.01ab
1.9 ± 0.09b
31.2 ± 2.04bc
7.5 ± 0.34b
Mean values in a column followed by different lowercase letters (a–c) are significantly different on the basis of ANOVA with Tukey’s test (p < 0.05) and nymphal survival rates followed by the same letter (p–q) in the same column are not significantly different (p > 0.05; Kaplan-Meier method, log rank test).
We conducted two types of experiments to test the antibiosis and antixenosis responses of five sugar beet cultivars against A. fabae. Evaluating the resistance of various cultivars and crop species to pests may offer useful information about their suitability or unsuitability for the target pest species. Evaluating the resistance through population growth parameters of an insect can indicate the degree of plant resistance to insects (Tsai & Wang 2001). Thus, the life table parameters estimated to A. fabae on five sugar beet cultivars selected from the screening test detected relatively resistant and susceptible cultivars to this aphid. Based on the results, relative high levels of susceptibility in Pershia cultivar to A. fabae were found; however, the cultivars Rozier and Perimer were relatively less susceptible. In the current study, only antibiosis resistance mechanism was
Age-specific survival rate (lx)
Discussion
depicted against black bean aphid. Adult aphids reared on Pershia cultivar produced the highest fecundity and longevity and lower mortality rate of nymphs indicating its higher suitability for aphid reproduction. Poor performance of aphids on Perimer and Rozier was a function of poor fecundity, adult longevity, and a lower nymphal survival rate (Table 1). No significant differences were found for the preference of the black bean aphid in the antixenosis experiments; however, Perimer and Rozier were relatively preferred less than others. Therefore, antixenosis had no effect in resistance against A. fabae.
6 Pershia
5
mx
0.06
4
Doroti
3
Perimer
2
Rozier
1 0 0
Age-specific fecundity (mx)
(λ) values of viviparous apterae were significantly lower on Perimer than on the other sugar beet cultivars. The mean generation time (T) of A. fabae was also different among cultivars tested (F = 7.58; df = 4, 124; p < 0.0001) with the cultivars Rozier, 006, and Perimer promoting the fast generation times (Table 2). Furthermore, significant effects were not observed for aphid doubling time (DT) when reared on studied sugar beet cultivars (F = 2.24; df = 4, 124; p = 0.069). The DT values were relatively higher on Rozier and Perimer cultivars than on Pershia cultivar (Table 2). The number of adult aphids attracted to each cultivar indicated that there were no significant differences among sugar beet cultivars within 24 h (χ2 = 5.147; p = 0.272), 48 h (χ 2 = 1.295; p = 0.862), and 72 h (χ 2 = 1.279; p = 0.865). However, Pershia and 006 attracted the higher number of apterous aphids as opposed to Perimer and Rozier, which attracted the lower number of apterous aphids (Table 3).
3
6
9
12
15
18
1 0.8
lx Pershia
0.6
0.06 Doroti
0.4
Perimer
0.2
Rozier
0 0
3
6
9
12
15
18
Age (day)
Fig 1 Age-specific survival rate and female offspring production by Aphis fabae caged on five sugar beet cultivars.
Susceptibility of sugar beets to Aphis fabae Table 2 Life table parameters of Aphis fabae reared on five sugar beet cultivars.
λ
Cultivar
R0
rm
T
DT
Doroti
20.7 ± 1.52b
0.383 ± 0.011b
1.47 ± 0.015b
7.9 ± 0.20a
1.8 ± 0.05a
Perimer Pershia
10.2 ± 1.66c 36.4 ± 2.20a
0.358 ± 0.017b 0.449 ± 0.013a
1.43 ± 0.023b 1.57 ± 0.020a
6.4 ± 0.28b 8.0 ± 0.27a
1.9 ± 0.13a 1.5 ± 0.05a
Rozier
13.4 ± 2.20c
0.362 ± 0.026b
1.44 ± 0.037b
7.2 ± 0.29ab
1.9 ± 0.15a
006
22.8 ± 1.51b
0.401 ± 0.009ab
1.49 ± 0.0135ab
7.8 ± 0.16a
1.7 ± 0.04a
Mean values in a column followed by different letters are significantly different on Tukey’s test (p < 0.05). R0 net reproductive rate (number of females produced/female), rm intrinsic rate of increase (number of females produced/female/day), λ finite rate of increase, T generation time (d), DT doubling time (d).
