Functional Response of Four Heteropteran Predators ... - BioOne

BIOLOGICAL CONTROL

Functional Response of Four Heteropteran Predators Preying on Greenhouse Whitefly (Homoptera: Aleyrodidae) and Western Flower Thrips (Thysanoptera: Thripidae) MARTA MONTSERRAT, RAMON ALBAJES,1

AND

˜ E´ CRISTINA CASTAN

Departament de Proteccio´ Vegetal, IRTA-Centre de Cabrils, 08348 Cabrils (Barcelona), Spain

Environ. Entomol. 29(5): 1075Ð1082 (2000)

ABSTRACT The mirid bugs Dicyphus tamaninii Wagner and Macrolophus caliginosus Wagner and the anthocorid bugs Orius majusculus (Reuter) and O. laevigatus (Fieber) are abundant generalist predators in unsprayed vegetable crops of the Spanish Mediterranean coast. We evaluated the functional response of these predators to greenhouse whiteßy pupae and western ßower thrips larvae (second instar) on cucumber leaf disks in the laboratory. Parameters of the random-predator equation obtained were compared among all predatorÐprey combinations to determine the potential role of the predators in the biological control of both pests in cucumber. D. tamaninii was efÞcient at consuming whiteßy pupae at high and low densities and thrips at high densities, and took less time to handle either of these prey than did the other predators. Anthocorid bugs were efÞcient at consuming thrips at low and high densities, but did not performed well as predators of whiteßies. M. caliginosus was less efÞcient when consuming whiteßies but performed better when preying on thrips. It is concluded that D. tamaninii may have a good action in the control of both greenhouse whiteßy and western ßower thrips, whereas M. caliginosus and both Orius species may be slower in controlling whiteßy and be similarly efÞcient in consuming western ßower thrips. KEY WORDS whiteßies, thrips, Heteropteran predators, functional response, biological control

PEST OF GREENHOUSE vegetal crops can reach high densities in the absence of their natural enemies. In multipest agroecosystems, the application of integrated pest management (IPM) programs based on the seasonal inoculative release of pest-speciÞc natural enemies becomes very expensive and complicated. In contrast, generalist predators are increasingly appreciated as they can simultaneously attack different unrelated prey species and have an impact on several pest populations (Albajes and Alomar 1999). Field and protected cucumber crops in the Mediterranean area have several pest species among which the greenhouse whiteßy, Trialeurodes vaporariorum Westwood, and the western ßower thrips, Frankliniella occidentalis Pergande, are consistent problems. When spraying of vegetable crops with pesticides is limited they can host a number of naturally occurring predatory species (Riudavets and Castan˜ e´ 1998), among which the mirid bugs Dicyphus tamaninii Wagner and Macrolophus caliginosus Wagner and the anthocorid bugs Orius laevigatus (Fieber) and Orius majusculus (Reuter) are the most consistently found. These four predators are largely polyphagous. Although Orius species are commercially released for thrips control in greenhouses (Castan˜ e´ et al. 1999), they may prey on quite a broad spectrum of arthropods (Albajes and Alomar 1999). M. caliginosus is used 1

Centre UdL-IRTA, Universitat de Lleida, 25198 Lleida, Spain.

for whiteßy, leafminer, and spider mite control in tomatoes (Albajes and Alomar 1999, Koskula et al. 1999, Nedstam and Johansson-Kron 1999). D. tamaninii has been evaluated for the control of T. vaporariorum on Þeld tomato crops (Alomar and Albajes 1996) and for this pest and F. occidentalis on greenhouse cucumbers (Gabarra et al. 1995, Castan˜ e´ et al. 1996, 1997) with good results and it may also prey on other insect pests of protected vegetables (Albajes et al. 1996). Other Dicyphus species such as D. hesperus Knight and D. hyalinipennis Burm. have shown a good potential for biological control in greenhouses (Ceglarska 1999, McGregor et al. 1999). Although some aspects of the biology of these predators are known, others remain poorly understood, among these the interactions that they establish with their prey. One of the elements describing predatorÐ prey relationships is the predatorÕs functional response, which relates the change in prey consumption with increasing prey density (Holling 1966). The use of functional response experiments has been considered too reductionist for selecting biological control candidates (Waage 1990), but, as stated by Kareiva (1990), only those agents that perform well in simple laboratory environments are worth examining under more challenging circumstances. The functional response of a natural enemy is important in ephemeral crop habitats, such as vegetable crops, while its numerical response is more important in stable crop habitats, such as perennial crops (Wiedenmann and

