Notes on Predatory Behaviour in Rhinacloa Forticornis (Hemiptera: Miridae)

Introduction

Rhinacloa forticornis Reuter is a polyphagous phyline mirid known originally from the Nearctic and Neotropical regions.¹ One of the “black fleahopper” complex, it is common in the western United States,² and is considered a major pest of cotton there^{3, 4} and in the West Indies.⁵ Despite its status as a crop pest, confusion exists concerning feeding patterns in the species, and there has been speculation and anecdotal suggestion that R. forticornis is primarily a predator. For example, Beingolea⁶ considered the mirid a predator of eggs and young larvae of tobacco budworm, Heliothis virescens (F.), in Peruvian cotton fields, and Johnson and Nafus⁷ regarded it as a predator of melon thrips, Thrips palmi Karny, in various crops in Hawaii, but in neither case was anyobservation of predatory behaviour reported. On the basis of its lack of host plant specificity, Knight⁸ and Gagné⁹ speculated that it was probably predaceous on other arthropods. Some clearer indications of predatory behaviour have been reported. McGregor and McDonough¹⁰observed R. forticornis to feed on spider mites, Tetranychus sp., in cotton fields and in the laboratory. Butler¹¹ provided circumstantial evidence for at least some facultative predation, reporting that laboratory colonies of the mirid could not be maintained on a diet of green beans alone, but required supplements of Heliothis sp. eggs. Stoner and Bottger¹² reported that adult R. forticornis reduced populations of 2nd-instar Lygus nymphs 72% in laboratory tests. However, these authors gave no details of their experimental methods. In a laboratory study of the life cycle, Herrera¹³ reported that, after taking plant sap for the first two instars, 3rd-instar nymphs fed on lepidopteran eggs, aphids, and larvae of H. virescens and cecidomyiids; the mirid was considered potentially effective in controlling H. virescens populations in cotton. However, Ingram⁵was unable to confirm any predatory behaviour in the bug.

After its discovery in Hawaii in 1962,¹⁴ R. forticornis soon became one of the more common mirids on vegetation from sea level to tree line.⁹ Observed behaviour of the mirid on star jasmine, Jasminum multiflorum (Burm.f.) Andr., suggested that it might be preying on thrips infesting the flowers. This paper details laboratory observations made to determine the possibility of thrips predation by R. forticornis and, thereby, to assess further the prevalence of predatory behaviour in this mirid species.

Material and Methods

Activity of both adult and nymphal R. forticornis initially was observed within a jasmine hedge located on the Manoa campus of the University of Hawaii. Bugs were observed only on inflorescences harboring Thrips orientalis (Bagnall) and T. hawaiiensis (Morgan). On occasion, an adult mirid would enter the corolla tube of an individual flower. These observations prompted a desire for more detailed study under controlled conditions. Thrips-infested flowers were cut at their bases with fine dissecting scissors and held in covered plastic petri dishes lined with moistened filter paper. Preliminary tests showed that jasmine flowers would remain fresh (indicated by absence of browning) for at least four days under these conditions. Adult bugs were aspirated from inflorescences. Aspirator vials were lined with a cotton ball to insure that bugs were not injured during collection. Flower and insect specimens were returned to the laboratory.

In the laboratory, two bugs were added to each of five petri dishes containing two thrips-infested flowers. The flowers contained only adult thrips, which generally restricted their activity to within corolla tubes and petal surfaces. Observations were made under a dissecting microscope during periods over the next 24 hours. In a second experiment, 10 R. forticornis (two 3rd-instar nymphs and eight adults) were collected (two per aspirator vial) from jasmine inflorescences. In the laboratory, they were introduced in pairs into each of five petri dishes containing two bean pods (Phaseolusvulgaris L.) infested with adults and larvae of western flower thrips, Frankliniellaoccidentalis (Pergande). Bugs were allowed one-half hour to become familiar with their new surroundings. Observations on all petri dishes were made continuously for a total period of more than three hours.

Results

Results of the first experiment were inconclusive. Bugs initially wandered throughout the dishes, but generally reduced their restlessness within one-half hour, and were often found, thereafter, on the flowers. They were not observed to probe flowers with their rostra. The mirids also showed no interest in the thrips even when a thrips ventured close. When contacted by a thrips, however, the bugs would immediately retreat, often resuming a brief roaming around the dish. After 24 hours, there was no evidence that any thrips had been consumed (i.e., no thrips cadavers were found in flowers or elsewhere in the petri dishes).