The intrinsic rate of increase (rm) summarizes all differences on development, survival, sex ration, and age-specific fecundity becoming the most important life table parameter for evaluating population development (Birch 1948, Carey 1993). The higher rm value of viviparous apterae found on Pershia compared with aphids caged on Perimer was mainly the result of higher overall fecundity and fast development. The finite rate of population increase (λ) is determined using rm values. Therefore, changes in λ followed the same pattern as changes in rm effects of plant phytochemicals in different cultivars manifested as increased life span, developmental time, fecundity, survival, and behavior changes (Croft 1990). The variations in finite rate of increase (λ) were similar to intrinsic rate of increase, and the former parameter was significantly influenced by different cultivars (Table 2). Several authors have studied the life table parameters of A. fabae on different plants or different cultivars. Esmaeili-Vardanjani et al (2013) have studied the life table parameters of A. fabae on bean cultivars. They clearly suggested that Sayad cultivar had the highest host resistance among the tested cultivars with a high potential to be used in the integrated management of A. fabae. In similar studies, Tahriri Adabi et al (2010) investigated the effects of four cultivars of sugar beet on biology and demographic parameters of A. fabae and Aphidius matricariae Haliday as a step toward biological control of black bean aphid, and found that the use of Shirin cultivar maximized the natural biological control of Table 3 Apterous adults (mean ± SE) of Aphis fabae selecting sugar beet cultivars after 24, 48, and 72 h. Cultivar
Aphids in 24 h
Aphids in 48 h
Aphids in 72 h
Doroti
11.7 ± 0.67a
8.0 ± 1.15a
5.7 ± 1.33a
Perimer Pershia Rozier 006
9.0 ± 0.58a 18.7 ± 1.20a 9.0 ± 0.58a 12.7 ± 0.88a
5.7 ± 0.88a 7.7 ± 0.88a 5.0 ± 1.15a 8.3 ± 0.33a
4.7 ± 0.88a 6.3 ± 0.88a 3.0 ± 0.58b 5.0 ± 0.58a
Mean values in a column followed by different lowercase letters are significantly different on the basis of chi-square test (p < 0.05).
A. fabae by A. matricariae. Razmjou & Fallahi (2009) obtained the highest and lowest rm values for A. fabae on Polyrave (0.2202) and 7233 (0.1336) among the various sugar beet cultivars they tested, respectively. Knowledge of the extent of susceptibility or resistance of cultivars as well as biology of a pest on a crop is a fundamental component of an integrated pest management (IPM) program for any crop, and can provide information on the detection and monitoring of pest infestations, cultivar selection and crop breeding. The low quality of plants can function as a defense mechanism against herbivorous insects (Legrand & Barbosa 2000). Therefore, host plant quality affects the fecundity of herbivorous insects at both individual and population scales (Awmack & Leather 2002). Our results clearly showed that the demographic parameters of A. fabae were differentially affected by the sugar beet cultivars. Information about the quality of sugar beet cultivars and the way it influences the demographic parameters and nonpreferences of A. fabae can help us understand the population dynamics and may assist in the development of better management programs for this pest. Our results indicated that the Perimer and Rozier cultivars were relatively resistant to A. fabae, which could prove useful in the development of IPM programs for this aphid in sugar beet fields. In summary, Pershia cultivar was the most suitable (least resistant) host plant for A. fabae among the tested sugar beet cultivars. The faster development rate and the higher fecundity rate are reflected in the highest intrinsic rate of increase of A. fabae on Pershia, and this would result in higher population growth that in turn should lead to higher subsequent infestations. Oppositely, two cultivars, Perimer and Rozier, were the least suitable (most resistant) host plants for A. fabae and these cultivars were less preferred by this aphid. The use of resistant cultivars could have an important role in the IPM of black bean aphid. However, nonpreference and plant tolerance assays and field-based studies are needed to fully understand the pest-plant interactions and to obtain additional information required for designing a comprehensive IPM of A. fabae in sugar beet fields.
