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Prey-mediated Dispersal Behavior of pumilio (Coleoptera: )

Article in Environmental Entomology · April 1987 DOI: 10.1093/ee/16.2.415

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CHRISTOPHER J. CEDEN,1 JOHN C. STOFFOLANO, JR., ANDJOSEPH S. ELKINTON Department of Entomology, University of Massachusetts, Amherst, Massachusetts01003

Environ.Entomol.16: 415-419 (1987) ABSTRACT Dispersal behavior of the histerid predator, Carcinops pu.milio (Erichson), was examined from the standpoint of life-history parameters and nutritional background. No significant differences were found between dispersing and nondispersing populations with respect to sex ratios, mating condition, parity, ovarian development, or morphometric characters. Flight and phototactic behaviors of dispersing were reversed following administration of a dipteran prey meal. Withholding prey from beetles that had previously fed on many prey induced a delayed flight response which began on day 4 after deprivation, peaked on days 5 and 6, and returned to initial levels by day 9.

KEY WORDS Carcinops pu.milio, dispersal, predation

Carcinops pumilio (Erichson), is a histerid pred- vestigate dispersal in C. pumilio with respect to ator commonly found in commercial egg-produc- the following: physiological age (mating condition, tion facilities (Legner & Olton 1970, Pfeiffer & parity, and ovarian state) of dispersers and non- Axtell 1980). Adult and immature beetles inhabit dispersers; sex ratios of dispersers compared with the surface layers of the manure and forage for nondispersers; morphometric analysis of dispersers dipteran and acarine prey, and thus are interesting and nondispersers; and potential for reversal and from the standpoint of filth fly pest management induction of dispersal under experimental condi- (Peck & Anderson 1969, Axtell 1981). Now cos- tions. mopolitan, C. pumilio is believed to have origi- nated in Africa (Hinton 1945), and may have lived Materials and Methods in the nests of wild birds prior to man's domesti- cation of fowl (Hicks 1959). Beetles were collected from a commercial egg- Despite the widespread distribution of this bee- production facility with a long history of natural tle in nature and the very high population densi- house fly suppression in Hubbardston, Mass. For ties found in poultry houses, little is known of its comparisons of "dispersing" and "nondispersing" means of movement from one farm to another, a C. pumilio, dispersers were defined as those bee- distance that frequently spans many kilometers. tles that were actively climbing the inside walls of Under normal circumstances, Carcinops is re- poultry houses, and were collected by gently pelled by strong light and rarely flies. During a scraping individuals from the walls with a putty study of the bionomics of fly predators in Massa- knife. Nondispersing beetles were collected be- chusetts (Geden & Stoffolano 1987), we occasion- neath the manure surface with a moistened paint- ally observed large numbers of adult beetles brush. climbing the inside walls of poultry houses, flying Morphometric Analysis of Dispersers and about the overhead lights, and initiating flight from Nondispersers. To test the possibility that dispers- windows. al was a delayed response to competition among Such incidents of dispersal did not appear to be larvae, which resulted in the production of smaller correlated with calender date, but occurred at var- adults, morphometric measurements of dispersers ious times and to varying degrees from May to and nondispersers collected in the field were made. September. Times of peak dispersal coincided with Only females were measured, because there are long manure accumulation times (3-4 mo), when slight size differences in certain characters be- adult C. pumilio populations are most abundant tween sexes (Ceden & Stoffolano 1987). Measure- and immature beetles are present in relatively low ments were made of 25 dispersing and nondis- numbers (Ceden 1984). persing C. pumilio using an ocular micrometer The objectives of the present study were to in- under a dissecting microscope. The following characters were measured for each individual: head width across eyes (HW); maximum pronotal width

I Currentaddress:Dep.of Entomology,NorthCarolinaState (PWM); pronotal width across points at head Univ.,Raleigh,NC 27695-7613. (PWH)j maximum pronotal length (PLM); right

