The Southern Pine Beetle

Chapter 3: Natural Enemies and Associated Organisms

C. Wayne Berisford – Department of Entomology, University of Georgia, Athens, GA

The southern pine beetle is intimately associated with a large number of other organisms. They directly or indirectly affect its development and survival through parasitism, predation, competition, and symbiosis. These associates include other insects, mites, birds, fungi, nematodes, and various insect and plant disease organisms.

Since the beetle is difficult and expensive to control with current technology, and some of its associates obviously can influence SPB population growth, the ESPBRAP supported studies seeking to better understand the roles of many associates. If we are to develop integrated suppression tactics, we must understand the life processes of the beetle and its associates.

Studies prior to ESPBRAP dealt primarily with compiling lists of SPB associates. Most of the attention was focused on other insects, mites, and nematodes. The known or suspected roles for the parasites, predators, and scavengers were indicated (Thatcher 1960, Dixon and Osgood 1961, Moser and Roton 1971, Moore 1972, Coulson et al. 1972a, Overgaard 1968). However, the impacts and interactions of these associates were unknown. Studies supported by ESPBRAP were oriented toward determining the specific roles and impacts of associates, particularly parasitoids and predators. We need this type of information to develop realistic SPB population models that can detect and/or forecast population trends, and to implement control strategies which can capitalize on SPB population suppression by natural enemies.

Arthropod Enemies of SPB

Insects and mites are among the principal natural enemies of the southern pine beetle. Recent research has identified these mortality agents and described their seasonal, geographic, and with in-tree distribution, and general biology. Some reports concentrate on one or a few species (Lenhard and Goyer 1979, Hain 1978 unpublished, Dixon and Payne 1979a, Gargiullo and Berisford 1980). Dixon and Payne (1979b) have provided information on SPB associates attracted to infested trees and include data on numbers and temporal and spatial distribution of the associates. An illustrated guide to insect associates of the SPB has been developed (Goyer et al. 1980). The guide includes color photographs and distinguishing characteristics of each insect. Using this manual, workers with minimal training in entomology can easily identify the associates. Stephen and Taha (1976) have developed a sampling system for estimating numbers of natural enemies in Arkansas. The system describes a sampling protocol and presents curves for number of samples v. sample unit sizes needed to obtain

Figure 3-1 – Relationships between number of samples needed and size of the sample unit to estimate the density of predators. The 90% confidence limits are included. (Redrawn from Stephen and Taha 1976).

90 percent statistical confidence (fig. 3-1; see also
fig. 6-8).

Predators

A number of arthropods, primarily insects, prey on the SPB (Appendix, table 2). Predators may attack SPB adults during tree colonization and/or prey on the egg and larval stages during brood establishment and development. Generally, predators are not closely associated with their prey for a long period of time. Each prey usually constitutes a single meal, and each predator may consume several prey during its lifetime. With the exception of predaceous mites, most predators of SPB are larger than their host(s).

Checkered Beetles

The most common, colorful insect predator of SPB is the checkered or clerid beetle, Thanasimus dubius (F.) (Coleoptera: Cleridae). Clerid adults eat attacking SPB adults, and clerid larvae attack SPB larvae. This predator responds to SPB attractants and aggregates on trees undergoing mass attack by the beetle (Vité and Williamson 1970).

Hopkins (1899) first recognized T. dubius as a potentially important natural enemy of pine bark beetles. Several subsequent studies examined its biology, behavior, and impact on the SPB. Dixon and Payne (1979a) described the temporal and spatial distribution of T. dubius on SPB trees under mass attack in Texas. They reported peak numbers of clerids 1 day after peak SPB attack (fig. 3-2). Clerids were most abundant 4 days after initial SPB attack. Attacks by both SPB and the clerids lasted up to 11 days. Highest numbers of both were trapped early and late in the day in Texas and in Georgia (Dix and Franklin 1977). About 64 percent of both species were trapped on the lower half of the infested bole (Dixon and Payne 1979a).

Figure 3-2 – Sequence of arrival of T. dubius and southern pine beetles on trees under mass attack by SPB. Vertical bars = ± SEx. Based on 7 trees, 3,173 T. dubius, and 29,896 SPB. (From Dixon and Payne 1979a).

