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ECOLOGY AND POPULATION BIOLOGY

Species Assemblage Arriving at and Emerging from Trees Colonizedby Ips pini in the Great Lakes Region: Partitioning by Time Since

Colonization, Season, and Host Species

BRIAN H. AUKEMA,1,2 GREG R. RICHARDS,1 STEVEN J. KRAUTH,1,3 AND KENNETH F. RAFFA1

Ann. Entomol. Soc. Am. 97(1): 117Ð129 (2004)

ABSTRACT Thepineengraver, Ipspini(Say), colonizes jack, red, andwhitepines in theGreatLakesregion. Males select suitable hosts, bore through the bark into phloem tissue, and emit aggregationpheromones. Pheromones attract conspeciÞcs, which aid in overcoming tree defenses, and predators,which exploit these cues as kairomones. Sampling was conducted over 2 yr to characterize theassemblageof insects that arrive at and reproduce in trees colonizedby I. pini, andhowthis assemblageis partitioned by host species, time after colonization, and seasonal phenology. Over 70 species fromthree orderswere obtained. I. piniwasmost abundant, especially during late summer. The Þrst naturalenemy to arrive wasMedetera bistriata Parent, which came simultaneously with I. pini. Other Dipterasuch as Lonchaea corticis Taylor and Zabrachia polita Coquillett were also abundant. Roptrocerusxylophagorum (Ratzeburg), a late instar parasitoid, arrived last. Its emergence most closely coincidedwith I. pini emergence, whereas the other species emerged substantially after I. pini. Host species didnot affect total I. pini emergence but strongly affected natural enemies. Most R. xylophagorum andMonochamus spp. emerged fromwhite pine, and most Z. polita emerged from red pine. I. pini had thehighest ratio of emergence to arrival per log. Only the predator T. dubius and the parasitoid R.xylophagorum showed numerical responses to the number of emerging I. pini. Exclusion of insectsduring the Þrst 2 wk of colonization decreased reproduction of I. pini and other wood borers in thespring, but not summer.

KEY WORDS host species, natural enemies, resource partitioning, tritrophic interactions, kairo-mones

THE PINE ENGRAVER, Ips pini (Say) (Coleoptera: Sco-lytidae), is endemic across North America and colo-nizes weakened or dead pines and sometimes spruce(Anderson 1948, Thomas 1961). Males select suitablehosts, bore into the bark, and construct subcortical“nuptial” chambers in which theymate.While boring,males emit a regionally speciÞc stereoisomeric blendof ipsdienol (2-methyl-6-methylene-2,7-octadien-4-ol) and lanierone (2-hydroxy-4,4,6-trimethyl-2,5-cy-clohexadien-1-one) that function as aggregationpher-omones (Lanier et al. 1972; Birch et al. 1980; Wood1982; Seyboldet al. 1992, 1993;Miller et al. 1997). I. piniis polygynous (Kirkendall 1983), with males typicallymating with two or three females (Thomas 1961,Schenk and Benjamin 1969). Females establish ovi-positional galleries radiating from the nuptial cham-ber. Eggs are laid along the gallery, and the larvaetunnel laterally, girdling the sapwood. The brood pu-

pate in oval chambers before the adults chew throughthe bark and seek new hosts.

I. pini cause relatively low economic losses undernatural forest conditions, but can be a pest duringharvesting operations and in forest plantations. Wis-consinpossesses 64millionm3ofgrowing stock in jack,Pinus banksiana Lamb; red, P. resinosa Aiton; andwhite, P. strobus L. pine plantations (Wisconsin Di-vision of Forestry Forest Health Protection Staff2001).Theabundanceofbroodmaterial after thinningoperations or natural windthrowmay promote a rapidincrease in beetle numbers, allowing healthy trees tobe attacked (Thomas 1961, Schenk and Benjamin1969, Livingston 1979, Gara et al. 1999).The use of natural enemies as biological control

agents is of great interest because the applicability ofchemical insecticides is limitedbyenvironmental con-siderations, themarginal economic return of tree pro-duction, and the inaccessibility of subcortical insects.The most studied predators in the Great Lakes regionare Thanasimus dubius (F.) (Coleoptera: Cleridae)and Platysoma spp. (Coleoptera: Histeridae) (Hermset al. 1991, Raffa 1991, Erbilgin et al. 2002). Our rel-atively higher knowledge of these species partly re-ßectsmethodological advances. These beetles are eas-

1 Department of Entomology, 345 Russell Laboratories, 1630 Lin-den Drive, University of Wisconsin, Madison, WI 53706.

2 Biometry Program, 345 Russell Laboratories, 1630 Linden Drive,University of Wisconsin, Madison, WI 53706.

3 InsectResearchCollection, 346Russell Laboratories, 1630LindenDrive, University of Wisconsin, Madison, WI 53706.

0013-8746/04/0117Ð0129$04.00/0 � 2004 Entomological Society of America

ily sampled using funnel traps, which are ideal forcapturing hard-bodied insects (Lindgren 1983), andthey respond to synthetic pheromone baits (Raffa andDahlsten 1995; Aukema et al. 2000a,b).Althoughbehavioral responses of somepredators to

I. pini pheromones have been studied in detail, inter-actions among I. pini and other associates are less wellunderstood. Relatively little is known about the di-versity of insects arriving at or reproducing in logscolonizedby I. piniorhowhost tree species affects thisassemblage or its performance (Erbilgin and Raffa2000). Furthermore, little is known about arrival pat-terns to logs after pheromone production by the pri-mary herbivore ceases, when natural enemies mayarrive andpreyon life stages other than adults. As barkbeetle broods and natural enemies develop, compet-itive or predatory balances within the tree may alsochange. We also lack data on how the assemblage ofnatural enemies may change throughout the ßightseason. Likewise, little is known about natural enemydevelopmental times, which could affect I. pini pop-ulation dynamics within seasons, among years, andamong pine species.The objectives of this research were to 1) charac-

terize the species assemblage responding to andemerging from host trees colonized by I. pini in theGreat Lakes region; 2) evaluate the effects of host treespecies, time since colonization, and seasonal phenol-ogy on the composition and numbers of this complex;and 3) assess the impacts of these associates by con-ducting exclusion experiments,modelingwithin-plantdevelopment, and estimating ratios of emerging toarriving insects on a per log basis.