Golizadeh et al Acknowledgments The work received financial support by the University of Mohaghegh Ardabili which is greatly appreciated.
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PEST MANAGEMENT
Susceptibility of Five Sugar Beet Cultivars to the Black Bean Aphid, Aphis fabae Scopoli (Hemiptera: Aphididae) A GOLIZADEH, Z ABEDI, E BORZOUI, N GOLIKHAJEH, M JAFARY Dept of Plant Protection, Fac of Agricultural Science, Univ of Mohaghegh Ardabili, Ardabil, Iran
Keywords Aphid performance, host suitability, life table parameters, plant resistance Correspondence A Golizadeh, Dept of Plant Protection, Fac of Agricultural Science, Univ of Mohaghegh Ardabili, Ardabil, Iran; [email protected] Edited by Jorge B Torres – UFRPE Received 17 May 2015 and accepted 16 February 2016 * Sociedade Entomológica do Brasil 2016
Abstract The black bean aphid, Aphis fabae Scopoli (Hemiptera: Aphididae), is one of the important pests of sugar beet. The relative impact of resistance, including antibiosis and antixenosis of five sugar beet cultivars (Doroti, Perimer, Pershia, Rozier and 006) on A. fabae was studied under laboratory conditions using clip cages. The antibiosis test was based on life table parameters. Significant differences on developmental time, mean number of nymphs/aphid/day, fecundity, and adult longevity of A. fabae were found across tested sugar beet cultivars. In addition, there were significant differences among the sugar beet cultivars for population growth parameters such as the intrinsic rate of natural increase (rm), net reproductive rate (R0), finite rate of increase (λ), doubling time (DT), and mean generation time (T) of A. fabae. The highest and lowest (rm) values were observed on Pershia (0.449 nymphs/female/day) and Perimer (0.358 nymphs/female/day), respectively. No significant differences were found for the preference of the black bean aphid, and antixenosis had no effect on resistance against this aphid. As a result, our findings showed that the Pershia cultivar was a relatively susceptible host plant. Two cultivars (Perimer and Rozier) were relatively resistant to A. fabae, which could prove useful in the development of IPM programs for this aphid in sugar beet fields.
Introduction Black bean aphid, Aphis fabae Scopoli (Hemiptera, Aphididae), is a serious pest causing significant crop losses (Sadek et al 2013). This aphid has a host-alternating life cycle (Sandrock et al 2011), overwintering on spindle tree (Euonymus europaeus) as its winter host or to a lesser extent the snowball tree, Viburnum opulus and the Sweet Mockorange, Philadelphus coronarius (Dixon 1998), migrating in the spring to a wide variety of summer hosts, which include broad beans (Vicia faba), as well as several species of Chenopodiaceae such as sugar beet (Beta vulgaris) and goosefoot (Chenopodium sp.) as secondary hosts. After settling on the summer host plant, the spring migrant aphid gives birth to wingless females (generalist wingless virginoparae) that undergo several generations of