0046-225X/00/1075Ð1082$02.00/0 䉷 2000 Entomological Society of America

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Smith 1997). The aim of this study was to compare the functional response of the four mentioned predators when feeding on F. occidentalis larvae and T. vaporariorum pupae, to estimate their potential capacity as biological control agents of these pests for cucumbers in conservation and augmentation programs. The following questions were considered: (1) Are the functional response parameters different among predators when they feed on the same prey? (2) Are the functional response parameters for each predator different when they feed on different prey? (3) What is the potential role of these predators in the biological control of both pests in cucumbers? Materials and Methods Functional Response Experiments. All insects came from cultures maintained at the Institut de Recerca i Tecnologia Agroalimentaries (IRTA) in north-eastern Spain. Colonies are renewed periodically with individuals collected in the area. We maintained colonies of predators and conducted all experiments under controlled conditions of 25 ⫾ 1⬚C, and 70 ⫾ 10% RH, and a photoperiod of 16:8 (L:D) h. Mirid bugs were reared on tobacco plants with eggs of Ephestia kuehniella (Zeller) (Lepidoptera: Pyralidae) as prey, and anthocorid bugs were reared on bean pods with the same prey. T. vaporariorum was reared on tobacco plants in a heated greenhouse, and only the pupal stage was used in our experiments. F. occidentalis was reared on cotton seedlings, as described by Riudavets et al. (1993) and only second-instar larvae were used. Before each experiment, reproductively mature predator females (13Ð16 d old) were fed the test prey for 24 h and then starved for 24 h. Arenas consisted of a cucumber leaf disk placed upside down on a 20 ml layer of agar (0.5%) in a 7-cm-diameter cage with ventilation. Different prey densities were offered to each predatory female. With T. vaporariorum, the densities tested were 1, 3, 6, 9, 15, 18, 30, and 39 for all predator species. With F. occidentalis the densities tested were the same for the mirids but 1, 3, 6, 9, 18, and 30 for anthocorids. The two prey species offered are similar in size: 1.2Ð1.3 mm long (including the antennae) for F. occidentalis second-instar larvae (Arzone et al. 1989) and 0.6 by 0.9 mm for T. vaporariorum pupae (Gomez-Menor 1943). We tested one individual predator and one density of prey species per arena, and the number of dead prey recorded 6 h after predator release. Every combination of predatory species, prey type and prey density was replicated 10 times. Prey were not replaced during the experiment. Data Analysis. To determine the shape of the functional response we used a logistic regression of the proportion of prey eaten (Ne/N0) as a function of prey offered (N0) (Juliano 1993). Data were Þtted to a polynomial function that describes the relationship between N e /N 0 and N0: exp共P 0 ⫹ P 1N 0 ⫹ P 2N 02 ⫹ P 3N 03兲 Ne ⫽ , N 0 1 ⫹ exp共P 0 ⫹ P 1N 0 ⫹ P 2N 02 ⫹ P 3N 03兲

[1]

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with P0, P1, P2 and P3 being the intercept, linear, quadratic, and cubic coefÞcients, respectively. These parameters were estimated using the method of maximum likelihood (PROC CATMOD, SAS Institute 1989). If P1 ⬎ 0 and P2 ⬍ 0, the proportion of prey eaten is initially positively density-dependent, thus describing a type III functional response. If P1 ⬍ 0, the proportion of prey eaten declines monotonically with the initial number of prey offered, thus describing a type II functional response (Juliano 1993). To estimate handling times (Th) and attack coefÞcients (a) we used the Holling Ôdisc equationÕ for type II responses and the Hassell equation (Hassell 1978) for type III responses. In both cases, depletion as predators fed is taken into account. Thus, we used the integral of the Ôrandom predatorÕ equation (Rogers 1972) for type II responses: N e ⫽ N 0兵1 ⫺ exp关a共T hN e ⫺ T兲兴其,

[2]

and the integral of the Hassell equation for type III responses: N e ⫽ N 0兵1 ⫺ exp关共d ⫹ bN 0兲共T hN e ⫺ T兲/共1 ⫹ cN 0兲兴其, [3] where T ⫽ total time available, and b, c, and d are constants from the function that relate a and N0 in type III functional responses: a ⫽ d ⫹ bN0/1 ⫹ cN0. Parameters were obtained by Þtting observed data to the models above using nonlinear least-square regression with iterative application of NewtonÕs method. This step is needed because both functions have Ne on both sides of the expression (PROC NLIN, SAS Institute 1989) (Juliano 1993). Logistic regression for D. tamaninii–F. occidentalis data had signiÞcant linear P1 ⬎ 0 and quadratic P2 ⬍ 0 parameters, suggesting a type III functional response. After Þtting equation 3 we used the likelihood ratio test (Messina and Hanks 1998, Trexler and Travis 1993) to determine if this equation Þt the data better than the simpler model of equation 2. The integral of the Hassell equation never produced a signiÞcantly better Þt than the integral of the random-predator equation (␹2 ⫽ 0.175, df ⫽ 1, P ⬎ 0.90). We therefore reestimated P0 and P1 with the simpler model. To compare type II functional responses of two groups we used the following equation: ˆ a 关 z兴兲共关Tˆ h ⫹ D ˆ Th 共z兲兴Ne ⫺ T兲兴其, Ne ⫽ N0 兵1 ⫺ exp关共aˆ ⫹ D [4] where z is an indicator variable that takes on the value 0 for population one and the value 1 for population 2. The parameters Da and DTh estimate the differences between the populations in the values of the parameters a and Th, respectively. If these parameters are signiÞcantly different from 0 then the two populations differ signiÞcantly in the corresponding parameters. For population 1, aˆ and Tˆ h are the estimates of the population parameters a1 and Th1. For population 2, ˆ a and Tˆ h ⫹ D ˆ Th are the estimates of the popuaˆ ⫹ D lation parameters a2 and Th2 (Juliano 1993). Nonlinear least square regressions were again used to obtain

