On Bark Beetle Larvae (Coleoptera: Scolytidae)

COMMUNITY AND ECOSYSTEM ECOLOGY Facultative Intraguild Predation by Larval Cerambycidae (Coleoptera) on Bark Beetle Larvae (Coleoptera: Scolytidae)

1 KEVIN J. DODDS, CAELIN GRABER, AND FREDERICK M. STEPHEN

Department of Entomology, University of Arkansas, A-320, Fayetteville, AR 72701

Environ. Entomol. 30(1): 17Ð22 (2001) Downloaded from https://academic.oup.com/ee/article/30/1/17/438228 by guest on 23 September 2021 ABSTRACT Larvae of the Carolina sawyer Monochamus carolinensis (Olivier) (Cerambycidae) and bark beetle larvae (Scolytidae) often simultaneously feed in phloem of recently killed pine trees. Our investigations reveal that M. carolinensis larvae may act as facultative intraguild predators of bark beetle larvae. Phloem sandwiches were used in four experiments to examine inter- and intraspeciÞc interactions. We discovered that all sizes of M. carolinensis larvae killed bark beetle larvae. Seventy- six percent of the killed bark beetle larvae were consumed by M. carolinensis, including 58% that were entirely ingested. Cannibalism in M. carolinensis occurred in every experimental trial. Based on this evidence, M. carolinensis, and possibly related cerambycid species associated with bark beetles, are facultative intraguild predators of larvae of other phloem inhabiting species. The consequences of this behavior may have important implications for bark beetle population dynamics.

KEY WORDS Ips calligraphus, Ips, Monochamus carolinensis, intraguild predation, Cerambycidae, Scolytidae

LARVAE OF CERAMBYCIDAE are normally considered beetle progeny by 78%. Coulson et al. (1976) de- phytophagous, feeding on most parts of living and scribed competition between the cerambycid dying plants and trees (Craighead 1923; Linsley 1958, Monochamus titillator (F.) and the scolytid D. fron- 1959). However, larval cannibalism (Victorsson and talis. However, Flamm et al. (1989) later suggested Wikars 1996) and facultative predation on bark bee- that interactions occurring between M. titillator and tles (Hellrigl 1971) have been observed in several D. frontalis might better be deÞned as commensalism. cerambycid species. Conifer-inhabiting cerambycids Miller (1984) reported that M. titillator competed for often rapidly colonize dying or dead trees attacked by phloem resources with Ips calligraphus (Germar) scolytid bark beetles. Among the Scolytidae, bark bee- (Scolytidae) and had a signiÞcant negative effect on tle species, including Dendroctonus brevicomis Le- some subcortical predators (Miller 1985). Conte (Stephen and Dahlsten 1976), D. ponderosae Although competition has commonly been used as Hopkins (Dahlsten and Stephen 1974), D. adjunctus an explanation for bark beetle mortality, seldom have Blandford (Chansler 1967), and D. frontalis (SPB) direct observations of interactions between phloem- Zimmermann (Overgaard 1968, Moser et al. 1971, feeding species been performed. Analysis of bark sam- Dixon and Payne 1979) all have cerambycids reported ples in which immature bark beetle density is com- as associates. Release of pine host volatiles (Fatzinger pared with and without cerambycid foraging, or adult et al. 1987, Schroeder and Weslien 1994a) and a bark beetle emergence density is estimated as a func- kairomonal response (Billings and Cameron 1984) to tion of cerambycid foraging, has been used to estimate bark beetle pheromones results in some cerambycids bark beetle mortality. In these cases, mortality is usu- arriving on host trees coincident with or shortly fol- ally attributed to competition (Coulson et al. 1976, lowing bark beetle attack. This leads to spatial and 1980). We suggest an alternative, more complete ex- temporal coexistence of these two families in newly planation of mortality suffered by bark beetle larvae colonized host tree phloem. within phloem is that larger, more mobile cerambycid Interactions between bark beetle and cerambycid larvae may also function as facultative intraguild pred- larvae coexisting in the subcortical region of host trees ators on bark beetle larvae. typicallyhavebeendescribedascompetitive.Schroed- Intraguild predation is a combination of predation er and Weslien (1994b) investigated competitive in- and competition, where members of the same feeding teractions occurring between Acanthocinus aedilis guild prey upon each other (Polis et al. 1989). Exam- (L.) (Coleoptera: Cerambycidae) and Tomicus pin- ples of intraguild predation occurring in predaceous iperda (L.) (Coleoptera: Scolytidae) and found the insects are common (Wissinger and McGrady 1993, presence of cerambycids reduced production of bark Currie et al. 1996, Kester and Jackson 1996, Lucas et al. 1998, Phoofolo and Obrycki 1998); however, there 1 Current address: Department of Forest Science, 321 Richardson, are fewer examples of facultatively predaceous non- Oregon State University, Corvallis, OR 97331. carnivorous insects (e.g., Wissinger et al. 1996).

