DOI: 10.1111/j.1570-7458.2007.00647.x

Blackwell Publishing Ltd Predatory response of flavipes to bruchid pests of stored food

Sharlene E. Sing1* & Richard T. Arbogast2 1Department of Land Resources and Environmental Sciences, Montana State University, PO Box 173120, Bozeman, MT 59717-3120, USA, 2US Department of Agriculture–Agricultural Research Service (USDA-ARS), Center for Medical, Agricultural, and Veterinary Entomology, 1700 S.W. 23rd Drive, Gainesville, FL 32608, USA Accepted: 25 September 2007

Key words: predator, stored products, biological control, obtectus, analis, , , Zabrotes subfasciatus, Heteroptera, Anthocoridae, Coleoptera, Bruchidae

Abstract Biological control may provide an affordable and sustainable option for reducing losses to Bruchidae in stored food legumes, a crucial source of human dietary protein. Previous investigations have focused primarily on the role of in bruchid biological control, while the potential of generalist predators has been comparatively unexplored. The true bug Xylocoris flavipes (Reuter) (Heteroptera: Anthocoridae) exhibited a Type II functional response to the majority of cosmopolitan bruchid species evaluated when data were fit to Holling’s disc equation. A negative correlation was detected between mean pest species body weight and rate of predation. The rate of attack on adult prey was quite low but fairly consistent, with the larger-sized female predators generally more effective. The eggs and neonate larvae of Say (Coleoptera: Bruchidae) were the only accessible immature stages among all prey species examined; predation on A. obtectus eggs and larvae was higher than on any adult bruchids. Mean predator kill of A. obtectus immature stages was 40 first instars or 10–20 eggs per 24-h interval. Further investigation of the biological control potential of X. flavipes against pest Bruchidae is merited due to the predator’s ability to kill adult stages of all prey species evaluated.

significant bruchid genera (Rees, 1996, 2004; Keals et al., Introduction 1998). Callosobruchus maculatus, the most widely distributed Food legumes (), also known generically as pulses of the Callosobruchus species, is thought to be of African or dried , are an economically significant commodity origin, but has now become established in the Americas, (Cardona, 2004) and an important source of affordable the West Indian and Pacific Islands, the Mediterranean and accessible dietary protein (Smartt, 1990). Bruchids region, and Australia (Southgate, 1978; Hill, 2002). Calloso- (Coleoptera: Bruchidae) are responsible for the greatest chinensis, native to Asia, is similarly widespread post-harvest loss to stored legumes, directly through although it has not yet attained pest status in Central and consumption of the resource, and secondarily through the South America, Europe, or North Africa (Rees, 2004). The qualitative deterioration of the commodity or reduced seed origins of C. analis are unclear, as specimens reported to be stock viability (Southgate, 1979; Salunkhe et al., 1985). C. analis have routinely been found to be misidentified Callosobruchus maculatus (Fabricius), Callosobruchus C. maculatus (Southgate et al., 1957). Although Rees (2004) chinensis (L.), Callosobruchus analis (Fabricius), Acantho- reports its distribution as limited to South and South-East scelides obtectus Say, and Zabrotes subfasciatus (Boheman) Asia, Southgate (1978) suggests that C. analis probably arose are representative species of the three key economically in South-East Asia and India and later became established in Africa. Acanthoscelides obtectus and Z. subfasciatus are New World *Correspondence: Sharlene E. Sing, Department of Land Resources and Environmental Sciences, 334 Leon Johnson Hall, Montana State species thought to have originated in South and Central University, PO Box 173120, Bozeman, MT 59717-3120, USA. America (Hill, 2002). The geographical distribution of E-mail: [email protected] both species is now considered cosmopolitan (Southgate,

© 2008 The Authors Entomologia Experimentalis et Applicata 126: 107–114, 2008 Journal compilation © 2008 The Netherlands Entomological Society 107