parthenogenetic viviparous reproduction (Muller et al 2001). Broad beans, sugar beet, and spinach (Spinacia oleracea) are economically important crops on which A. fabae causes considerable damage, either directly through feeding or by acting as a vector of multiple viral plant diseases (Ngumbi et al 2007). High population density on the secondary host plant causes the production of specialist winged virginoparae, which migrate to other summer host plants to start new colonies (Sadek et al 2013). The majority of sugar beet producers often apply synthetic aphicides to manage black bean aphid (FernandezQuintanilla et al 2002). The negative impacts of aphicides on natural enemies of aphids are extensively recognized (Hardin et al 1995, Torres et al 2003, Torres & Ruberson 2004). Continuous aphicide usage can produce undesirable environmental effects and has led to resistance of various
Golizadeh et al
aphid species (Foster et al 2007). Ioannidis (2000) reported that A. fabae from sugar beet in Greece showed 50-fold resistance to methamidophos, 8-fold resistance to pirimicarb, and 7-fold resistance to imidacloprid. Host plant resistance is an alternative method for pest management since it is both economically and environmentally acceptable (Karimi et al 2012). Plant species are different in terms of their suitability as hosts for different insect pests when their performance and preference are measured on these plants (Razmjou & Golizadeh 2010, Razmjou et al 2012). Antixenosis, antibiosis, and tolerance are three resistance mechanisms against insects in plants (Kogan & Ortman 1978, Mottaghinia et al 2011). For aphids, antixenosis and antibiosis can be effective in preventing their populations from reaching economic damage levels (Kennedy et al 1987). Variation in host plant quality is known to affect development, survivorship, reproduction and, hence, population growth of target herbivorous insects (Kim & Lee 2002, La Rossa et al 2013). Recently, Stout (2013) developed a new conceptual framework guiding host-plant resistance studies. This author proposed a dichotomous tolerance/resistance scheme that better reflects the strategies available to plants for reducing the impact of herbivores and better incorporates the known range of resistance mechanisms. The biological characteristics of aphids on host plants species and cultivars could be used as host plant susceptibility indices, and this information is needed to conduct successful pest management programs against aphids. The purpose of this study was to assess the response of black bean aphid A. fabae to sugar beet cultivars. Our findings suggest relatively low and high levels of resistance in the antibiosis experiment across the tested sugar beet cultivars.
Material and Methods Plant material Seeds of five sugar beet (B. vulgaris) cultivars—Doroti, Perimer, Pershia, Rozier, and 006—were obtained from Seed and Plant Breeding Research Institute, Karaj, Iran. These cultivars are commonly grown in sugar beet growing plantations in Iran and were selected based on visual observation in the fields of region because some cultivars were severely infested but some cultivars seemed to be attacked at low density by the black bean aphid. The plants were obtained by sowing in plastic pots (30 cm in diameter and 30 cm in height) filled with a suitable mixture of soil (2:1:1 field soil, sand, and rotten dung, respectively). Each pot contained at least three seeds but when the seedlings were emerged, the plants were thinned and only one plant remained in each pot. The plant grown was carried out at 25 ± 5°C, 60 ± 10% RH, and an approximate photoperiod of 16:8 h (L:D).
