Insect Science (2014) 21, 334–341, DOI 10.1111/1744-7917.12114


How does the host-specialized aphid deal with food deficiency? Ting-Ting Xu, Ting-Ting Ma and Xiang-Dong Liu Department of Entomology, Nanjing Agricultural University, Nanjing, China

Abstract Aphis gossypii Glover shows obvious host specialization, with cucurbit- and cotton-specialized biotypes or host races in many regions. Because its annual natal host crops senesce earlier the cucurbit-specialized biotype may suffer food deficiency. The method this biotype uses to overcome this challenge is still poorly understood. In order to understand the potential of the cucurbit-specialized biotype aphids in host shift and usage, the performance of this biotype on cotton (Gossypium hirsutum), a common but poor quality host plant, was explored in this study. The cucurbit-specialized aphids could establish populations on cotton only when these plants had at least nine leaves, and subsequent populations developed rather slowly. The presence of whitefly populations on cotton improved the success rate of cucurbit-specialized aphids. The cucurbit-specialized aphids were mainly distributed on the older leaves of cotton, with only a few settling on the upper leaves. The cucurbit-specialized aphids reared on cotton for 40, 54 and 61 days still maintained strong preference for their natal host plant, cucumber (Cucumis sativus), rather than cotton, and their net reproductive rates and intrinsic rates of natural increase were dramatically lower when they were transferred onto new six-leaf cotton plants or detached leaves. Therefore, we concluded that the cucurbit-specialized aphids have the potential to utilize mature or whitefly-stressed cotton plants, but that this feeding experience on cotton did not alter their specialization for cucurbits. Some cotton plants could act as a temporary host for the cucurbit-specialized aphids to overcome food deficiency arising from senescing cucurbits. Key words Aphid gossypii, cotton-melon aphid, host shift, host specialization, temporary host, whitefly-stressed cotton

Introduction The cotton-melon aphid, Aphis gossypii Glover has strong fidelity to host plants (Zhang & Zhong, 1990; Ando et al., 1992; Guldemond et al., 1994; Blackman & Eastop, 2000; Br´evault et al., 2008; Liu et al., 2008). Host-specialized Aphis gossypii populations show different levels of performance and specialization on different host plants (Table 1).

Correspondence: Xiang-Dong Liu, Department of Entomology, Nanjing Agricultural University, Nanjing 210095, China. Tel: +86 25 84396204; fax: +86 25 84395242; email: [email protected]

Host specialization confers aphids some obvious advantages, such as escaping enemies and avoiding plant defense (Gratton & Welter, 1999; Wiklund & Friberg, 2008; Newton et al., 2009; Sarria et al., 2010; Tariq et al., 2012). However, host-specialized aphids are exposed to the possibility of food deficiency because of their limited host range, especially for specialized aphids living on annual herbaceous crops. In China, the cottonspecialized A. gossypii is known to be holocyclic (Zhang & Zhong, 1982), but the cucurbit-specialized form was assumed to be anholocyclic. This is because it was easy to produce sexual forms of the cotton-specialized aphids under short photoperiods and lower temperature conditions, while this proved impossible for cucurbitspecialized forms (Zhang & Zhong, 1982; Gao & Liu, 334

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Zoology, Chinese Academy of Sciences

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Cotton Cucumber Cucumber

Hibiscus (Hibiscus syriacus)

Eggplant (Solanum melongena)

Institute of Zoology, Chinese Academy of Sciences, 21, 334–341 Cucumber Cucumber, citrus (Citrus aurantium), sweet pepper (Capsicum annuum)




Citrus, eggplant and okra (Abelmoschus esculentus) Sweet pepper and cucumber Melon (Cucumis melo), pumpkin (Cucurbita maxima), zucchini (Cucurbita pepo), cucumber, green pepper, cotton, potato (Solanum tuberosum), citrus, chrysanthemum, and hibiscus Cucurbitaceae, cotton, potato, eggplant, strawberry (Fragaria ananassa), citrus, hibiscus, pepper, tomato (Solanum lycopersicum)

High rm

rm : intrinsic rate of population growth; NA: not available.