Lenhard and Goyer (1980) reared T. dubius from log bolts taken during 1975 through 1977 in Louisiana. SPB activity was very high during this period. Clerids were found to be most active during spring and winter. Clerid densities did not strongly correlate with either SPB egg gallery length or bark thinkness. Frazier et al. (1980) described in detail the predatory behavior of adult T. dubius. They found that both sexes go through six typical behavioral acts as they prey on SPB (figs. 3-3 and 3-4). Frazier’s team determined the average time invested in each act and calculated the predator’s efficiency. Studies of developmental rates of T. dubius revealed that immature stages developed more rapidly as temperatures increased from 12.5° C to 27° C (Nebeker and Purser 1980). Total developmental time (egg to adult) was the same whether clerid larvae were fed small or large SPB larvae or large pupae. But the prepupal and pupal periods were longer for clerids that had been fed on large SPB larvae and pupae.

Figure 3-3 – The behavioral sequence of events in predation by Thanasimus dubius adults. (From Frazier et al. 1980).

Figure 3-4 – Predatory behavior of adult Thanasimus dubius. A = ambush, B = searching, C = catching, D = prey orientation and locomotion, E = prey consumption, F = grooming and nonlocomotion. (From Frazier et al. 1980).

Corticeus Predators

Beetles in the genus Corticeus (Coleoptera: Tenebrionidae) are very abundant and are commonly observed on SPB-infested trees (fig. 3-5). Although they are generally considered to be facultative predators (Moser, Thatcher, and Pickard 1971), their sheer abundance has attracted considerable attention. Smith (1978) described the immature stages of C. glaber and C. parallelus and determined that they both have five larval instars. Controlled laboratory studies showed that both species complete their development from eggs to adults in 30 to 41 days. Observers found that Corticeus adults enter SPB entrance or reemergence holes and egg galleries by removing frass (waste products and sawdust). Adults frequently feed on SPB frass and blue-stain fungi (Ceratocystis minor Hedgecock) prior to mating and oviposition. Gut analysis of adult Corticeus spp. (Smith 1978) revealed that 80 percent of the beetles had consumed SPB frass

Figure 3-5 – Adult of the tenebrionid beetle Corticeus glaber. Photo by R.A. Goyer.

and/or blue-stain fungi. Stomachs of the remaining beetles contained fatty material, possibly some SPB life stage. Corticeus females oviposit in SPB egg galleries, laying single or small groups of eggs.

Laboratory experiments (Smith 1978) confirmed that Corticeus spp. adults were facultative predators and fed on SPB eggs, first- and second- instar larvae, as well as SPB frass and blue-stain fungus.

In Louisiana, C. glaber is almost four times more abundant than C. parallelus (Smith and Goyer 1980). Corticeus spp. arrive at SPB-infested trees for up to 14 days after SPB mass attack. C. glaber is most abundant in March-April and October-November, while C. parallelus is more abundant from February through June. The predators are more abundant in the lower parts of SPB-infested trees.

Miscellaneous Predators

Lenhard and Goyer (1980) (table 3-1, figs. 3-6 and 3-7) found that in Louisiana the most frequently encountered predators included Corticeus spp., Scoloposcelis mississippensis (Hemiptera: Anthocoridae), Aulonium ferrugineum (Coleoptera: Colydiidae), and Medetera bistriata (Diptera: Dolichopodidae). Numbers of predators were generally poorly correlated with SPB egg gallery length and bark thickness.

Figure 3-6 – Estimated numbers of SPB predators except Corticeus spp., 1975-1977. (From Lenhard and Goyer 1980).

Figure 3-7 – Numbers of Corticeus spp. associated with SPB, 1975-1977. (From Lenhard and Goyer 1980).

When the impact of individual predaceous species is known, we can contribute to models to evaluate the efficacy of the predator complex under different conditions.

Parasitoids

Parasitoids differ from predators in that parasitoids are more intimately associated with their host. Whereas predators feed as adults and/or larvae on several hosts, parasitoids usually develop from egg to adult on a single host. Parasitoids known to attack SPB are listed in the Appendix, table 2.

Some parasitoids are host specific: they attack only one host species or a group of closely related species with similar habits. Only a few host-specific parasitoids are known for SPB.

Table 3-1. – Mean number of predators per 100 cm² and percent of total predators considered.

Most SPB parasitoids are common on, or will accept, other bark beetle or ambrosia beetle hosts (Dixon and Osgood 1961, Thatcher 1960, Bushing 1965). Many parasitoids of SPB also attack one or more species of Ips ark beetles (Berisford, Kulman, and Pienkowski 1970; Berisford et al. 1971; Berisford 1974a; Kudon and Berisford 1980b). Parasitism of more than one bark beetle species is not surprising since one or more Ips spp. often occur in the same parts of the same trees attacked by SPB.