0046-225X/01/0017Ð0022$02.00/0 ᭧ 2001 Entomological Society of America 18 ENVIRONMENTAL ENTOMOLOGY Vol. 30, no. 1

The cerambycid Monochamus carolinensis colonizes were still feeding in phloem tissue when they were weakened and dying pine trees in the southeastern removed from bolts. Third and fourth stage larvae of United States (Baker 1972) and is often found in as- Ips calligraphus were obtained from a laboratory col- sociation with bark beetles (Moser et al. 1971). ony at University of Arkansas, Fayetteville. Monochamus carolinensis develop in phloem of host Phloem sandwiches were made using disposable trees for Ϸ3Ð4 wk before entering sapwood to con- polystyrene petri dishes (100 by 15 mm). A disk of struct U-shaped galleries in which pupation will later phloem (Ϸ8 cm in diameter) was cut to Þt into the top occur (Pershing and Linit 1986). During construction half of the petri dish. The smaller bottom half of the of sapwood galleries, larvae frequently return to the petri dish was placed so that its outer surface pushed phloem and feed near their entrance hole. Larval the phloem sample ßat. ParaÞlm was wrapped around length of M. carolinensis ranges from 2 mm at hatching the dish to maintain a seal and keep phloem pressed to Ϸ4 cm before pupation occurs. ßat between the petri dish halves. All surfaces, includ-

Ips calligraphus is a multivoltine polygynous bark ing the petri dishes and phloem samples, were steril- Downloaded from https://academic.oup.com/ee/article/30/1/17/438228 by guest on 23 September 2021 beetle found throughout eastern North America, ized using a weak bleach solution (Ϸ0.05%). where it inhabits most species of pine (Baker 1972). Before placement in the phloem sandwich, ceram- Freshly killed or injured trees are usually colonized by bycids were slightly ßattened between clean petri I. calligraphus but in drought years living trees may dishes and measured from the tip of the mandibles to also undergo attack. In the southern United States, I. the most posterior point of the abdomen using cali- calligraphus is often found inhabiting phloem of trees pers. To introduce cerambycids into the phloem, a killed and also colonized by D. frontalis (Paine et al. small (1.5 cm diameter) cork borer was used to make 1981, Wagner et al. 1985). Eggs of I. calligraphus are a circular hole into the phloem. In all experiments, deposited in galleries created within phloem of host cerambycid larvae were placed in the hole where the trees. Larvae develop, feed, and pupate in the phloem phloem was removed and held for 24 h until feeding region of host trees; those larvae developing in phloem was initiated and they had become established. range in length from 1 to 4 mm. Experiment 1: Predaceous Behavior of M. carolin- Larvae of Monochamus carolinensis and I. calligra- ensis Larvae. Experiment 1 tested the hypothesis that phus often simultaneously occupy and feed in phloem larvae of M. carolinensis were predaceous on larval Ips of recently killed pine trees. Because the newly cre- calligraphus. Ten cerambycid larvae were used in daily ated phloem resource is subject to rapid colonization experiments over a 6-d period leading to a total of 60 by an extensive and predictable complex of insects, trials. Each day, larva of one I. calligraphus was added mites, and fungi (Stephen et al. 1993), the ability to act to phloem sandwiches and interactions were observed as a facultative intraguild predator could provide M. for 1 h. Each larva of I. calligraphus was placed in the carolinensis with additional nutrition in an area where cerambycid gallery, as far away from the cerambycid competition for resources may be high. As an addi- larva as possible. Phloem sandwiches were resealed tional advantage, predation may eliminate present or and an attempt was made to minimize disturbance to future competitors and thus help to ensure that re- cerambycid galleries. Results of interactions of cer- sources remain plentiful. ambycid larvae with I. calligraphus larvae were noted Our initial observations of interactions occurring and recorded at 10-min intervals. between M. carolinensis and I. calligraphus suggested Interaction results were categorized as “unat- the possibility of a predator-prey interaction between tacked,”“attacked,”“killed,”“ingested,” or “con- these two phloem feeding species. Preliminary labo- sumed.” If a cerambycid larva encountered an I. cal- ratory experiments demonstrated that a high fre- ligraphus larva directly, but no aggressive reaction was quency of bark beetle larvae were killed and con- observed, the I. calligraphus was considered “unat- sumed by cerambycid larvae. Additionally, response tacked.” If a larva was “attacked,” and the I. calligra- to bark beetle larvae seemed to be dependent on the phus larva was still mobile and no damage to its cuticle size of cerambycid larvae. If predation is frequent, could be detected, it was considered “not killed.” The then it is possible that cerambycid species may play a I. calligraphus larva was recorded as “killed” only if more signiÞcant role in the population dynamics of visceral contents could be clearly identiÞed oozing bark beetles than previously believed. The objective around the attacked larva and all movement had of the research reported here is to better deÞne the ceased. “Ingestion” was said to take place if the I nature and frequency of this phenomenon. Intraspe- calligraphus larva had been noticeably reduced in size ciÞc interactions of cerambycids were also made and or if M. carolinensis larva grasped the I. calligraphus are here reported. larva in its mandibles and chewing motions were observed for Ͼ1 min. The larva was classiÞed as “completely consumed” only if the entire larva was eaten Materials and Methods during the 1-h observation period. Larvae of Monochamus carolinensis were obtained Experiment 2: Effects of M. carolinensis Larval Size from infested logs originating from a laboratory colony on Predaceous Behavior. Experiment 2 tested the hy- held by M. J. Linit at University of Missouri, Columbia. pothesis that length of larval cerambycids affected Larvae were Ϸ25 d old when our experiments were their response to bark beetle larvae. To determine if initiated, and varied in length from 1.0 to 2.6 cm. cerambycid larval size affected aggressive behavior, Larvae had not begun to create sapwood galleries and logistic regression of frequency of trials on larval February 2001 DODDS ET AL.: PREDATION BY LARVAL CERAMBYCIDAE ON BARK BEETLE LARVAE 19