Materials and Methods

Temporal andHostTreePartitioning. Jack, red, andwhitepine treesof�20cm indiameter atbreastheight(dbh) were removed from a mixed plantation nearMazomanie,WI, cut into 1-m lengths, and taken to thelaboratory. Four to eightmale I. pini from a laboratorycolony rearedon similar host treeswereplaced evenlyalong each section, coveredwith gelatin capsules, andallowed to bore for 24 h. The colonized logs weretaken to two neighboring red pine plantations (�45yr) in Sauk County, Wisconsin (latitude N 43� 33.41�,longitudeW89� 50.61�; latitudeN 43� 33.43�, longitudeW 89� 50.61�). The logs were deployed in groups con-taining one log from each species, with 10Ð15 m be-tween each log and a minimum of 100 m betweengroups. In 2000, three 1-m sections were collectedfrom each of four jack, red, and white pines, and in2001 seven 1-m sections were collected from one redand one white pine tree each. The two sites receivedeight and four groups in 2000, and four and three,respectively, in 2001.Insects arriving at the infested logs were sampled

with Þberglass screens thatwere sprayedwithTangle-Trap (The Tanglefoot Co., Grand Rapids, MI) andplaced on the logs, and 12-funnel traps (Lindgren1983). A 2 by 2-cm piece of Revenge bug strip (18.6%2Ð2-dichlorovinyl dimethyl phosphate; Roxide Inter-

national, Inc., New Rochelle, NY) was placed in eachcup to kill arriving insects and prevent destruction oftrap contents by predators. The cups were emptiedand the screens were replaced at approximate 3-dintervals for six or seven sample periods. At the end ofsampling, the logs were taken back to the laboratoryandplaced in 30-cm-diameter construction Sonotubes(Potter Form and Tie, Co., Madison, WI), whichserved as insect rearing chambers. Collections wereperformed three times per week for 204 d. The logswere kept within the tubes for at least 298 d, at whichtime all insects that had emerged but not reached thecollection cups were collected. Dissection of a subsetof logs revealed no distinguishable insects that haddied before emergence.This experiment was performed three times: 21

JulyÐ16 August 2000, 31 MayÐ26 June 2001, and 2AugustÐ27August 2001. Jackpinewasnotused in2001,and only screen traps were used in the spring of 2001.A Poisson generalized linear mixedmodel was used

to examine the Þxed effect of tree species on totalarrival and emergence of each species on a per logbasis, by using a penalized quasi-likelihood approach,glmmPQL (Breslow and Clayton 1993, Venables andRipley 2002) implemented inR(Ihaka andGentleman1996). The total number of insects arriving at the logwas the sum of the screen and funnel trap catches.Groups nested within each plantation were used asrandom effects. The suitability of these models wasconÞrmed by examination of residual plots.To examine the effect of time on the arrival and

reproduction of insects, we standardized all values toa constant surface area of bark. Although small vari-ations in log size did not affect total reproduction (P �0.05 for most species examined), standardizing botharrival and reproduction facilitates comparisonsamong them. The average catch per day per 10 dm2

was centered on each sample period. Arrival andemergence curves were then constructed using re-gression splines on �y transformed data to satisfyassumptions of normality (Venables andRipley 2002).The relative reproductive increase (ratio of emer-

gence to arrival) and emergencemodels (functions ofvarious insects with arriving and emerging associates)were examined using the data set from summer 2000.We focused our analyses on that year because �90%of I. pini and 70% of all insects sampled were obtainedthen, there were signiÞcant year � experiment inter-actions (P � 0.05), and a portion of 2001 did notinclude funnel traps. All estimates of reproductiveincrease should be viewed as of relative value only:although emergence is standardized by containeriza-tion, trapping efÞciencies surely vary among insectspecies.Moreover, emergencevaluesprovide full cen-suses of brood per female for insects such as Ips spp.that construct single ovipositional galleries, but only asubset for species that oviposit in multiple trees orparts of trees.We evaluated relationships of insect emergence to

thearrival andemergenceofother speciesonaper-logbasis usingmultiple regression.Because thenumberofadministered I. pini that actually entered the logs

118 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 97, no. 1

varied slightly (range of four to eight) among repli-cates, we included the number of initial borers as avariable to test whether this could potentially affectrecruitment and emergence. Again, predictors werestandardized to the total number of insects arrivingand reproducing per 10 dm2 for a given log. Modelswere constructed using backwards elimination from afull model comprising themost abundant insects. Spe-cies that showed signiÞcant host tree effects wereexamined with a model restricted to that host tree.

Effect of Natural Enemies on Reproduction of I.pini. We conducted an exclusion screening experi-ment to examine how temporarily restricting access tologs infested with I. pini affected the reproduction ofI. pini and associates. One red and one white pine(�20 cm dbh)were felled inMazomanie,WI, and cutinto23-cm logs.Each log received fourmalebeetleson25 May 2001 and then eight females the next day tosimulate an active infestation. The logs were groupedinto quartets of two red pine and two white pine logs.Each pair of the same species in a quartet came fromadjacent positions in the tree.One log in each pair was randomly selected and

encased in aluminum screening. This screening wasstapled to a lengthwise slice of foam pipe insulationwrapped around the top and bottom of the log, so thescreen did not touch the log and predators could notoviposit into the bark. On 27 May, four quartets weredeployed in each of the two red pine plantations asdescribed above. Each quartet was arranged in a ran-dom square at 2-m spacing in a site, and each groupwas separated by a minimum of 50 m. Seven cm wideÞberglass screening sprayed with Tangle-Trap waswrapped around the middle of each log and held inplace with a binder clip. The screens were sampled 31May, 4 June, 8 June, 12 June, 16 June, and 20 June.On 8 June, 12 d postdeployment, the aluminum

screening was moved to the other bolt in each pair,thus restricting access for the second 12 d of coloni-zation. On 20 June, the bolts were retrieved from theÞeld. All screening was removed, and the logs wereplaced in 19-liter rearing cans. Black cloth and a tightÞttingmesh lid sealed the cans. Insects were collectedas they emerged into glass emergence jars, three timesper week.This experimentwas conducted a second time,with

Þeld deployment from 26 JulyÐ20 August, by usingsimilar sample intervals and 12-d exclusion intervals.The total numbers of insects reared from each log

were analyzedwith aPoissongeneralized linearmixedmodel, again by using group within site as a randomeffect and a penalized quasi-likelihood approach(Breslow andClayton 1993). Fixed effect factorsweretree species (red or white pine), time of exclusion(Þrst or second 12-d interval), and their interaction.

Results

Overall Diversity and Seasonal Trends. A diversegroupofmore than 70 insect species from three orderswas obtained arriving to or emerging from the logscolonized with I. pini (Aukema 2003). Of these, 27

emerged from logs after time intervals consistent withknown developmental periods, indicating reproduc-tion within this habitat. A summary of the insectsobtained and their likely association with the colo-nized logs is given inTable 1. This assemblage includesherbivores, which compete with I. pini for phloemresources, fungivores, predators, and parasitoids.There were signiÞcant year � season and within-

year interactions for most insects, including I. pini(P � 0.05). Therefore, relationships of arrival andemergence with host tree species were analyzed sep-arately by year and are shown for 2000 and 2001 inTables 2 and 3, respectively. Seventy percent of allinsects were obtained in 2000. Overall, the primaryherbivore, I. pini, was the most abundant, with a totalof 769arrivingat and7,781emerging frominfested logs(Tables 2 and 3). In 2001, when we performed bothspring and summer assays, there was a signiÞcant ef-fect due to phenology. Therefore, relationships of ar-rival and emergence with host tree species were an-alyzed separately by segment of the ßight season andare shown for early spring and late summer in Table3A and B, respectively. I. pini were more abundant inthe summer than spring, with 91.2% of 1,879 I. piniemerging from logs deployed in the Þeld during thesummer trial (Table 3).Overall, a total of 3,731 insects other than I. pini

were obtained arriving at the infested logs, and 1,447emerged from the logs in the laboratory (Tables 2 and3). Funnel traps were most effective for samplingarriving hard-bodied insects (such as Coleoptera),and sticky screens were more effective for trappingsoft-bodied insects (primarily Diptera and Hymenop-tera).