Identification of Parasitoids

All of the more common parasites are illustrated in the SPB associates identification guide by Goyer et al. (1980).

Until recently, no single source existed for identifying immature parasitoids of southern pine bark beetles. Finger and Goyer (1978) have published descriptions of the mature larvae of the most common hymenopterous parasitoids of the SPB. Their article includes a key for identifying late-stage larvae and adults (Appendix, table 3). This will help investigators considerably in determining the identities, biologies, roles, and interactions of individual parasitic species.

Parasitoid Attack Behavior

Adult parasitoids apparently respond to insect- and host-produced odors to locate trees infested with advanced SPB brood stages (Camors and Payne 1973). How female parasitoids locate potential hosts beneath the bark is unknown. Some experimental evidence from studies of other bark beetles suggests that they orient to sound (Ryan and Rudinsky 1962) or heat (Richerson and Borden 1972). Female parasitoids generally oviposit through the bark onto third- or fourth- instar larvae (Berisford 1976 unpublished). Most parasitoids apparently sting the host to immobilize it before depositing their eggs. But one of the most common SPB parasitoids, Roptrocerus xylophagorum Ratzeburg, enters the bark through SPB entrance and air holes and oviposits in the SPB egg galleries. Another parasitoid, Heydenia unica Cook and Davis, arrives during the beetle’s attack stage, possibly to mate, since no SPB larvae are available to parasitize (Camors and Payne 1971, Dixon and Payne 1979b). Most of the parasitoids associated with SPB arrive at infested trees when large numbers of acceptable hosts are available (Camors and Payne 1973, Dixon and Payne 1979b). Figure 3-8 shows arrival patterns of some common parasitoids relative to SPB brood development.

Figure 3-8 – Sequence of arrival of the SPB parasitoids Coeloides pissodis, Dendrosoter sulcatus, Heydenia unica, and Spathius pallidus, in relation to SPB brood development. Numbers trapped are shown in parentheses. Totals were from seven trees. (From Dixon and Payne 1979b).

Factors Influencing Parasitoid Populations

Numbers of parasitoids in SPB-infested trees may be strongly influenced by beetle brood density and bark thickness (Goyer and Finger 1980, Gargiullo and Berisford 1980). Regressions of numbers of parasitoids against SPB brood density for different bark thickness categories revealed the relative effect of each factor on individual parasitic species. Figure 3-9 shows regressions calculated for two common SPB parasitoids, Spathius pallidus and Coeloides pissodis. Bark thickness. – Most of the parasitoids—Heydenia unica Cook and Davis, Cecidostiba dendroctoni Ashmead, Dendrosoter sulcatus Musebeck, Coeloides pissodis Ashmead, Eurytoma spp., Rhopalicus spp., Spathius pallidus Ashmead—increased in number as the bark became thinner. Roptrocerus xylophagorum was strongly affected by bark thickness even though it enters the SPB galleries to lay its eggs. Most of the parasitoid species reached maximum numbers at intermediate host densities, with the exception of Eurytoma spp. Spathius pallidus was apparently unaffected by host density, and R. xylophagorum became increasingly abundant as host density increased and bark became thinner. It was the only parasitoid that showed a significant interaction between bark thickness and host density.

Figure 3-9 – Numbers of the parasitoids Spathius pallidus (A) and Coeloides pissodis (B) relative to numbers of SPB at different bark thicknesses. (From Gargiullo and Berisford 1980).

Figure 3-10 – Numbers of natural enemies, including parasitoids relative to numbers of SPB brood adults at three locations in North Carolina. (From Hain 1978 unpublished).