bark beetle larva. Monochamus carolinensis attacked the other larvae in 74% of the trials. Eighty-Þve percent of those attacks resulted in immediate mortality to I. calligraphus larvae, and 76% of the larvae were at least partially ingested. Fifty-eight percent of those larvae that were ingested were entirely consumed. Experiment 2: Effects of M. carolinensis Larval Size on Predaceous Behavior. Whether or not an I. calligraphus larva was attacked (P Ͼ 0.36) or was killed (P Ͼ 0.33) was not signiÞcantly related to cerambycid larval size. Although there was a trend to feed upon I. calligraphus larvae more frequently, this was not sig-

niÞcant (P Ͼ 0.11). Larger M. carolinensis larvae were Downloaded from https://academic.oup.com/ee/article/30/1/17/438228 by guest on 23 September 2021 signiÞcantly more likely to consume bark beetle larvae, however (P Ͼ 0.01). Small cerambycids were never seen consuming I. calligraphus larvae completely, and often ignored bark beetle larvae once they had been attacked and killed. Experiment 3: Cannibalistic Behavior in M. carolinensis Larvae. In all Þve replicates of this experiment, one cerambycid larva attacked, killed, and at least partially consumed the other once an encounter occurred. Encounters did occur in all replicates within 5 d of initiating the experiment.