Effect of Host Species on Composition of ArrivingInsects. Statistically signiÞcant relationships (P �0.05) due to host tree species were observed for 26species (Tables 2 and 3). I. pini were more attractedtoconspeciÞcs tunneling inwhitepine thanredor jackpine, with a 1.7 times difference among these hostspecies in 2000 (Table 2). This effect was signiÞcantamong females but not males. The southern pine saw-yer,Monochamus titillator (F.), the secondmost abun-dant phloeophagous herbivore, was obtained arrivingat white and red pine more than jack pine (Table 2).Other herbivores arriving at the pines over both yearsincluded Ips grandicollis(Eichhoff)(5),Dendroctonusvalens LeConte (12), Dryocoetes autographus (Ratze-burg) (19), Dryophthorus americanus Bedel (18),Monochamus carolinensis (Olivier) (3), Monochamusscutellatus (Say) (1), Orthotomicus caelatus (Eich-hoff) (2), and Orthosoma brunneum (Forster) (9).

Five species of predacious Cleridae were capturedarriving at the logs, including Enoclerus muttkowki(Wolcott) (7), Enoclerus nigrifrons (Say) (22), Eno-clerus nigripes (Say) (1), Thanasimus undulatus (Say)(1), and Zenodosus sanguineus (Say) (4). The red-bellied checkeredbeetle,Thanasimusdubius (F.),wasthe most prevalent, with �4 times more arriving atwhite and red pine than jack pine (Table 2). Othercoleopteran predators included Platysoma cylindrica(Paykull) (7), Platysoma parallelum (Say) (2), Cor-

January 2004 AUKEMA ET AL.: ASSOCIATES OF I. pini 119

ticeus parallelus (Melsheimer) (3), Grynocharisquadrilineata (Melsheimer) (2), Tenebroides spp.(predominantly marginatus Beauvois) (5), two cucu-jids, and 24 staphylinids not identiÞed to species.Among Diptera, the most prevalent predator was thedolichopodid Medetera bistriata (Parent). M. bistriatashowed slightly higher arrival rates on white than redpine in the spring of 2001 (Table 3A), but otherwiseshowed no preferences among the three host speciesinfestedwith I. pini (Tables 2 and 3B). The dolichopo-did Gymnopternus politus Loew was present in lower

numbers thanM. bistriata, in an approximate 1:4 ratio,and showed no host tree preferences (Table 2). Ap-proximately 20 Zabrachia polita Coquillett were cap-tured landing on each red pine log in the summer of2000, whereas only 15 total were obtained the follow-ing year (Table 2). Z. polita preferred red pine overjack or white pine. Host tree species did not affectlanding rates by the other Diptera sampled in highnumbers in the summer of 2000: Clusoides albimanaMeigen, Clusoides melanostoma (Loew) (Diptera:Clusiidae), and Sceptonia spp. (Diptera: Mycetophili-

Table 1. Insects obtained arriving to or emerging from logs of jack, red, and white pine colonized by I. pini in the summers of 2000and 2001 in red pine plantations in Wisconsin

Order/Family Insect Association Referencesa

ColeopteraScolytidae I. pini Phloeophagous 1Ð3

I. grandicollis Phloeophagous 3Ð5D. valens Phloeophagous on lower stem, roots 3D. autographus Phloeophagous on lower stem, roots 6, 7G. materarius Fungivorous; subcortical in stumps 7, 8Hylastes spp. Root herbivore 3O. caelatus Fungivorous; subcortical in stumps 3, 7, 9

Cerambycidae A. pusillus Phloeophagous 8b

M. titillator Phloeophagous early, then xylophagous 3, 9Ð11O. brunneum Phloeophagous, decaying logs 3, 12

Curculionidae D. americanus Under bark of logs 3, 13Ð15Pissodes spp. Phloeophagous 3, 8, 9, 16, 17

Carabidae P. pallens Predator 8b

Cleridae E. nigrifrons Predator of adult and larval bark beetles 8, 18, 19E. nigripes Predator of adult and larval bark beetles 3, 7, 8E. muttkowski Predator of adult and larval bark beetles, weevils, and wood borers 17T. dubius Predator of adult and larval bark beetles 3, 8, 20, 21

Histeridae P. cylindrica Predators under bark 8, 9P. parallelum Predators under bark 8, 9

Nitidulidae E. labilis Attracted to ßowers and sap ßow 22b, 23, 24b

Silvanidae S. bidentatus Under bark of logs 8, 13Staphylinidae Staphylinidae Fungivores and predators 3, 7Tenebrionidae C. parallelus Fungivore; larvae are egg predators 8, 25, 26Trogossitidae T. marginatus Predators under bark 27

T. collaris Predators under bark 8, 9DipteraAsilidae Asilidae Generalist predators; bark surface 3, 28Clusiidae C. johnsoni Saprophagous/fungivorous in moist, rotting wood 29

C. melanostoma Saprophagous/fungivorous in moist, rotting wood 29Dolichopodidae M. bistriata Larval predators under bark 3, 8, 30, 31

G. politus Predator under moist bark 32Lonchaeidae L. corticis Necrophagous, predator, possibly parasitic on Pissodes strobi Peck 7, 33Ð35Mycetophilidae Sceptonia spp. Larvae associated with fungi 36Stratiomyidae Z. polita Scavenger and predator in stumps 3, 7, 37, 38

HymenopteraBraconidae Coeloides sp.c Bark beetle parasitoid 39Ð42

Spathius sp.c,d Bark beetles parasitoid 40, 43Ð45Pteromalidae Rhopalicus pulchripennisc Bark beetle parasitoid 46, 47

R. xylophagorum Parastitoid of late instar bark beetles 48Ð51T. tibialis Parasitoid of adult Ips, Orthotomicus, Pityophthorus spp. 47, 52Ð53

Only species of which Þve or more were captured, or those with deÞnite associations with I. pini, are listed. For a list of all species, includingHymenoptera, see Aukema (2003).