When the sugar beet seedlings reached 4–6 leaf stage, they were transferred and placed in a growth chamber under conditions of 25 ± 1°C, 60 ± 5% RH, and a photoperiod of 16:8 h (L:D) in order to conduct the experiments. Before using the leaves in the experiments, they were checked and cleaned of aphids and other pests if required (Razmjou & Golizadeh 2010). Aphids The aphid colony originated from sugar beet fields in Ardabil County, Iran, in July 2014. Colonies were established on broad bean seedlings (local variety) in framed plastic cages inside a growth chamber under the same conditions used to grown the sugar beet plants. The aphid population was reared for at least 1 month before experiments were initiated. Newly emerged adult apterous aphids were used at the beginning of each experiment. Every 2 weeks, 10–15 aphids were transferred from an infested plant to a young plant to maintain the colony. Newly emerged apterous adult aphids were used at the start of the experiments (Mohamadi et al 2012). Antibiosis experiment Experiments were conducted in a growth chamber under conditions of 25 ± 1°C, 60 ± 5% RH, and a photoperiod of 16:8 h (L:D) using clip cages (6-cm diameter and 1.5-cm high). All aphids used in the experiments were apterous viviparous adults of roughly similar size. Developmental time and survival rate In order to assess the developmental time, adult apterous aphids were randomly selected from the stock culture and placed on the lower leaf surface, each confined inside a clip cage (6-cm diameter and 1.5-cm high) to prevent escape and parasitism. They were then allowed to produce nymphs for 24 h. The adults and all nymphs except one were removed from the leaf cage. The remaining nymph was daily monitored to assess developmental performance of the aphid on each cultivar. Forty nymphs were monitored on each cultivar. Nymph developmental time and their survival rate were recorded. Adult fecundity, longevity, and life table On each cultivar, newly emerged apterous adults were taken from the previous experiment. We selected and transferred only one newly emerged adult to a new leaf clip cage. They were left for 24 h and then all aphids were removed maintaining only one nymph per plant. The number of nymphs produced by the apterous aphid was recorded, and the offspring were discarded daily until death of the adult. The experiment was arranged in the complete randomized design. In this way, we evaluated the fecundity of 25 adult
Susceptibility of sugar beets to Aphis fabae
aphids per each cultivar. The developmental time, immature survival rate, and adult fecundity were used to calculation of life table parameters. A complete life table (Carey 1993) was calculated including life expectation (ex) (the mean number of remaining days of life at age x). Antixenosis experiment The five sugar beet cultivars were randomly planted in round plastic pots (50-cm diameter × 15-cm deep), which were filled with suitable field soil and maintained in the growth chamber at 25 ± 1°C, 60 ± 5% RH, and a photoperiod of 16:8 h (L:D). These plants were used in the experiment when reached 3–4 leaf developmental stage. The plastic pots were surrounded with clear cylindrical plastics covered with muslin (50 meshes) for ventilation. For each replicate, 120 viviparous apterous adults were randomly selected from the colony and released in the center of each plastic on the soil surface and allowed to choose the plants. The number of aphids on each plant was counted and recorded after 24, 48, and 72 h. This experiment was conducted with three replications.
developmental times (7.4 days), whereas the shortest times were found on Pershia cultivar (6.3 days) (Table 1). The adult longevity of A. fabae was also different on the sugar beet cultivars (F = 21.97; df = 4, 124; p < 0.0001). The shortest and longest longevity were observed on Perimer (4.9 days) and Pershia (9.2 days), respectively (Table 1). The fecundity of A. fabae differed significantly among the tested sugar beet cultivars (F = 7.84; df = 4, 124; p < 0.0001). Aphid fecundity was lowest on Rozier and highest on Pershia, respectively (Table 1). In addition, the mean number of nymphs produced per female per day of A. fabae was significantly affected by cultivars studied (F = 17.36; df = 4, 124; p < 0.0001). Those females reared on the Pershia cultivar produced the highest mean number of nymphs per day, whereas those reared on the Perimer cultivar produced the lowest mean number of nymphs per day (Table 1). The age-specific fecundity rate (mx) and age-specific survival rate (lx) of A. fabae on different cultivars is shown in Fig 1. The lx of aphid started to drop earlier on Rozier and Perimer in comparing with Pershia. The width of the mx peak, i.e., the fecundity period, was narrower on Rozier and Perimer than on Pershia.
Statistical analysis Nymphal survival rate Daily recorded survival rate and fecundity were integrated into a life table format (Carey 1993) and were used to calculate net reproductive rate (R0), mean generation time (T), intrinsic rate of increase (rm), doubling time (DT), and finite rate of increase (λ). Jackknife pseudo-values computed for life table parameters on five cultivars were analyzed by ANOVA (SAS Institute 2002) (Meyer et al 1986, Maia et al 2000). Additionally, developmental time, mean numbers of offspring per aphid per day, longevity, and fecundity data were analyzed by ANOVA with mean separation at 5% level of significance by Tukey’s test. Nymphal survival rates recorded from five sugar beet cultivars were used to build survival curves through the Kaplan-Meier method, and comparisons were made by log rank test using the SPSS v. 16.0 statistical program (SPSS Inc 2007). Data from antixenosis experiment were analyzed under the null hypothesis in which an equal number of aphids present per plant (20:20:20:20:20% ratio; no selection behavior). These analyses were performed using chi-square test (α = 0.05).
