Journal of Chemical Ecology, Vol. 7, No. 5, 1981
MITE PREDATOR RESPONSES TO PREY AND PREDATOR-EMITTED STIMULI
R O B E R T G. HISLOP and R O N A L D J. P R O K O P Y Department of Entomology, University of Massachusetts, Amherst, Massachusetts 01003 (Received October 28, 1980; revised January 12, 1981) Abstract--We found that the searching behavior of two acarine predators,
Amblyseius fallacis and Phytoseiulus macropilis, for prey, Tetranychus urticae, is affected by the following stimuli: (1) prey silk and associated feces, whose combined physical and chemical properties elicit reduction in the rate of predator movements and longer halts; (2) kairomone extracted from prey silk and associated feces, which, upon contact, elicits frequent predator return to prey-inhabited locales; and (3) predator-emitted marking pheromone, which elicits shorter duration of search in presearched prey locales. We also found that treatment of filter paper with prey kairomone or silk enhanced predator location of prey eggs, leading us to speculate that application of synthetic prey kairomone could be useful in pest management programs. Key Words--Kairomone, silk, marking pheromone, host finding, Am-
blyseius fallacis, Phytoseiulus macropilis, Tetranychus urticae.
INTRODUCTION
Amblyseiusfallacis (Garman) and Phytoseiulus macropilis (Banks) (Acarina: Phytoseiidae) are important predators of spider mites, especially Tetranychus urticae Koch. A. fallacis occurs in northeastern U.S. commercial apple orchards (Croft, 1975), while P. macropilis is undergoing experimentation in greenhouse integrated mite control programs in Florida (Hamlen, 1980). Although reports exist describing various aspects of the biology (Ballard, 1954; Prasad, 1967; McClanahan, 1968; Smith and Newsom, 1970a, b; Rock et al., 1976; Johnson and Croft, 1976; Shih et al., 1979; Hamlen, 1978, 1980) and pesticide resistance (Motoyama et al., 1970; Croft and Nelson, 1972; Hislop and Prokopy, 1981) of these predators, the role of kairomones and marking pheromones in A. fallacis or P. macropilis host searching behavior 895 0098/0331/0900-089550.300/09 1981PlenumPublishingCorporation
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HISLOP AND PROKOPY
has received little attention. This is true as well for most other predatory mites, notable exceptions being the work of Farish and Axtell (1966) and Jalil and Rodriguez (! 970) demonstrating the role of kairomones in attraction to prey of predacious mites of the families Machrochelidae and Uropodidae. In spring, A. fallacis is normally associated with T. urticae, a preferred prey in the orchard understory. In summer, this predator migrates into the trees in search of additional prey, often borne there by wind currents (Johnson and Croft, 1976). In the greenhouse, P. macropilis does not usually migrate over long distances in search of new prey but instead tends to remain in close proximity to existing prey. In a related species, P. persimilis Athias-Henriot, Mori and Chant (1966) demonstrated changes in predation behavior as a function_of humidity and starvation level. Several factors may influence arthropod predator searching behavior leading to contact with prey: physical substrate characteristics; temperature, humidity, and starvation level (Rasmy and E1-Banhawy, 1974, Elsey, 1974; Blommers et al., 1977); and prey silk (Schmidt, 1976; Ohnesorge, 1978). Here we examine for the first time two sorts of factors influencing the host searching behavior of A. fallacis and P. macropilis (A. fallacis was examined in greater detail because of its importance in our apple integrated pest management program): (1) physical and kairmonal cues emitted by T. urticae, and ('2) predator-emitted stimuli influencing duration of search in presearched areas. M E T H O D S AND MATERIALS
A.fallacis was collected in Massachusetts apple orchards and cultured in the laboratory on lima bean leaves infested with T. urticae. P. macropilis was obtained from a colony at the University of Massachusetts Suburban Experiment Station in Waltham. ; For collection and bioassay of prey silk, hundreds of T. urticae were brushed from bean leaves onto 12-cm-diam glass plates using a mite brushing machine (Henderson and McBurnie, 1943). Pieces of bean leaves ca. 2 cm diam were placed around the edges of each plate to collect the dispersing mites. Leaf pieces containing 300-500 mites were placed individually under 2-cm-diam glass rings for 24 hr, after which the leaf and all mites were removed. Silk spun by the mites across the ring hole was gathered on a 1.5-cm-diam filter paper disk by passing the disk through the ring. After manual removal of eggs and debris from the silk, each disk was bioassayed for predator response. Because we were unable to remove prey feces from the silk, our terminology for silk throughout this paper includes the element of associated prey feces. For collection and bioassay of kairomone, each of several 12-cm-diam glass plates containing thousands of T. urtieae brushed from bean leaves was
MITE PREDATOR RESPONSES TO PREY AND PREDATOR-EMITTED S T I M U L I
897
placed in a petri dish, over which was positioned an acetate cone (12 cm bottom diam, 2 cm top diam). Each was then placed under a fluorescent light, which attracted the mites to the top of the cone. After 24 hr, the mites were removed and the silk was gathered by passing a 1.5-cm-diam preweighed (on a Cahn electrobalance) filter paper disk through the hole in the top of the cone. After manual removal of eggs and debris, the filter paper and silk were weighed and placed into 1 ml of solvent. After 24 hr, the filter paper was removed and the extract centrifuged at 10,000 rpm for 30 min. Final extract concentration was 0.1 mg silk/ml solvent. We used the following four solvents: water, methanol, chloroform, and hexane. Because preliminary assays proved the methanol extract to contain the most active kairomonal components, this extract was chosen for use in the assays reported here. The assays were conducted in the following manner. One 1.5-cm-diam filter paper disk left untreated (= a control) or containing either silk, 0.02 ml methanol extract of silk (= kairomone), or methanol (= a control) was placed in the center of a 5-cm-diam glass arena surrounded by water to prevent emigration of predators. The surface of the water was ca. 2 mm below the surface of the glass arena. One A.fallacis or P. macropilis female, starved for 6-8 hr, was placed at the arena edge and allowed to enter the disk at will. Bioassay periods lasted for 90 sec (silk) or 6 min (kairomone) following initial predator contact with the disk. Speed of movement (A. fallacis only) was obtained by analyzing the path of predator movement traced for the first 90 sec onto a piece of clear acetate taped to a magnifying glass to enlarge the image. Visual interference of the tracing movements with predator activity was eliminated by reflecting the predator image off two mirrors prior to image magnification. Tracing was performed in dim light to avoid back-reflection. Influence of prey-emitted stimuli on A. fallaeis predation efficieney was determined by placing a single T. urticae egg midway between the edge and center of a 0.5-cm-diam filter paper disk containing either prey silk, 0.01 ml of methanol solution of kairomone, or methanol alone (= control). The percentage of predators which consumed an egg in a 5-min time period was compared among treatments. The average time A. fallacis remained on or within 1 cm of each disk following prey consumption was also measured. P. macropilis was not tested. In examining factors influencing duration of predator searching in presearched areas, we assayed females ofA. fallacis and P. macropilis which had been placed in contact prior to assay with a filter paper disk containing prey silk. In the assay, a filter paper disk (0.5 cm diam) containing T. urtieae silk was placed in the center of a glass arena. A single predator was introduced and allowed to enter the disk at will. We measured the following: (1) duration of first visit to (within 1 cm of) a disk not previously visited by a predator (= control disks); and (2) duration of first visit to (within 1 cm of) a disk previously searched for ca. 30-40 min prior to assay by 5 conspecific predators.