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MONTSERRAT ET AL.: FUNCTIONAL RESPONSE OF FOUR PREDATORS

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Table 1. Maximum-likelihood estimates from logistic regression of proportion of prey eaten as a function of initial prey densities by two mirid and two anthocorids bugs Predators D. tamaninii M. caliginosus O. majusculus O. laevigatus

Parameter Intercept (P0) Linear (P1) Intercept (P0) Linear (P1) Intercept (P0) Linear (P1) Quadratic (P2) Intercept (P0) Linear (P1) Quadratic (P2)

T. vaporariorum

F. occidentalis

Estimate

SE

␹2

P

Estimate

SE

␹2

P

0.443 ⫺0.037 ⫺0.519 ⫺0.044 2.549 ⫺0.219 0.003 0.610 ⫺0.145 0.002

0.139 0.005 0.160 0.006 0.328 0.031 0.001 0.277 0.030 0.001

10.23 52.01 10.54 46.50 60.39 48.63 22.13 4.85 23.45 7.78

0.0014 0.0001 0.0012 0.0001 0.0001 0.0001 0.0001 0.0277 0.0001 0.0053

⫺0.057 ⫺0.017 ⫺0.391 ⫺0.019 2.216 ⫺0.080 Ñ 3.216 ⫺0.251 0.005

0.138 0.005 0.144 0.005 0.229 0.009 Ñ 0.481 0.055 0.001

0.17 11.78 7.36 13.46 93.83 71.63 Ñ 44.62 20.75 12.01

0.6796 0.0006 0.0067 0.0002 0.0001 0.0001 Ñ 0.0001 0.0001 0.0005

parameter estimates. The four predators were compared with each other when fed each prey, and each predator was examined individually when fed the two prey. We conducted Student t-test for the null hypothesis that Da and DTh were 0. Multiple tests were used when comparing among predators fed with the same prey. To avoid false rejections of one or more true null hypotheses the sequential Bonferroni technique of signiÞcant level was applied (Rice 1989). Results Functional Response with T. vaporariorum as Prey. The logistic regression for all predatory species had a signiÞcant linear parameter P1 ⬍ 0 (Table 1) and the

proportion of prey eaten by all predators declined with increasing prey density. This suggested a type II functional responses (Fig. 1), therefore we used equation 2 to estimate functional response parameters. The random-predator equation Þtted the observed data quite well for all predators (see determination coefÞcients, R2, Table 2). Estimates of attack coefÞcients and handling times for each predator and their signiÞcances are summarized in Table 2. Attack coefÞcients of the three predators were not signiÞcantly different from one another (Table 3). On the contrary, D. tamaninii spent less time handling whiteßy pupae than did O. majusculus and M. caliginosus (Table 4). The attack coefÞcient of O. laevigatus was not signiÞcantly different from 0 as

Fig. 1. Functional responses of predators when exposed to different densities of T. vaporariorum pupae. Points are means ⫾ SE of observed values (N ⫽ 10, t ⫽ 6 h).

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Table 2. Attack coefficients (a) (hoursⴚ1) and handling times (Th) (hours) from nonlinear regressions of the number of prey eaten by two mirid and two anthocorid predators as a function of initial prey density T. vaporariorum Predators

Th (Probability) (Asym. 95% CI)

0.185 (P ⬍ 0.001) (0.079Ð0.291) 0.124 (P ⬍ 0.05) (0.004Ð0.244) 0.802 (P ⬍ 0.05) (0.104Ð1.500) 0.305 (P ⬍ 0.1) (⫺0.019Ð0.629)

0.381 (P ⬍ 0.001) (0.226Ð0.537) 1.229 (P ⬍ 0.001) (0.736Ð1.722) 0.778 (P ⬍ 0.001) (0.677Ð0.879) 1.547 (P ⬍ 0.001) (1.208Ð1.885)

R

D. tamaninii

0.81

M. caliginosus

0.63

O. majusculus

0.91

O. laevigatus

0.76

F. occidentalis

a (Probability) (Asym. 95% CI)

2

2

R

0.83 0.71 0.90 0.94

a (Probability) (Asym. 95% CI)