Parasitoid population differences. – Hain (1978 unpublished) reported quantitative and qualitative differences in natural enemy populations at three locations in North Carolina. But differences were not as well correlated with SPB brood adult densities as in Louisiana (fig. 3-10). In Louisiana highest numbers of parasitoids occurred during April-June, with a second peak in August. Lowest parasitoid populations were found in the fall and winter, when SPB populations were also low (fig. 3-11). Similar seasonal patterns were observed in Texas (Stein and Coster 1977) and Arkansas (Stephen 1980). Figure 3-11 – Seasonal abundance of parasitoids relative to numbers of SPB eggs in SPB-infested trees in Louisiana. (From Goyer and Finger 1980). Parasitoid Responses to Behavioral Chemicals The response of parasitoids to beetle- and/or tree- produced compounds released from SPB-infested trees has received only limited attention. Camors and Payne (1971) showed that one parasitoid, Heydenia unica, responds to host tree terpenes and a component of the SPB attractant chemical, or pheromone. Dixon and Payne (1980) caught four species of SPB parasitoids in traps baited with various combinations of SPB- and tree-produced compounds, plus bolts artificially infested with SPB females. Although no host larvae are present at the time of SPB mass attack, Dixon and Payne suggest that the compounds may serve to concentrate parasitoids in areas where hosts in suitable life stages would soon be available.

Kudon and Berisford (1980a) developed an olfactometer to evaluate the response of SPB parasitoids to insect- and tree-produced odors. This device will aid in preliminary screening of compounds that may attract parasitoids. Final determinations of attractancy must be made in the field, however.

Nonhost-Specific Parasitoids

Many of the parasitoids that attack SPB also attack other bark beetles, as noted previously. In fact, the parasitoid complexes associated with Ips avulsus Eichoff, I. grandicollis Eichoff, I. calligraphus (Germar), I. pini Say, and the eastern juniper bark beetle (Phloeosinus dentatus [Say]) share with the SPB three of the most common species - Roptrocerus xylophagorum (= eccoptogastri), Heydenia unica, and Coeloides pissodis (Berisford et al. 1970 and 1971, Berisford and Franklin 1971, Berisford 1974a and b).

It has been generally assumed that the SPB parasitoids which were not host-specific would utilize the most abundant acceptable hosts available and that other bark beetles (e.g., Ips spp.) would serve as reservoir hosts when SPB populations were low. However, Berisford (1974a) found that when both SPB and Ips spp. were available, parasitism did not readily shift from one species to the other. This fact suggests that some parasitoids may prefer a particular host, if they are not host specific.

Kudon and Berisford (1980b) showed that when adult parasitoids were reared from SPB-infested logs in field cages and given simultaneous choices between different logs containing late-instar larvae of SPB and Ips or SPB and P. dentatus, a high percentage of the parasitoids selected logs with SPB (fig. 3-12A and B). When parasitoids were reared from Ips or P. dentatus, the parasitoids reversed their preferences. The preferences were even greater when the parasitoids could select both beetle hosts (SPB v. P. dentatus) and tree hosts (pine v. cedar) instead of beetle hosts only (SPB v. Ips) in loblolly pine (fig. 3-12C and D).

Figure 3-12 – Parasitoids reared from SPB (A) and Phloeosinus dentatus (B) presented with simultaneous choices of logs infested with SPB or Phloeosinus dentatus. Parasitoids reared from SPB (C) and Ips grandicollis (D) presented with simultaneous choices of logs infested with SPB or Ips grandicollis. (From Kudon and Berisford 1980b).

Thus, it seems that the parasitoids, although not host-specific, are entrained to initially select the host on which they were reared. This phenomenon appears to be the first documented manifestation of Hopkins’ (1916) Host-Selection Principle among insects that prey on other insects.

Identification of Previous Hosts of Predators and Parasitoids

Knowing the identity of previous hosts of adult parasitoids or predators that respond to SPB-infested trees would help to determine if other bark beetles are acting as alternate and/or reservoir hosts. Miller et al. (1979) and Miller (1979) have utilized immunodiffusion and immunoelectrophoresis techniques to produce antisera which are specific for SPB and some of its bark beetle associates (Ips spp. and black turpentine beetle). These techniques may be used to help determine the prey of SPB predators such as Thanasimus dubius and may help estimate the number of prey consumed. Kudon and Berisford (1980c) found that the fatty acid composition of parasitoids reared from SPB and some if its common associates closely matched the composition of their beetle host(s). With this discovery the host origin of a single parasitoid can be determined, provided that the host’s lipid profile has already been established. Figure 3-13A and B shows the similarity between the lipid profile of SPB and a parasitoid, Heydenia unica, reared on SPB. Figure 3-13C and D shows lipid profiles for I. calligraphus and H. unica reared on I. calligraphus. The technique of comparing lipid profiles may also help to determine predator hosts if they feed on a single prey species. The clerid Thanasimus dubius was fed on SPB and the cowpea weevil (Callosobruchus maculatus). The profile of T. dubius reared on SPB matches the host profile well. But the profile of those reared on the weevil—an unnatural host—differs from that of clerids fed on the SPB.