Discussion Our experiments clearly demonstrate that M. carolinensis is a facultative predator of bark beetle larvae and thus should be considered an intraguild predator during periods of its subcortical development. Facul- tative predation is not uncommon in phytophagous insects (Girault 1908, China 1953, Gangwere 1961, Fig. 1. Predatory behavior of cerambycid larvae in re- Lavigne and Pfadt 1964, Bowden and Phipps 1967, sponse to the presence of one I. calligraphus larvae added to Cooke 1968, Root and Chaplin 1976, Whitman and arena gallery. Raw numbers are shown in parentheses. Flow Orsak 1985, Root 1986, Trichilo and Leigh 1986, New chart begins with 60 trials (10 individuals observed daily for 1991, Wilson et al. 1996) and has been reported with 6 d). other bark beetle associates (Parker and Davis 1971, Goyer and Smith 1981). To our knowledge, however, with the exception of a brief comment by Hellrigl length was performed (SAS Institute 1996). Larval (1971), facultative predation by Cerambycidae has instar determination was not possible, although judg- not been previously described. ing from molting patterns, the size categories most We consider the aggressive behavior exhibited by probably reßected two different instars. Larval sizes M. carolinensis to be predator-like, although it is prob- fell within the range that is found in the Þeld in ably facultative rather than active. Monochamus caro- association with bark beetle broods (Graber 2000). linensis usually ignored I. calligraphus larvae in gal- Experiment 3: Cannibalistic Behavior in M. caro- leries unless close contact was made. Occasionally, linensis Larvae. Experiment 3 was conducted to de- even if M. carolinensis had direct contact with I. cal- termine if larvae of M. carolinensis were cannibalistic. ligraphus larvae, no attacks were observed. Ceramby- Two M. carolinensis larvae, matched according to their cid larvae actively pursuing I. calligraphus larvae in the size, were simultaneously placed at opposite margins phloem was rare, although we observed one larva from one another in petri dishes. Five replicates were enlarging an established I. calligraphus gallery in pur- conducted and results of interactions determined af- suit of its prey. Although phloem sandwiches used in ter 24 h of exposure. this study were small, we believe that ample phloem was available for cerambycid feeding throughout the study period. We also believe it is unlikely that the Results small size of the arena resulted in an artiÞcially high Experiment 1: Predaceous Behavior of M. carolin- probability of contact between the two beetle species. ensis Larvae. Illustrated in Fig. 1 is a dichotomous ßow The majority of I. calligraphus larvae encountered chart showing the outcome of 60 interactions between by M. carolinensis in experiment 1 were attacked and M. carolinensis and I. calligraphus larvae. In 10% of the killed, supporting our hypothesis that the cerambycid trials, the cerambycid failed to notice or ignored the would prey upon larvae of bark beetles. Seventy-six 20 ENVIRONMENTAL ENTOMOLOGY Vol. 30, no. 1 percent of I. calligraphus larvae killed were consumed calligraphus larvae consumed exhibited signiÞcant to some degree. Of the I. calligraphus larvae ingested, size dependence. Possibly, a pivotal point during de- roughly half were completely consumed by M. caro- velopment may exist where larvae will switch to more linensis. Predator satiation may explain why more I. predator-like behavior, however, aggressive or pro- calligraphus larvae were not fed upon. In some in- tective behavior, as shown by the number of attacks stances, M. carolinensis larvae were preparing to molt and kills, appears to lack size dependence. when Ips larvae were introduced and in these cases, Because predator-like behavior was so prevalent in cessation of feeding had already taken place. our initial trials, experiment 3 was conducted to ex- Monochamus carolinensis may incur multiple bene- amine the possibility of cannibalism in this species. Þts from ingestion of I. calligraphus larvae. Intraguild Cannibalism has been documented previously in a predation, a combination of competition and preda- laboratory experiment with a European cerambycid tion, offers many advantages (Polis et al. 1989). First, Monochamus sutor (L.) (Victorsson and Wikars 1996),