415 416 ENVIRONMENT AL ENTOMOLOGY Vol. 16, no. 2 elytral width at anterior end (EW A); maximum Flight initiation was investigated by the use of right elytrallength (ELM); diagonal length of right take-off chambers. Each chamber consisted of a elytron from inner left (anterior) to outer right ca. 500-ml paper container with a clear plastic lid. (posterior) points (ELD); and the lengths of the A 30-ml plastic cup filled two-thirds full with sand, fore, middle, and hind femora (FF, MF, HF) and with a dental-wick bridge arching across the sur- tibiae (FT, MT, HT). Data were analyzed by one- face of the sand, was placed inside the chamber. way analysis of variance. The bridge was essential for monitoring flight ini- Sex Ratios and Reproductive Status of Dispers- tiation because beetles were reluctant to take off ers and Nondispersers. Sex ratios of dispersers and from the flat surface of the sand. nondispersers were determined by dissecting 200 Beetles were introduced, in replicates of 20 bee- beetles collected on each of three sample dates in tles per chamber, onto the surface of the sand in 1980 and 1981. Additional female beetles were the inner container. Chambers were then placed collected for determinations of mating condition, near a south-facing window in a room with no parity (oviposition history), and ovarian condition. artificial lighting for a I-h observation period. Be- One hundred live dispersing and nondispersing C. cause beetles were unable to climb the surface of pumilia females were dissected in physiological the inner container, any that were found in the saline for determination of parity as evidenced by outer container after 1 h were scored as positive the presence of follicular relics ("yellow bodies," for flight initiation. Ten replicates of dispersers and corpora lutea) at the bases of the lateral oviducts. nondispersers were tested in both the phototactic In addition, the spermathecae of 25 beetles from and flight assays. Differences between dispersers each group were examined under a compound mi- and nondispersers were analyzed by one-way anal- croscope for the presence of sperm. Possible dif- ysis of variance (ANOV A). ferences between dispersing and nondispersing Effects of Feeding Treatments on Dispersing beetles with respect to sex ratios, parity, and mat- C. pumilio. To test whether dispersal was appeti- ing condition were analyzed by two by two x2 tests tive and driven by hunger, dispersers were col- of independence (Sokal & Rohlf 1981). Finally, the lected from the field, subjected to pretreatment ovarian condition of 25 female dispersers and non- phototactic and flight assays as described above, dispersers was determined. C. pumilia has four then held for 24 h on four different feeding treat- ovarioles per ovary and develops and deposits eggs ments. These were: water only (saturated dental singly (Ceden 1984). The condition of the two wick); water plus granulated sucrose; "prey-free" most-developed oocytes was therefore determined manure, which had been collected in the field, by dissecting specimens under a dissecting micro- thoroughly dried in a microwave oven, and re- scope and ascribing an index value ranging from moistened to ca. 60% water; and water plus house 1 to 3 according to the following criteria: 1, un- fly eggs and newly hatched larvae. After 24 h on developed oocyte, no visible yolk deposition these feeding treatments, beetles were assayed through early-developed oocyte, some yolk, length again for phototaxis and flight initiation. Phototax- :::;0.35mm; 2, oocyte length 0.35-0.65 mm; 3, ma- is tests were run with 50 beetles per replicate and ture oocyte, length >0.65. Separate G tests of in- five replicates per treatment, and flight assays were dependence (Sokal & Rohlf 1981) were conducted conducted with 25 beetles per replicate and five on the frequency of dispersing and nondispersing replicates per treatment. Differences among treat- beetles that fell into the described oocyte cate- ments within flight and phototaxis assays were gories for the most and second most-developed 00- analyzed by one-way analysis of variance and Stu- cytes. dent-Newman-Keuls range test (Newman 1939). Phototactic and Flight Initiation Responses of Induction of Dispersal in Prey-deprived Bee- Dispersers and Nondispersers. Dispersing and tles. The effect of prey deprivation on flight in- nondispersing c. pumilia were first tested for pho- duction was also investigated. Beetles used in this totactic response in a simple light/dark choice study were obtained from a laboratory culture and chamber, which consisted of a 30-cm length of were approximately 4 wk old at the start of the clear plastic tubing (20 mm diameter) with clear experiment. For the first 4 wk of life, beetles were plastic cups affixed to either end. Half the length maintained in CSMA house fly medium with high of the tubing and one of the collecting cups were densities of larvae of the small dung fly, Coproica wrapped in black electrical tape; the other half hirtula (Rondani) (Diptera: Sphaeroceridae), in a and its cup were left clear. The light end of the rearing room maintained at 30-31°C, 24 h light chamber was oriented toward a south-facing win- and 60-70% RH. C. hirtula is a natural prey item dow in a room with no artificial lighting. Tests in the diet of C. pumilio in the field and is more were run within 4 h of collections between easily manipulated for beetle maintenance than is 1300 and 1500 hours (EST). A replicate consisted the house fly (Ceden 1984). After 4 wk on this diet, of 50 beetles introduced into the middle of the beetles were transferred to containers with mois- chamber through a hole at its midpoint. For the tened dental wick only and assayed daily for flight following 5 min, beetles found in the light end of initiation. Assays were conducted with 20 beetles the chamber were counted and scored as photo- per replicate, 15 replicates per day. Between assays, positive. beetles were returned to the rearing room. An equal April 1987 GEDEN ET AL.: DISPERSAL BEHAVIOR OF Carcinops pumilio 417