Figure 3-13 – Lipid profile of SPB (A) and a parasitoid, Heydenia unica (B), that had been reared on SPB. Lipid profile of Ips calligraphus (C) and the same Heydenia unica (D) which had been reared on I. calligraphus. (From Kudon and Berisford 1980c).

The host-induced preferences of parasitoids may be a factor affecting the impact of the parasitoid complex on SPB populations. Although the relatively high populations of Ips spp. usually present in logging slash, damaged trees, lightning strikes, etc., can support substantial parasitoid populations, Ips may not be a reservoir for SPB parasitoids, due to their host preferences. On the other hand, the parasitoids seem able to attack other hosts if the preferred host is not readily available. This adaptability may be a survival-enhancing mechanism.

At this point we do not understand the mechanism of parasitoid switching from one host to another. If we assume that the preferences will create a lag in acceptance of nonpreferred hosts, this may reduce potential parasitism in at least one generation of hosts. A theoretical conceptual model of parasitoid-host interactions among SPB, Ips, and their common parasitoid complex has been proposed (Berisford and Kudon unpublished). The model is based on a relatively stable Ips population v. fluctuating SPB populations. It describes the shifts of parasitoids between the beetle hosts as each host becomes more or less abundant relative to the other host over time. During SPB epidemics, Ips populations will also increase since Ips spp. normally attack SPB-infested trees. The relative populations, however, still fit the hypothesis of the model, i.e., that the relatively scarce host loses parasitoids to the relatively abundant one regardless of absolute populations.

Figure 3-14 illustrates the theoretical parasitoid-host relationships of SPB populations for a full cycle from endemic to epidemic to endemic states. At endemic SPB levels, Ips populations in logging slash, damaged trees, etc., are relatively large compared to SPB, and most parasitoids would go from Ips- to Ips-infested material since they developed on this host. As SPB populations begin to expand, parasitoids find SPB increasingly easier to locate relative to Ips and they begin to shift from Ips- to SPB-infested trees. As SPB reaches epidemic levels, the shift to SPB becomes very pronounced. There is no tendency to select the now relatively low populations of Ips beetles. As SPB populations decline, the parasitoids switch back to the relatively more abundant Ips as the preferred host (SPB) becomes less available. The same phenomenon may occur within individual trees. During SPB epidemics, a high percentage of an infested tree bole is occupied by SPB. Any shift of parasitoids is most likely to be from Ips to SPB since searching adult parasitoids would frequently encounter SPB. When SPB is at endemic levels, though, it frequently occupies only a small part of a tree; the remainder is occupied by Ips. The parasitoids will cycle from Ips to Ips and have reduced impact on the less abundant SPB. Mites A large number of phoretic mites are associated with the southern pine beetle (Moser and Roton 1971, Moser 1975). Several species prey on SPB. Some indirectly affect SPB by reducing flight and mobility, while others indirectly benefit the beetle by preying on parasitic nematodes (Kinn and Witcosky 1977, Kinn 1980). Figure 3-15 shows an SPB adult with mites attached. Predaceous Mites Moser (1975) conducted laboratory tests to determine which mite species prey on SPB. He found that 32 of 51 species were predaceous on one or more SPB life stages (Appendix, table 4). First-instar larvae were the preferred host life stage.

Figure 3-14 – Theoretical stand model of parasitoid shifts from the relatively scarce hosts to the more abundant host bark beetles (Ips spp. and SPB) during the buildup of SPB from endemic to epidemic levels and the subsequent decline to endemic populations. (From Berisford and Kudon 1979 unpublished).

Figure 3-15 – An SPB adult with phoretic mites attached. Photo by J.C. Moser.

Four mite species appeared to be good candidates for natural control of the SPB: Histiogaster arborsignis Woodring, Proctolaelaps dendroctoni Lindquist and Hunter, Macrocheles boudreauxi Krantz, and Dendrolaelaps neodisetus Hurlbutt. Subsequent studies revealed that M. boudreauxi feeds primarily on nematodes. In laboratory rearing experiments, its presence did not affect SPB egg hatch or brood production (Kinn and Witcosky 1977). Four other species - Eugamasus lyriformis McGraw and Farrier, Dendrolaelaps neocornutus Hurlbutt, D. isodentatus Hurlbutt, and Proctolaelaps fiseri Samsinak-were suggested as secondary choices for control of SPB in the field.

