- Top of page
- 1 INTRODUCTION
- 2 MATERIALS AND METHODS
- 3 RESULTS
- 4 DISCUSSION
Cultivated cotton, Gossipium hirsutum, is the prime cash crop and an important source of foreign exchange earnings for Pakistan and other countries. This crop is attacked by a variety of chewing and sucking pests that remain active for almost the entire growing season and have detrimental effects to crop productivity. Phenacoccus solenopsis Tinsley (Homoptera: Pseudococcidae) is of great concern to cotton producers owing to its polyphagous nature and potential to cause heavy crop losses. P. solenopsis is a soft-bodied insect that damages the crop by sucking the cell sap. Attacked cotton plants remain stunted and produce fewer bolls of smaller size; leaves become distorted, yellow and finally drop off.[6, 7] Boll opening is also adversely affected, and yield reduction ranges from 58 to 73%. The attacked leaves and shoots are malformed as a result of direct feeding damage of P. solenopsis, and honeydew excreted by the pest also favours mouldy growth, which ultimately hinders the process of photosynthesis. As much as 90% damage may result from attack by P. solenopsis.
In Pakistan, from 2005 onwards, P. solenopsis has been recorded as a threatening pest of cultivated cotton.[11-13] During 2007, this insect was responsible for the loss of more than 40% of the cotton crop in Pakistan. It has also been reported as a serious pest in the United States, Thailand and Taiwan and India and China.[15, 16] Different insecticides such as organophosphate, pyrethroid and neonicotinoid have been used for the control of this pest. However, resistance to insecticides is a main problem linked with uninformed and excessive use of the chemical control of insect pests. The widespread application of conventional insecticides such as organophosphate, carbamate and pyrethroid has provided an ideal environment for resistance evolution in Pakistan. Resistance to acetamiprid has been reported in a number of insects, including Plutella xylostella,[18, 19] Bemisia tabaci and Leptinotarsa decemlineata, from different parts of the world. However, to the authors' knowledge, there have been no reports of acetamiprid resistance in P. solenopsis.
Neonicotinoids are the latest major class of insecticides with a novel mode of action. These insecticides are very important in agriculture because they are efficient against a broad spectrum of insect pests. Nicotinergic acetylcholine receptors are the target sites of this class of insecticides, which agonise the receptors, thus hindering nerve impulse transmission as a result of a depolarising effect within the central nervous system of insects. Acetamiprid is a neonicotinoid that is effective against both soil and plant insects, including insects of the orders Lepidoptera, Coleoptera, Homoptera and Thysanoptera. Acetamiprid has contact, systemic and osmotic action and is recommended especially for P. solenopsis.
Insecticides are chemical weapons used to control insects by killing them or preventing them from engaging in undesirable or destructive behaviours. Insecticides could affect the physiological make-up of the target pests by causing changes in growth, development and reproduction parameters, or by causing changes in the nutritional contents of the host plants, which may result in enhanced developmental time, decreased survival, fecundity and reproduction or other changes in the behaviour of the target pest. Insecticidal effects on biological parameters of insects potentially have an ecological impact. Previously, attempts have been made to examine the effects of different insecticides on biological parameters of different insects. The effects of imidacloprid on Nilaparvata lugens, tebufenozide on P. xylostella and Spodoptera exigua, thiamethoxam on B. tabaci, trichlorphon on Bactrocera dorsalis, imidacloprid on S. litura and emamectin benzoate on Chrysoperla carnea have been reported.
Bearing in mind the significance of P. solenopsis as an invasive pest in Pakistan and many other countries, this research was carried out with the objective of investigating the effect of acetamiprid on the biological parameters of different populations of P. solenopsis. Moreover, cross-resistance to different insecticides in an acetamiprid-selected population (Aceta-SEL Pop) and the stability of acetamiprid resistance were determined.