Results Developmental time, adult fecundity, and longevity The developmental time of viviparous apterae (mean number of days from birth to first reproduction) was different (F = 4.61; df = 4, 180; p = 0.0018) among cultivars. On Rozier cultivar, aphids were generally found to have the longest
The survival rate throughout the nymphal stage ranged from 67.5 to 90.0% with the lower and greater survival rate observed on Rozier and Pershia cultivars, respectively (Table 1). However, this survival rates generated similar curves of survival among the cultivars (Kaplan-Meier method, log rank test; χ2 = 0.75; df = 4; p = 0.944) (Fig 1). The life expectancy of newly born nymphs was estimated to be 13.82, 12.30, 10.78, 9.22, and 9.10 days on Pershia, 006, Doroti, Perimer, and Rozier, respectively. Life table parameters Population growth parameters of viviparous apterous A. fabae were significantly affected by studied cultivars (F = 30.25; df = 4, 124; p < 0.001). The cohorts reared on Pershia had the highest R0 value, and those on Perimer and Rozier had the the lowest R0 value, whereas on Doroti and 006, R0 showed intermediate values (Table 2). In addition, the intrinsic rate of increase (rm) of viviparous apterae of A. fabae was found to be significantly different (F = 4.93; df = 4, 124; p = 0.001) depending on the sugar beet cultivars on which they were reared. The rm values ranged from 0.358 to 0.449 nymphs per female per day (Table 2). The lowest rm value resulted from rearing the aphid on Perimer and the highest value on Pershia. The variations in finite rate of increase (λ) were similar to the intrinsic rate of increase, and the former parameter was significantly influenced by different cultivars (F = 5.52; df = 4, 124; p = 0.0004) (Table 2). The
Golizadeh et al Table 1 Survival rate of nymphs, developmental time, mean number of nymphs per aphid per day, fecundity, and adult longevity of Aphis fabae reared on five sugar beet cultivars. Cultivar
Developmental data (mean ± SE) Adult longevity (d)
Nymphal survival rate % (n)
Developmental time (d)
Mean number of nymphs/aphid/ day
Total number of offspring/ female
Doroti
75.0 ± 6.85p
7.3 ± 0.01a
1.9 ± 0.08b
35.8 ± 1.26ab
5.8 ± 0.32c
Perimer Pershia
70.0 ± 7.25p 90.0 ± 4.74p
7.3 ± 0.02a 6.3 ± 0.01b
1.3 ± 0.14c 2.8 ± 0.14a
33.7 ± 6.21bc 48.7 ± 2.84a
4.9 ± 0.42c 9.2 ± 0.37a
Rozier
67.5 ± 7.41p
7.4 ± 0.03a
1.7 ± 0.17bc
22.5 ± 2.21c
5.2 ± 0.48c
006
82.5 ± 6.01p
7.0 ± 0.01ab
1.9 ± 0.09b
31.2 ± 2.04bc
7.5 ± 0.34b
Mean values in a column followed by different lowercase letters (a–c) are significantly different on the basis of ANOVA with Tukey’s test (p < 0.05) and nymphal survival rates followed by the same letter (p–q) in the same column are not significantly different (p > 0.05; Kaplan-Meier method, log rank test).