Table 1. Comparisons of sex ratios, parity, and ovarian condition of dispersing and nondispersing C. pumilia collected from poultry bouses

Sex ratios" Collection no. Dispersers Nondispersers

%d 61 64 %2 39 36 x2 = 0.192; P > 0.05 %a 2 58 54 %2 2 42 46 x2 = 0.325; P > 0.05 %d 3 54 57 %9 3 46 43 x2 = 0.182; P > 0.05 Parity· % parous 94 98 % nulliparous 6 2 x2 = 2.08; P > 0.05

Ovarian condition, oocyte I b No. in oocyte category 1 2 2 No. in oocyte category 2 7 9 No. in oocyte category 3 16 14 G/q = 0.202; P > 0.05 Ovarian condition, oocyte 2b No. in oocyte category 1 6 7 No. in oocyte category 2 16 15 No. in oocyte category 3 3 4 G/q = 0.549: P > 0.05

a X2 test based on numbers of beetles; df = 1. b df = 2. number of replicates were assayed using beetles persers (F = 193.70; df = 1,18; P < 0.001; that were fed daily on frozen house fly eggs. ANOVA). Observation of beetles in the flight chambers confirmed that those that were found in the outer Results containers at the end of the observation period had Morphometric Analysis of Dispersers and flown and not crawled from the inner container. Nondispersers. No significant morphometric dif- Dispersing beetles displayed a characteristic be- ferf.'nces (F < 3.0 in all cases; df = 1,48; P > 0.05; havior of crossing and recrossing the dental wick ANOVA) were found between dispersing and non- bridge before taking off. Beetles that flew struck dispersing beetles for any of the characters that the walls of the outer container and fell to the were examined (not presented in a table). bottom. Nondispersing beetles, on the other hand, Sex Ratios and Reproductive Status of Dispers- usually did not climb the arched wick, but bur- ers and Nondispersers. No significant differences rowed into the sand at its base. Most nondispersers in sex ratios were found between dispersing and which did climb the wick did not display the cross- nondispersing beetles on any of the three collec- ing and recrossing behavior of the dispersers, ex- tion dates, with a total, male-biased sex ratio of cept for the small percentage that flew. male/female 348:252 (Table 1). Similarly, no sig- During handling of these beetles collected in the nificant differences between dispersers and non- field, another behavioral difference was noted. dispersers were found with respect to parity or the Nondispersers, when touched by the paint brush, condition of the two most-developed oocytes (Ta- frequently exhibited thanatosis (Hinton 1945), re- ble 1). All beetles that were examined for mating tracting the head and legs for as long as 1 min. status were found to have mated (not presented in Dispersers, on the other hand, did not show this table). behavior, but continued to move actively when Phototactic and Flight Initiation Responses of contacted. Field-collected Dispersers and Nondispersers. Effects of Feeding Treatments on Dispersers. When field-collected dispersing and non dispersing Results of the tests for the effect of diet on the c. pumilio were assayed for phototactic response, behavior of dispersers collected in the field are 47.0 dispersers (94.0%) oriented towards the light presented in Table 2. Pretreatment assays on the end of the chamber; in contrast, only 14.4 (28.8%) day of collection confirmed that beetles were in of the nondispersers were positively phototactic dispersal mode, with 90% showing a positive pho- (F = 780.81; df = 1,18; P < 0.001; ANOV A). Dif- totactic response and 92% initiating flight. Main- ferences were even more pronounced in flight ini- taining these beetles for 24 h on water and water tiation assays, where 18.1 dispersers initiated flight plus sucrose had no significant effect on either dis- (90.4%) compared with 0.4 (2.2%) of the nondis- persal-related behavior. Administration of "prey- 418 ENVIRONMENTAL ENTOMOLOGY Vol. 16, no. 2

Table 2. Phototactic response and Bight initiation of dispersing C.pumilio collecled in the field before and after 80 being maintained for 24 h on four different feeding treat- ments

f no. f no. l- 60 positively initiating I phototactic" flightb Cl :J u.. Pretreatment 44.8a 22.9a I- Z 40 After 24 h on W () Water only 43.6a 23.4a a: Water and sucrose 4l.0a 19.3a W D.. Prey-free manure 34.3ab 13.6ab 20 Water and prey l.8b l.2b