M. carolinensis may gain nutrition by ingesting animal and evidence for cannibalistic behavior in M. titillator Downloaded from https://academic.oup.com/ee/article/30/1/17/438228 by guest on 23 September 2021 material if phloem resources are limited or if phloem larvae has been observed in the Þeld (K.J.D., unpub- nutrient content is low. Insect bodies contain between lished data). Rose (1957) also found that several stages 6.6 and 12.0% dry weight nitrogen, while phloem con- of M. scutellatus (Say) were cannibalistic in logs of tains 0.1Ð2.2% dry weight nitrogen (Slansky and Abies balsamea. Scriber 1985). In circumstances when densities of In experiment 3, M. carolinensis killed and at least phloem feeding species are high, phloem resources partially consumed conspeciÞcs within phloem sand- may subsequently become less available. Further- wiches; however, they frequently tended to avoid more, phloem thickness has been shown to inßuence each other in these arenas until resources became performance of phloem-feeding species (Haack and scarce. This observation suggests that risking the Slansky 1987) and by feeding on other phloem inhab- chance of a cannibalistic encounter may be advanta- iting larvae cerambycids may gain essential nutrients geous only in high density circumstances. The advan- when phloem resources are of poor quality. tages of cannibalism would probably be similar to It has been demonstrated that improved nutritional those derived from interspeciÞc predation. quality may have an adaptive advantage for ceramby- The probability of cannibalism may have been ex- cid larvae by shortening development time. Hellrigl aggerated by creation of small arenas where ceram- (1971) found that another cerambycid species bycids were more likely to encounter each other, Monochamus sartor F. grew three times faster when however, the subcortical region of pine trees is a fed bark beetle larvae than when fed phloem alone. similarly closed system where high densities of cer- Evidence also exists that feeding cerambycids on an ambycids may crowd residents to a comparable de- artiÞcial diet shortens development time substantially gree. The size-dependent component of intraspeciÞc (references in Haack and Slansky 1987). It is likely that predation was not examined for M. carolinensis, al- M. carolinensis develops faster as a result of feeding on though this effect may be similar to laboratory trials I. calligraphus larvae, but this remains to be tested. conducted with M. sutor in which larger larvae can- In addition to possible nutritive beneÞts, M. caroli- nibalized smaller ones in most cases (Victorsson and nensis may reduce competition for limited food re- Wikars 1996). sources and simultaneously minimize numbers of Analysis of bark beetle population ßuctuations in predators within the phloem by acting as an intraguild the southern United States has resulted in different predator. Intraguild predation to reduce competition opinions as to factors responsible for the observed has been documented in marine arthropods (Ambrose changes that occur. Although density-independent 1984), ants (Rosengren 1986), termites (Leving and factors including climate and rainfall affect bark beetle Adams 1984), and parasitoids (Askew 1971). Miller populations (King 1972, Michaels 1984), recent re- (1985) reported that foraging by M. titillator reduced search supports the importance of density dependent numbers of natural enemies in pine bolts colonized by factors, particularly predation (Turchin et al. 1991, I. calligraphus. 1999; Reeve 1997). The effectiveness of M. carolinensis as a facultative In the southern United States, M. titillator popula- predator, or intraguild predator, may be size depen- tions are often found associated with D. frontalis in dent and may change through its developmental pe- bark beetle killed trees (Overgaard 1968, Moser et al. riods in phloem of host trees. Unfortunately, there is 1971, Dixon and Payne 1979). Dendroctonus frontalis no known technique for distinguishing instars of M. ßight and reproduction is continuous throughout carolinensis (Pershing and Linit 1989), although body much of the year in the South. It is an aggressive bark length appears well correlated with developmental beetle, which during outbreaks kills large numbers of stages (C.G., unpublished data). pine trees in discrete groups. Adult cerambycids that Preliminary laboratory experiments indicated that are present in D. frontalis infestations rapidly respond M. carolinensis size inßuences the behavioral outcome and colonize the freshly killed trees, continually of interspeciÞc encounters. Smaller cerambycids did breeding and numerically increasing in these bark not consume I. calligraphus larvae as frequently as beetle infestations. Because M. titillatorÕs life history is larger ones. Larger cerambycid larvae often consumed so similar to M. carolinensis, it is highly probable that some portion of I. calligraphus larvae provided during they are facultative predators on D. frontalis larvae in the experiment. In experiment 2, the number of I. phloem of host trees. Polis et al. (1989) suggest that February 2001 DODDS ET AL.: PREDATION BY LARVAL CERAMBYCIDAE ON BARK BEETLE LARVAE 21 intraguild predation can drastically reduce or elimi- Craighead, F. C. 1923. North American cerambycid larvae: nate local populations of prey items and that may be a classiÞcation and the biology of North American cer- important in the decline of D. frontalis populations ambycid larvae. Can. Dep. Agric. Tech. Bull. 27. following density-dependent intraguild predation by Currie, C. R., J. R. Spence, and J. Niemela¨. 1996. Competi- several generations of M. titillator. tion, cannibalism and intraguild predation among ground Quantitative surveys of cerambycid populations in beetles (Coleoptera: Carabidae): a laboratory study. Co- leopt. Bull. 50: 135Ð148. areas of active D. frontalis outbreaks may be required Dahlsten, D. L., and F. M. Stephen. 