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All experiments were performed under conditions of ca. 24 + 2 ~ C and 70 _ 10% relative humidity. D a t a were submitted to analysis of variance and D u n c a n ' s multiple range test or a paired t test at the 5% level.
RESULTS
Influence of Prey Silk on Searching Behavior. A. fallacis females spent a significantly greater a m o u n t of time per visit on disks having fresh or 14-dayold prey silk and associated feces than on control disks. Also, the average duration of stops was significantly greater, and the walking speed significantly less, on the silk disks t h a n on the controls (Table 1). These data suggest that fresh as well as 14-day-old T. urticae silk has physical a n d / o r chemical properties which stimulate searching A.fallacis females to walk more slowly and stop longer within areas of prey habitation. Influence of Prey Kairomone on Searching Behavior. The average time spent between A. fallacis visits to disks treated with fresh, 3-day-old, or 7-day-old extract of silk and associated feces was significantly less than the time between visits to control disks (Table 2). A. fallacis returned to treated disks at an average turning angle of 148~ c o m p a r e d with 97 ~ for the controls. In similar fashion, P. maeropilis returned to disks treated with fresh silk extract in significantly less time (15.3 sec) than to control disks (40.5 sec) (20 replicates). These data clearly demonstrate that a k a i r o m o n e is present in the extract which stimulates A. fallacis and P. maeropilis females to return to extract disks and that k a i r o m o n a l activity (for A. fallacis) is present for at least 7 days. In contrast to when k a i r o m o n e was present together with silk (Table 1), the average duration of visits and stops (A.fallacis) on silk extract disks was no different f r o m controls, a l t h o u g h the speed of m o v e m e n t was significantly less than on the controls (Table 2). Figure 1 shows a typical A. fallacis search pattern on silk, silk extract, and methanol control disks.
TABLE 1. INFLUENCEOF T. urticae SILK AND ASSOCIATED FECES ON A.fallacis SEARCHING BEHAVIOR (20 REPLICATES/TREATMENT)
Disk type
Avg. duration of visit (sec)a
Avg. time betweenvisits (see)
Avg, duration of stops on disk (see)
Avg. walking speed on disk (cm/sec)
Fresh silk 14-day-old silk Untreated
42.5 a 57.0 a 12.2 b
11.8 a 14.0 a 24.5 a
12.2 a 16.3 a 0.4 b
0.12 a 0.15 a 0.29 b
aMeans in each column followed by a different letter are significantly different at the 0.05 level.
899
MITE PREDATOR RESPONSES TO PREY AND PREDATOR-EMITTED STIMULI TABLE 2. INFLUENCE OF METHANOL EXTRACT OF T. urticae SILK AND ASSOCIATED FECES (=KAIROMONE) ON .4. fallacis SEARCHING BEHAVIOR (20 REPLICATES/TREATMENT)
Disk type
Avg. duration of visit (sec)a
Avg. time between visits (sec)
13.2 a 14.2 a 10.9 a 9.9 a
33.0 a 33.7 a 28.0 a 66.5 b
Fresh extract 3-day extract 7-day extract Methanol
Avg. duration of stops on disk (sec) 0 0 0.I 0.1
a a a a
Avg. walking speed on disk (cm/sec) 0.20 a 0.19 a 0.18 a 0.24 b
aSee footnote a of Table 1.
D a t a on the influence of visit sequence on A. fallacis r e s p o n s e to silk e x t r a c t a n d c o n t r o l disks are given in T a b l e 3. F o r the first three visits, the r e t u r n time to silk e x t r a c t disks was significantly s h o r t e r t h a n the r e t u r n time to c o n t r o l disks. F o r visists 4 - 6 a n d 7 - 9 there was no significant difference b e t w e e n t r e a t m e n t s in r e t u r n time. N o r was there at a n y time a significant difference between t r e a t m e n t s in average d u r a t i o n o f visits. Initial r e t e n t i o n time (i.e., time over which A. fallacis was r e t a i n e d within 1 cm o f a t r e a t m e n t disk f o l l o w i n g the first visit) was significantly l o n g e r on disks t r e a t e d with fresh, 3 - d a y - o l d , a n d 7 - d a y - o l d silk e x t r a c t (51.0, 69.6, a n d 63.0 see, respectively) t h a n on c o n t r o l disks (22.8 sec). Thus, c o n t a c t with the k a i r o m o n e a p p e a r e d to elicit initial r e t e n t i o n of A.fallacis within the vicinity, after which A. fallacis m a y have p h y s i o l o g i c a l l y a d a p t e d or h a b i t u a t e d to it. W e s e l o h (1980) r e p o r t e d h a b i t u a t i o n o f Apanteles melanoscelus ( R a t z b u r g ) females to silk k a i r o m o n e o f host Lymantria dispar L. larvae. In a test to d e t e r m i n e w h e t h e r the k a i r o m o n e is p e r c e i v e d b y c o n t a c t o r o l f a c t o r y means, A. fallacis e x h i b i t e d little or no r e s p o n s e to w i n d c u r r e n t s b l o w n over k a i r o m o n e or c o n t r o l disks at velocities b e l o w the t h r e s h o l d eliciting c h a r a c t e r i s t i c dispersal b e h a v i o r ( J o h n s o n a n d Croft, 1976). W i n d velocities e x c e e d i n g this t h r e s h o l d f r e q u e n t l y elicited d i s p e r s a l f r o m b o t h
O
FiG. 1. Typical A. fallacis search patterns (90-sec period following first contact with disk) when encountering: (A) T. urticae silk and associated feces, (B) methanol extract of silk and associated feces (= kairomone), or (C) methanol control disks.