We conducted two types of experiments to test the antibiosis and antixenosis responses of five sugar beet cultivars against A. fabae. Evaluating the resistance of various cultivars and crop species to pests may offer useful information about their suitability or unsuitability for the target pest species. Evaluating the resistance through population growth parameters of an insect can indicate the degree of plant resistance to insects (Tsai & Wang 2001). Thus, the life table parameters estimated to A. fabae on five sugar beet cultivars selected from the screening test detected relatively resistant and susceptible cultivars to this aphid. Based on the results, relative high levels of susceptibility in Pershia cultivar to A. fabae were found; however, the cultivars Rozier and Perimer were relatively less susceptible. In the current study, only antibiosis resistance mechanism was
Age-specific survival rate (lx)
Discussion
depicted against black bean aphid. Adult aphids reared on Pershia cultivar produced the highest fecundity and longevity and lower mortality rate of nymphs indicating its higher suitability for aphid reproduction. Poor performance of aphids on Perimer and Rozier was a function of poor fecundity, adult longevity, and a lower nymphal survival rate (Table 1). No significant differences were found for the preference of the black bean aphid in the antixenosis experiments; however, Perimer and Rozier were relatively preferred less than others. Therefore, antixenosis had no effect in resistance against A. fabae.
6 Pershia
5
mx
0.06
4
Doroti
3
Perimer
2
Rozier
1 0 0
Age-specific fecundity (mx)
(λ) values of viviparous apterae were significantly lower on Perimer than on the other sugar beet cultivars. The mean generation time (T) of A. fabae was also different among cultivars tested (F = 7.58; df = 4, 124; p < 0.0001) with the cultivars Rozier, 006, and Perimer promoting the fast generation times (Table 2). Furthermore, significant effects were not observed for aphid doubling time (DT) when reared on studied sugar beet cultivars (F = 2.24; df = 4, 124; p = 0.069). The DT values were relatively higher on Rozier and Perimer cultivars than on Pershia cultivar (Table 2). The number of adult aphids attracted to each cultivar indicated that there were no significant differences among sugar beet cultivars within 24 h (χ2 = 5.147; p = 0.272), 48 h (χ 2 = 1.295; p = 0.862), and 72 h (χ 2 = 1.279; p = 0.865). However, Pershia and 006 attracted the higher number of apterous aphids as opposed to Perimer and Rozier, which attracted the lower number of apterous aphids (Table 3).
3
6
9
12
15
18
1 0.8
lx Pershia
0.6
0.06 Doroti
0.4
Perimer
0.2
Rozier
0 0
3
6
9
12
15
18
Age (day)
Fig 1 Age-specific survival rate and female offspring production by Aphis fabae caged on five sugar beet cultivars.
Susceptibility of sugar beets to Aphis fabae Table 2 Life table parameters of Aphis fabae reared on five sugar beet cultivars.
λ
Cultivar
R0
rm
T
DT
Doroti
20.7 ± 1.52b
0.383 ± 0.011b
1.47 ± 0.015b
7.9 ± 0.20a
1.8 ± 0.05a
Perimer Pershia
10.2 ± 1.66c 36.4 ± 2.20a
0.358 ± 0.017b 0.449 ± 0.013a
1.43 ± 0.023b 1.57 ± 0.020a
6.4 ± 0.28b 8.0 ± 0.27a
1.9 ± 0.13a 1.5 ± 0.05a
Rozier
13.4 ± 2.20c
0.362 ± 0.026b
1.44 ± 0.037b
7.2 ± 0.29ab
1.9 ± 0.15a
006
22.8 ± 1.51b
0.401 ± 0.009ab
1.49 ± 0.0135ab
7.8 ± 0.16a
1.7 ± 0.04a
Mean values in a column followed by different letters are significantly different on Tukey’s test (p < 0.05). R0 net reproductive rate (number of females produced/female), rm intrinsic rate of increase (number of females produced/female/day), λ finite rate of increase, T generation time (d), DT doubling time (d).