Th (Probability) (Asym. 95% CI)

0.119 (P ⬍ 0.001) (0.063Ð0.176) 0.099 (P ⬍ 0.005) (0.036Ð0.162) 0.688 (P ⬍ 0.05) (0.059Ð1.318) 0.332 (P ⬍ 0.001) (0.192Ð0.471)

0.213 (P ⬍ 0.02) (0.045Ð0.382) 0.341 (P ⬍ 0.02) (0.065Ð0.617) 0.369 (P ⬍ 0.001) (0.272Ð0.466) 0.280 (P ⬍ 0.001) (0.199Ð0.361)

df (all predators with T. vaporariorum) ⫽ 78, df (miridae with F. occidentalis) ⫽ 58, df (anthocoridae with F. occidentalis) ⫽ 78. R2 are the coefÞcients of determination obtained from R2 ⫽ 1 ⫺ (sum of squares of residuals/total sum of squares).

the asymptotic 95% conÞdence interval overlapped this value (Table 2). At the highest whiteßy density tested it was D. tamaninii which consumed more prey, eating ⬎10 pupae in 6 h. The maximum number of prey attacked by the other predators was lower, ranging from three to seven whiteßy pupae (Fig 1). When only one or three whiteßy pupae were offered, it consumed an average of 0.8 and two, respectively, indicating that the predator was also efÞcient in Þnding this prey at low densities. In addition, this predator continued to consume more prey even at the highest densities tested. O. majusculus was also a good searcher of whiteßy pupae at low prey density, because it fed on an average of 1 and 2.7 pupae at densities of one and three whiteßies (Table 2; Fig. 2). But it was less efÞcient than D. tamaninii at high densities, not consuming ⬎7.5 pupae (Fig. 1). M. caliginosus was only able to eat an average of 0.2 whiteßy pupae when one pupa was offered, and it was not able to consume more than Þve pupae when whiteßy densities were high (Fig. 1). Functional Response with F. occidentalis as Prey. Equation 2 (type II functional response) produced the best Þt for the four predators tested. Estimates of attack coefÞcients and handling times for each predator and their signiÞcances are summarized in Table 2. As shown in Tables 3 and 4, there were no signiÞcant differences either in attack coefÞcients or in handling times among the four predators. At high prey densities, all predators fed similarly, consuming an average of more than nine second-instar larvae in 6 h. At a low prey density both anthocorid bugs were the best predators because they fed on an

average of 0.8 Ð 0.9 when only one thrips larva was offered (Fig. 2). Between–Prey Comparisons for Each Predator. We compared attack coefÞcients (Table 3) and handling times (Table 4) of each predator when feeding on whiteßy pupae versus thrips larvae. O. laevigatus was discarded for such comparisons because it had an attack coefÞcient not signiÞcantly different from zero with whiteßy as prey. Values of a did not depend on prey type species for any of the three predators evaluated (Tables 3 and 4). M. caliginosus and O. majusculus spent signiÞcantly more time handling whiteßies than thrips (Tables 2 and 4), whereas no such difference was found for D. tamaninii (Table 4).

Discussion For all predatorÐprey relationships analyzed, the type II functional response described the data well. This response is deÞned by two parameters, the attack coefÞcient (or instantaneous attack rate) and the handling time. The four predators tested had similar attack coefÞcients, ranging from 0.119 to 0.802, when feeding on each of the two prey species offered. Therefore, they had similar abilities to Þnd greenhouse whiteßy pupae as well as second-instar western ßower thrips. O. laevigatus, however, did not show a signiÞcant increase in consumption of whiteßies as prey density increased, suggesting that whiteßy pupae were not a suitable prey. For D. tamaninii feeding on Aphis gossypii Glover Þrst-instar nymphs, Alvarado et al. (1997) found a similar attack coefÞcient (a ⫽ 0.1014 hÐ1)

Table 3. Da values when comparing attack coefficients among predators preying on T. vaporariorum and F. occidentalis, and within predators for the two prey Species D. tamaninii M. caliginosus O. majusculus

T. vaporariorum

F. occidentalis

M. caliginosus

O. majusculus

M. caliginosus

O. majusculus

O. laevigatus

T. vaporariorum F. occidentalis

0.060 (NS)* Ñ Ñ

⫺0.617 (NS)* ⫺0.678 (NS)* Ñ

⫺0.020 (NS)* Ñ Ñ

0.569 (NS)* 0.590 (NS)* Ñ

0.212 (NS)* 0.233 (NS)* ⫺0.357 (NS)*

⫺0.065 (NS) ⫺0.025 (NS) ⫺0.114 (NS)

Comparisons involving O. laevigatus preying on T. vaporariorum were not made as the attack coefÞcient in this case was not statistically different from 0. (NS)* and (P)* are level of signiÞcance obtained after correcting by sequential Bonferroni technique.