Genetic diversity using eight microsatellites



Population establishment easy Population establishment difficult Population establishment easy Population establishment difficult High mortality of larval, less progeny, and long period of larval Low mean relative growth rate and high larval mortality Low mean relative growth rate, and higher larval mortality Population establishment difficult Population establishment difficult High immature mortality, and low rm

Performance in life-history trait

Cotton Low rm Genetic differentiation by RAPD fingerprints



Chrysanthemum (Dendranthema Cucumber grandiflora) Cucumber Chrysanthemum

Cotton (Gossypium hirsutum) Cucumber (Cucumis sativus)

Tested host plant/check method

Catalpa (Catalpa bignonioides)

Natal plant

Table 1 Summary on host specialization in Aphis gossypii populations.

Ando et al., 1992; Meng & Li, 2001; Wu et al., 2013

Zhang & Zhong, 1990; Guldemond et al., 1994

Ando et al., 1992

Kring, 1959; Liu et al., 2008

Kring, 1959


Five host races: on cucurbitaceae, cotton, eggplant, potato, and pepper

Cucurbits and non cucurbits biotype

Carletto et al., 2009

Vanlerberghe-Masutti & Chavigny, 1998

Two groups: (1) a generalist Satar et al., 2013 population from cucumber, sweet pepper, citrus, eggplant and okra, and (2) a population from cotton



Host races on cucumber and chrysanthemum

Not designated

Not designated

Not designated

Host specialization

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2008; Liu & Gao, 2010). In Europe, the reproductive mode of A. gossypii was considered to be exclusively parthenogenetic (Fuller et al., 1999; Blackman & Eastop, 2000). Cucurbitaceous crops, such as cucumber and zucchini (Cucurbita pepo), usually have shorter growing seasons than cotton, and when cucurbits become senescent or are rotated in summer, the cucurbit-specialized A. gossypii may face a shortage of food. However, it is still unknown how the cucurbit-specialized aphids deal with this challenge. Here we put forward a hypothesis that widespread mature cotton plants could become a temporary host for the cucurbit-specialized aphids when the preferred host plant is absent. The performances of the cucurbitspecialized aphids on different growing stages of cotton and on whitefly-stressed cotton were studied.

ferred to a new cotton plant with four leaves, and covered by a transparent cage. After 6 days, all the adults were removed, and the eggs and larvae were maintained on the cotton. After 17 days from the infestation of whitefly adults (when the cotton had six leaves, and the whiteflies developed into pupae), 30 apterous adults of the cucurbitspecialized aphid were released onto the cotton with five aphids per leaf. Thereafter, the number of aphids on cotton was surveyed every other day, and the aphids on each leaf were counted and recorded in order to measure the distribution pattern. Fifteen cotton plants infested by whiteflies were tested for the cucurbit-specialized aphids.

Materials and methods

The cucurbit-specialized aphids reared on the whitefly stressed cotton for 40, 54 and 61 days were used to establish life tables on cotton and cucumber. Cucumber and cotton plants used here were four-leaf stage and sixleaf stage, respectively. Ten to 20 apterous adult aphids were transplanted onto an excised leaf of cucumber or cotton in a Petri dish (86 mm diameter) with the petiole wrapped in wet cotton wool. The next morning, only 10 new-born aphids were kept on the leaf to initiate a cohort for establishing a life table. Thereafter, survival and reproduction of the cohort were surveyed daily. During the reproductive period of resulting adults, newborn aphids were recorded and removed daily, and this was continued until all of the adult aphids had died. The excised leaf was replaced by a fresh one every 3–4 days. Three to four cohorts of aphids were replicated for each life table at 25 °C, 14 : 10 h (L : D). At the same time, the life tables of these cucurbit-specialized aphids reared on whiteflystressed cotton plants were established on the new six-leaf cotton plants.

Aphids Aphis gossypii Glover were collected from cucumber plants in April, 2012, in Nanjing, China. The aphids were reared on the seedlings of cucumber (var. Lufeng) for more than 3 months at 27 ± 1 °C and photoperiod 14 h : 10 h (L : D). It has been shown that A. gossypii from cucumber do not utilize seedlings of cotton, and thus have been considered as a cucurbit-specialized biotype (Liu et al., 2008; Wu et al., 2013). Population establishment of cucurbit-specialized aphids on different growth stages of cotton Cotton (var. Ningzamian 3) was planted in plastic cups (bottom diameter 54 mm, top diameter 74 mm, height 100 mm) in a 27 °C constant temperature chamber. Four growth stages of cotton plants: cotyledon, three, six, and nine leaves stages, were used to establish on them populations of the cucurbit-specialized aphids. Thirty apterous adult aphids were transferred onto each growth stage of cotton, and these aphids were evenly distributed on the plant leaves. The plant was then covered by a transparent plastic cage. Seven to 10 repetitions were performed for each growth stage of cotton. The aphids on cotton plants were surveyed every other day. Population establishment of cucurbit-specialized aphids on whitefly-stressed cotton Whitefly Bemisia tabaci (Gennadius) adults were collected from cotton plants in a greenhouse at Nanjing Agricultural University. Thirty newly born adults were trans C 2014

