Eur. J. Entomol. 110(4): 617–625, 2013 http://www.eje.cz/pdfs/110/4/617 ISSN 1210-5759 (print), 1802-8829 (online) Relation between plant water status and Macrosiphum euphorbiae (Hemiptera: Aphididae) population dynamics on three cultivars of tomato 1 2 2 2 2 ANNA R. RIVELLI , VINCENZO TROTTA , IRENE TOMA , PAOLO FANTI and DONATELLA BATTAGLIA * 1 2 School of Agricultural, Forestry, Food and Environmental Sciences, and Department of Sciences, University of Basilicata, Viale dell’Ateneo Lucano 10, 85100 Potenza, Italy; e-mails: [email protected]; [email protected]; [email protected]; [email protected] Key words. Hemiptera, Aphididae, Macrosiphum euphorbiae, aphid population dynamics, Lycopersicon esculentum, water stress, trophic interaction Abstract. Deficit irrigation scheduling is used to increase the efficiency with which water is used in many crops including tomato, however a water deficit is predicted to favour phloem feeding insects. We tested if and how different cultivars of tomato grown under water deficit conditions affect the population growth of the aphid Macrosiphum euphorbiae. Three tomato cultivars (Scintilla, Beefmaster and Rio Grande) were used in the experiments. The results for three watering regimes were compared with those of a control, which was well watered every three days: stressed plants received one third of the water supplied to the control over each three-day interval (experiment 1); stressed plants received a gradually decreasing amount of water (100% at the first watering and then 80%, 60%, 50%, 40% and 20%) every three days (experiment 2); stressed plants received the same amount of water as the con- trol but at longer intervals, that is when evident signs of wilting appeared (experiment 3). The results showed that water stress either enhanced, had an adverse effect or had no effect on aphid population growth, depending on the cultivar and watering regime. No dif- ference was recorded in the population dynamics of M. euphorbiae feeding on Beefmaster tomato plants subjected to different levels of water stress. In the case of the cultivar Scintilla, live aphids were less abundant on stressed plants than on well watered ones in experiment 1 and 3 but not in experiment 2. The highest variability in aphid population dynamics on the plants grown under the dif- ferent water stress protocols was recorded on the cultivar Rio Grande. In experiment 1, the initial peak in aphid numbers was higher on the water stressed plants than on the control and then decreased to lower numbers than on the control. In experiment 2, there were no differences in the numbers of aphids infesting stressed and control plants. In experiment 3, there were fewer aphids on stressed than on control plants after six days, as in experiment 1, but there was no initial peak in aphid numbers. INTRODUCTION constant by means of polyethylene glycol used as a There are two hypotheses that address the effect of host medium for growing plants (Sumner et al., 1983), in other plant stress on arthropod pest populations: the “plant cases the maximum level of stress is kept constant by stress” hypothesis (White, 1969) and the “plant vigour” varying the water supply (Fereres et al., 1988). Some- hypothesis (Price, 1991). The plant stress hypothesis, times the level of stress experienced by plants is not based on empirical data on pest outbreaks during drought measured (Kennedy et al., 1958; Wearing, 1967; Wearing periods, predicts that stressed plants are better hosts for & van Emden, 1967) or an indirect measure is provided herbivores (White, 1984; Mattson & Haack, 1987). The (McVean & Dixon, 2001). The main negative effect of plant vigour hypothesis, in contrast, predicts that phy- water stress on the aphids is recorded in terms of the tophagous arthropods will prefer and perform better on reduction in their reproductive capacity (Fereres et al., rapidly growing plants and, consequently, less well when 1988; Pons & Tatchell, 1995) and sometimes in terms of the plants are subject to stress. The plant vigour their “restless” behaviour (Kennedy et al., 1958; Miles et hypothesis (Price, 1991) is mainly based on experimental al., 1982). Nevertheless, the response to stress is not the studies showing that imposed water stress conditions same for all species of aphid and is affected by feeding often negatively affect herbivore performance, either in site (Wearing, 1967; Wearing & Van Emden, 1967). terms of reduced population growth (Pons & Tatchell, Arthropod pests infesting plants experiencing water 1995; McVean & Dixon, 2001), reduced fecundity and stress may simultaneously experience both favourable and reproduction (Kennedy et al., 1958; Wearing & van detrimental conditions. In fact, during water stress, pro- Emden, 