a Means followed by the same letter within a column are not si\nificantly different (P > 0.05; Student-Newman-Keuls test). Based on five replicates of 50 and 25 beetles per treatment in o phototactic and flight initiation assays, respectively. 2 3 4 5 6 7 8 9 10 DA YS SINCE FEEDING free" manure had a slight, but not statistically sig- Fig. 1. Flight initiation response of C. pumilio that nificant, effect on both behaviors. Beetles that were were placed on water-only regimes after being main- allowed to feed on prey showed a profound re- tained for 4 wk on a diet rich in dipteran prey. versal in dispersal behavior, with only ca. 4% at- tracted to light and initiating flight. Induction of Dispersal in Prey-deprived C. has several parallels with other species, although pumilio. The effect of prey deprivation on colony most examples of this phenomenon are from phy- beetles previously fed on many prey is illustrated tophagous species. Meyer (1982) has shown that in Fig. 1. On the first day of starvation, virtually the alfalfa weevil exhibits two flight periods, one none of the beetles initiated flight. Flight initiation of which is a postteneral, prereproductive, predia- remained infrequent on the following 2 d, but on pause syndrome. A second, postdiapause period of day 4, a sudden increase in flight propensity was flight may be induced by withholding fresh alfalfa observed, which increased further on day 5 to 67% from the beetles (Meyer 1982). Dingle & Arora and remained high on day 6. Flight initiation then (1973) found that female Dysdercus spp. histolyze dropped on day 7. On days 9 and 10, no flight was the flight muscles and develop eggs when fed con- observed at all. No flight was observed at any time tinuously after eclosion, but undergo flight if among prey-fed controls (not presented in figure). starved for several days following emergence. The bugs continue to fly and do not histolyze the flight muscles until they are presented with food. Sol- Discussion breck & Pehrson (1979) found similar results with The majority of migrating species that have been another seed bug, Neacoryphus bicrucis (Say), and studied migrate as postteneral adults before the noted a critical balance among food density, egg development or deposition of the first egg batch production, diapause-inducing conditions, and mi- (Dingle 1965, 1966, Johnson 1969, Messina 1982, gration. Meyer 1982). In the present study, no evidence for Rankin (1978) investigated hormonal regulation this "oogenesis flight syndrome" was found in C. of flight in Oncopeltus fasciatus (Say) and re- pumilio, most dispersing beetles having under- viewed the literature available on other species. In gone at least one oviposition. In this species, the Oncopeitus, starvation or feeding on suboptimal use of follicular relics as an indicator of age may, food items causes recently emerged females to de- however, mask real age differences between the lay reproduction and undergo long flights. Juve- two groups. Mated, parous females may have lived nile hormone (JH) was found to playa dual role as long as 8 or 380 d (Ceden 1984). Further ex- in modulating reproductive and migratory efforts. perimental work with individuals of known pre- Stengel (1974) found that JH plays a role in the cise age is needed. direction, as well as the expression, of flight in the Administration of prey in the form of house fly migratory cockchafer, Me/oiontha melolontha L. eggs and larvae was found to reverse both param- In the present study, Carcinops also showed a de- eters of dispersal measured in this study, photo- layed response to starvation, with virtually no flight taxis and flight initiation. Water-only and water- being noted until day 4 of deprivation. JH may plus-sucrose treatments had no significant effect on play a role in the flight of this species as well, these behaviors, suggesting that if dispersal in this although perhaps in a different manner. Because species is appetitive, it is not driven and main- ovarian condition appears to have no effect on tained by water or carbohydrate deprivation. flight, it is possible that high JH titers associated The observation that flight could be induced by with feeding and subsequent ovarian development withholding the usual food source from Carcinops inhibit flight, this behavior being released in re- April 1987 GEDEN ET AL.: DISPERSAL BEHAVIOR OF Carcinops pumilio 419