Life table establishment of cucurbit-specialized aphids on cotton and cucumber

Data analysis The life table parameters of aphids on cotton and cucumber, including the net reproductive rate (R0 ), average generation time (T) and intrinsic rate of natural increase (rm ) were calculated by the following formulations: R0 = ࢣlx mx , T = (ࢣxlx mx )/(ࢣlx mx ) and rm = (lnR0 )/T, where lx is the proportion of individuals in the original cohort alive at age x, and mx is the mean number of female progeny produced per female alive in the age interval x. Because the cucurbit-specialized aphids could not produce offspring on an excised cotton leaf (mx = 0), 1 was added to mx at the second last age x for all the life tables in order to calculate the rm values. The difference Institute of Zoology, Chinese Academy of Sciences, 21, 334–341

Host use of host-specialized aphid


Fig. 1 Population dynamics of the cucurbit-specialized aphids on different growth stages of cotton plant.

of R0 , T and rm of aphid populations between cotton and cucumber leaves and cotton plants were compared by Tukey’s Honestly Significant Difference (HSD) method at P = 0.05 level after one-way analysis of variance (ANOVA). Results Cucurbit-specialized aphids on different growth stages of cotton The cucurbit-specialized aphids could not establish populations on cotton plants which had less than nine leaves, but they could on cotton plants with nine leaves (Fig. 1). The population of aphids started to increase after 10 days from transplantation onto the nine-leaf cotton, and increased quickly after 16 days. When the cucurbitspecialized aphids lived on vigorous cotton plants with three or six leaves, they could survive only 14 to 26 days and did not establish populations. On the cotyledon of cotton seedlings, the cucurbit-specialized aphids could survive 40 days, but they did not establish populations. Cucurbit-specialized aphids on whitefly-stressed cotton The presence of whiteflies on cotton plants improved the fitness of the cucurbit-specialized aphids. Aphids could establish populations on nine out of 15 whiteflystressed plants, and after 24 days from transplantation, the population developed quickly (Fig. 2A), whereas on the other six stressed cotton plants, the aphids could not survive and reproduce normally, and after 30 days from transplantation, all the aphids died (Fig. 2B).  C 2014

Fig. 2 Population dynamics of the cucurbit-specialized aphids on cotton infested with whiteflies. (A) Aphid-established population on cotton (n = 9), and (B) aphids failed to establish population on cotton (n = 6).

Distribution of cucurbit-specialized aphids on cotton plants The cucurbit-specialized aphids fed mainly on the upper leaves of the whitefly-stressed cotton plants for the first eight days after they were transferred. Then they primarily occupied the middle leaves after 10–20 days. Finally, they established populations predominantly on the lower and middle leaves. The cucurbit-specialized aphids had the potential to use the lower leaves of cotton, and the upper leaves of cotton were not suitable for these aphids (Fig. 3). Performances of cucurbit-specialized aphids on cotton and cucumber The cucurbit-specialized aphids reared on whiteflystressed cotton plants for 40, 54 and 61 days still maintained a preference for cucumber, and the net reproductive rate (R0 ) and intrinsic rate of natural increase (rm ) were significantly higher on cucumber than

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Fig. 3 Distribution pattern of the cucurbit-specialized aphids on whitefly-stressed cotton.