Dendrolaelaps neodisetus apparently has a mutualistic relationship with the SPB (Kinn 1980). In this study progeny production by the SPB was not different in broods reared from adult beetles with and without D. neodisetus. However, emerging brood adults had a significantly lower incidence of parasitism by the nematode Contortylenchus brevicomi if D. neodisetus mites were present on the parent SPB. In field-collected samples from SPB-infested trees, there was a strong negative correlation between numbers of the nematode C. brevicomi and presence of D. neodisetus. Therefore, SPB populations with only a few of the phoretic D. neodisetus would be more likely to have a higher incidence of parasitism by C. brevicomi. The mutual benefits to SPB and D. neodisetus are obvious. The SPB provides a mechanism for the flightless mites to move to new beetle infestations, and the SPB benefits by having a reduced chance of nematode parasitism because the mites feed on the free-living stages of C. brevicomi.

Mites Associates Key

Kinn (1976) published a key that identifies 15 species of phoretic mites most commonly associated with SPB (Appendix, table 5). The key is written with minimal acarology jargon so that researchers and students untrained in mite taxonomy can use it efficiently. It also contains instructions for mounting mites on slides for identification.

Phoretic Mites

A nondestructive SPB trap (Moser and Browne 1978) has been used to evaluate the effect of phoretic mites on the flight of SPB adults (Kinn and Witcosky 1978). The researchers found that 36 percent of SPB adults trapped (primarily males) carried uropodid mites or their attachment pedicels. It was also found that the color of mite pedicels indicated the relative age of SPB to which they were attached. Callow SPB adults or other newly emerged adults have white pedicels; reemergent parent adults have amber or black pedicels.

Under forest conditions at least one-third of the SPB carry mites (Moser 1976a). Further, beetles attacking lower portions of trees have more attached mites that those attacking upper stems. Flying SPB can carry at least 20 percent of their weight in mites (Moser 1976b). These and results from other investigators (Dixon and Osgood 1961) indicate that mites may have a significant effect on flight dispersal.

Although many of the mites are usually regarded as phoretic on the SPB alone, many species also ride on other bark beetles and associated species to get to other host material (Moser 1976a). Therefore, mites associated with SPB-infested trees may have gotten there on a variety of insects.

Profile of Mite Associates

Stephen and Kinn (1980) reported the distribution, seasonal fluctuation, and relative diversity of mites associated with SPB. More mite species are found in the upper boles of SPB-infested trees than in the lower boles, due to higher numbers of other bark beetles in that portion of the bole and larger numbers of a few mite species in the lower bole. The distribution of Tarsonemus krantzi Smiley and Moser was somewhat uniform over the entire bole. Trichouropoda australis Hirschmann and Dendrolaelaps neodisetus were more abundant in the lower bole. Pygmephorellus bennetti (Cross and Moser) and Tarsonemus ips Lindquist were most abundant in the upper bole.

Seasonal distribution. – The relative abundance of the common mite associates varied seasonally. Proctolaelaps dendroctoni, Longoseius cuniculus Chant, and Macrocheles boudreauxi were most common in early summer. During midsummer, D. neodisetus, Eugamasus lyriformis, and Trichouropoda australis were most abundant. Tarsonemus krantzi and T. ips increased in numbers from midsummer through early fall. Anoetus varia Woodring and Moser and Histiogaster arborsignis were most abundant