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Table 4. DTh values when comparing handling times among predators preying on T. vaporariorum and F. occidentalis, and within predators for the two prey Species D. tamaninii M. caliginosus O. majusculus

T. vaporariorum

F. occidentalis

M. caliginosus

O. majusculus

M. caliginosus

O. majusculus

O. laevigatus

T. vaporariorum F. occidentalis

⫺0.847 (P ⬍ 0.01)* Ñ Ñ

⫺0.397 (P ⬍ 0.012)* 0.450 (NS)* Ñ

0.127 (NS)* Ñ Ñ

0.155 (NS)* 0.028 (NS)* Ñ

0.066 (NS)* ⫺0.0611 (NS)* ⫺0.0890 (NS)*

⫺0.168 (NS) ⫺0.888 (P ⬍ 0.02) ⫺0.089 (P ⬍ 0.001)

Comparisons involving O. laevigatus preying on T. vaporariorum were not made as the attack coefÞcient in this case was not statistically different from 0. (NS)* and (P*) are level of signiÞcance obtained after correcting by sequential Bonferroni technique.

under the same experimental conditions as in the current study. It is known that functional responses parameters depend on the experimental design (van Alphen and Jervis 1996). When determined experimentally, attack coefÞcient values are higher than those calculated with the Holling disc equation, because the resting time of the predator is included in the searching time. For example, by observation, Podisus maculiventris (Say) was shown to spend a larger proportion of time resting rather than searching (Wiedenmann and OÕNeil 1991). Therefore, it is important to complement the information obtained in the functional response experiments with continuous behavioral observations of the predatorÐprey relationship. In a previous experiment (Montserrat et al. 2000) we did this type of observation and we did not Þnd signiÞcant differences among M. caliginosus, D. tamaninii, and O.

majusculus in the time they spend resting when preying at low or at high densities of whiteßy pupae. However, because predators were allowed to leave the patch freely before ending the experiment, most D. tamaninii and O. majusculus did so, whereas M. caliginosus remained when low prey density. However, when predators are forced to remain in the patch, as in the current work, resting time may be considerably higher. Moreover, the attack rate could underestimate predator killing capacity, a more useful parameter for biological control purposes, because, when we continuously observed predators (Montserrat et al. 2000), they reencountered and ate dead prey that had been partially consumed, especially at low prey densities. This phenomenon may be observed when prey capture threshold coincides with the gut capacity and occurs with small or easy prey in which

Fig. 2. Functional response of predators when exposed to different densities of F. occidentalis second-instar larvae. Points are means ⫾ SE of observed values (N ⫽ 10, t ⫽ 6 h).

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predators consume less on each prey item as prey density increases (Sabelis 1992). Predators tested in this study did not differ in time spent handling second-instar larvae of F. occidentalis in accordance with Riudavets and Castan˜ e´ (1998) who did not Þnd differences in daily consumption values for these same four predators when they were fed ad libitum with thrips larvae. However, these predators differed in their ability to handle greenhouse whiteßy pupae, with D. tamaninii being signiÞcantly more efÞcient than M. caliginosus or O. majusculus. M. caliginosus spent 1 h 19 min handling fourth-instar nymphs of Myzus persicae (Sultzer) (Foglar et al. 1990), a time similar to that observed in the current study with whiteßy pupae, but just 36 min for adult females of Tetranychus urticae Koch (Foglar et al. 1990), and only 20 min for western ßower thrips larvae in the current study. Although whiteßy pupae are the size of a mite or thrips larvae, M. caliginosus spent the same time consuming whiteßy pupae than it did consuming an old aphid nymph, which is 2.5 times bigger. Some authors postulate that handling time is proportional to the size of the prey (Flinn et al. 1985), and therefore whiteßy pupae may have some physical characteristics that help them to resist predation. The harder tegument of whiteßy pupae in comparison with thrips larvae may make them less suitable for feeding on, except for D. tamaninii, which is larger than the other predators. Furthermore, this predator is equipped with more teeth on the mandibular stylet tips than the other predators (unpublished data), allowing it to hold the prey (Cohen 1996). As for attack coefÞcients, estimates of handling time from experimental data may be overestimated as they usually include resting periods. Because of its lower handling time, D. tamaninii showed a higher maximal intake of whiteßy pupae than M. caliginosus and O. majusculus and these two last predators showed a higher maximal intake when fed thrips than when fed whiteßy, also because of their lower handling times with thrips. A high handling time in a predator may be counterbalanced by increased longevity. This is the case for the anthocorid bugs tested, whose females show a longevity twice that of D. tamaninii when feed on F. occidentalis (Riudavets and Castan˜ e´ 1998). At low prey densities, D. tamaninii and O. majusculus consumed more prey than M. caliginosus. This apparent superiority of the two Þrst predators in prey consumption at low prey densities, however, may be meaningless in the Þeld if predators leave low prey density patches before attacking prey, as observed in behavioral studies for these two predatory species preying on greenhouse whiteßy pupae (Montserrat et al. 2000). In light of the functional response parameters estimated for the predators tested, several considerations may be done for their use in biological control. For greenhouse whiteßy control, D. tamaninii may be more efÞcient than M. caliginosus and O. majusculus as it had a lower handling time. This should be conÞrmed for whiteßy immature stages other than those tested in the current work. In addition, D. tamaninii increased