By contrast, within 20 minutes of commencing observations in the second experiment, the first attack was seen. A Rhinacloa nymph, previously observed feeding on a bean pod, moved rapidly into the field of vision and came upon a 2nd-instar¹⁵ thrips larva cannibalizing a conspecific of similar age. The larva was immediately pierced with the rostrum (as evidenced by flexing of the labial sheath) through the dorsum of the abdomen and pulled away from the cannibalized victim. Feeding by the bug continued for more than eight minutes, during which time the thrips, its antennae in feeble motion the entire time, became progressively deflated and curled ventrally. The attack ceased abruptly when the nymph was disturbed by an adult thrips. (This nymph was later observed feeding on a 1st-instar thrips.)

In a second observed attack, by an adult bug, the body of a 1st-instar larva was alternately drained of fluid almost completely, then re-expanded (presumably with saliva) six times over a period of about eight minutes. The victim was finally abandoned as a dried, wrinkled, and flattened husk. This inflation-deflation action was observed in a number of subsequent attacks on other thrips.

In addition to attacking active prey, R. forticornis adults were observed to feed upon moribund larvae and the partially desiccated cadavers of larvae. Prey of all instars were commonly held in position by adult bugs with the fore tarsi, and probed with the rostrum through various areas of the head, thorax, and abdomen until drained of fluid.

Adult thrips were not successfully attacked. However, the R. forticornis nymph, on which first observations were made, was observed twice in brief, apparent attacks on adult thrips. These were aborted immediately as the thrips moved rapidly away.

Both nymphal and adult bugs were often observed feeding at the freshly cut ends of bean pods. While engaged in such feeding, bugs would often ignore nearby thrips larvae, showing no aggressive response even to contact by larvae.

Discussion

This study clearly demonstrated predation on thrips by R. forticornis. More than 10 separate attacks, by several individuals of different stages, were carefully observed, suggesting that the behaviour is not uncommon for the bug and that thrips are acceptable prey. Other mirids have been reported as occasionally taking thrips prey in the laboratory (e.g., Rajasekhara et al.,).¹⁶ In the present circumstances, successful attacks were made only on thrips larvae. The rostra of phytophagous Heteroptera are more limited in their freedom of movement and penetrability than are those of predatory forms,¹⁷ and thrips larvae may have been preferred as prey by R. forticornis over adult thrips because their less sclerotized cuticle could be more easily pierced. Also, thrips larvae are smaller and slower in their movements than adults and probably represent an easier target of opportunity with a higher probability of successful capture. Prey of R. forticornis reported by Herrera¹³ were similarly sedentary and soft-bodied. Under such circumstances, given a choice of prey stage, bugs of predaceous groups (e.g., Anthocoridae)¹⁸ similarly opt to attack thrips larvae over adults.

The manner in which R. forticornis handled prey was suggestive of similar repertoires of predaceous Heteroptera. In particular, the mirid’s use of its fore tarsi to position and manipulate prey and its probing in different body regions also are common behaviours in anthocorids.^4,19,20 Moreover, the rather lengthy duration of feeding, accompanied by the apparent alternation between egestion and re-ingestion of saliva, employed typically by predaceous types to liquefy and further digest prey tissues,^21,22 suggested a tendency in R. forticornis towards some predation. This mode of feeding, characterized by extra-oral digestion, is suggested as one factor contributing to the high incidence of omnivory in Heteroptera.²³

The opportunistic taking of animal food is known in a number of mirid species, some of which are notorious crop pests (e.g., Lygus),²⁴ and may be an important factor in their nutritional ecology.²⁵ Although predatory behaviour in R. forticornis was plainly evident in the present study, its prevalence and importance to the species remain in doubt. Observations of apparently preferential feeding on freshly exposed bean pod tissue, while ignoring easy prey nearby and even in contact, suggest that phytophagy is an important, perhaps predominant, feeding mode in this plant bug, with predation occurring in nature in the absence of acceptable plant food.

Acknowledgements

I thank D.M. Tsuda, University of Hawaii, for making and confirming thrips determinations, and A.G. Wheeler, Jr., Clemson University, for his critical review of an earlier draft of the manuscript.