- Top of page
- 1 INTRODUCTION
- 2 MATERIALS AND METHODS
- 3 RESULTS
- 4 DISCUSSION
Acetamiprid binds to nicotinic acetylcholine receptors (nAChRs), has high toxicity against many insect pests and is mainly used to control the sucking insect pests of cotton, vegetables and ornamental plants. Acetamiprid resistance has previously been reported in different insect pests from Pakistan.[18-20] There was no previous report of insecticide resistance in P. solenopsis to acetamiprid. At the time of collection, the field population showed low levels of resistance to acetamiprid and imidacloprid, with resistance ratios of nine- and sevenfold, respectively, compared with the control. The same population also demonstrated very low resistance to chlorpyrifos and deltamethrin, with resistance ratios of threefold for each (Table 1). After five rounds of selection with acetamiprid, resistance to this compound increased to 315.20-fold that of UNSEL Pop, suggesting that selection had a marked effect on resistance. The high level of acetamiprid resistance in Aceta-SEL Pop after five rounds of selection could be due to enhanced detoxification of the insecticide by metabolic enzymes. Although this hypothesis has not been tested in the present study, research being carried out in the authors' laboratory suggests that the presence of monooxygenase and esterases is the major mechanism of resistance in P. solenopsis from Pakistan (Afzal MBS, unpublished data).
There are no previous reports of cross-resistance to acetamiprid in P. solenopsis, but cross-resistance to acetamiprid has been reported in many other insects, such as in an acetamiprid-selected strain of B. tabaci which suggested very high cross-resistance to thiamethoxam (>500-fold). A 110-fold acetamiprid-resistant strain of P. xylostella (L.) displayed low cross-resistance to cartap and phenthoate. A 118-fold acetamiprid-resistant B. tabaci strain has been reported to develop very low cross-resistance to endosulfan (fivefold) and bifenthrin (fourfold). In the present study, Aceta-SEL Pop (315-fold) showed moderate cross-resistance to imidacloprid (28.48-fold) and deltamethrin (30.84-fold), and very low cross-resistance to chlorpyrifos (8.68-fold) compared with the field population. In general, cross-resistance to compounds within the same chemical group may generally be observed, although without supporting experimentation it remains hard to predict in advance. The cross-resistance among insecticides having different structures and modes of action (intergroup cross-resistance) is extremely unpredictable, but the cross-resistance to unrelated insecticides could be due to a common mechanism affecting the insecticides or to genetically linked independent mechanisms. Cross-resistance among insecticides from different chemical groups could also be possible when an isoenzyme from insects acts on different types of insecticide.
Knowledge of the stability of resistance after exposure to insecticides has important practical implications. This knowledge, along with regular resistance monitoring, is crucial for developing effective insecticide resistance management strategies. For example, if resistance is unstable, then removal of the insecticides from spray schedules could bring the resistance level down, and thus the efficacy of a chemical can be prolonged. Rapid decrease in insecticide resistance has been reported for insect populations selected for resistance in the laboratory or field. A high fitness cost and incomplete resistance might be associated with rapid reversion of insecticide resistance. In the present study, resistance to acetamiprid also remained unstable in Aceta-SEL Pop in the absence of insecticide exposure. Similarly to the present results, unstable acetamiprid resistance has also been reported in highly resistant P. xylostella and B. tabaci. The present finding on the rate of resistance decline suggests that the fitness cost of maintaining the resistance gene(s) might be high. The present study suggests that the acetamiprid selection pressure to the field strain was not intense in the field, and, because of this, deleterious mutations may have appeared in the strain. It has been shown that, in the absence of selection, the average fitness of individuals could be reduced by the accumulation of deleterious mutations. The reversion of resistance is also likely to be due to the presence of heterozygotes in the selected population. The decline in resistance in the Aceta-SEL population indicates that, if the insecticides are removed from the spray schedule, the resistance may drop in the field.
Insecticides can alter the biology of resistant insects. Many studies suggest that resistant insects show fitness costs.[51, 52] Studying the relative fitness costs of the resistant population is the basis for understanding and resolving the problem of resistance. It is usually believed that biological characteristics (prolonged growth period and declined fecundity) change the relative fitness cost. The present study shows that, under continuous selection pressure, Aceta-SEL Pop had a significantly lower survival rate, longer male and female nymphal duration, longer developmental time from egg to female adult, reduced fecundity and low percentage hatching. Therefore, acetamiprid resistance in the P. solenopsis population corresponded to a significant decrease in many biological fitness parameters, which indicates a trade-off in distribution of resources among resistance and fitness costs.