sponse to lower titers. Because males appear to vidual milkweed bugs (Oncopeltus). J. Exp. BioI. 44: disperse as readily as females, other hemolymph- 335-343. borne factors associated with feeding may be in- Dingle, H. & G. K. Arora. 1973. Experimental stud- volved as well. ies of migration in bugs of the genus Dysdercus. Oecologia (Berlin) 12: 119-140. The observed decline in £light after day 6 is Elsey, K. D. 1974. Jalysus spinosus: effect of age, more difficult to interpret. Beetles that have fed starvation, host plant, and photoperiod on £light ac- on many prey can survive on water alone for 30 tivity. Environ. Entomol. 3: 653-655. d before significant mortality is observed (Geden Geden, C. J. 1984. Population dynamics, spatial dis- 1984). On days 7-10, when flight declined, beetles tribution, dispersal behavior and life history of the clearly had not exhausted their nutrient reserves, predaceous histerid, Carcinops pumilio (Erichson), but appeared to have responded to internal cues with observations of other members of the poultry that shut off flight. A similar rise and fall in levels manure community. Ph.D. dissertation, of flight behavior in response to starvation has been Univ. of Massachusetts, Amherst. Geden, C. J. & J. G. Stoffolano, Jr. 1987. Succession observed in the stilt bug, lalysus spinosus (Say) of manure at a poultry farm in Massa- (Elsey 1974), and represents one of the few inves- chusetts, with observations on Carcinops pumilio sex tigations of this phenomenon in a generally flight- ratios, ovarian condition and body size. J. Med. Ento- less predator. J. spinosus, when deprived of its mol.: 24: 214-222. usual prey (tobacco horn worm eggs), did not show Hicks, E. A. 1959. Check-list and bibliography on significant flight activity until day 4 after depri- the occurrence of in birds' nests. Iowa State vation. Flight continued to increase and peaked Univ., Ames. on day 7, followed by a gradual decline to the level Hinton, H. E. 1945. The Histeridae associated with of fed controls on day 12. In contrast to Carcinops, stored products. Bull. Entomol. Res. 35: 309-340. Johnson, C. G. 1969. Migration and dispersal of in- however, the decline in lalysus flight appeared to sects by £light. Methuen, London. be associated with decreasing fuel reserves, be- Legner, E. F. & G. S. Olton. 1970. Worldwide survey cause mortality was much higher toward the end and comparison of adult predator and scavenger in- of the starvation period than at the beginning, and sect populations associated with domestic ma- higher than the fed controls at the same time (El- nure where livestock is artificially congregated. HiI- sey 1974). gardia 40: 225-256. Before the domestication of fowl and the ensu- Messina, F. J. 1982. Timing of dispersal and ovarian ing artificial accumulation of large and stable de- development in goldenrod leaf beetles, Trirhabda posits of poultry