108 Sing & Arbogast

1978; Hill, 2002). Zabrotes subfasciatus has not been reported functional response, which serves as a predictor of attainable from Asia or the Australasian region, and European records top-down, density-dependent regulation of a given pest are limited to Italy and Portugal (Southgate, 1978; Rees, 2004). species (Murdoch & Oaten, 1975). Published accounts of With the exception of A. obtectus, eggs of the species anthocorid functional response to stored product listed above are adhered to the outer testa of the host seed pests have thus far excluded evaluations of the predator’s during the oviposition process (Hill, 2002; Rees, 2004). potential to control bruchid prey (LeCato & Arbogast, This ovipositional exudate additionally functions as a 1979; Parajulee et al., 1994; Donnelly & Phillips, 2001). fairly impenetrable protective coating once it becomes In LeCato & Arbogast (1979), the functional response of hardened (Southgate, 1979). Hatching larvae do not wander X. flavipes to the eggs and early instars of the Angoumois but bore directly into the host seed where all development grain moth, Sitotroga cerealella (Olivier), indicated a is completed. In contrast, A. obtectus eggs are deposited preference for larval prey; the authors suggested that prey loosely throughout the bulk of stored host seeds leaving stage preference was linked to the predator’s stimulation by eggs and first instars susceptible to mortality by predation the movement and the small size of the larval prey. Adult and desiccation until the enters a host seed (Howe & bruchids capable of actively avoiding or defending against Currie, 1964; Hill, 2002). attacks might be considered ‘difficult prey’ for no other Surface and fumigant chemical applications are thought reason than their considerable body size advantage. to be the most effective methods for managing bruchid However, X. flavipes is known to attempt and persist in infestations, especially for large scale or extended storage attacking non-preferred prey species/stages when faced (Rahman, 1990; Visarathanoth et al., 1990; Cardona, 2004; with starvation if preferred prey was unavailable (LeCato, Mbata, 2004). Prohibitive costs and the risk of adverse 1976). Larval A. obtectus may similarly avoid or defend secondary effects from such treatments have necessitated against X. flavipes attack, but lacking the armature or the exploration of alternative control measures, such as mass of adult bruchids might in fact attract predators as biological control, and the adoption of a more integrated ‘stimulating prey’ through their defensive behavior. Egg management approach (Brower et al., 1996; Abate et al., prey provides neither resistance nor stimulation to predators; 2000; Adebowale & Adedire, 2006). although this stage might be categorized as ‘easy prey’, it Xylocoris flavipes (Reuter) (Heteroptera: Anthocoridae) does require predator initiative to be recognized as such. is a cosmopolitan predator of multiple species and stages of Functional response is an appropriate way to characterize stored product pests (Arbogast, 1979), although it is most the interaction of X. flavipes with a number of different successful against small-sized, externally developing prey, bruchid prey species and stages in a highly simplified particularly accessible eggs and early larval stages that are environment. The objectives of this study were first to neither heavily sclerotized nor overly hirsute (LeCato & substantiate observational reports that this predator could Davis, 1973). Researchers have determined that X. flavipes kill adult bruchids, and then to determine in the context of is largely ineffective in predating upon the larval stages of functional response, if male and female X. flavipes predated stored product pests, such as bruchids, that typically at different rates on the adults of the various bruchid develop within seeds (Arbogast, 1979, but see Donnelly & species listed above. Phillips, 2001). Records of specific associations between X. flavipes and bruchid prey are limited. Xylocoris flavipes Materials and methods has reportedly been collected from legumes infested by Bruchidius incarnatus Boh. and Bruchus rufimanus Boh. Bruchid prey in Egyptian storage facilities, although both species are Bruchids used in this study were obtained from continuous regarded primarily as field crop rather than storage pests cultures maintained at the Stored-Product Research (El-Nahal et al., 1985). Xylocoris flavipes has also been and Development Laboratory (SPIRDL), Savannah, GA, recovered from imported , Vigna unguiculata (L.) USA. The A. obtectus, Z. subfasciatus, C. analis, and Walp., by the US Department of Agriculture Insect C. chinensis cultures were started in 1981 from specimens Identification and Parasite Introduction Research Branch, provided by the Pest Infestation Control Laboratory, Beltsville, MD, although no record of the specific prey is Slough, Bucks, UK, while the C. maculatus culture originated given (Jay et al., 1968). from US Department of Agriculture–Agricultural Research Functional response characterizes the relationship Service (USDA-ARS) research laboratories in Fresno, CA, between the number of prey consumed by individual USA. Food legumes used in all bruchid cultures were predators and the density of available prey (Solomon, purchased locally and certified as organically produced. 1949; Holling, 1959a,b). The potential biocontrol efficacy Bulk 11.4 kg bags of black-eyed /cowpea (V. unguiculata), of candidate agents can be extrapolated by quantifying white navy ( L.), and garbanzo