1974. Natural enemies to investigate the impact of intraguild predation by and insect associates of the mountain pine beetle, Den- Monochamus spp. on D. frontalis and other bark beetle droctonus ponderosae (Coleoptera: Scolytidae), in sugar population ßuctuations. Because cannibalistic inter- pine. Can. Entomol. 106: 1211Ð1217. actions are often self-regulating on populations Dixon, W. N., and T. L. Payne. 1979. Sequence of arrival and (Walker 1984), the ubiquity of cannibalistic interac- spatial distribution of entomophagous and associate in- tions within this system may limit the effect of insects on southern pine beetle-infested trees. Tex. Agric. Downloaded from https://academic.oup.com/ee/article/30/1/17/438228 by guest on 23 September 2021 creasing cerambycid densities on bark beetle mortal- Exp. Stn. Misc. Publ. 1432. ity. Additional research exploring interactions among Fatzinger, C. W., B. D. Siegried, R. C. Wilkinson, and J. L. bark beetle associated insects in phloem of host trees Nation. 1987. Trans-verbenol, turpentine, and ethanol as trap baits for the black turpentine beetle, Dendroctonus appears important if we are to increase our under- terebrans, and other forest Coleoptera in North Florida. standing of bark beetle population dynamics. J. Entomol. Sci. 22: 201Ð209. Flamm, R. O., R. N. Coulson, P. Beckley, P. E. Pulley, and Acknowledgments T. L. Wagner. 1989. Maintenance of a phloem-inhabiting guild. Environ. Entomol. 18: 381Ð387. We thank Marc J. Linit (University of Missouri) for pro- Gangwere, S. K. 1961. A monograph on food selection in viding larval cerambycids for this research. Timothy D. Paine Orthoptera. Trans. Am. Entomol. Soc. 87: 67Ð230. and John D. Reeve provided valuable comments on an earlier Girault, A. A. 1908. An aphid feeding on coccinellid eggs. version of this work. Research was supported in part by the Entomol. News. 19:132Ð133. University of Arkansas, Arkansas Agricultural Experiment Goyer, R. A., and M. T. Smith. 1981. The feeding potential Station, and the Arkansas Forest Resources Center, Monti- of Corticeus glaber and Corticeus parallelus (Coleoptera: cello, AR. Published with the approval of the director, Ar- Tenebrionidae), facultative predators of the southern kansas Agricultural Experiment Station. pine beetle, Dendroctonus frontalis (Coleoptera: Scolyti- dae). Can. Entomol. 113: 807Ð811. Graber, C. 2000. Interactions between some members of References Cited the southern pine beetle feeding guild. M.S. Thesis, Uni- Ambrose, W. 1984. Role of predatory fauna in structuring versity of Arkansas, Fayetteville, AR. marine soft bottom communities. Mar. Ecol. Prog. Ser. 17: Haack, R. A., and F. Slansky, Jr. 1987. Nutritional ecology of 109Ð115. wood-feeding Coleoptera, Lepidoptera, and Hymenop- Askew, R. R. 1971. Parasitic insects. Heinemann Educa- tera, pp. 449Ð486. In F. Slansky, Jr. and J. Rodriguez tional Books. London. [eds.], Nutritional ecology of insects, mites, spiders, and Baker, W. L. 1972. Eastern Forest Insects. USDA-ARS Misc. related invertebrates. Wiley, New York. Publ. 1175. Hellrigl, K. G. 1971. Die Bionimie der europa¨ischen Billings, R. F., and R. S. Cameron. 1984. Kairomonal re- Monochamus- arten (Coleopt., Cerambycid) und ihre Be- sponses of Coleoptera, Monochamus titillator (Ceramby- deutung fu¨ r die Forst- und Holzwirtschaft. Redia 52: cidae), Thanasimus dubius (Cleridae), and Temnochila 367Ð510. virescens (Trogositidae), to behavioral chemicals of Kester, K. M., and D. M. Jackson. 1996. When good bugs go southern pine beetles (Coleoptera: Scolytidae). Environ. bad: intraguild predation by Jalysus wickhami on the Entomol. 13: 1542Ð1548. parasitoid, Cotesia congregata. Entomol. Exp. Appl. 81: Bowden, J., and J. Phipps. 1967. Cockroaches (Periplaneta 271Ð276. americana (L.)) as predators. Entomol. Mon. Mag. 103: King, E. W. 1972. Rainfall and epidemics of the southern 175Ð179. pine beetle. Environ. Entomol. 1: 279Ð285. Chansler, J. F. 1967. Biology and life history of Dendrocto- Lavigne, R. J., and R. E. Pfadt. 1964. The role of rangeland nus adjunctus (Coleoptera: Scolytidae). Ann. Entomol. grasshoppers as scavengers. Kans. Entomol. Soc. 37: 1Ð4. Soc. Am. 60: 760Ð767. Leving, S., and E. Adams. 1984. Intra- and interspeciÞc ter- China, W. E. 1953. The new species of the genus Cyrtipeltis ritoriality in Nasutitermes (Isoptera: Termitidae) in a Pan- (Hemiptera) associated with sundews in western Aus- amanian mangrove forest. J. Anim. Ecol. 53: 705Ð714. tralia. West. Aust. Nat. 4: 1Ð8. Linsley, E. G. 1958. The role of Cerambycidae in forests, Cooke, J.A.L. 1968. A further record of predation by cock- urban and agricultural environments. Pan-Pac. Entomol. roaches Periplaneta americana. Entomol. Mon. Mag. 104: 34: 105Ð124. 1244Ð1246. Linsley, E. G. 1959. Ecology of Cerambycidae. Annu. Rev. Coulson, R. N., A. M. Mayyasi, J. L. Foltz, and F. P. Hain. Entomol. 4: 99Ð138. 1976. InterspeciÞc competition between Monochamus Lucas, E., D. Coderre, and J. Brodeur. 1998. Intraguild pre- titillator and Dendroctonus frontalis. Environ. Entomol. 5: dation among aphid predators: characterization and in- 235Ð247. ßuence of extraguild prey density. Ecology 79: 1084Ð1092. Coulson, R. N., D. N. Pope, J. A. Gagne, W. S. Fargo, P. E. Michaels, P. J. 1984. Climate and the southern pine beetle in Pulley, L. J. Edson, and T. L. Wagner. 1980. Impact of atlantic coastal and piedmont regions. For. Sci. 30: 143Ð foraging by Monochamus titillator (Col: Cerambycidae) 156. on within-tree populations of Dendroctonus frontalis Miller, M. C. 1984. Mortality contribution of insect natural (Col: Scolytidae). Entomophaga 25: 155Ð170. enemies to successive generations of Ips calligraphus 22 ENVIRONMENTAL ENTOMOLOGY Vol. 30, no. 1