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HISLOP AND PROKOPY
TABLE 3. INFLUENCE OF VISIT SEQUENCE ON RESPONSE OF A. fallacis TO METHANOL EXTRACT OF T. urticae SILK AND ASSOCIATED FECES (20 REPLICATES/TREATMENT) Avg. duration of visit (sec) ~ Visit no.
Visit no. 7-9
Visit no.
1-3
Visit no. 4-6
15.9 a 18.8 a 18.2 a 11.1 a
14.3 a 10.3 a 9. I a 8.8 a
8.5 9.3 8.1 9.2
24.2 29.6 24.2 62.7
Disk type Fresh extract 3-day extract 7-day extract Methanol
Avg. time between visits (sec)
a a a a
1-3
a a a b
Visit no. 4-6
Visit no. 7-9
32.5 a 28.2 a 24.0 a 38.5 a
28.1 24.3 21.0 22.4
a a a a
"See footnote a of Table 1.
treatments. These observations suggest that the kairomone principally or exclusively by contact.
is p e r c e i v e d
Influence o f Prey Silk or Kairomone on Predation Efficiency. A.fallacis a c h i e v e d m a x i m u m p r e d a t i o n e f f i c i e n c y w h e n s e a r c h i n g f o r p r e y (a s i n g l e T. urticae egg) o n a d i s k t r e a t e d w i t h p r e y silk, a l t h o u g h s e a r c h i n g f o r p r e y o n a d i s k t r e a t e d w i t h m e t h a n o l silk e x t r a c t a l s o r e s u l t e d i n s i g n i f i c a n t l y g r e a t e r prey consumption compared with searching for prey on control disks which h a d p r e y ( T a b l e 4). F o l l o w i n g p r e y c o n s u m p t i o n , A. fallacis r e m a i n e d o n ( w i t h i n 1 c m of) d i s k s t r e a t e d w i t h silk s i g n i f i c a n t l y l o n g e r t h a n o n c o n t r o l disks which had prey. They remained on the latter significantly longer than on c o n t r o l d i s k s w i t h o u t p r e y ( T a b l e 4). T h e s e d a t a d e m o n s t r a t e t h a t p r e y c o n s u m p t i o n elicits r e t e n t i o n of A.fallacis i n a r e a s o f p r e y h a b i t a t i o n a n d t h a t t h e p r e s e n c e o f p r e y silk o r k a i r o m o n e e x t e n d s t h i s r e t e n t i o n t i m e . TABLE 4. INFLUENCE OF T. urlicae SILK AND ASSOCIATED FECES, OR METHANOL EXTRACT OF SILK AND ASSOCIATED FECES, ON A. fallacis PREDATION EFFICIENCY AND POST-PREY-CoNSUMPTION BEHAVIOR (20 REPLICATES/TREATMENT)
Disk treatment Silk plus 1 prey egg Silk extract plus 1 prey egg Methanol plus 1 prey egg Methanol ~See footnote a of Table 1. bOn or within 1 cm of disk.
A. fallacis which consumed prey egg in 5 min~ (%)
Avg. duration of visit to disk after prey consumption (sec) b
88 a 67 b 35 c
287.7 a 219.0 b 173.3 b 42.1 c
MITE PREDATOR RESPONSES TO PREY AND PREDATOR-EMITTED STIMULI
901
Influence of Presearched Areas on Predator Searching Behavior. Both A. fallacis (N = 14) and P. macropilis (N = 14) remained a significantly shorter time during the first visit to prey-silked disks presearched by five different conspecific predators for 30--40 min prior to assay (55.3 and 107.2 sec, respectively) than during the first visit to nonpresearched silked disks (496.1 and 492.3 sec, respectively). A preliminary test revealed that P. macropilis females spent ca. 98 sec searching silked disks treated with a methanol extract of presearched disks compared with ca. 129 sec searching silked disks treated with methanol alone (P -- _< 0.30, t test, N = 12). We interpret these results as suggesting that both species release marking pheromone during host searching behavior. DISCUSSION
The literature suggests that host-finding by predatory arthropods is mediated more often by visual or tactile stimuli than by chemosensory stimuli (Rowlands and Chapin, 1978, Greany and Hagen, 1981). However, in predators with limited visual capacity, such as A. fallacis appears to have, possession of chemosensory mechanisms for prey detection would be a distinct advantage. Wilbert (1974) and McLain (1979) found that certain predators, with limited visual capabilities, altered their search pattern upon encountering host odors or aqueous solutions of host frass or hemolymph (= kairomones). Similarly, Lewis et al. (1977) discovered a kairomone in Heliothis zea (Boddie) moth scales which stimulates larvae of Chrysopa carnea Stephens to remain in areas containing moth eggs. Our results suggest that A.fallacis utilizes a combination of physical and chemical stimuli in prey location. Exposure to prey silk and associated feces elicits reduction in the speed of predator movement (inverse orthokinesis; Kennedy, 1977) and elicits longer halts, thus increasing the probability of encountering nearby prey. We do not believe that these influences of silk on predator behavior are the result of silk impeding predator movement because, upon gentle prodding, predators are able to exit from a silked area just as rapidly as from a nonsilked area. Schmidt (1976) likewise found that exposure of P. persimilis to T. urticae silk resulted in predator arrestment, leading to greater prey consumption. Exposure to a methanol extract of prey silk and associated feces (kairomone) elicits frequent predator return to the stimulus area (direct klinokinesis; Kennedy, 1977). The parasite Trichogramma evanescens Westwood is arrested in similar fashion after contact with kairomone separate from or together with scales of ovipositing Heliothis zea (Boddie) moths (Lewis et al., 1972). Our findings suggest a possible disadvantage to A. fallacis when encountering old silk of prey. The demonstrated arrestant effect of 14-day-old
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HISLOP AND PROKOPY
silk could conceivably result in waste of predator time and energy when foraging in areas previously but no longer containing prey. Ohnesorge (1978) observed a similar situation in P. persimilis. T. urticae, a principal prey of A. fallacis, tends to occur in relatively clumped distributions. A. fallacis may achieve maximal predation efficiency by remaining in areas where prey aggregations occur. Our findings suggest that the same host cues (silk in combination with kairomone) which elicit predator retention also lead to increased predation efficiency. In fact, encounters with prey eggs alone, even in the absence of additional prey stimuli, retain searching A. fallacisin prey areas for a greater time than in areas devoid of prey. Such a response may be of substantial benefit in discovering additional prey within areas of prey aggregation. Similar alterations in predator searching behavior following prey encounter or consumption have been demonstrated in Anthocaris nemoralis (F.) (Brunner and Burts, 1975), Anthocaris confusis (Evans, 1976), Coccinella septempunctata (Marks, 1977), and Hippodamia convergens (Rowlands and Chapin, 1978). Prey kairomone influencing the searching behavior of A. fallacis or P. macropilis could be of significant value to pest management programs. For example, if the kairomone secreted by T. urticae could be identified, synthesized, and applied together with artificial food substances (such as honeydew or pollen; e.g., Hagen et al., 1970), the result might be greater retention of A. fallacis or P. macropilis on the foliage in times of low natural prey densities, Such artificially retained predators could function to "guard" against possible spider mite outbreaks. Finally, our data suggest that during searching of prey-silked areas, A. fallacis and P. macropilis deposit pheromone which marks such sites as already having been recently explored. Marking pheromones have been discovered in predatory insects (Marks, 1977), parasitoids (Vinson, 1976), and phytophagous insects (Prokopy, 1981), but this appears to be the first such case in a predatory acarine.