Predatory response of Xylocoris flavipes 109 bean/ (Cicer arietinum L.) were disinfested in cold treatments: control (no predators – to determine naturally storage at –17.8 °C for at least 2 weeks (Johnson & occurring mortality during the experiment), one male Valero, 2003), then acclimated before use in a walk-in predator, or one female predator. Arenas were inspected at environmental growth chamber at 29 ± 2 °C, 65 ± 5% r.h., 24-h interval over the 72 h duration of the experiment. the controlled conditions used for both culture maintenance During each inspection, the number of dead prey was and all experiments. Environmental equilibrium was verified recorded then replaced with 0–24-h-old live prey to maintain by repeated dry weight determination of grain the level of available live prey per observation interval. moisture content. Adult bruchids of a known age (0–24 h) were obtained Predatory response of to immature stages of by sifting the contents of culture jars in a US Standard no. Acanthoscelides obtectus 6 sieve 24 h after an initial sifting that had removed all Experiments assessing the functional response of X. flavipes previously emerged adults. Individual adult bruchids were to the egg and larval stages of A. obtectus egg and larval sexed according to authoritative keys (Southgate et al., prey followed the protocol described above, except that 1957; Southgate, 1958; Halstead, 1963), then collected and experiments were terminated after 24 h. Prey densities used retained in male:female (1:1) pairs in 18.3-ml plastic shell were 5, 10, 15, 20, or 50 individual eggs or larvae, subjected vials (7 × 2.5 cm in diameter). to the same three predator treatments listed above. The Acanthoscelides obtectus eggs used in the present study experimental assessment of the functional response of were 0–24 h old, gathered from oviposition jars fitted with X. flavipes to all prey species/stages was performed twice in screened platforms that allowed eggs to drop through to entirety. Petri dishes positioned below. Acanthoscelides obtectus larvae were collected from Petri dishes where newly Statistical analyses collected eggs were retained until hatching occurred, Data were fitted to models representing a characteristic generally 96–120 h after oviposition. Type I (Na = aTN), II [Na = aTN/1 + (aThN)], or III {Na = N[1 – e–a(T – NaTh)]} functional response (Holling, 1959a,b) Predators using PROC NLIN (SAS Institute, 2004).