a 1 (Thomas 1961); 2 (Schenk and Benjamin 1969); 3 (Drooz 1985); 4 (Ayres et al. 2001); 5 (Erbilgin and Raffa 2001); 6 (Johansson et al.1994); 7 (Thomas 1955); 8 (Howden and Vogt 1951); 9 (Savely 1939); 10 (Dodds et al. 2001); 11 (Alya and Hain 1985); 12 (Yanega 1996); 13(Downie andAmett 1996); 14 (Blatchley andLeng 1916); 15 (Kissinger 1964); 16 (Graham1925); 17 (Boucher et al. 2001); 18 (Mawdsley 1999);19 (Aukema and Raffa 2000); 20 (Thatcher and Pickard 1966); 21 (Mignot and Anderson 1969); 22 (Schroeder andWeslien 1994); 23 (Parsons1943); 24 (Schroeder 1996); 25 (Smith and Goyer 1980); 26 (Goyer and Smith 1981); 27 (Lescher 2002); 28 (Wood 1987); 29 (Caloren andMarshall 1971); 30 (Williamson1971); 31 (Bickell 1985); 32 (RobinsonandVockeroth1987); 33 (Hulme1990); 34 (Hulme1989); 35 (MacAloney1930); 36 (Laffoon 1965); 37 (Kraft andCook 1961); 38 (James 1965); 39 (Kenis 1997); 40 (Townes 1969); 41 (Pettersson et al. 2001); 42 (Mason1978); 43(Sullivanet al. 1997); 44(Langor1991); 45(Matthews1970); 46(Espelieet al. 1990); 47(Burks1979); 48(Samson1984); 49(Petterssonet al. 2000); 50 (Sullivan et al. 2000); 51 (Grissell 1979); 52 (Senger and Roitberg 1992); 53 (Rice 1968).

b Reference indicates different species within same genus.c Collected from white pine infested with I. pini in August 2002, in red pine plantation in Mazomanie, WI. Collections were not part of

experiments described in this article.d Reared from I. pini larvae.


dae) (Table 2). Low numbers of Lonchaea corticisTaylor (12)andasilids (18)werealso sampledarrivingto the logs.The most prevalent parasitic Hymenoptera were

the pteromalids Roptrocerus xylophagorum (Ratze-burg) and Tomicobia tibialis Ashmead. These insectswere most abundant in summer 2000 and orientedmost strongly to colonized white pine (Tables 2 and3). On average, we captured one R. xylphagorum oneach white pine log and two T. tibialis on each whitepine log, all on sticky screens. Other Hymenopteraarriving at pine logs included bethylids such as Dis-omphalus apertus Kieffer (1) and Pristocera armifera(Say) (1); braconids such as Euphoriella sp. (1), Dis-tatrix spp. (2), and Apantales sp. (1); diapriids such asAclista spp. (3), Basalys sp. (1), Belyta spp. (3), andPantoclis spp. (2); and ichneumonids such as Hypo-soter pilosulus (Provancher) (1), Phobocampe bicin-gulata vernalis (Viereack) (1), Gnotus sp. (1), Aro-trpehes pusillus (Cresson) (1), Lissonota acrobasidisAshmead (1), Mesochorus curvulus Thomson (1), De-mopheles corruptor maturus (Provancher) (1),Euster-inx bispinosa Stroble (1), and Stenomacrus ulmicola(Ashmead) (2). Two siricids, Tremex columba (L.),were also sampled.

Effect of Host Species on Composition of EmergingInsects. Although I. pini were most attracted to con-speciÞcs tunneling inwhite pine, host tree species had

no effect on the total number of I. pini that emerged.The relative reproductive increase of I. pini (ratio ofemergence to arrival per log) ranged from 9.4 in redpine to 14.2 in jack pine (Table 4). The relative rateof increase inwhite pinewas�34% higher for femalesthanmales. Between 112 and 195 I. pini emerged fromeach log in the July and August trials, but fewer than20 I. piniemergedper log in theMay trial of 2001.Morespeciesof scolytidswere reared from logs in this springtrial. Ips grandicollis (Eichhoff), Gnathotrichus mat-erarius (Fitch), and Orthotomicus caelatus (Eichhoff)were present in low numbers (Table 3A), and theirreproduction did not vary among tree species. MoreMonochamus spp. emerged from white pine than jackor red pine in summer 2000, with almost seven per log(Table2).Their relative reproductive success inwhitepinewas double that in redpine, but only onehalf thatof I. pini (Table 4). High numbers of AcanthosinuspusillusKirbyemerged from logs in spring 2001 (Table3A), although reproduction was highly heteroge-neous: 138 of 189 emerged from two red pine logs. Themost prevalent subcortical borers in the spring of 2001were Pissodes spp. weevils, with an average of 46 perwhite pine log and 13 per red pine (Table 3A). Otheremerging herbivores included Dryophthorus america-nus (1),Dryocoetes autographus (1),D. valens (1), andMonochamus notatus (Drury) (1), and Rhagium in-quisitor (L.) (2).

Table 2. Mean � SEM numbers of insects captured (A) arriving at and (B) emerging per log from jack, red, and white pine infestedwith I. pini and deployed in a red pine plantation from 21 July–16 August 2000

Order/Family Insect Totala Jackb Redb Whiteb F2,22 P

A. ArrivalColeopteraScolytidae I. pini 537 11.58 � 2.04b 14.00 � 1.12b 19.17 � 1.41a 5.31 0.0131

Males 226 4.83 � 0.88 6.00 � 0.86 8.00 � 0.95 3.05 0.0676Females 311 6.75 � 1.29b 8.00 � 0.77ab 11.17 � 1.12a 4.04 0.0320

Cerambycidae M. titillator 29 0.08 � 0.08b 1.08 � 0.31a 1.25 � 0.30a 10.17 0.0007Cleridae T. dubius 74 0.67 � 0.43b 2.67 � 0.62a 2.83 � 0.68a 19.04 0.0000Trogossitidae Tenebroides spp.c 28 0.50 � 0.19 0.75 � 0.28 1.08 � 0.26 1.61 0.2224

DipteraClusiidae Clusiodes spp.c 405 10.83 � 3.64 14.08 � 4.68 8.83 � 3.35 2.69 0.0901Dolichopodidae M. bistriata 1,076 19.75 � 4.91 33.00 � 3.23 36.92 � 6.35 3.41 0.0515

G. politus 242 8.25 � 2.17 5.08 � 1.08 6.83 � 1.60 1.57 0.2296Mycetophilidae Sceptonia spp. 146 5.50 � 1.56 4.00 � 0.67 2.67 � 0.41 2.64 0.0939Stratiomyidae Z. polita 468 6.67 � 1.14c 19.83 � 2.98a 12.50 � 1.77b 10.92 0.0005

HymenopteraPteromalidae R. xylophagorum 20 0.33 � 0.19b 0.08 � 0.08b 1.25 � 0.43a 6.33 0.0067

T. tibialis 42 0.42 � 0.34b 0.92 � 0.23ab 2.17 � 0.46a 4.97 0.0165B. EmergenceColeopteraScolytidae I. pini 5,902 165.00 � 31.72 131.83 � 19.43 195.00 � 26.10 1.55 0.2354