Acknowledgments--This research was supported by Massachusetts Agricultural Experiment Station Project No. 380. Paper No. 2360of the Mass. Agric. Exp. Sta. REFERENCES 1954. The biology of the predacious mite Typhlodromusfallacis (Garman) (Phytoseiidae)at 78~F. Ohio J. Sci. 54(3):175-179. BLOMM~RS,L., LOBBES,P., VINK, P., and WEGDAM,F. 1977. Studies on the response of Amblyseius bibens (Acarina: Phytoseiidae)to conditions of prey scarcity. Entomophaga 22(3):247-258. BRUNNER,J.F,, and BURTS,E.C. 1975. Searching behavior and growth rates of Anthocaris nemoralis (Hemiptera:Anthocoridae),a predator of the pear psylla, Psyllapyricola. Ann. Entomol Soc. Am. 68(2):311-315. BALLARD, R.C.
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CROFT,B.A. 1975. Integrated control of apple mites. Extension Bull. C-825, Mich. St. Univ. Ext. Ser. 12 pp. CROFT, B.A., and NELSON, E.E. 1972. Toxicity of apple orchard pesticides to Michigan populations of Amblyseius fallacis. Environ. EntomoL 2:576-579. ELSEY, K.D. 1974. Influence of plant host on searching speed of two predators. Entomophaga 19(1):3-6. EVANS, H.F. 1976. The searching behaviour ofAnthocaris confusis (Reuter) in relation to prey density and plant surface topography. Ecol. EntomoL 1:163-169. FARISH, D.J., and AXTELL, R.C. 1966. Sensory functions of the palps and first tarsi of Macrocheles muscaedomesticae (Aearina: Macrochelidae), a predator of the house fly. Ann. Entornol Soc. Am. 59(1):165-170. GREANY, P.D., and HAGEN, K.S. 1981. Role and significance of allelochemics in prey selection, pp. 89-95, in D.A. Nordlund, R.L. Jones, and W.J. Lewis (eds.). Semiochemicals: Their Role in Pest Control, John Wiley & Sons, New York. HAGEN, K.S., SAWALL, E.F., Jr., and TASSAN, R.L. 1970. The use of food sprays to increase effectiveness of entomophagous insects. Proc. Tall Timb. Conf. on EcoL Anita. Cont. by Habit. Manag. 2:59-81. HAMLEN, R.A. 1978. Biological control of spider mites on greenhouse ornamentals using predaceous mites. Proc. Fla. State Hort. Soc. 91:247-249. HAMLEN, R.A. 1980. Report of Phytoseiulus macropilis management of Tetranychus urticae on greenhouse grown dieffenbachia. Bull. I O B C / W P R S 111/3:65-73. HENDERSON,D.F., and MCBURNIE, H.V. 1943. Sampling technique for determining populations of the citrus red mite and its predators. USDA Circ. 671. I I pp. nisLoP, R.G., and PROKOPY, R.J. 1981. Integrated management of phytophagous mites in Massachusetts (USA) apple orchards: (2). Influence of pesticides on the predatorAmblyseius fallacis (Acarina: Phytoseiidae) under laboratory and field conditons. Prot. Ecol. In press. JALIL, M., and RODRIGUEZ,J.G. 1970. Studies of the behavior ofMacrocheles muscaedomesticae (Acarina: Macrochelidae) with emphasis on its attraction to the house fly. Ann. EntomoL Soc. Am. 63(3):738-744. JOHNSON, D.T., and CROFT, B.A. 1976. Laboratory study of the dispersal behavior of Amblyseius fallacis (Acarina: Phytoseiidae). Ann. Entomol. Soc. Am. 69(6):1019-I023. KENNEDY, J.S. 1977. Olfactory responses to distant plants and other odor sources, pp. 67-9 l, in H.H. Shorey, J.J. McKelvey (eds.), Chemical Control of Insect Behavior, John Wiley & Sons, New York. LEWIS, W.J., JONES, R.L., and SPARKS,A.N. 1972. A host-seeking stimulant for the egg parasite, Trichogramma evanescens: Its source and a demonstration of its laboratory and field activity. Ann. Entomol Soc. Am. 65:1087-1089. LEWIS, W.J., NORDLUND, D.A., Ggoss, H.R.,JR., JONES, R.L., and JONES, S.L. 1977. Kairomones and their use for management of entomophagous insects V. moth scales as a stimulus for predation of Heliothis zea (Boddie) eggs by Chrysopa carnea Stephens larvae../. Chem. Ecol. 3(4):483-487. M ARKS,R.J. 1977. Laboratory studies of plant searching behaviour by Coccinella septempunctata L. larvae. Bull. Entomol. Res. 67:235-241. MCCLANAHAN, R.J. 1968. Influence of temperature on the reproductive potential of two mite predators of the two-spotted spider mite. Can. Entomol. 100:549-556. MCLAIN, K. 1979. Terrestrial trail following by three species of predatory stink bugs. Fla. Entomol. 62:152-154. MORI, H., and CHANT, D.A. 1966. The influence of prey density, relative humidity, and starvation on the predacious behavior of Phytoseiulus persimilis Athias-Henriot (Acarina: Phytoseiidae). Can. J. Zool. 44:483-491. MOTOYAMA,N., ROCK, G.C., and DAUTERMAN,W. C. 1970. Organophosphorous resistance in an