Predators used in this study were obtained from a continuous Models were then parameterized, with Na as the number culture of X. flavipes originating from specimens collected of prey killed, T as the duration of prey exposure to the in 1977 from a population that had self-infested an predator(s), N as the initial density of prey, a as the experimental warehouse facility at SPIRDL. Predators were instantaneous rate of discovery (‘attack rate’), and Th reared under the environmental conditions stated above in indicating the length of time prey were handled by the 3.78-l glass jars outfitted with Hexcel® (Dublin, CA, USA) predator (handling time). PROC NLIN (SAS Institute, paperboard harborage and provisioned with previously 2004) was used to discriminate contributions of predator frozen then thawed Plodia interpunctella (Hübner) eggs. sex and prey density to total variation observed in the Culture jars were cleared of all adult predators and number of bruchids killed. experimental subjects were then collected from the pool of newly emerged adults 0–6 days after the initial sorting. Results Subjects were sexed according to Arbogast et al. (1971) and retained individually in gelatin capsules. Preliminary analyses indicated that the coefficients of determination (r2 values) for X. flavipes’ Type I, II, and III Predatory response of Xylocoris flavipes to adult bruchid prey functional responses to bruchid prey were similar (Table 1), Experimental arenas consisted of glass Petri dishes, 9.0 cm a trend also reported in Donnelly & Phillips (2001). However, in diameter. Liquid Teflon® (Wilmington, DE, USA) was although similar, the r2 value for Type I functional applied to the interior walls of each arena and allowed to response was consistently lower than that reported for cure for a minimum of 24 h in a fume hood before use; this Type II within the same predator sex/bruchid species prey was a prophylactic treatment to prevent the potential escape stage combination. Furthermore, we found that fitting the of experimental subjects. A fine mesh nylon fabric circle data to a Type III functional response equation resulted in was placed on the bottom of each arena to ensure that the a negative, essentially biologically untenable parameter prey remained accessible to X. flavipes, which experienced value for Th, the length of time prey was handled by the difficulty walking on the smooth glass surfaces of the predator. We therefore concluded that the functional arenas. Five replicates of 1, 2, 3, or 4 male:female (1:1) response of both sexes of X. flavipes to most bruchid prey adult prey pairs were added to each arena. Sixty arenas in species and stages evaluated was generally best described total per bruchid species were exposed to one of three by the Type II Holling’s disc equation.

110 Sing & Arbogast

Table 1 Coefficients of determination (r2) for fit of Type I, II, and relative contribution of the sexes to prey suppression III functional response curves to male or female Xylocoris flavipes (Donnelly & Phillips, 2001). An evaluation of the contribu- predation on bruchid prey tion of prey density, predator sex, and their interaction to variation observed in the functional response of X. flavipes Functional to bruchid prey confirmed that the difference was significant response equation Bruchid prey Prey Predator in the number of prey attacked due to predator sex, for all species stage sex Type I Type II Type III prey species/stages evaluated, other than for A. obtectus A. obtectus Adult Female 0.5663 0.6376 0.8266 larval prey (Table 3). A. obtectus Adult Male 0.5253 0.6073 0.7708 The immature stages of A. obtectus were readily attacked A. obtectus EggFemale 0.8973 0.9446 0.9016 by both sexes of X. flavipes. Handling times of egg prey A. obtectus EggMale 0.6711 0.8524 0.7330 were considerably different for the two predator sexes, but A. obtectus Larva Female 0.9516 0.9612 0.9531 not for larval prey (Table 2). Acanthoscelides obtectus eggs A. obtectus Larva Male 0.9716 0.9824 0.9720 were more heavily predated upon by female X. flavipes at C. analis Adult Female 0.8321 0.8730 0.9213 the two highest densities evaluated (Figure 1, Table 4). The C. analis Adult Male 0.6995 0.7195 0.8807 active neonate larvae were attacked by both predator sexes C. chinensis Adult Female 0.8244 0.8544 0.9114 at a more equivalent (Table 3) and higher rate (Table 4) C. chinensis Adult Male 0.4950 0.5426 0.8957 than A. obtectus eggs. When the difference in predation by C. maculatus Adult Female 0.7559 0.7575 0.9430 the two sexes was evaluated at each adult prey density level, C. maculatus Adult Male 0.5772 0.5869 0.8642 Z. subfasciatus Adult Female 0.8192 0.8433 0.9160 variation in the mean number of kills was found to be Z. subfasciatus Adult Male 0.5667 0.5764 0.8771 statistically and consistently significant only for Z. subfasciatus and C. chinensis, the two smallest bruchid species (Table 5).