Decreased relative fitness associated with insecticide resistance has been demonstrated for many insects, including S. litura, P. xylostella,[29, 54] B. dorsalis, N. lugens, S. exigua, B. tabaci and L. decemlineata. The present study also indicates that the acetamiprid resistance could decrease relative fitness in P. solenopsis. Aceta-SEL Pop expressed a relative fitness of 0.22 compared with UNSEL Pop. This finding suggests that Aceta-SEL Pop would not increase as rapidly as UNSEL Pop if acetamiprid selection were discontinued. Although fitness cost determination is important in the homozygous resistant population, it is impossible to ignore the fitness in heterozygotes because, in the early stages of resistance evolution, heterozygous individuals mostly act as carriers of resistant gene alleles. In the present study, fitness costs are not only evident in Aceta-SEL Pop but also in reciprocal crosses (Cross1 and Cross2). Results illustrated that heterozygous genotypes, Cross1 and Cross2, exhibited advantageous traits, with a relative fitness of 1.32 and 1.78, respectively, compared with UNSEL Pop. This phenomenon could be the result of fitness reduction associated with extensive inbreeding in Aceta-SEL Pop and UNSEL Pop. The crossing between Aceta-SEL Pop and UNSEL Pop may result in recovery of advantageous traits in heterozygous progeny (reciprocal crosses). Another possibility is that, in hybrids, the level of enhancement in vigour was significantly higher than the level of decrease in fitness as a result of resistance development. Therefore, examination of biological parameters in reciprocal crosses and resistant populations is crucial to the formulation of a resistance management strategy. The present study provides valuable information on biological fitness parameters in UNSEL, reciprocal crosses and Aceta-SEL populations.
The intrinsic rate of natural increase (rm) provides an estimate of growth potential of insect populations, which provides considerable insight, aside from individual life history parameters. The net reproductive rate (R0) is not, however, the only component needed to assess the potential of population growth, because the intrinsic rate of natural increase depends on fecundity, percentage hatching, growth and adult eclosion.[57, 58] Therefore, variations in the above life history qualities could influence the rate of P. solenopsis population increase. The intrinsic rate of natural increase (rm) of males and females in Aceta-SEL Pop was significantly less compared with that in UNSEL Pop and reciprocal crosses (Fig. 1). There is a positive relation between intrinsic rate of natural increase and mean relative growth rate.[33, 59-62] It was previously reported that the intrinsic rate of natural increase in imidacloprid-resistant S. litura, in pyrethroid- and organophosphate-resistant C. carnea, in deltamethrin- and indoxacarb-resistant H. virescens and in spinosad-resistant P. xylostella demonstrated a positive association with mean relative growth rate. In the present study, a positive relationship was found with the mean relative growth rate, resulting in a subsequent decrease in intrinsic rate of natural increase in Aceta-SEL Pop of P. solenopsis. The lower rate of population increase appeared to be mainly due to decreased fecundity and low percentage egg hatching, and also the longer developmental time from egg to adult emergence. In insect populations with non-overlapping generations, such developmental asynchrony could lead to non-random (assortative) mating among resistant insects and, through interaction with season length, increase or slow down the evolution of resistance.
Management of insecticide resistance depends on fitness costs, such that the removal of selection pressure will lead to decrease in the number of resistance alleles. Incomplete resistance and fitness costs can delay the insecticide resistance developed within an insect population. Resistant individuals also suffer some impairment in performance in the presence of insecticides in comparison with their performance in the absence of insecticides owing to the phenomenon of incomplete resistance. To the best of the authors' knowledge, this is the first report of cross-resistance and fitness cost to acetamiprid in P. solenopsis worldwide. Based on the findings of the present research it can also be concluded that, for good management of P. solenopsis under field conditions, only those insecticides that have lower stability and correlate with a high reversion rate of insecticide resistance should be used. Consequently, rotation of insecticides can be implemented in resistance management strategies.