on cotton (R0 : 40 days F2,8 = 23.196, P = 0.0005; 54 days F2,9 = 25.855, P = 0.0002; 61 days F2,8 = 12.48, P = 0.0035; rm : 40 days F2,7 = 28.521, P = 0.0004; 54 days F2,9 = 4.746, P = 0.0391; 61 days F2,8 = 9.858, P = 0.0069). Moreover, few aphids could grow into adults and produce offspring on the excised leaves of cotton (Fig. 4A), and the intrinsic rates of natural increase (rm ) were always negative (Fig. 4C). The average generation times (T) of the cucurbit-specialized aphids were significantly longer on the cotton plants than on the excised cucumber and cotton leaves (40 days: F2,8 = 35.157, P = 0.0001; 54 days: F2,9 = 25.037, P = 0.0002; 61 days: F2,8 = 39.75, P = 0.0001; Fig. 4B). The R0 , T and rm of the cucurbit-specialized aphids on cucumber showed no significant difference among 40, 54 and 61 days of feeding experience on cotton (R0 : F2,9 = 0.37, P = 0.7009; T: F2,9 = 2.138, P = 0.1739; rm : F2,9 = 2.738, P = 0.1178). When the aphids were transferred onto a new cotton plant, neither the R0 nor the rm showed significant differences among the 40, 54 and 61 days of feeding experience (R0 : F2,9 = 0.191, P = 0.8291; rm : F2,9 = 0.09, P = 0.9148), whereas the average generation time (T) of the aphids reared for 54 days on cotton was significantly longer than that of the aphids reared for 40 and 61 days (F2,9 = 7.168, P = 0.0137). The cucurbit-specialized aphids did not lose their preference for their original host plant, cucumber, even if they had been reared for several generations on a novel host, cotton, and the fitness of cucurbit-specialized aphids on cotton did not improve with the increase of feeding experience on this plant. The cotton plants only acted as a temporary host for the cucurbit-specialized aphids when they faced food deficiency (Fig. 4).

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Discussion The cucurbit-specialized A. gossypii performed poorly during the first few generations after transfer to cotton at the nine-leaf stage, but could slowly adapt to the novel host and establish populations on it. Other studies have shown that adaptation of A. gossypii to host plants varied slightly (Liu et al., 2008; Satar et al., 2013). Ebert & Cartwright (1997) reported that A. gossypii required time to adapt when switching host or feeding on artificial diet. The aphids did not adapt to a new host plant within 3 months when they were transferred between Cucurbitaceae and Solanaceae plants (Saito, 1991). The nymphs mortality of the cucumber clones of A. gossypii decreased over three generations on chrysanthemum, although their performance measured as developmental time and adult weight at the day of first reproduction did not become better (Guldemond et al., 1994). Satar et al. (2013) reported that A. gossypii from cucumber in Turkey was a generalist which exhibited better development on cotton, and the intrinsic rate of natural increase (rm ) on cotton leaves showed no significant changes over four generations. However, we found that the performance of the cucurbit-specialized aphids in China obviously declined when they were transferred to cotton. This difference may result from the aphid populations, because the aphids used in the present study were reared for at least 10 generations on cucumber host plants, whereas the aphids in the study by Satar et al. (2013) were only reared for five generations on cucumber. Moreover, there might be some genetic differences in A. gossypii populations between Turkey and China. In the present study, we also found the average

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Fig. 4 Net reproductive rate R0 (A), average generation time T (B) and intrinsic rate of natural increase rm (C) of the cucurbitspecialized aphids on cucumber and cotton leaf, and six-leaf cotton plant when they had been reared for 40, 54 and 61 days on whitefly-stressed cotton plants. Different lower case letters mean significant differences among cucumber, cotton leaf and cotton plant at the P = 0.05 level.

generation time of the cucurbit-specialized aphids significantly increased when they were reared for 54 days on cotton plants with six leaves, but it declined again when they were reared for 61 days (Fig. 4). This result suggested that the cucurbit-specialized aphids would attempt to adapt the novel host plant, but they failed. Therefore, the longer generation time appeared only in the populations reared for 54 days on cotton. The cucurbit-specialized aphids had a slight and limited adaptation to the six-leaf cotton, although they adapted quickly to the nine-leaf cotton. The cucurbit-specialized aphids do maintain the potential to use cotton. They would temporarily transfer into cotton fields when the cucumber crops became exhausted.  C 2014