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prey consumption as density of whiteßy increased without reaching a plateau, whereas the other predators did not. This high prey consumption capacity is particularly important in predators like D. tamaninii, in which aggregative responses in high whiteßy density patches may be hypothesised from behavioral studies (Montserrat et al. 2000). The good perspectives for using D. tamaninii for whiteßy control concluded in these functional response experiments are conÞrmed by the successful whiteßy control with this predator in Þeld-cage experiments with cucumber (Gabarra et al. 1995). On the contrary, M. caliginosus does not seem to be a good candidate for whiteßy despite being widely used in European greenhouse vegetable crops for the control of this pest (Courbet and Maisonneuve 1999, Klapwijk 1999). From the high handling time calculated in the current work and its poor capacity to aggregate in high prey density patches (Montserrat et al. 2000) a slow control action on whiteßy populations may be expected. Although several Orius species have been reported to feed on whiteßies in the Þeld (Ekbom, 1981; Hagler and Naranjo 1994) the length of time spent by O. laevigatus and O. majusculus in consuming this prey may indicate that whiteßies are not a preferred prey, at least the pupal stage. For the control of F. occidentalis, no evidence has been obtained from the current functional response studies of which predator can be the optimal candidate. However, both anthocorid bugs showed higher, but not signiÞcant, attack coefÞcients and they also showed higher prey consumption than mirid bugs at low thrips densities. In fact, Orius spp. are known as specialized thrips predators (Fischer et al. 1992, Riudavets 1995, Nicoli and Tommasini 1996). Despite this, the usefulness of mirid bugs for thrips control cannot be neglected, especially in multiprey situations in which more than one prey must be controlled by biological control agents. The potential of D. tamaninii for F. occidentalis control in exclusion cages and in the greenhouse has been shown in cucumber crops (Gabarra et al. 1995, Castan˜ e´ et al. 1996). EfÞciency of M. caliginosus manipulating thrips larvae is a new aspect not yet described for this widely used polyphagous predator. Prey preference and switching behavior to feeding on the most abundant prey is an additional character to be considered when evaluating polyphagous predators for biological control in multipest agroecosystems. Although they are commonly released for the control of an speciÞc pest, all predators examined in the current study are polyphagous (Albajes and Alomar 1999) and there are no data in the literature that justify such a narrow use. Nothing is known about prey preference and switching behavior in the predators we studied, but the common enhancement of development rate and fecundity in heteropteran predators when they are fed multiprey diets (Toft 1995) may indicate that even in the case of strong preferences for one prey, it could be counterbalanced by the necessity to diversify the diet. More research focused on measuring overall searching efÞciency in multipatch and

October 2000


multiprey environments would be necessary to conÞrm such an hypothesis. It can thus be concluded that there are no differences in attack coefÞcients either among-predators or between-prey when the four predators were fed on whiteßy pupae or second-instar F. occidentalis larvae. On the contrary, there were differences in their handling times. D. tamaninii had a lower handling time than M. caliginosus and O. majusculus when preying on whiteßy pupae and the two latter predators spent more time handling whiteßy than thrips. When second-instar larvae of F. occidentalis were offered to the four predators considered, handling times were not different. Despite the current use of these predators in the biological control of a single pest, it can be expected that the four predators will consume the two prey species considered when naturally occurring in multiprey agroecosystems. In fact, they are abundant in several vegetable crops that have whiteßies and thrips as main pests (Riudavets and Castan˜ e´ 1998). Further research dealing with prey preference, switching behavior, and aggregative responses in high prey density patches should be undertaken for each predator. However, it can be concluded from the current functional response studies that D. tamaninii may be efÞcient in control of both greenhouse whiteßy and western ßower thrips, whereas M. caliginosus and both Orius species may be slower in controlling whiteßy but as efÞcient as D. tamaninii at controlling western ßower thrips. Acknowledgments We thank Robert N. Wiedenmann, Judit Arno´ , Oscar Alomar, and Javier Iriarte for their comments on an early draft, and Maurice W. Sabelis, Arne Janssen, Steven A. Juliano, and Jordi Moya-Laran˜ o for their helpful suggestions during the study. We also thank the helpful comments of two anonymous reviewers and the editor. The technical assistance of Pilar Herna´ndez, Victor Mun˜ oz, and Carmen Montero is also gratefully acknowledged. This research was funded by the Instituto Nacional de Investigacio´ n y Tecnologõ´a Agraria y Alimentaria (INIA), project N⬚ SC95Ð 052. M.M. was supported by a grant from the Ministerio de Educacio´ n y Cultura (MEC). Sam Elliot is also gratefully thanked.