manure, C. pumilio was presum- virgata and T. borealis. Ann. Entomol. Soc. Am. 74: 78-83. ably associated with the nests of wild birds, where Meyer, J. R. 1982. Physical and biological prereq- it fed on dipterans and other prey. Given the tem- uisites for flight activity in the alfalfa weevil, Hypera porary nature of these natural habitats, selection postica (Coleoptera: Curculionidae). Ann. Entomol. for prey-mediated dispersal behavior seems to have Soc. Am. 75: 922-998. been strong. In modern, multihouse poultry-pro- Newman, D. 1939. The distribution of range in sam- duction facilities, this behavior may result in bee- ples from a normal population, expressed in terms of tles leaving poultry houses where there are few an independent estimate of standard deviation. Bio- prey and colonizing adjacent houses where flies are metrika 31: 20-30. more abundant. Further work is needed to deter- Peck, J. H. & J. R. Anderson. 1969. Arthropod pred- ators of immature Diptera developing in poultry mine the distance that individual Carcinops can droppings in northern California. I. Determination, fly, and the factors that shut off flight and lead to seasonal abundance and natural cohabitation with foraging in new habitats. prey. J. Med. Entomol. 6: 163-167. Pfeiffer, D. G. & R. C. Axtell. 1980. Coleoptera of poultry manure in caged layer houses in North Car- Acknowledgment olina. Environ. Entomol. 9: 21-28. We thank Louis Ruggles for his helpful comments Rankin, M. A. 1978. Hormonal control of mi- and suggestions, and the Massachusetts Society for Pro- gratory behavior, pp. 5-32. In H. Dingle [ed.], Evo- moting Agriculture for support. Support was also pro- lution of insect migration and dispersal. Springer, vided by Massachusetts Agricultural Experiment Station New York. Project 471. Paper No. 2679, Massachusetts Agricultural Sokal, R. R. & F. J. Rohlf. 1981. Biometry. W. H. Research Station, University of Massachusetts, Amherst. Freeman, San Francisco. Solbreck, C. & I. Pehrson. 1979. Relationship be- tween environment, migration and reproduction in References Cited a seed bug, Neacoryphus bicrucis (Say) (Heterop- tera: Lygaeidae). Oecologia (Berlin) 43: 51-62. Axtell, R. C. 1981. Use of predators and parasites in Stengel, M. M. C. 1974. Migratory behavior of the filth fly IPM programs in poultry housing. Status of female of the common cockchafer Melolontha mel- biological control of filth flies. U.S. Dep. Agric. olontha L. and its neuroendocrine regulation. pp. AI06.2.F64: 26-43. 297-303. In L. Barton-Browne [ed.], Experimental Dingle, H. 1965. The relation between age and flight analysis of insect behavior. Springer, New York. activity in the milkweed bug, Oncopeltus. J. Exp. BioI. 42: 269-283. Received for publication 16 August 1985; accepted 8 1966. Some factors affecting flight activity in indi- December 1986.

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