The intrinsic rate of increase (rm) summarizes all differences on development, survival, sex ration, and age-specific fecundity becoming the most important life table parameter for evaluating population development (Birch 1948, Carey 1993). The higher rm value of viviparous apterae found on Pershia compared with aphids caged on Perimer was mainly the result of higher overall fecundity and fast development. The finite rate of population increase (λ) is determined using rm values. Therefore, changes in λ followed the same pattern as changes in rm effects of plant phytochemicals in different cultivars manifested as increased life span, developmental time, fecundity, survival, and behavior changes (Croft 1990). The variations in finite rate of increase (λ) were similar to intrinsic rate of increase, and the former parameter was significantly influenced by different cultivars (Table 2). Several authors have studied the life table parameters of A. fabae on different plants or different cultivars. Esmaeili-Vardanjani et al (2013) have studied the life table parameters of A. fabae on bean cultivars. They clearly suggested that Sayad cultivar had the highest host resistance among the tested cultivars with a high potential to be used in the integrated management of A. fabae. In similar studies, Tahriri Adabi et al (2010) investigated the effects of four cultivars of sugar beet on biology and demographic parameters of A. fabae and Aphidius matricariae Haliday as a step toward biological control of black bean aphid, and found that the use of Shirin cultivar maximized the natural biological control of Table 3 Apterous adults (mean ± SE) of Aphis fabae selecting sugar beet cultivars after 24, 48, and 72 h. Cultivar
Aphids in 24 h
Aphids in 48 h
Aphids in 72 h
Doroti
11.7 ± 0.67a
8.0 ± 1.15a
5.7 ± 1.33a
Perimer Pershia Rozier 006
9.0 ± 0.58a 18.7 ± 1.20a 9.0 ± 0.58a 12.7 ± 0.88a
5.7 ± 0.88a 7.7 ± 0.88a 5.0 ± 1.15a 8.3 ± 0.33a
4.7 ± 0.88a 6.3 ± 0.88a 3.0 ± 0.58b 5.0 ± 0.58a
Mean values in a column followed by different lowercase letters are significantly different on the basis of chi-square test (p < 0.05).
A. fabae by A. matricariae. Razmjou & Fallahi (2009) obtained the highest and lowest rm values for A. fabae on Polyrave (0.2202) and 7233 (0.1336) among the various sugar beet cultivars they tested, respectively. Knowledge of the extent of susceptibility or resistance of cultivars as well as biology of a pest on a crop is a fundamental component of an integrated pest management (IPM) program for any crop, and can provide information on the detection and monitoring of pest infestations, cultivar selection and crop breeding. The low quality of plants can function as a defense mechanism against herbivorous insects (Legrand & Barbosa 2000). Therefore, host plant quality affects the fecundity of herbivorous insects at both individual and population scales (Awmack & Leather 2002). Our results clearly showed that the demographic parameters of A. fabae were differentially affected by the sugar beet cultivars. Information about the quality of sugar beet cultivars and the way it influences the demographic parameters and nonpreferences of A. fabae can help us understand the population dynamics and may assist in the development of better management programs for this pest. Our results indicated that the Perimer and Rozier cultivars were relatively resistant to A. fabae, which could prove useful in the development of IPM programs for this aphid in sugar beet fields. In summary, Pershia cultivar was the most suitable (least resistant) host plant for A. fabae among the tested sugar beet cultivars. The faster development rate and the higher fecundity rate are reflected in the highest intrinsic rate of increase of A. fabae on Pershia, and this would result in higher population growth that in turn should lead to higher subsequent infestations. Oppositely, two cultivars, Perimer and Rozier, were the least suitable (most resistant) host plants for A. fabae and these cultivars were less preferred by this aphid. The use of resistant cultivars could have an important role in the IPM of black bean aphid. However, nonpreference and plant tolerance assays and field-based studies are needed to fully understand the pest-plant interactions and to obtain additional information required for designing a comprehensive IPM of A. fabae in sugar beet fields.
Golizadeh et al Acknowledgments The work received financial support by the University of Mohaghegh Ardabili which is greatly appreciated.
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