The attack rates for both predator sexes against bruchid Discussion prey were comparable within prey species/stage groupings (Table 2). However, the reported parameter estimates Although most predators attack the largest available indicate that prey handling time for the larger-sized female individuals of their prey species, those species are predators was consistently lower than for the smaller male generally smaller in body size than the predator. Predatory X. flavipes (Table 2). Adult X. flavipes are sexually dimorphic are known to be an exception to these limiting in body size, with gravid females averaging 2.55 mm in predator:prey relative body size ratios, because maximum length compared to 1.93 mm for males (Arbogast et al., prey size can be increased through the use of venoms, traps, 1971); previous studies have detected a difference in the or group hunting (Sabelis, 1992). The results of the present

Table 2 Parameter estimates for the functional response of Xylocoris flavipes to bruchid prey according to predator sex and prey species/stage

2 Bruchid prey species/stage Predator sex Attack rate (a) Handling time (Th)r A. obtectus eggs Female 0.0457 ± 0.0046 0.5318 ± 0.0696 0.9446 A. obtectus eggs Male 0.0597 ± 0.0147 1.8877 ± 0.2332 0.8524 A. obtectus larvae Female 0.0464 ± 0.0037 0.1775 ± 0.0434 0.9612 A. obtectus larvae Male 0.0467 ± 0.0025 0.1885 ± 0.0290 0.9824 A. obtectus adults Female 0.0457 ± 0.0709 27.3858 ± 8.1259 0.6376 A. obtectus adults Male 0.0219 ± 0.0318 48.7082 ± 15.9215 0.6073 C. analis adults Female 0.0326 ± 0.0117 7.4750 ± 2.0196 0.8730 C. analis adults Male 0.0214 ± 0.0130 13.0739 ± 5.3581 0.7195 C. chinensis adults Female 0.0270 ± 0.0104 8.8910 ± 2.6229 0.8544 C. chinensis adults Male 0.0244 ± 0.0330 31.2443 ± 12.5168 0.5462 C. maculatus adults Female 0.0080 ± 0.0007 n/a1 0.7559 C. maculatus adults Male 0.0157 ± 0.0143 24.4738 ± 11.5153 0.5869 Z. subfasciatus adults Female 0.0224 ± 0.0084 7.8998 ± 2.9303 0.8433 Z. subfasciatus adults Male 0.0077 ± 0.0055 19.8166 ± 16.1709 0.5764 1Data for female predator’s functional response to adult Callosobruchus maculatus fitted to Type II model yielded a negative handling time; data were therefore fit to Type I model. Predatory response of Xylocoris flavipes 111