during the fall. One species, Ereynetoides scutulis Hunter, showed little change in seasonal abundance (D.N. Kinn personal communication). Sampling methods. – Sampling for mites phoretic on SPB and other bark beetles is best accomplished with emergence traps (Kinn 1979). The traps described by McClelland et al. (1978) give reliable estimates because they minimize losses due to rearing, dessication, and transporting samples. Also, fewer nonphoretic stages accumulate in collecting medium. The various species of mites associated with SPB perform different functions. Some are predators, while others are scavengers, facultative predators, predators of other natural enemies, or even mechanical barriers to normal SPB flight. Avian Predators Birds, especially woodpeckers, have been credited as important natural enemies of the SPB since the earliest beetle studies (Hopkins 1899 and 1909a, St. George 1931). But despite their apparent importance in regulating beetle populations, there have been few attempts to quantify the role of woodpeckers or to describe the forest conditions under which such predation is most effective. Dixon and Osgood (1961) reported higher mortality of SPB from low temperatures in trees where bark had been partially removed by woodpeckers than in trees with no evidence of foraging. In fact, woodpeckers feeding on SPB trees often remove most of the bark (fig. 3-16). Overgaard (1970) reported a 24 percent reduction in SPB populations by woodpeckers. Moore (1972) concluded that woodpeckers were very effective SPB predators. In a comprehensive study, Kroll and Fleet (1979) studied four species of woodpeckers (downy, hairy, pileated, and red-bellied) (fig. 3-17A - C) to determine their role in SPB population dynamics in Texas. They found that all of the woodpecker species studied preyed heavily on SPB. During a period of rapid SPB buildup in Texas (1966-76), woodpecker censuses showed a strong correlation between numbers of birds and numbers of SPB spots. Woodpeckers were found to feed heavily on SPB when they were very abundant and on soft mast when beetle populations were low.	Figure 3-16 – A tree that has been heavily foraged by woodpeckers and contains SPB brood. (From Kroll et al. 1980).
	Figure 3-17 – A: Adult downy (below left) and hairy (above right) woodpeckers. (From Kroll et al. 1980).
Figure 3-17 – B: Pileated woodpecker. (From Kroll et al. 1980).	Figure 3-17 – C: Red-bellied woodpecker. (From Kroll et al. 1980). Highest numbers of woodpeckers were found in SPB spots during late summer and lowest numbers

in late winter (fig.3-18). Woodpeckers were up to 50 times more numerous in stands infested with SPB than in neighboring, noninfested stands. All four woodpecker species showed some ability to shift from uninfested to infested stands. Downy and hairy woodpeckers accounted for most of the predation of SPB by birds. In uninfested stands, mixed pine-hardwoods generally had higher densities of woodpeckers than pure pine stands, probably because there were more nesting sites and other food sources (e.g., mast).

Figure 3-18 – Densities of woodpeckers in SPB spots at different times of the year. (From Kroll 1979 unpublished).

Figure 3-19 – Distribution of woodpecker feeding activity on the boles of SPB-infested trees during different seasons. (From Kroll 1979 unpublished).

In SPB-infested trees, woodpecker activity was greatest in the midbole-where the beetle congregate. Predation was greatest during fall and summer and least during spring (when SPB spots begin to become active and proliferate) (fig. 3-19).

Woodpeckers preyed mainly on SPB brood adults (64 percent) and least often on eggs (4 percent). Foraging was almost twice as great on shortleaf as on loblolly pine, probably because the woodpeckers could flake off the thinner bark of shortleaf pines more easily to get at the SPB. The seasonal impact of woodpeckers on the SPB and some of its associates was evaluated by protecting portions of SPB-infested trees from woodpeckering as SPB broods matured. Beetle mortality was highest during the winter (36 to 63 percent) and lowest in summer (12 to 30 percent). Figure 3-20 illustrates survival of SPB in screened and unscreened sections of trees. The portions of trees from which woodpeckers were excluded had substantially higher beetle survival than unscreened parts of the same trees. Kroll, Conner, and Fleet (1980) proposed the adoption of timber management practices to increase the number of woodpeckers and their impact on SPB. They advocate maintaining mixed pine-hardwood stands and promoting shortleaf and

Figure 3-20 – Survival of SPB in trees which were screened to prevent woodpecker predation and survival in unscreened trees. (From Kroll 1979 unpublished).

longleaf pine stands where suitable. Other woodpecker-enhancing tactics include providing more nesting sites for woodpeckers and modifying current cut-and-leave suppression tactics to leave standing those trees already vacated by SPB broods for woodpecker nesting sites.

Competitors

The southern pine beetle competes with other insects for the same food supply during a part of its developmental period. This competition for available food and/or space may significantly reduce SPB survival.

Southern Pine Sawyer

Although this associate has been known for some time, the first comprehensive study of its role as an SPB competitor was conducted only recently (Coulson et al. 1976b). Results confirmed that foraging by larvae of the southern pine sawyer (fig. 3-21), Monochamus titillator (Fab.) (Coleoptera: Cerambycidae), significantly reduced SPB survival. The distribution of M. titillator over the bole of infested trees has been described and mathematical models have been developed to account for SPB mortality caused by sawyer larvae. Figure 3-22 shows the impact of cerambycid foraging when observed and expected numbers of SPB were compared in areas foraged by M. titillator.