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apple orchard population of Typhlodromus (Amblyseius) fallacis. J. Econ. Entomol. 63(5):1439-1442. OnNESORGE, B. 1978. Der Einfluss der Besiedlungsdauer spinnmilbenverseuchter Bohnenbliitter auf die raiimuliche Verteilung der Raubmilbe Phytoseiulus persimilis A. and H. (Acarina, Phytoseiidae). Z. Angew. Entomol. 85:337-340. PRASAD, V. 1967. Biology of the predatory mite Phytoseiulus macropilis in Hawaii (Acarina: Phytoseiidae). Ann. Ent. Soc. Am. 60:905-908. PROKOPY, R.J. 1981. Epideictic pheromones influencing spacing patterns of phytophagous insects, pp. 181-213, in D.A. Nordlund, R.L. Jones, and W.J. Lewis (eds.). Semiochemicals: Their Role in Pest Control. John Wiley & Sons, New York. RASMY, A.H., and EL-BANHAWY, E.M. 1974. Behaviour and bionomics of the predatory mite, Phytoseius plumifer (Acarina: Phytoseiidae) as affected by physical surface features of host plants. Entornophaga 19(3):255-257. ROCK, G.C., MONROE, R.J., and YEARGAN,D.R. 1976. Demonstration of a sex pheromone in the predaceous mite Neoseiulus fallacis. Environ. Entomol. 5(2):264-266. ROWLANDS, M.L.J., and CHAPIN, J.W. 1979. Prey searching behavior in adults of Hippodarnia convergens (Coleoptera: Coccinellidae). 3. Ga. EntomoL Soc. 13(4):309-315. SCHMIDT, G. 1976. Der Einfluss der yon den Beutetieren hinterlassenen Spuren auf Suchverhalten und Sucherfolg von Phytoseiulus persimilis A. and H. (Acarina: Phytoseiidae). Z. Angew. Entomol. 82:216-218. SrlIH, C.I., POE, S.L., and CROMROY, H.L. 1979. Biology and predation of Phytoseiulus macropilis on Tetranychus urticae. Fla. Ent. 62:48-53. SMITH, J.C. and NEWSOM, L.D. 1970a. The biology of Arnblyseius fallacis (Acarina: Phytoseiidae) at various temperature and photoperiod regimes. Ann. Entomol. Soc. Am. 63(2):460-462. SMITH, J.C., and NEWSOM, L.D. 1970b. Laboratory evaluation of Amblyseius fallacis as a predator of tetranychid mites. J. Econ. Entomol. 63(6): 1876-1878. VINSON, S.B. 1976. Host selection by insect parasitoids. Annu. Rev. Entomol. 21:109-133. WESELOH, R.M. 1980. Behavioral changes in Apanteles melanoscelus females exposed to Gypsy Moth silk. Environ. Entomol. 9:345-349. WILBERT, H. 1974. Die Wahrnehmung von Beute durch die Eilarven yon Aphidoletes aphidimyza (Cecidomyiidae). Entomophaga 19(2): 173-181.
MITE PREDATOR RESPONSES TO PREY AND PREDATOR-EMITTED STIMULI
R O B E R T G. HISLOP and R O N A L D J. P R O K O P Y Department of Entomology, University of Massachusetts, Amherst, Massachusetts 01003 (Received October 28, 1980; revised January 12, 1981) Abstract--We found that the searching behavior of two acarine predators,
Amblyseius fallacis and Phytoseiulus macropilis, for prey, Tetranychus urticae, is affected by the following stimuli: (1) prey silk and associated feces, whose combined physical and chemical properties elicit reduction in the rate of predator movements and longer halts; (2) kairomone extracted from prey silk and associated feces, which, upon contact, elicits frequent predator return to prey-inhabited locales; and (3) predator-emitted marking pheromone, which elicits shorter duration of search in presearched prey locales. We also found that treatment of filter paper with prey kairomone or silk enhanced predator location of prey eggs, leading us to speculate that application of synthetic prey kairomone could be useful in pest management programs. Key Words--Kairomone, silk, marking pheromone, host finding, Am-
blyseius fallacis, Phytoseiulus macropilis, Tetranychus urticae.