Table 3 Contribution of prey density, predator sex, and the with daily ingestion rate and gut capacity; the nutritional interaction of prey density and predator sex to total variation resources of large prey generally exceed the daily food observed in functional response of Xylocoris flavipes to requirements of small predators (Peters, 1983). Predation bruchid prey of additional adult bruchids in experimental arenas may also have been reduced due to return feeding on the readily Source d.f. F P>F apparent previous kills. A. obtectus – egg stage Xylocoris flavipes killed significantly more ‘stimulating’ Prey density 5,108 61.62 <0.0001 larval prey than ‘easy’ egg prey, reiterating earlier results Predator sex 1,108 52.09 <0.0001 (LeCato & Arbogast, 1979; Russo et al., 2004). The functional Prey density*predator sex 5,108 13.96 <0.0001 response of the predator to both the egg and larval stages A. obtectus – larval stage of A. obtectus indicates that X. flavipes has potential as a Prey density 5,108 304.71 <0.0001 biological control agent of this particular bruchid species. Predator sex 1,108 0.00 0.9580 Prey density*predator sex 5,108 0.04 0.9990 Predation on adult A. obtectus may have been confounded A. obtectus – adults by the presence of eggs freshly oviposited by the experimental Prey density 3,72 0.71 0.5505 subjects. Predator sex 1,72 9.88 0.0024 The potential of a ‘knock down’ or disorientation effect Prey density*predator sex 3,72 0.12 0.9509 from the scent-gland secretion (Phillips et al., 1995) com- C. analis – adults bined with the catastrophic disruption of neuromuscular Prey density 3,72 6.76 0.0004 function (Blum, 1981) caused by the injection of salivary Predator sex 1,72 20.17 <0.0001 venom could account for the predator’s ability to kill the Prey density*predator sex 3,72 4.34 0.0072 comparatively more ‘difficult’ adult bruchid prey. Howe & C. chinensis – adults Currie (1964) list the mean body weights of all bruchid Prey density 3,72 3.21 0.0280 species discussed here; results of the current study indicate Predator sex 1,72 37.22 <0.0001 Prey density*predator sex 3,72 1.41 0.2477 that highest rate of predation occurred with the lightest C. maculatus – adults weight species, Z. subfasciatus and C. chinensis, and decreased Prey density 3,72 9.84 <0.0001 with increasing mean body weight of the heaviest prey Predator sex 1,72 7.35 0.0084 species, A. obtectus, C. analis, and C. maculatus. Additionally, Prey density*predator sex 3,72 2.42 0.0726 observation of predator interaction with mated pairs of Z. subfasciatus – adults bruchid prey indicated a high level of mating and oviposi- Prey density 3,72 6.67 0.0005 tion disruption, and opportunistic predation on bruchids Predator sex 1,72 48.81 <0.0001 engaged in copulation (SE Sing, pers. obs.) indicates that Prey density*predator sex 3,72 2.89 0.0413 presence of X. flavipes in the bruchid–grain legume complex may significantly impact prey populations. study indicate that X. flavipes is capable of low level but fairly consistent success in killing its larger adult bruchid prey. Stimulated X. flavipes direct a scent-gland exudate thought to be defensive in nature over a wide area (Remold, 1963). Phillips et al. (1995) determined that the terpene constituents of this secretion, particularly α-terpineol and linalool, have significant toxic activity against adult Tribolium castaneum (Herbst) and Oryzaephilus surinamensis (L.), with the potential mode of toxicity being competitive inhibition of acetylcholinesterase. Furthermore, the consistent rapid liquefaction of large adult bruchid prey after attack by X. flavipes (SE Sing, unpubl.) suggests that the predator utilizes an enzymatic salivary venom for extraoral digestion, a common strategy of predaceous arthropods preying on large prey with intractable cuticles Figure 1 Predation on Acanthoscelides obtectus eggs within (Cohen, 1995). Finally, the low level of X. flavipes predation a 24-h period by Xylocoris flavipes adults as a function of prey on adult bruchids can be explained not only by the greater density, -, female predator, -, male predator. Lines plotted challenge to subdue large prey, but is also correlated are Holling’s disc equation fitted to the data. 112 Sing & Arbogast

Table 4 Female or male Xylocoris flavipes mean kill by density of Acanthoscelides obtectus eggs and larvae per 24-h exposure period

Prey density Kills by female X. flavipes Kills by male X. flavipes Prob>|T| A. obtectus – eggs 2 1.6500 ± 0.2115 1.7500 ± 0.1951 0.7322 5 4.4800 ± 0.3384 4.4800 ± 0.2286 1.0000 10 8.7800 ± 0.5546 6.8800 ± 0.0171 0.1183 15 10.8800 ± 1.7308 7.3800 ± 0.8475 0.0860 20 16.2900 ± 1.4534 10.1900 ± 1.2543 0.0052 50 24.5000 ± 1.0462 10.2000 ± 1.6111 <0.0001 A. obtectus – larvae 2 1.6000 ± 0.2000 1.8000 ± 0.0000 0.3306 5 4.5000 ± 0.4000 4.9000 ± 0.0000 0.3306 10 9.9200 ± 0.0067 9.8200 ± 0.1024 0.3306 15 14.8500 ± 0.1012 14.8500 ± 0.0989 1.0000 20 19.9600 ± 0.0000 19.7600 ± 0.2000 0.3306 50 39.3000 ± 3.1342 38.8000 ± 2.0645 0.8955 Prob>|T|, probability of a greater absolute value of t when the null hypothesis that the means of the two groups are equal.