Males 2,289 70.50 � 13.51 52.33 � 7.62 67.92 � 7.95 1.16 0.3318Females 3,613 94.50 � 18.45 79.50 � 11.98 127.08 � 18.53 2.18 0.1373

Cerambycidae Monochamus spp. 91 0.17 � 0.11b 0.50 � 0.23b 6.92 � 0.91a 71.28 0.0000Cleridae T. dubius 40 1.42 � 0.36 0.83 � 0.44 1.08 � 0.29 0.78 0.4723

DipteraDolichopodidae M. bistriata 82 0.92 � 0.36 4.33 � 1.96 1.58 � 0.63 2.99 0.0712Lonchaeidae L. corticis 228 3.50 � 1.33b 12.75 � 4.44a 2.75 � 1.12b 4.19 0.0287Stratiomyidae Z. polita 55 0.00 � 0.00b 4.42 � 1.96a 0.17 � 0.11b 10.80 0.0005

HymenopteraPteromalidae R. xylophagorum 34 0.00 � 0.00b 0.00 � 0.00b 2.83 � 0.96a 34.96 0.0000

Means followed by the same letter across a row are not signiÞcantly different at � 0.05. Statistical tests are limited to those species forwhich we obtained a minimum of 20 individuals.

a Total number of insects from all logs (N 3 host trees � 12 replicates).b Jack pine logs were 33.7 � 1.3 dm2, red pine 32.6 � 0.8 dm2, and white pine 37.2 � 1.6 dm2.c C. johnsoni and C. melanostoma.


Tab

le3

.M

ean

�SE

Mnu

mbe

rsof

inse

cts

per

log

capt

ured

atan

dem

ergi

ngfr

omre

dan

dw

hite

pine

infe

sted

wit

hI.

pini

and

depl

oyed

ina

red

pine

plan

tati

onin

(A)

spri

ngan

d(B

)su

mm

er2

00

1

Order/Fam

ily

Insect

Arrival

Emergence

Totala

Red

bWhitec

F1.6

PTotala

Red

bWhitec

F1.6

P

A.Early

spring(30MayÐ26June)

Coleoptera

Sco

lytidae

I.pin

i0

0.00

�0.00

0.00

�0.00

NA

NA

165

20.43

�14.26

3.14

�2.82

3.32

0.1182

Males

00.00

�0.00

0.00

�0.00

NA

NA

9411.71

�8.50

1.71

�1.55

3.04

0.1320

Females

00.00

�0.00

0.00

�0.00

NA

NA

718.71

�5.80

1.43

�1.27

3.50

0.1104

I.gr

andic

ollis

00.00

�0.00

0.00

�0.00

NA

NA

212.86

�2.23

0.14

�0.14

3.70

0.1027

G.m

ate

rarius

00.00

�0.00

0.00

�0.00

NA

NA

340.43

�0.30

4.43

�4.26

2.75

0.1481

O.ca

elatu

s1

0.14

�0.14

0.00

�0.00

NA

NA

192.43

�1.78

0.29

�0.18

2.95

0.1369

Cerambycidae

A.pusillus

00.00

�0.00

0.00

�0.00

NA

NA

189

20.71

�12.89

6.29

�3.30

1.72

0.2375

Curculionidae

Pisso

des

spp.

420.29

�0.18

5.71

�2.99

8.44

0.0272

414

13.29

�5.83

45.86

�16.02

4.80

0.0709

Cleridae

Enoc

leru

san

dThanasim

usspp.

20.29

�0.18

0.00

�0.00

NA

NA

151.43

�0.30

0.71

�0.36

2.57

0.1600

Tenebrionidae

C.para

llel

us

00.00

�0.00

0.00

�0.00

NA

NA

233.29

�3.29

0.00

�0.00

4.00

0.0923

Diptera

Dolich

opodidae

M.bistr

iata

389

34.71

�10.28

20.86

�6.49

8.60

0.0262

60.86

�0.86

0.00

�0.00

NA

NA

G.pol

itus

666.00

�3.41

3.43

�1.66

2.74

0.1490

00.00

�0.00

0.00

�0.00

NA

NA

B.Latesummer(02AugustÐ27August)

Coleoptera

Sco

lytidae

I.pin

i232

11.29

�3.10

21.86

�5.67

6.00

0.0498

1,714

132.43

�31.33

112.43

�25.15

0.25

0.6338

Males

914.86

�1.56

8.14

�2.10

2.09

0.1989

635

50.00

�11.50

40.71

�10.22

0.37

0.5670

Females

141

6.43

�1.74

13.71

�4.14

5.87

0.0517

1,079

82.43

�19.87

71.71

�15.09

0.19

0.6801

Cleridae

Allspecies

443.43

�1.25

2.86

�1.01

0.13

0.7328

232.14

�1.18

1.14

�0.55

0.56

0.4831

T.dubiu

s26

2.43

�1.15

1.29

�0.52

0.95

0.3670

232.14

�1.18

1.14

�0.55

0.56

0.4831

Tenebrionidae

C.para

llel

us

40.43

�0.30

0.14

�0.14

NA

NA

171.86

�1.86

0.57

�0.30

0.35

0.5756

Diptera

Dolich

opodidae

M.bistr

iata

390

29.57

�6.50

26.14

�9.31

0.09

0.7754

281.29

�0.42

2.71

�0.94

2.05

0.2024

G.pol

itus

201.00

�0.58

1.86

�0.59

5.08

0.0651

00.00

�0.00

0.00

�0.00

NA

NA

Lonch

acidae

L.co

rtic

is0

0.00

�0.00

0.00

�0.00

NA

NA

829.86

�3.11

1.86

�0.96

48.60

0.0004

Statistical

testsarelimitedto

those

speciesforwhichweobtainedaminim

um

of18

individuals.NA,notap

plicable.

aTotalnumberofinsectsfrom

alllogs(N

2host

trees

�7replicates).

bRedpinelogswere

50.8

�2.4dm

2in

(A)springexp

erimentan

d55.5

�1.0dm

2in

(B)summerexp

eriment;whitepinelogswere

53.0

2.1dm

2in

(A)springexp

erimentan

d51.1

�1.9dm

2in

(B)summer

exp

eriment


The relative rate of increase ofT. dubiuswashighestin jack pine, where the emergence/arrival ratio was2.1 (Table 4). Other emerging beetles included T.undulatus (1), E. nigripes (3), P. cylindrica (8), Silva-nus bidentatus (F.) (3), Corticeus parallelus (Melshei-mer) (7), and Plochionus pallens (F.) (10). The high-est relative rate of increase for all predators was 25.5,for the dipteran L. corticis in red pine. L. corticis alsohad emergence/arrival ratios �10 per log in the otherhosts, in contrast to M. bistriata and Z. polita, whichhad relative reproductive ratios �1 in all pine species.Thehighestmeannumbers ofM.bistriata (4),Z. polita(4), and L. corticis (13) emerged from colonized redpine logs (Table 2). Of parasitoids, R. xylophagorumhad higher emergence and relative reproductive in-crease in white pine than red or jack pine in 2000(Table 2). On average, three R. xylophagorumemerged from each log (Table 2). Three T. tibialis, allfrom white pine, were reared in 2000.