Refrences

1. Carvalho, J. C. M. Mirídeos neotropicais, XXX: gêneros Ellenia Reuter, Eurychilopterella Reuter, e Rhinacloa Reuter, com descrições de espécies novas (Hemíptera). Bol. Mus. Nac. (N.S.) Zool. (85): 1-12 (1948).
2. Knight, H. H. The plant bugs, or Miridae, of Illinois. Bull. Ill. Nat. Hist. Surv.22(1): 1-234 (1941).
3. Wene, G. P. and Sheets, L. W. Relationship of predatory and injurious insects in cotton fields in the Salt River Valley of Arizona. J. Econ. Entomol.55(3): 395-398 (1962).
   CrossRef
4. Robinson, R. R., Young, J. H., and Morrison, R. D. Strip-cropping effects on abundance of predatory and harmful cotton insects in Oklahoma. Environ. Entomol.1(2): 145-149 (1972).
   CrossRef
5. Ingram, W. R. Preliminary indications of the status of Rhinacloa forticornis as a pest of Sea Island cotton in Barbados. Trop. Pest Manage.26(4): 371-376 (1980).
   CrossRef
6. Beingolea G., O. D. Notas sobre la bionómica de arañas e insectos benéficos que ocurren en el cultivo de algodón. Revta. Peru. Ent. Agríc.2(1): 36-44 (1959).
7. Johnson, M. W. and Nafus, D. M. Melon thrips. In: Biological Control in the Western United States: Accomplishments and Benefits of Regional Research Project W-84, 1964–1989 (Eds.: J. R. Nechols, L. A. Andres, J. W. Beardsley, R. D. Goeden, and C. G. Jackson). University of California, Division of Agriculture and Natural Resources, Berkeley, CA, pp. 79-80 (1995).
8. Knight, H. H. Taxonomic review: Miridae of the Nevada Test Site and the western United States. Brigham Young Univ. Sci. Bull. Biol. Ser.9(3): 1-282 (1968).
9. Gagné, W. Stenotus binotatus (Fabricius), Rhinacloa forticornis Reuter, and Xylosandrus compactus Eichhoff. Notes and exhibitions. Proc. Hawaii. Entomol. Soc. 21(1): 18-19 (1971).
10. McGregor, E. A. and McDonough, F. L. The red spider on cotton. USDA Bull. (416): 1-72 (1917).
11. Butler, G. D., Jr. Temperature and the development of Spanagonicus albofasciatus and Rhinacloa forticornis. J. Econ. Entomol.63(2): 669-670 (1970).
    CrossRef
12. Stoner, A. and Bottger, G. T. Spanogonicus [sic] albofasciatus and Rhinacloa forticornis on cotton in Arizona. J. Econ. Entomol.58(2): 314-315 (1965).
    CrossRef
13. Herrera Arangüena, J. M. Investigaciones sobre las chinches del género Rhinacloa (Hemiptera: Miridae) controladores importantes del Heliothis virescens en el algodón. Revta. Peru. Ent.8(1): 44-60 (1965).
14. Joyce, C. R. Rhinacloa forticornis Reuter. Notes and exhibitions. Proc. Hawaii. Entomol. Soc.18(2): 207 (1963).
15. Vance, T. C. Larvae of the Sericothripini (Thysanoptera: Thripidae), with reference to other larvae of the Terebrantia, of Illinois. Ill. Nat. Hist. Surv. Bull.31(5): 145-208 (1974).
16. Rajasekhara, K., Chatterji, S., and Ramdas Menon, M. G. Biological notes on Psallus species (Miridae: Hemiptera), a predator of Taeniothrips nigricornis Schmutz (Thripidae: Thysanoptera). Indian J. Ent. 26(1): 62-66 (1964).
17. Elson, J. A. A comparative study of Hemiptera. Ann. Entomol. Soc. Am.30(4): 579-597 (1937).
    CrossRef
18. Bailey, S. F. The biology of the bean thrips. Hilgardia7(12): 467-522 (1933).
19. Salas-Aguilar, J. and Ehler, L. E. Feeding habits of Orius tristicolor. Ann. Entomol. Soc. Am.70(1): 60-62 (1977).
    CrossRef
20. Isenhour, D. J. and Yeargan, K. V. Interactive behavior of Orius insidiosus (Hem.: Anthocoridae) and Sericothrips variabilis (Thys.: Thripidae): predator searching strategies and prey escape tactics. Entomophaga26(2): 213-220 (1981).
21. Miles, P. W. The saliva of Hemiptera. Adv. Insect Physiol.9: 183-255 (1972).
    CrossRef
22. Cohen, A. C. Feeding adaptations of some predaceous Hemiptera. Ann. Entomol. Soc. Am.83(6): 1215-1223 (1990).
    CrossRef
23. Coll, M. and Guershon, M. Omnivory in terrestrial arthropods: mixing plant and prey diets. Annu. Rev. Entomol.47: 267-297 (2002).
    CrossRef
24. Wheeler, A. G., Jr. Lygus bugs as facultative predators. In: Lygus Bug: Host-Plant Interactions (Eds.: D. R. Scott and L. E. O’Keeffe). University Press of Idaho, Moscow, ID, pp. 28-35 (1976).
25. Wheeler, A. G., Jr. Studies on the arthropod fauna of alfalfa. VI. Plant bugs (Miridae). Can. Ent.106(12): 1267-1275 (1974).
    CrossRef