(Germar) (Coleoptera, Scolytidae) in loblolly pine. lytidae) and Acanthocinus aedilis (Col.: Cerambycidae), J. Appl. Entomol. 98: 495Ð500. and the predator Thanasimus formicarius (Col.: Cleridae) Miller, M. C. 1985. The effect of Monochamus titillator (F.) with special reference to brood production. Ento- (Col., Cerambycidae) foraging on the emergence of Ips mophaga 39: 149Ð157. calligraphus (Germ.) (Col., Scolytidae) insect associates. Slansky, F., Jr., and J. M. Scriber. 1985. Food consumption J. Appl. Entomol. 100: 189Ð197. and utilization, pp. 87Ð164. In G. A. Kerkut and L .I. Moser, J. C., R. C. Thatcher, and L. S. Pickard. 1971. Relative Gilbert [eds.], Comprehensive insect physiology, bio- abundance of southern pine beetle associates in East chemistry, and pharmacology. Permagon, England. Texas. Ann. Entomol. Soc. Am. 64: 72Ð77. Stephen, F. M., and D. L. Dahlsten. 1976. The arrival se- New, T. R. 1991. Insects as predators. The New South Wales quence of the arthropod complex following attack by University Press, Kensington, Australia. Dendroctonus brevicomis (Coleoptera: Scolytidae) in Overgaard, N. A. 1968. Insects associated with the southern ponderosa pine. Can. Entomol. 108: 283Ð304. pine beetle in Texas, Louisiana, and Mississippi. J. Econ. Stephen, F. M., C. W. Berisford, D. L. Dahlsten, P. Fenn, and