1967; Wearing, 1972; Sumner et al., 1983; Inbar teins can be hydrolyzed and plants may produce and et al., 2001) or survival (Sumner et al., 1983; Watt, 1986). accumulate nitrogen-containing osmoprotectants, re- Most of these references relate to work with aphids, and sulting in increased levels of free amino acids (Brodbeck in particular with different species of aphid, feeding on & Strong, 1987), but turgor pressure and water content different host plants, and experiencing a variety of water decrease (Hsiao, 1973, Inbar et al., 2001) and levels of stress treatments. In some cases the level of stress is kept allelochemicals may occasionally increase (Gershenzon, 1984; Mattson & Haack, 1987; Inbar et al., 2001). * Corresponding author; e-mail: [email protected] 617 Larsson (1989) suggests that physiological responses of climates (i.e. Mediterranean) where water stress is rather plants to water deficit produce quite different conse- frequent. Moreover, deficit irrigation techniques, charac- quences for specific feeding guilds of herbivorous insects. terized by a reduced restoration of crop maximum evapo- Since allelochemicals are less concentrated in vascular transpiration, may be applied to tomato crops in order to than leaf tissue (Raven, 1983), phloem feeders are pre- increase water use efficiency (Perniola et al., 1994). dicted to show a stronger positive response to plant stress Physiological responses of tomato to drought stress than chewing insects (Larsson, 1989). Nevertheless, the largely depend on the characteristics of the cultivar, as net reduction in turgor pressure may compromise the poten- photosynthetic rate, stomatal conductance, transpiration tial benefits of elevated nitrogen and low allelochemical rate and osmotic adjustment may differ significantly concentration for phloem feeding insects. Finally, the under the same water deficit conditions (Srinivasa Rao et effect of concurrent favourable and detrimental factors al., 2001). Different tomato genotypes also display dif- may be in any case difficult to forecast. In the case of ferent levels of resistance to pests and diseases (Scott et aphids (Aphididae), for example, drought stress enhances al., 1995, 2001; Goggin et al., 2001; Cooper & Goggin, insect performance in some cases, increasing reproduc- 2005). tion rate (Wearing, 1967), or speeding nymphal develop- The effects of water stress (Aloni & Pressman, 1981; ment (Miles et al., 1982), or promoting outbreaks in the Van Ieperen et al., 2003) and aphid infestation (Walgen- field (Li et al., 2008). Nevertheless, in some other cases, bach, 1997) on the growth, development and yield of all relating to aphids, drought stress has a detrimental tomato are fairly well known, while information on the (Miles et al., 1982; Sumner et al., 1986; Pons & Tatchell, interaction between these effects, e.g. which stresses are 1995; McVean & Dixon, 2001) or little effect (McMurtry, combined with each other, is limited. This study aimed to 1962; Salas & Corcuera, 1991). test the role of host plant cultivar in determining the Huberty & Denno (2004), reviewing the literature on aphid-plant relationship when the host plant is subjected plant water stress and its consequences for herbivorous to pulsed water stress. As a model, we chose the aphid insects, proposed the “pulsed stress hypothesis”, which Macrosiphum euphorbiae (Hemiptera: Aphididae), a suggests that phloem-feeding insects, like aphids, are worldwide pest of tomato of economic importance in expected to respond positively to intermittently stressed terms of both direct damage (Houser et al., 1917; Wal- plants, where the recovery of turgor allows sap-feeders to genbach, 1997) and virus transmission (Braithwaite & benefit from increases in plant nitrogen induced by the Blake, 1961; Chowfla et al., 1999). stress, but are expected to perform poorly on continu- In this paper we report the effects of pulsed water stress ously stressed plants. Huberty & Denno (2004) in their on the population growth of M. euphorbiae feeding on meta-analysis of published studies, categorized stress three cultivars of tomato (Lycopersicon esculentum treatments as intermittent if the experimental protocol Mill.). involved sporadic watering of plants throughout the MATERIAL AND METHODS study, or continuous if plants were never watered after the start of the experiment. Insects and plants The results presented in most of the literature on the Three cultivars of tomato were used in our experiments: Scin- performance of aphids on continuously stressed plants tilla (cherry tomato, F1 hybrid), Beefmaster (beefsteak tomato, support the “pulsed stess” hypothesis (Kennedy et al., F1 hybrid) and Rio Grande (pear-shaped processing tomato for 1958; Sumner et al., 1986; McVean