Sequence of Arrival to and Emergence from Colo-nized Logs. The various insect species associated withI. pini showeddistinct arrival sequences relative to thetime of colonization by the primary herbivore (Figs.1-3). Because of host tree effects on the large number

of species arriving at red and white pines (Figs. 2 and3), we display herbivores, predators, and parasitoidson separate panels to facilitate visual comparisons.TheÞrst responders to all logswere I. pini,M. bistriata,G.politus,andT.dubius. Inparticular,mostM.bistriatatypically were captured before most I. pini. The ma-jority of cerambycids arrived during the Þrst 12 d afterÞeld deployment. Z. polita began to arrive in red pineduring the Þrst 12 d after colonization of the logs byI. pini (Fig. 2B) and R. xylophagorum began to arrive�2 wk after colonization, in white pine (Fig. 3C).Figure 4AÐC shows the emergence patterns of in-

sects reared from the logs. I. pini began to emerge at�30 d. Peak M. bistriata and L. corticis emergenceoccurred at �55Ð60 d, although there was a moreextended emergence pattern for L. corticis than otherspecies. Z. polita exhibited an apparently bimodalemergence pattern in red pine, with a small peak at�60 d and a larger one after 80 d (Fig. 4B). Theparasitoid R. xylophagorum emerged shortly after I.pini, when present in white pine (Fig. 4C). Most T.dubius emerged from the logs after 80 d. All ceram-bycids emerged after 100 d.

Effect of Numbers of Arriving and Emerging Asso-ciates of I. pini on Insect Emergence. The emergingnumbers of clerids and R. xylophagorum were goodpredictors of the number of emerging I. pini: y 31.54 39.63 clerids 10.85 pteromalids (F2,33 11.74, P �0.0001, R2 0.38). Similarly, the number of emerging

Fig. 1. Arrival of I. pini and predators to P. banksianacolonized with I. pini and deployed in a red pine plantationfor 25 d. The bolts were colonized on day 0 and taken to theplantation on day 1.

Fig. 2. Arrival of (A) herbivores and (B) predators to P.resinosa colonized with I. pini and deployed in a red pineplantation for 25 d. The bolts were colonized on day 0 andtaken to the plantation on day 1.

Table 4. Effect of host tree species on relative rate of increase(ratio of emergence to arrival) per log of I. pini and associates inred pine plantations, Wisconsin

Insect Jack Red White

HerbivoresI. pini 14.24 9.42 10.17Males 14.59 8.72 8.49Females 14.00 9.94 11.38

Monochamus spp. 2.00 0.43 4.88Predators and parasitoids

T. dubius 2.12 0.31 0.38M. bistriata 0.05 0.13 0.04L. corticis 10.50 25.50 16.50Z. polita 0.00 0.22 0.01R. xylophagorum 0.00 0.00 2.27


T. dubius could be predicted by the number of emerg-ing I. pini: y �0.068 0.008 I. pini (F1,34 17.18, P 0.0002; R2 0.32). Within white pine, the number ofemerging R. xylophagorum could be predicted by thenumber of arriving I. pini: y 0.390 0.023 I. pini(F1,10 17.14 P 0.0201, R2 0.59).

ExclusionScreeningExperiments.O. caelatus and I.pini comprised 80% of the 4,893 insects that emergedfrom the logs in the exclusion screening experimentconducted in the spring (Table 5A). Exclusion of in-sects during the Þrst 2wk after the administered I. pinicolonized the logs decreased reproductionof I. piniby37%,Dryocoetes autographus (Ratzeburg) by 78%, andO. caelatus by 87% (Table 5A). The most prevalentpredators were Corticeus parallelus (Melsheimer),Platysoma spp., and T. dubius. More C. parallelusemerged in red than white pine, although there was

high variation. The timing of exclusion screening didnot affect C. parallelus development in red pine, al-though almost all C. parallelus emerged from whitepine logs with unrestricted access immediately after I.pini colonization. Neither differential exclusionscreening nor pine species affected reproduction ofPlatysoma spp. and T. dubius.

I. piniwas themost abundant insect reared from thelogs colonized during mid- to late summer 2001, al-though its total emergence was only half that in thespring (Table 5B). Most insects emerged from redpine, and exclusion screening did not affect repro-duction. Predator emergence was much lower than inthe spring. The most abundant predator was Sivlanusbidentatus (F.), of which all 31 were reared from the

Fig. 3. Arrival of (A) herbivores, (B) predators, (C)parasitoids to P. strobus colonized with I. pini and deployedin a red pine plantation for 25 d. The bolts were colonized onday 0 and taken to the plantation on day 1.

Fig. 4. Emergence of I. pini and associated insects from(A)P. banksiana, (B)P. resinosa, and(C)P. strobuscolonizedwith I. pini anddeployed in a redpineplantation for 25d.Thebolts were colonized on day 0 and taken to the plantation onday 1. Predators includeM. bistriata,G. politus, Z. polita, andT. dubius. R. xylophagorum is a parasitoid.


Tab

le5

.E

ffec

tof

host

tree

spec

ies,

tim

eof

excl

usio

nsc

reen

ing

(day

s1

–12

orda

ys1

3–2

4),

and

thei

rin

tera

ctio

non

the

repr

oduc

tion

ofin

sect

s(m

ean

�SE

Mpe

rlo

g)in

red

and

whi

tepi

ne(n

�8

repl

icat

esea

ch)

colo

nize

ddu

ring

earl

yan

dla

tefli

ght

seas

on

OrderFam

ily

Insect

Total

Redpine

Whitepine

Tree

Tim

eTree

�Tim

e

1Ð12

d13Ð24d

1Ð12

d13Ð24d

F1.21

PF1.21

PF1.21

P

A.Spring(25MayÐ20June2001)

Coleoptera

Sco

lytidae

I.pin

i1,912

46.75

�9.02

64.38

�8.74

45.50

�10.55

82.38

�17.97

0.45

0.5094

5.99

0.0233

0.54

0.4700

Males

873

21.13

�4.85

30.88

�4.70

19.00

�5.30

38.13

�9.30

0.12

0.7340

5.88

0.0244

0.48

0.4951

Females

1,039

25.63

�4.61

33.50

�4.24

26.50

�5.61

44.25

�9.08

0.95

0.3410

5.23

0.0327

0.54

0.4705

I.gr

andic

ollis

161

0.50

�0.50

0.00

�0.00

7.13

�3.61

12.50

�10.08

11.53

0.0027

0.01

0.9177

0.94

0.3444

D.vale

ns

20.00

�0.00

0.13

�0.13

0.13

�0.13

0.00

�0.00

NA

NA

NA

NA

NA

NA

D.auto

graphus

550.63

�0.38

2.25

�1.66

0.63

�0.26

3.38

�1.51

0.21

0.6543

5.60

0.0276

0.21

0.6543

G.m

ate

rarius

250.00

�0.00

0.25

�0.25

0.38

�0.26

2.50

�1.67

7.32

0.0132

5.50

0.0290

0.59

0.4503

Hyla

stes

spp.