Entomol. 61: 1197Ð1201. J. C. Moser. 1993. Invertebrate and microbial associates, Downloaded from https://academic.oup.com/ee/article/30/1/17/438228 by guest on 23 September 2021 Paine, T. D., M. C. Birch, and P. Svihra. 1981. Niche breadth pp. 129Ð153. In T. D. Schowalter and G. M. Filip [eds.], and resource partitioning by four sympatric species of Beetle-pathogen interactions in conifer forests. Aca- bark beetles (Coleoptera: Scolytidae). Oecologia 48: 1Ð6. demic, London. Parker, D. C., and D. W. Davis. 1971. Feeding habits of Trichilo, P. J., and T. G. Leigh. 1986. Predation on spider Corticeus substriatus (Coleoptera: Tenebrionidae) asso- mite eggs by the western ßower thrips, Frankliniella oc- ciated with mountain pine beetle in lodgepole pine. Ann. cidentalis (Thysanoptera: Thripidae), an opportunist in a Entomol. Soc. Am. 64: 293Ð294. cotton agroecosystem. Environ. Entomol. 15: 821Ð825. Pershing, J. C., and M. J. Linit. 1986. Biology of Monochamus Turchin, P., P. L. Lorio, A. D. Taylor, and R. F. Billings. 1991. carolinensis (Coleoptera: Cerambycidae). Kans. Ento- Why do populations of southern pine beetles (Co- mol. Soc. 59: 706Ð711. leoptera: Scolytidae) ßuctuate? Environ. Entomol. 20: Pershing, J. C., and M. J. Linit. 1989. Variation in number of 401Ð409. instars of Monochamus carolinensis (Coleoptera: Ceram- Turchin, P., A. D. Taylor, and J. D. Reeve. 1999. Dynamical bycidae). Kans. Entomol. Soc. 61: 370Ð378. role of predators in population cycles of a forest insect: an Phoofolo, M. W., and J. J. Obrycki. 1998. Potential for in- experimental test. Science 285: 1068Ð1071. traguild predation and competition among predatory Victorsson, J., and L. Wikars. 1996. Sound production and Coccinellidae and Chrysopidae. Entomol. Exp. Appl. 89: cannibalism in larvae of the pine-sawyer beetle Monocha- 47Ð55. mus sutor L. (Coleoptera: Cerambycidae). Entomol. Tid- Polis, G. A., C. A. Myers, and R. D. Holt. 1989. The ecology skr. 117: 29Ð33. and evolution of intraguild predation: potential compet- Wagner, T. L., R. O. Flamm, and R. N. Coulson. 1985. Strat- itors that eat each other. Annu. Rev. Ecol. Syst. 20: 297Ð egies for cohabitation among the southern pine bark 330. beetle species: comparisons of life-process biologies. Reeve, J. D. 1997. Predation and bark beetle dynamics. Oe- USDA For. Serv. Gen. Tech. Rep. SO-56: 87Ð101. cologia. 112: 48Ð54. Walker, T. J. 1984. Do populations self-regulate? In E. B. Root, R. B. 1986. The life of a Californian population of the Huffaker and R. L. Rabb [eds.], Ecological entomology. facultative milkweed bug, Lygaeus kalmii (Heteroptera: Wiley, New York. Lygaeidae). Proc. Entomol. Soc. Wash. 88: 201Ð214. Whitman, D. W., and L. J. Orsak. 1985. Biology of Tae- Root, R. B., and S. J. Chaplin. 1976. The life-styles of tropical niopoda eques (Orthoptera: Acrididae) in southeastern milkweed bugs, Oncopeltus (Hemiptera: Lygaeidae), uti- Arizona. Ann. Entomol. Soc. Am. 78: 811Ð825. lizing the same host. Ecology 57: 132Ð140. Wilson, L. J., L. R. Bauer, and G. H. Walter. 1996. Phyto- Rose, A. H. 1957. Some notes on the biology of Monochamus phagous thrips are facultative predators of twospotted scutellatus (Say) (Coleoptera: Cerambycidae). Can. En- spider mites (Acari: Tetranychidae) on cotton in Austra- tomol. 87: 547Ð553. lia. Bull. Entomol. Res. 86: 297Ð305. Rosengren, R. 1986. Competition and coexistence in an in- Wissinger, S. A., and J. McGrady. 1993. Intraguild predation sular ant communityÐa manipulation experiment. Ann. and competition between larval dragonßies: direct and Zool. Fenn. 23: 297Ð302. indirect effects on shared prey. Ecology 74: 207Ð218. SAS Institute. 1996. UserÕs manual, JMP version 3.1.5. SAS Wissinger, S. A., G. B. Sparks, G. L. Rouse, W. S. Brown, and Institute, Cary, NC. H. Steltzer. 1996. Intraguild predation and cannibalism Schroeder, L. M., and J. Weslien. 1994a. Reduced offspring among larvae of detritivorous caddisßies in subalpine production in bark beetle Tomicus piniperda in pine bolts wetlands. Ecology 77: 2421Ð2430. baited with ethanol and ␣-pinene, which attract antago- nistic insects. J. Chem. Ecol. 20: 1429Ð1444. Schroeder, L. M., and J. Weslien. 1994b. Interactions be- Received for publication 1 June 2000; accepted 20 October tween the phloem-feeding Tomicus piniperda (Col.: Sco- 2000.