INTRODUCTION
Amblyseiusfallacis (Garman) and Phytoseiulus macropilis (Banks) (Acarina: Phytoseiidae) are important predators of spider mites, especially Tetranychus urticae Koch. A. fallacis occurs in northeastern U.S. commercial apple orchards (Croft, 1975), while P. macropilis is undergoing experimentation in greenhouse integrated mite control programs in Florida (Hamlen, 1980). Although reports exist describing various aspects of the biology (Ballard, 1954; Prasad, 1967; McClanahan, 1968; Smith and Newsom, 1970a, b; Rock et al., 1976; Johnson and Croft, 1976; Shih et al., 1979; Hamlen, 1978, 1980) and pesticide resistance (Motoyama et al., 1970; Croft and Nelson, 1972; Hislop and Prokopy, 1981) of these predators, the role of kairomones and marking pheromones in A. fallacis or P. macropilis host searching behavior 895 0098/0331/0900-089550.300/09 1981PlenumPublishingCorporation
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HISLOP AND PROKOPY
has received little attention. This is true as well for most other predatory mites, notable exceptions being the work of Farish and Axtell (1966) and Jalil and Rodriguez (! 970) demonstrating the role of kairomones in attraction to prey of predacious mites of the families Machrochelidae and Uropodidae. In spring, A. fallacis is normally associated with T. urticae, a preferred prey in the orchard understory. In summer, this predator migrates into the trees in search of additional prey, often borne there by wind currents (Johnson and Croft, 1976). In the greenhouse, P. macropilis does not usually migrate over long distances in search of new prey but instead tends to remain in close proximity to existing prey. In a related species, P. persimilis Athias-Henriot, Mori and Chant (1966) demonstrated changes in predation behavior as a function_of humidity and starvation level. Several factors may influence arthropod predator searching behavior leading to contact with prey: physical substrate characteristics; temperature, humidity, and starvation level (Rasmy and E1-Banhawy, 1974, Elsey, 1974; Blommers et al., 1977); and prey silk (Schmidt, 1976; Ohnesorge, 1978). Here we examine for the first time two sorts of factors influencing the host searching behavior of A. fallacis and P. macropilis (A. fallacis was examined in greater detail because of its importance in our apple integrated pest management program): (1) physical and kairmonal cues emitted by T. urticae, and ('2) predator-emitted stimuli influencing duration of search in presearched areas. M E T H O D S AND MATERIALS
A.fallacis was collected in Massachusetts apple orchards and cultured in the laboratory on lima bean leaves infested with T. urticae. P. macropilis was obtained from a colony at the University of Massachusetts Suburban Experiment Station in Waltham. ; For collection and bioassay of prey silk, hundreds of T. urticae were brushed from bean leaves onto 12-cm-diam glass plates using a mite brushing machine (Henderson and McBurnie, 1943). Pieces of bean leaves ca. 2 cm diam were placed around the edges of each plate to collect the dispersing mites. Leaf pieces containing 300-500 mites were placed individually under 2-cm-diam glass rings for 24 hr, after which the leaf and all mites were removed. Silk spun by the mites across the ring hole was gathered on a 1.5-cm-diam filter paper disk by passing the disk through the ring. After manual removal of eggs and debris from the silk, each disk was bioassayed for predator response. Because we were unable to remove prey feces from the silk, our terminology for silk throughout this paper includes the element of associated prey feces. For collection and bioassay of kairomone, each of several 12-cm-diam glass plates containing thousands of T. urtieae brushed from bean leaves was
MITE PREDATOR RESPONSES TO PREY AND PREDATOR-EMITTED S T I M U L I
897
placed in a petri dish, over which was positioned an acetate cone (12 cm bottom diam, 2 cm top diam). Each was then placed under a fluorescent light, which attracted the mites to the top of the cone. After 24 hr, the mites were removed and the silk was gathered by passing a 1.5-cm-diam preweighed (on a Cahn electrobalance) filter paper disk through the hole in the top of the cone. After manual removal of eggs and debris, the filter paper and silk were weighed and placed into 1 ml of solvent. After 24 hr, the filter paper was removed and the extract centrifuged at 10,000 rpm for 30 min. Final extract concentration was 0.1 mg silk/ml solvent. We used the following four solvents: water, methanol, chloroform, and hexane. Because preliminary assays proved the methanol extract to contain the most active kairomonal components, this extract was chosen for use in the assays reported here. The assays were conducted in the following manner. One 1.5-cm-diam filter paper disk left untreated (= a control) or containing either silk, 0.02 ml methanol extract of silk (= kairomone), or methanol (= a control) was placed in the center of a 5-cm-diam glass arena surrounded by water to prevent emigration of predators. The surface of the water was ca. 2 mm below the surface of the glass arena. One A.fallacis or P. macropilis female, starved for 6-8 hr, was placed at the arena edge and allowed to enter the disk at will. Bioassay periods lasted for 90 sec (silk) or 6 min (kairomone) following initial predator contact with the disk. Speed of movement (A. fallacis only) was obtained by analyzing the path of predator movement traced for the first 90 sec onto a piece of clear acetate taped to a magnifying glass to enlarge the image. Visual interference of the tracing movements with predator activity was eliminated by reflecting the predator image off two mirrors prior to image magnification. Tracing was performed in dim light to avoid back-reflection. Influence of prey-emitted stimuli on A. fallaeis predation efficieney was determined by placing a single T. urticae egg midway between the edge and center of a 0.5-cm-diam filter paper disk containing either prey silk, 0.01 ml of methanol solution of kairomone, or methanol alone (= control). The percentage of predators which consumed an egg in a 5-min time period was compared among treatments. The average time A. fallacis remained on or within 1 cm of each disk following prey consumption was also measured. P. macropilis was not tested. In examining factors influencing duration of predator searching in presearched areas, we assayed females ofA. fallacis and P. macropilis which had been placed in contact prior to assay with a filter paper disk containing prey silk. In the assay, a filter paper disk (0.5 cm diam) containing T. urtieae silk was placed in the center of a glass arena. A single predator was introduced and allowed to enter the disk at will. We measured the following: (1) duration of first visit to (within 1 cm of) a disk not previously visited by a predator (= control disks); and (2) duration of first visit to (within 1 cm of) a disk previously searched for ca. 30-40 min prior to assay by 5 conspecific predators.
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All experiments were performed under conditions of ca. 24 + 2 ~ C and 70 _ 10% relative humidity. D a t a were submitted to analysis of variance and D u n c a n ' s multiple range test or a paired t test at the 5% level.
RESULTS
Influence of Prey Silk on Searching Behavior. A. fallacis females spent a significantly greater a m o u n t of time per visit on disks having fresh or 14-dayold prey silk and associated feces than on control disks. Also, the average duration of stops was significantly greater, and the walking speed significantly less, on the silk disks t h a n on the controls (Table 1). These data suggest that fresh as well as 14-day-old T. urticae silk has physical a n d / o r chemical properties which stimulate searching A.fallacis females to walk more slowly and stop longer within areas of prey habitation. Influence of Prey Kairomone on Searching Behavior. The average time spent between A. fallacis visits to disks treated with fresh, 3-day-old, or 7-day-old extract of silk and associated feces was significantly less than the time between visits to control disks (Table 2). A. fallacis returned to treated disks at an average turning angle of 148~ c o m p a r e d with 97 ~ for the controls. In similar fashion, P. maeropilis returned to disks treated with fresh silk extract in significantly less time (15.3 sec) than to control disks (40.5 sec) (20 replicates). These data clearly demonstrate that a k a i r o m o n e is present in the extract which stimulates A. fallacis and P. maeropilis females to return to extract disks and that k a i r o m o n a l activity (for A. fallacis) is present for at least 7 days. In contrast to when k a i r o m o n e was present together with silk (Table 1), the average duration of visits and stops (A.fallacis) on silk extract disks was no different f r o m controls, a l t h o u g h the speed of m o v e m e n t was significantly less than on the controls (Table 2). Figure 1 shows a typical A. fallacis search pattern on silk, silk extract, and methanol control disks.