References Cited Albajes, R., O. Alomar, J. Riudavets, C. Castan˜ e´, J. Arno´ , and R. Gabarra. 1996. The mirid bug Dicyphus tamaninii: an effective predator for vegetable crops. IOBC/WPRS Bull. 19: 1Ð 4. Albajes, R., and O. Alomar. 1999. Current and potential use of polyphagous predators, pp. 265Ð275. In R. Albajes, M. L. Gullino, J. C. van Lenteren, and Y. Elad [eds.], Integrated pest and disease management in greenhouse crops. Kluwer Academic, Dordrecht. Alomar, O., and R. Albajes. 1996. Greenhouse whiteßy (Homoptera: Aleyrodidae) predation and tomato fruit injury by the zoophytophagous predator Dicyphus tamaninii (Heteroptera: Miridae), pp. 155Ð177. In O. Alomar and R. N. Wiedenmann [eds.], Zoophytophagous Heteroptera: implications for life history and integrated pest man-

1081

agement. Entomological Society of America, Lanham, MD. van Alphen, J.J.M., and M. A. Jervis. 1996. Foraging behaviour, pp. 1Ð 62. In M. Jervis and N. Kidd [eds.], Insects natural enemies. Practical approaches to their study and evaluation. Chapman & Hall, London. Alvarado, P., O. Balta` , and O. Alomar. 1997. EfÞciency of four Heteroptera as predators of Aphis gossypii Glover and Macrosiphum euphorbiae (Thomas) (Hom.: Aphididae). Entomophaga 42: 215Ð226. Arzone, A., A. Alma, and S. Rapetti. 1989. Frankliniella occidentalis (Perg.) (Thysanoptera: Thripidae) nuovo Þtomizo delle serre in Italia. Inf. Fitopatol. 10: 43Ð 48. Castan˜ e´, C., O. Alomar, and J. Riudavets. 1996. Management of western ßower thrips on cucumber with Dicyphus tamaninii (Heteroptera: Miridae). Biol. Control 7: 114 Ð 120. Castan˜ e´, C., O. Alomar, and J. Riudavets. 1997. Biological control of greenhouse cucumber pests with the mirid bug Dicyphus tamaninii. IOBC/WPRS Bull. 20: 237Ð240. Castan˜ e´, C., J. Riudavets, and E. Yano. 1999. Biological control of thrips, pp. 244 Ð253. In R. Albajes, M. L. Gullino, J. C. van Lenteren, and Y. Elad [eds.], Integrated pest and disease management in greenhouse crops. Kluwer Academic, Dordrecht. Ceglarska, E. B. 1999. Dicyphus hyalinipennis Burm. (Heteroptera: Miridae): a potential biological control agent for glasshouse pests in Hungary. IOBC/WPRS Bull. 22: 33Ð36. Cohen, A. C. 1996. Plant feeding by predatory Heteroptera: evolutionary and adaptational aspects of trophic switching, pp. 1Ð17. In O. Alomar and R. N. Wiedenmann [eds.], Zoophytophagous Heteroptera: implications for life history and integrated pest management. Entomological Society of America, Lanham, MD. Courbet, S., and J. C. Maisonneuve. 1999. Biological pest control in greenhouses in France during 1998. IOBC/ WPRS Bull. 22: 37Ð 40. Ekbom, B. S. 1981. EfÞciency of the predator Anthocoris nemorum (Het: Anthocoridae) against the greenhouse whiteßy, Trialeurodes vaporariorum (Hom: Aleyrodidae). J. Appl. Entomol. 92: 26 Ð34. Fischer, S., C. Linder, and J. Freuler. 1992. Biologie et utilisation de la punaise Orius majusculus Reuter (Heteroptera: Anthocoridae) dans la lutte contre les thrips Frankliniella occidentalis Perg. et Thrips tabaci Lind. en serre. Rev. Suisse Vitic. Arboric. Hortic. 24: 119 Ð127. Flinn, P. W., A. A. Hower, and R.A.J. Taylor. 1985. Preference of Reduviolus americoferus (Hemiptera: Nabidae) for potato leafhopper nymphs and pea aphids. Can. Entomol. 117: 1503Ð1508. Foglar, H., J. C. Malausa, and E. Wajnberg. 1990. The functional response and preference of Macrolophus caliginosus (Heteroptera: Miridae) for two of its prey: Myzus persicae and Tetranychus urticae. Entomophaga 35: 465Ð 474. Gabarra, R., C. Castan˜ e´, and R. Albajes. 1995. The mirid bug Dicyphus tamaninii as a greenhouse whiteßy and western ßower thrips predator on cucumber. Biocontrol Sci. Technol. 5: 475Ð 488. Gomez-Menor, J. 1943. Contribucio´ n al conocimiento de los aleuro´ didos de Espan˜ a (Hem. Homoptera). 1 nota EOS. Madrid 19: 173Ð209. Hagler, J. R., and S. E. Naranjo. 1994. Determining the frequency of Heteropteran predation on sweetpotato whiteßy and pink bollworm using multiple ELISAs. Entomol. Exp. Appl. 72: 63Ð70.