100.13

�0.13

0.25

�0.25

0.25

�0.16

0.63

�0.50

NA

NA

NA

NA

NA

NA

O.ca

elatu

s2,026

19.63

�13.16

89.38

�37.32

10.38

�5.74

133.88

�37.92

0.09

0.7721

18.69

0.0003

1.16

0.2946

Curculionidae

D.am

eric

anus

240.00

�0.00

0.88

�0.61

0.00

�0.00

2.13

�1.34

1.47

0.2391

23.76

0.0001

1.47

0.2391

Pisso

des

spp.

982.38

�1.08

7.75

�4.57

1.13

�0.48

1.00

�0.33

5.89

0.0243

1.61

0.2190

1.95

0.1770

Cleridae

Total

701.75

�0.53

1.25

�0.75

3.13

�0.91

2.63

�0.73

4.53

0.0454

0.66

0.4274

0.05

0.8305

E.nig

ripes

130.25

�0.16

0.00

�0.00

0.88

�0.52

0.50

�0.33

NA

NA

NA

NA

NA

NA

T.dubiu

s56

1.50

�0.46

1.25

�0.75

2.25

�0.70

2.00

�0.80

1.82

0.1916

0.33

0.5696

0.01

0.9427

T.undula

tus

10.00

�0.00

0.00

�0.00

0.00

�0.00

0.13

�0.13

NA

NA

NA

NA

NA

NA

Histendae

Pla

tyso

maspp.

912.63

�0.92

2.50

�1.21

2.38

�0.89

3.88

�1.23

0.55

0.4653

0.47

0.4993

0.93

0.3461

P.cy

lindrica

501.38

�0.60

1.00

�0.68

2.13

�0.91

1.75

�0.80

1.10

0.3069

0.25

0.6236

0.01

0.9412

P.para

llel

um

411.25

�0.59

1.50

�1.10

0.25

�0.16

2.13

�0.58

0.37

0.5486

3.44

0.0776

2.73

0.1135

Nitidulidae

Eupara

ela

bilis

70.00

�0.00

0.25

�0.16

0.38

�0.38

0.25

�0.25

NA

NA

NA

NA

NA

NA

Silvan

idae

S.bid

enta

tus

200.00

�0.00

0.00

�0.00

1.88

�1.74

0.63

�0.50

9.23

0.0063

0.67

0.4228

0.67

0.4228

Staphylinidae

Total

40.00

�0.00

0.13

�0.13

0.25

�0.16

0.13

�0.13

NA

NA

NA

NA

NA

NA

Tenebrionidae

C.para

llel

us

216

0.25

�0.16

11.75

�7.78

7.38

�4.83

7.63

�7.06

9.59

0.0055

14.71

0.0010

15.73

0.0007

Diptera

Dolich

opodidae

M.bistr

iata

60.38

�0.68

0.00

�0.00

0.13

�0.13

0.25

�0.25

NA

NA

NA

NA

NA

NA

Lonch

aeidae

L.co

rtic

is1

0.00

�0.00

0.00

�0.00

0.13

�0.13

0.00

�0.00

NA

NA

NA

NA

NA

NA

Hymenoptera

Ichneumonidae

Org

illu

ssp.

10.00

�0.00

0.13

�0.13

0.00

�0.00

0.00

�0.00

NA

NA

NA

NA

NA

NA

B.Summer(26JulyÐ20August

2001)

Coleoptera

Sco

lytidae

I.pin

i1,082

18.75

�4.29

18.75

�6.18

52.75

�16.87

45.00

�10.27

13.02

0.0017

0.11

0.7487

0.06

0.8080

Males

515

8.25

�2.15

9.25

�3.49

23.38

�6.49

23.50

�5.33

15.50

0.0008

0.04

0.8427

0.00

0.9898

Females

567

10.50

�2.18

9.50

�2.98

29.38

�10.45

21.50

�5.12

9.75

0.0051

0.55

0.4647

0.22

0.6476

I.gr

andic

ollis

270

8.13

�4.46

5.50

�4.54

8.25

�4.98

11.88

�7.44

0.70

0.4116

0.02

0.8970

0.64

0.4323

Hyla

stes

spp.

140.25

�0.25

0.13

�0.13

0.50

�0.38

0.88

�0.64

NA

NA

NA

NA

NA

NA

O.ca

elatu

s103

6.88

�4.00

0.88

�0.52

0.88

�0.52

4.25

�2.51

0.29

0.5982

0.29

0.5982

7.21

0.0139

Cerambycidae

Total

30.00

�0.00

0.13

�0.13

0.13

�0.13

0.13

�0.13

NA

NA

NA

NA

NA

NA

Cleridae

Total

60.13

�0.13

0.50

�0.38

0.00

�0.00

0.13

�0.13

NA

NA

NA

NA

NA

NA

T.dubiu

s5

0.00

�0.00

0.50

�0.38

0.00

�0.00

0.13

�0.13

NA

NA

NA

NA

NA

NA

T.undula

tus

10.13

�0.13

0.00

�0.00

0.00

�0.00

0.00

�0.00

NA

NA

NA

NA

NA

NA

Cucu

jidae

Total

20.00

�0.00

0.25

�0.16

0.00

�0.00

0.00

�0.00

NA

NA

NA

NA

NA

NA

Histeridae

Pla

tvso

maspp.

30.00

�0.00

0.38

�0.26

0.00

�0.00

0.00

�0.00

NA

NA

NA

NA

NA

NA

P.cy

lindrica

10.00

�0.00

0.13

�0.13

0.00

�0.00

0.00

�0.00

NA

NA

NA

NA

NA

NA

P.para

llel

um

20.00

�0.00

0.25

�0.16

0.00

�0.00

0.00

�0.00

NA

NA

NA

NA

NA

NA

Silvan

idae

S.bid

enta

tus

313.38

�2.59

0.00

�0.00

0.50

�0.38

0.00

�0.00

2.35

0.1403

11.91

0.0024

2.35

0.1403

Staphylinidae

Total

20.00

�0.00

0.00

�0.00

0.25

�0.25

0.00

�0.00

NA

NA

NA

NA

NA

NA

Diptera

Lonch

aeidae

L.co

rtic

is4

0.13

�0.13

0.38

�0.38

0.00

�0.00

0.00

�0.00

NA

NA

NA

NA

NA

NA

Statistical

testsarelimitedto

those

speciesforwhichweobtainedaminim

um

of18

individuals.

NA,notap

plicable.


set of logs that were open to colonizers during days13Ð24. Emergence of Platysoma spp. and T. dubiusfrom all logs decreased 97 and 91% from the spring tosummer, respectively.During the summer, we obtained three species not

found in other experiments. Single specimens of twoichneumonids, Dusona americana (Ashmead) andCratichneumon rubricus (Provancher), were capturedarriving at red pine. We obtained one specimen eachof the braconid wasp Cyanopterus sp. on both red andwhite pine bolts colonized by I. pini (Table 5).