Not all the growing stages of cotton would be used by the cucurbit-specialized aphids. We found that the cucurbit-specialized aphids survived and reproduced only on these cotton plants with more than six leaves, and the aphids usually settled down on the lower leaves of cotton plants. The older leaves in a novel host would act as the shelter for the host-specialized aphids. In India, A. gossypii were always more abundant on older leaves of eggplant and moved to younger tissues only when forced by population pressure (Banerjee & Raychaudhuri, 1985). In the USA, A. gossypii was most abundant on the basal portion of vines in cantaloupe Cucumis melo L. (Edelson, 1986), and the aphids were most abundant in the middle canopy of cotton, followed by the upper canopy (Hardee et al., 1994; Slosser et al., 1997). In Brazil, A. gossypii is mainly distributed in the top and middle of leaves in cotton at the early growing stages, and then mainly settled down on the middle and bottom leaves (Fernandes et al., 2012a, b). In our experiment, we found that the cotton-specialized A. gossypii preferred the upper and middle leaves of cotton at 25 °C, but the cucurbitspecialized aphids preferred the old ones. At the same time, the cucurbit-specialized aphids preferred the young leaves of cucumber to old ones. Nymphal mortality of A. gossypii on older leaves of cucumber was higher than that on middle-aged and young leaves, and fecundity on older leaves was significantly lower than that on middle and young leaves (van Steenis & EI-Khawass, 1995; Ebert & Cartwright, 1997). Aphis gossypii prefers the young leaves in the natal host plants as a flush-feeder, but it prefers the older leaves in an unfavorable novel host as a senescence-feeder. This result implies that the resistance of the younger leaves of cotton to aphids would be stronger than the older ones, although they have abundant nutrients. The cucurbit-specialized aphids could use the cotton leaves with a relatively lower resistance. Additionally, plant cultivar and stress would affect the use pattern of aphids. In chrysanthemum, survival of A. gossypii was unaffected by leaf position in cultivars Hero and Purple Anne, whereas it was highest on lower leaves in cultivar Surfine (Storer & van Emden, 1995). In comparison to non-Bacillus thuringiensis (Bt) cotton, Bt cotton had significant effects on the vertical, horizontal, spatial and temporal distribution patterns of A. gossypii (Fernandes et al., 2012b). The whitefly infestation would impair cotton photosynthesis and nutrient transfer, and accelerate the process of senescence (Lin et al., 1999, 2000). The cucurbit-specialized aphids preferred the senescent cotton leaves (Figs. 1, 3). Therefore, the whitefly-stressed cotton improved the performances of the cucurbit-specialized aphids. On the other hand, herbivore stress leads to a change of components in the phloem sap of cotton which might result in the decline

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of plant resistance to aphids. Consequently, the six-leaf cotton infested with whiteflies became more suitable for the cucurbit-specialized aphids. In the present study, the cucurbit-specialized aphids established populations on nine cotton plants stressed by whiteflies, but failed on the other six. This difference might result from the different infestation degrees of whiteflies on cotton, because the 30 whitefly adults might produce different offspring and result in different infestation scales. The precise relationship between status of stress in cotton and utilization capability of the cucurbit-specialized aphids needs further study. The outbreak of whitefly in cotton fields would benefit the cucurbit-specialized aphid populations. The feeding experience of the cucurbit-specialized aphids on cotton did not alter the host specialization to cucumber. The performances of the cucurbit-specialized aphids transferred onto a new six-leaf cotton was still very poor even if these aphids had been reared for 61 days on a old cotton plant, but they used cucumber very well. The feeding experience of Rhopalosiphum maidis and Acyrthosiphon pisum on a novel host plant also did not alter the specialization to their original host plants (Via, 1991; Caballera et al., 2001). We assumed that the cucurbit-specialized aphids would only temporarily use the older cotton plants during migration or dispersal in fields. The potential of the cucurbit-specialized aphids to use some specific cotton plants is advantageous not only for population propagation, but also for maintenance of host specialization. The host-specialized aphid can deal with the deficiency of natal host plants through temporarily using a relatively unsuitable plant. Therefore, the management of aphids in cotton after cucumber senescing would be an effective approach to control aphids in cucumber fields in the next season or year. Acknowledgments This work was supported by the National Natural Science Foundation of China (Grant No. 31070377). We thank the anonymous reviewers for the language improvement. Disclosure The authors declare no conflict of interests.

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Institute of Zoology, Chinese Academy of Sciences, 21, 334–341

How does the host-specialized aphid deal with food deficiency?

Aphis gossypii Glover shows obvious host specialization, with cucurbit- and cotton-specialized biotypes or host races in many regions. Because its ann...
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