1082


Hassell, M. P. 1978. The dynamics of arthropod predatorprey systems. R. M. May [ed.], Monographs in population biology, vol. 13. Princeton University Press, Princeton, NJ. Holling, C. S. 1966. The functional response of invertebrate predators to prey density. Mem. Entomol. Soc. Can. 48: 1Ð 86. Juliano, S. A. 1993. Nonlinear curve Þtting: predation and functional response curves, pp. 159 Ð182. In S. M. Scheiner and J. Gurevitch [eds.], Design and analysis of ecological experiments. Chapman & Hall, New York. Kareiva, P. 1990. The spatial dimension in pest-enemy interactions, pp. 213Ð227. In M. Mackauer, L. E. Ehler, and J. Roland [eds.], Critical issues in biological control. Intercept, Andover. Klapwijk, J. N. 1999. Biological control of tomato pests in The Netherlands. IOBC/WPRS Bull. 22: 125Ð128. Koskula, H., I. Va¨ nninen, and I. Lindqvist. 1999. The role of Macrolophus caliginosus (Het. Miridae) in controlling the twospotted spider mite in greenhouse tomato under North-European conditions. IOBC/WPRS Bull. 22: 129 Ð 132. McGregor, R. R., D. R. Gillespie, D.M.J. Quiring, and M.R.J. Foisy. 1999. Potential use of Dicyphus hesperus Knight (Heteroptera: Miridae) for biological control of pests of greenhouse tomatoes. Biol. Control 16: 104 Ð110. Messina, F. J., and J. B. Hanks. 1998. Host plant alters the shape of the functional response of an aphid predator (Coleoptera: Coccinellidae). Environ. Entomol. 27: 1196 Ð1202. Montserrat, M., R. Albajes, and C. Castan˜ e´. 2000. Comparative behaviour of three predators used in biological control in greenhouse crops. IOBC/WPRS Bull. 23: 267Ð272. Nedstam, B., and M. Johansson-Kron. 1999. Diglyphus isaea (Walker) and Macrolophus caliginosus Wagner for biological control of Liriomyza bryoniae (Kaltenbach) in tomato. IOBC/WPRS Bull. 22: 185Ð187. Nicoli, G., and G. Tommasini. 1996. Orius laevigatus. Info. Fitopatol. 4: 21Ð26.

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Rice, W. R. 1989. Analysing tables of statistical tests. Evolution 43: 223Ð225. Riudavets, J., R. Gabarra, and C. Castan˜ e´. 1993. Frankliniella occidentalis predation by native natural enemies. IOBC/ WPRS Bull. 16: 137Ð140. Riudavets, J. 1995. Predators of Frankliniella occidentalis (Perg.) and Thrips tabaci Lind.: a review. Wageningen Agric. Univ. Pap. 95: 43Ð 87. Riudavets, J., and C. Castan˜ e´. 1998. IdentiÞcation and evaluation of native predators of Frankliniella occidentalis (Thysanoptera: Thripidae) in the Mediterranean. Environ. Entomol. 27: 86 Ð93. Rogers, D. J. 1972. Random search and insect population models. J. Anim. Ecol. 41: 369 Ð383. Sabelis, M. W. 1992. Arthropod predators, pp. 225Ð264. In M. J. Crawley [ed.], Natural enemies: the population biology of predators, parasites and diseases. Blackwell, Oxford, UK. SAS Institute. 1989. Guide for personal computers, version 6. SAS Institute, Cary, NC. Toft, S. 1995. Value of the aphid Rhopalosiphum padi as food for cereal spiders. J. Appl. Ecol. 33: 552Ð560. Trexler, J. C., and J. Travis. 1993. Non-traditional regression analyses. Ecology 74: 1629 Ð1637. Waage, J. K. 1990. Ecological theory and the selection of biological control agents, pp. 135Ð157. In M. Mackauer, L. E. Ehler, and J. Roland [eds.], Critical issues in biological control. Intercept, Andover. Wiedenmann, R. N., and R. J. O’Neil. 1991. Laboratory measurement of the functional response of Podisus maculiventris (Say) (Heteroptera: Pentatomidae). Environ. Entomol. 20: 610 Ð 614. Wiedenmann, R. N., and J. W. Smith, Jr. 1997. Attributes of natural enemies in ephemeral crop habitats. Biol. Control 10: 16 Ð22. Received for publication 29 October 1999; accepted 20 June 2000.