TABLE 1. INFLUENCEOF T. urticae SILK AND ASSOCIATED FECES ON A.fallacis SEARCHING BEHAVIOR (20 REPLICATES/TREATMENT)
Disk type
Avg. duration of visit (sec)a
Avg. time betweenvisits (see)
Avg, duration of stops on disk (see)
Avg. walking speed on disk (cm/sec)
Fresh silk 14-day-old silk Untreated
42.5 a 57.0 a 12.2 b
11.8 a 14.0 a 24.5 a
12.2 a 16.3 a 0.4 b
0.12 a 0.15 a 0.29 b
aMeans in each column followed by a different letter are significantly different at the 0.05 level.
899
MITE PREDATOR RESPONSES TO PREY AND PREDATOR-EMITTED STIMULI TABLE 2. INFLUENCE OF METHANOL EXTRACT OF T. urticae SILK AND ASSOCIATED FECES (=KAIROMONE) ON .4. fallacis SEARCHING BEHAVIOR (20 REPLICATES/TREATMENT)
Disk type
Avg. duration of visit (sec)a
Avg. time between visits (sec)
13.2 a 14.2 a 10.9 a 9.9 a
33.0 a 33.7 a 28.0 a 66.5 b
Fresh extract 3-day extract 7-day extract Methanol
Avg. duration of stops on disk (sec) 0 0 0.I 0.1
a a a a
Avg. walking speed on disk (cm/sec) 0.20 a 0.19 a 0.18 a 0.24 b
aSee footnote a of Table 1.
D a t a on the influence of visit sequence on A. fallacis r e s p o n s e to silk e x t r a c t a n d c o n t r o l disks are given in T a b l e 3. F o r the first three visits, the r e t u r n time to silk e x t r a c t disks was significantly s h o r t e r t h a n the r e t u r n time to c o n t r o l disks. F o r visists 4 - 6 a n d 7 - 9 there was no significant difference b e t w e e n t r e a t m e n t s in r e t u r n time. N o r was there at a n y time a significant difference between t r e a t m e n t s in average d u r a t i o n o f visits. Initial r e t e n t i o n time (i.e., time over which A. fallacis was r e t a i n e d within 1 cm o f a t r e a t m e n t disk f o l l o w i n g the first visit) was significantly l o n g e r on disks t r e a t e d with fresh, 3 - d a y - o l d , a n d 7 - d a y - o l d silk e x t r a c t (51.0, 69.6, a n d 63.0 see, respectively) t h a n on c o n t r o l disks (22.8 sec). Thus, c o n t a c t with the k a i r o m o n e a p p e a r e d to elicit initial r e t e n t i o n of A.fallacis within the vicinity, after which A. fallacis m a y have p h y s i o l o g i c a l l y a d a p t e d or h a b i t u a t e d to it. W e s e l o h (1980) r e p o r t e d h a b i t u a t i o n o f Apanteles melanoscelus ( R a t z b u r g ) females to silk k a i r o m o n e o f host Lymantria dispar L. larvae. In a test to d e t e r m i n e w h e t h e r the k a i r o m o n e is p e r c e i v e d b y c o n t a c t o r o l f a c t o r y means, A. fallacis e x h i b i t e d little or no r e s p o n s e to w i n d c u r r e n t s b l o w n over k a i r o m o n e or c o n t r o l disks at velocities b e l o w the t h r e s h o l d eliciting c h a r a c t e r i s t i c dispersal b e h a v i o r ( J o h n s o n a n d Croft, 1976). W i n d velocities e x c e e d i n g this t h r e s h o l d f r e q u e n t l y elicited d i s p e r s a l f r o m b o t h
O
FiG. 1. Typical A. fallacis search patterns (90-sec period following first contact with disk) when encountering: (A) T. urticae silk and associated feces, (B) methanol extract of silk and associated feces (= kairomone), or (C) methanol control disks.
900
HISLOP AND PROKOPY
TABLE 3. INFLUENCE OF VISIT SEQUENCE ON RESPONSE OF A. fallacis TO METHANOL EXTRACT OF T. urticae SILK AND ASSOCIATED FECES (20 REPLICATES/TREATMENT) Avg. duration of visit (sec) ~ Visit no.
Visit no. 7-9
Visit no.
1-3
Visit no. 4-6
15.9 a 18.8 a 18.2 a 11.1 a
14.3 a 10.3 a 9. I a 8.8 a
8.5 9.3 8.1 9.2
24.2 29.6 24.2 62.7
Disk type Fresh extract 3-day extract 7-day extract Methanol
Avg. time between visits (sec)
a a a a
1-3
a a a b
Visit no. 4-6
Visit no. 7-9
32.5 a 28.2 a 24.0 a 38.5 a
28.1 24.3 21.0 22.4
a a a a
"See footnote a of Table 1.
treatments. These observations suggest that the kairomone principally or exclusively by contact.
is p e r c e i v e d
Influence o f Prey Silk or Kairomone on Predation Efficiency. A.fallacis a c h i e v e d m a x i m u m p r e d a t i o n e f f i c i e n c y w h e n s e a r c h i n g f o r p r e y (a s i n g l e T. urticae egg) o n a d i s k t r e a t e d w i t h p r e y silk, a l t h o u g h s e a r c h i n g f o r p r e y o n a d i s k t r e a t e d w i t h m e t h a n o l silk e x t r a c t a l s o r e s u l t e d i n s i g n i f i c a n t l y g r e a t e r prey consumption compared with searching for prey on control disks which h a d p r e y ( T a b l e 4). F o l l o w i n g p r e y c o n s u m p t i o n , A. fallacis r e m a i n e d o n ( w i t h i n 1 c m of) d i s k s t r e a t e d w i t h silk s i g n i f i c a n t l y l o n g e r t h a n o n c o n t r o l disks which had prey. They remained on the latter significantly longer than on c o n t r o l d i s k s w i t h o u t p r e y ( T a b l e 4). T h e s e d a t a d e m o n s t r a t e t h a t p r e y c o n s u m p t i o n elicits r e t e n t i o n of A.fallacis i n a r e a s o f p r e y h a b i t a t i o n a n d t h a t t h e p r e s e n c e o f p r e y silk o r k a i r o m o n e e x t e n d s t h i s r e t e n t i o n t i m e . TABLE 4. INFLUENCE OF T. urlicae SILK AND ASSOCIATED FECES, OR METHANOL EXTRACT OF SILK AND ASSOCIATED FECES, ON A. fallacis PREDATION EFFICIENCY AND POST-PREY-CoNSUMPTION BEHAVIOR (20 REPLICATES/TREATMENT)
Disk treatment Silk plus 1 prey egg Silk extract plus 1 prey egg Methanol plus 1 prey egg Methanol ~See footnote a of Table 1. bOn or within 1 cm of disk.