The results of our analyses indicate that the percentage dynamics, the theoretical hallmark of pest population of adult bruchid prey attacked by X. flavipes decreased as regulation through biological control, would not be attained prey availability increased, typifying a Type II density- following the release of X. flavipes in food legume storage independent functional response. We would therefore facilities pest. However, Schenk & Bacher (2002) state that expect that an equilibrium in predator:prey population evaluations performed under restrictive conditions (cages;

Table 5 Female or male Xylocoris flavipes mean kill by density of adult bruchids per 24-h exposure period

Prey density Kills by female X. flavipes Kills by male X. flavipes Prob>|T| A. obtectus – adults 2 0.6333 ± 0.1356 0.3000 ± 0.1048 0.0676 4 0.7000 ± 0.2015 0.4333 ± 0.1000 0.2513 6 0.8333 ± 0.2003 0.5333 ± 0.1133 0.2088 8 0.7667 ± 0.1928 0.3333 ± 0.0994 0.0611 C. analis – adults 2 0.9333 ± 0.1556 0.7667 ± 0.1795 0.4919 4 1.5333 ± 0.1587 0.9667 ± 0.2191 0.0507 6 2.3333 ± 0.1405 0.8333 ± 0.1667 <0.0001 8 1.8333 ± 0.2992 1.5000 ± 0.2447 0.3998 C. chinensis – adults 2 0.9000 ± 0.1117 0.4667 ± 0.1237 0.0181 4 1.3000 ± 0.1606 0.5333 ± 0.1423 0.0022 6 1.5667 ± 0.2724 0.7333 ± 0.2096 0.0261 8 1.8000 ± 0.2061 0.6000 ± 0.2155 0.0008 C. maculatus – adults 2 0.4000 ± 0.1089 0.5667 ± 0.1495 0.3794 4 0.7667 ± 0.1795 0.5333 ± 0.1133 0.2862 6 0.9667 ± 0.1160 0.3333 ± 0.1721 0.0069 8 1.6667 ± 0.2981 1.0333 ± 0.1753 0.0837 Z. subfasciatus – adults 2 0.6333 ± 0.1444 0.3667 ± 0.1356 0.1951 4 1.5333 ± 0.1507 0.3667 ± 0.1356 <0.0001 6 1.4000 ± 0.1778 0.5667 ± 0.1575 0.0025 8 1.8000 ± 0.2685 0.7000 ± 0.1528 0.0022 Predatory response of Xylocoris flavipes 113 single prey species) routinely indicate a Type II functional Blum MS (1981) Chemical Defenses of Arthropods. Academic response in generalist insect predators. Van Lenteren & Press, New York, NY, USA. Bakker (1976) and van Alebeek et al. (1996) suggest that Brower JH, Smith L, Vail PV & Flinn PW (1996) Biological control. the constraints of experimental design might actually Integrated Management of Insects in Stored Products (ed. by obfuscate the true nature of the functional response curve B Subramanyam & DW Hagstrum), pp. 223–286. Marcel Dekker, New York, NY, USA. in the context of invertebrate predators, specifically citing Cardona C (2004) Common beans: Latin America. Crop Post- how in a confined arena the increased chance of prey Harvest: Science and Technology, Vol. 2, Durables (ed. by RJ discovery might exaggerate the steepness of the response Hodges & G Farrell), pp. 145–150. Blackwell Scientific, Ames, curve at the lowest prey densities. 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