Discussion

A diverse assemblage of species from a variety offeeding guilds arrives at and exploits trees colonizedby I. pini.However, these associates are dominated byone or a few species within each taxon and feedingguild (Table 1). The most abundant species partitionthe resource based on time since I. pini colonization,host tree species, and/or seasonal phenology.There was strong partitioning among species in the

sequence of arrival to colonized tissue. This sequencemayprovide clues about the chemical ecologyof somenatural enemies whose behavior has not been thor-oughly studied. For example, M. bistriata arrived con-currently with, or slightly before, conspeciÞcs of theprimary herbivore I pini (Figs. 1Ð3). Orientation tocues associated with bark beetles by M. bistriata andG.politus is notwell understood,but these speciesmayuse pheromones and host tree volatiles to select ovi-position sites (Williamson1971).Thearrival of variousparasitoid species correlates with the life stage at-tacked. T. tibialis parasitizes adult I. pini and arrivesimmediately, exploiting aggregation pheromone sig-nals (Rice 1968).R. xylophagorum enters galleries andparasitizes late instars (Samson 1984) and arrives pre-dominantly 15Ð26 d after colonizationwhen larvae arepresent (Fig. 3C).R. xylophagorummay usemicrobialvolatiles or other cues particular to the preferred lifestage to aid in host Þnding (Sullivan et al. 2000, Pet-tersson et al. 2000).The total emergence of I. pini did not vary across

host trees. In contrast, some members of the naturalenemy complex, such as the competitor and faculta-tivepredatorMonochamus spp. (Doddset al. 2001)andthe parasitoid R. xylophagorum, showed strong hosttree associations. Host tree partitioning may be facil-itated by favorable physiological properties, such asbark thickness and nutritional properties of thephloem tissue, or phytochemistry (Savely 1939, Law-son et al. 1996). For example, the soft bark of whitepine may facilitate oviposition by Monochamus spp.,which chew egg niches into the stem surface. Whitepine also has higher concentrations of oxygenatedmonoterpenes, which are attractive to R. xylophago-rum (Pettersson et al. 2000). Partitioning among hosttree speciesmay reduce interspeciÞc competition andintraguild predation, because many of the subcorticallarval predators, such as T. dubius and dolichopodidßies, are feeding generalists once in the bark beetle

habitat (Thomas 1955, Dahlsten and Stephen 1974,Lawson et al. 1996, Ounap and Elberg 1999).The numbers and distribution of insects that re-

spond to pine logs colonized by I. pini are also parti-tioned by seasonal phenology, which could affectcompetition, predation, and the population dynamicsof I. pini.Most I. pini emerged from logs in the summertrials (Tables 2 and 3). More potentially competitivephloeophagous species, such as G. materarius, O. cae-latus, D. autographus, Dryophthorus americanusBedel,and Pissodes spp., were present in the spring thansummer. Resulting interspeciÞc competition, as wellas possible kairomonal attraction of predators to cuesassociated with these insects (Thomas 1955), couldsuppress I. pini early in the ßight season. Competitionfromother Ips speciespresent in the region, suchas Ipsgrandicollis (Eichhoff) and Ips perroti (Swaine), waslow, even though the former are often abundant (Ay-res et al. 2001, Erbilgin and Raffa 2001, Wallin andRaffa 2001).The relative rate of increase, or the ratio of emer-

gence to arrival, varied among different host treeswithin insect species. I. piniÕs relative rate of increasewas highest in jack pine (Table 4), perhaps becausethere were fewer predators overall in this tree (Table2; Fig. 4A). The rate of increase of T. dubius estimatedfrom this Þeld study agrees closely with that obtainedfromcontrolled laboratory studies (AukemaandRaffa2002). In each case, replacement rates by this predatorwere less than one on a per log basis, indicating theneed for this species to undertake multiple oviposi-tional events to be successful (Table 4; Aukema andRaffa 2002). Between-insect differences in ratios ofemergence to arrival need to be treated with cautiondue to differences in relative effectiveness of varioustrap types and sampling efÞciencies, and varying mat-ing and ovipositional strategies.Although exclusion experiments provide a useful

tool for estimating natural enemy impacts in somesystems, the concurrent arrival of predators and col-onizing herbivores poses serious challenges to studiesof bark beetle population dynamics (Linit and Ste-phen 1983). In our experiments, the reduced emer-genceofbarkbeetles after enclosureof logsduring theÞrst 2wkpost-colonization cannot be attributed solelyto predation, because it also limited the number ofcojoining herbivores. An alternate approach is to fullycolonize the logs with herbivores in the laboratorybefore exposing them to Þeld populations. However,the cessation of pheromone production under theseconditions may decrease predator arrival (Miller1984). A nonmanipulative alternative is to model nu-merical responses among bark beetles and associates.For example, both clerids and R. xylophagorum exhib-ited positive numerical responses to I. pini emergenceor arrival (Aukema 2003). However, there can bepronounced multicollinearity in bark beetleÐnaturalenemy population data, at both the plantation (Erbil-gin et al. 2002) andwithin-tree (Aukema 2003) levels.This demands caution when inferring causeÐeffectrelationships. Controlled laboratory-amending exper-iments can complement such studies (Aukema and


Raffa 2002), and the confounding effects of multiplepredators may be separated by studies of individualand collective predator behaviors and impacts(Rosenheim 1998). However, like all laboratory stud-ies, these may be less realistic than Þeld conditions.Given the diversity of this assemblage, the responsesby several species to common chemical signals, andthe interactions among these insects at several levelsof scale, a combination of approaches seems neces-sary.

Acknowledgments

We thank the Wisconsin Department of Natural Re-sources, J. Lentz, and A. Petrulis for providing the trees andstudy sites. Field and laboratory assistance by R. Chrouser, S.Eastwood,R.Hoffman, andJ. “Chainsaw”Luddenwasgreatlyappreciated. J. Luhman (Minnesota Department of Agricul-ture),M. Sharkey (Department ofEntomology,University ofKentucky, Lexington), and M. Yoder (Department of Ento-mology, Texas A&M University, College Station) providedvaluable helpwith insect identiÞcation.M. Clayton (Depart-ment of Statistics, University of Wisconsin, Madison) pro-vided statistical advice. This study was supported by the U.S.Department of Agriculture USDA NRI AMD 96 04317, theWisconsin Department of Natural Resources, the Universityof Wisconsin-Madison College of Agricultural and Life Sci-ences, and S.C. Johnson & Son, Inc. We thank R. Lindroth,J. Handelsman, T. Ives, M. Eubanks, and an anonymous re-viewer for helpful critiques on an earlier version of thismanuscript.

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Received for publication 24 January 2003; accepted 1 Oc-tober 2003.


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