A. fallacis which consumed prey egg in 5 min~ (%)
Avg. duration of visit to disk after prey consumption (sec) b
88 a 67 b 35 c
287.7 a 219.0 b 173.3 b 42.1 c
MITE PREDATOR RESPONSES TO PREY AND PREDATOR-EMITTED STIMULI
901
Influence of Presearched Areas on Predator Searching Behavior. Both A. fallacis (N = 14) and P. macropilis (N = 14) remained a significantly shorter time during the first visit to prey-silked disks presearched by five different conspecific predators for 30--40 min prior to assay (55.3 and 107.2 sec, respectively) than during the first visit to nonpresearched silked disks (496.1 and 492.3 sec, respectively). A preliminary test revealed that P. macropilis females spent ca. 98 sec searching silked disks treated with a methanol extract of presearched disks compared with ca. 129 sec searching silked disks treated with methanol alone (P -- _< 0.30, t test, N = 12). We interpret these results as suggesting that both species release marking pheromone during host searching behavior. DISCUSSION
The literature suggests that host-finding by predatory arthropods is mediated more often by visual or tactile stimuli than by chemosensory stimuli (Rowlands and Chapin, 1978, Greany and Hagen, 1981). However, in predators with limited visual capacity, such as A. fallacis appears to have, possession of chemosensory mechanisms for prey detection would be a distinct advantage. Wilbert (1974) and McLain (1979) found that certain predators, with limited visual capabilities, altered their search pattern upon encountering host odors or aqueous solutions of host frass or hemolymph (= kairomones). Similarly, Lewis et al. (1977) discovered a kairomone in Heliothis zea (Boddie) moth scales which stimulates larvae of Chrysopa carnea Stephens to remain in areas containing moth eggs. Our results suggest that A.fallacis utilizes a combination of physical and chemical stimuli in prey location. Exposure to prey silk and associated feces elicits reduction in the speed of predator movement (inverse orthokinesis; Kennedy, 1977) and elicits longer halts, thus increasing the probability of encountering nearby prey. We do not believe that these influences of silk on predator behavior are the result of silk impeding predator movement because, upon gentle prodding, predators are able to exit from a silked area just as rapidly as from a nonsilked area. Schmidt (1976) likewise found that exposure of P. persimilis to T. urticae silk resulted in predator arrestment, leading to greater prey consumption. Exposure to a methanol extract of prey silk and associated feces (kairomone) elicits frequent predator return to the stimulus area (direct klinokinesis; Kennedy, 1977). The parasite Trichogramma evanescens Westwood is arrested in similar fashion after contact with kairomone separate from or together with scales of ovipositing Heliothis zea (Boddie) moths (Lewis et al., 1972). Our findings suggest a possible disadvantage to A. fallacis when encountering old silk of prey. The demonstrated arrestant effect of 14-day-old
902
HISLOP AND PROKOPY
silk could conceivably result in waste of predator time and energy when foraging in areas previously but no longer containing prey. Ohnesorge (1978) observed a similar situation in P. persimilis. T. urticae, a principal prey of A. fallacis, tends to occur in relatively clumped distributions. A. fallacis may achieve maximal predation efficiency by remaining in areas where prey aggregations occur. Our findings suggest that the same host cues (silk in combination with kairomone) which elicit predator retention also lead to increased predation efficiency. In fact, encounters with prey eggs alone, even in the absence of additional prey stimuli, retain searching A. fallacisin prey areas for a greater time than in areas devoid of prey. Such a response may be of substantial benefit in discovering additional prey within areas of prey aggregation. Similar alterations in predator searching behavior following prey encounter or consumption have been demonstrated in Anthocaris nemoralis (F.) (Brunner and Burts, 1975), Anthocaris confusis (Evans, 1976), Coccinella septempunctata (Marks, 1977), and Hippodamia convergens (Rowlands and Chapin, 1978). Prey kairomone influencing the searching behavior of A. fallacis or P. macropilis could be of significant value to pest management programs. For example, if the kairomone secreted by T. urticae could be identified, synthesized, and applied together with artificial food substances (such as honeydew or pollen; e.g., Hagen et al., 1970), the result might be greater retention of A. fallacis or P. macropilis on the foliage in times of low natural prey densities, Such artificially retained predators could function to "guard" against possible spider mite outbreaks. Finally, our data suggest that during searching of prey-silked areas, A. fallacis and P. macropilis deposit pheromone which marks such sites as already having been recently explored. Marking pheromones have been discovered in predatory insects (Marks, 1977), parasitoids (Vinson, 1976), and phytophagous insects (Prokopy, 1981), but this appears to be the first such case in a predatory acarine.
Acknowledgments--This research was supported by Massachusetts Agricultural Experiment Station Project No. 380. Paper No. 2360of the Mass. Agric. Exp. Sta. REFERENCES 1954. The biology of the predacious mite Typhlodromusfallacis (Garman) (Phytoseiidae)at 78~F. Ohio J. Sci. 54(3):175-179. BLOMM~RS,L., LOBBES,P., VINK, P., and WEGDAM,F. 1977. Studies on the response of Amblyseius bibens (Acarina: Phytoseiidae)to conditions of prey scarcity. Entomophaga 22(3):247-258. BRUNNER,J.F,, and BURTS,E.C. 1975. Searching behavior and growth rates of Anthocaris nemoralis (Hemiptera:Anthocoridae),a predator of the pear psylla, Psyllapyricola. Ann. Entomol Soc. Am. 68(2):311-315. BALLARD, R.C.
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