Figure 3-21 – The southern pine sawyer, Monochamus titillator. (From Goyer et al. 1980).

Figure 3-22 – Impact of foraging by pine sawyer larvae on SPB broods. Curves show differences between expected numbers of SPB and those actually observed. (From Coulson et al. 1980a).

Procedures have been developed for predicting SPB mortality based on M. titillator activity. Coulson et al. (1980a) showed that the sawyer foraged up to 20 percent of the inner bark/outer wood surface area of SPB-infested trees, killing about 14 percent of the SPB per tree. However, SPB mortality in foraged areas ranged up to 70 percent. Sawyer feeding was greater in larger trees. Foraging and subsequent SPB mortality increased from the base to the top of the infested trees.

Bark Beetle Associates

Four other bark beetles — Dendroctonus terebrans (Olivier), Ips avulues, I. grandicollis, I. calligraphus — are commonly associated with the SPB. The black turpentine beetle, D. terebrans, frequently attacks the basal portion of SPB-infested trees. But it overlaps with SPB in only a small proportion of the colonized bole. Thus competition for the same food supply is small.

Three species of engraver beetles, Ips spp., frequently attack portions of the trees concurrently attacked by SPB. I. avulsus, I. grandicollis, and I. calligraphus may compete with SPB for the same food supply and space. Birch and Svihra (1979) studied the competitive interactions among the five bark beetle species in Texas. Examination of loblolly pines felled shortly after bark beetle attack showed that SPB and the associated Ips all attacked within a short timespan. Southern pine beetle was the first to initiate attacks in most cases, but only two of 28 trees were attacked solely by SPB. After the SPB attacked, I. avulsus and I. calligraphus moved in quickly. I. grandicollis rarely infested boles of standing trees but was frequently found in branches. The portions of the main bole occupied by the various species of bark beetles are shown in figure 3-23. Paine, Birch, and Svihra (1980) determined how much of the tree was occupied by SPB and four species of competitors and how much over-lap occurred among them. I. avulsus occupied the greatest length of bole and I. grandicollis the shortest length. The upper parts of infested trees were dominated by I. avulsus, while the lower parts were dominated by SPB. I. avulsus thus overlapped only slightly with SPB. I. calligraphus showed considerable overlap with SPB. More bark beetle species occupied the mid-bole area than any other part of the tree. Fewer species overlapped each other at the extremes of the infested area. Pheromones

Figure 3-23 – Area of the main bole of loblolly pine occupied by each of five species of bark beetles. (From Birch and Svihra 1979).

The southern pine beetle and its associated bark beetle competitors all produce aggregation pheromones (Birch 1978). Some bark beetles may use pheromones as species isolation mechanisms (Wood 1970, Lanier and Wood 1975). Birch and Wood (1965) and Byers and Wood (1980) demonstrated that two closely associated bark beetles may utilize reciprocal inhibition to avoid competing for the same food. These species may colonize the same tree but occupy different parts due to inhibition of attacks by species that follow the primary attacker.

Birch et al. (1980) determined the response of different beetles to logs infested with various combinations of SPB, I. avulsus, I. grandicollis, and I. calligraphus. The first beetles to arrive were generally SPB if SPB females were present in experimental logs. Southern pine beetles did not respond, however, to logs infested with any Ips species. Response by I. avulsus and I. grandicollis was enhanced when SPB and males of either of the Ips spp. were present. The response of I. avulsus to its own attractant was also enhanced by the presence of I. grandicollis. This phenomenon was previously reported by Hedden, Vité, and Mori (1976). I. calligraphus was inhibited by I. avulsus. Conversely, I. avulsus response was enhanced by the presence of I. calligraphus. Reciprocal inhibition occurred between SPB and I. grandicollis. The olfactory interactions during attack on new host material resulted in rapid colonization of trees and minimal competition between the species.

Pathogenic Organisms

The southern pine beetle is attacked by a variety of organisms that may kill the beetle outright or reduce its egg production and survival. Although occasional references to diseases of SPB may be found, serious attempts to identify these disease organisms and determine their roles in regulating beetle populations have received little attention in the past. Moore (1971) found that fungi and bacteria caused an average SPB mortality of 22 percent in North Carolina. Mortality varied with the stage of beetle development, season, location on trees, and species of host trees. Diseases were more common in spring and winter, and higher percentages of infected SPB were found in the midbole region of infected trees. In North Carolina, disease incidence was higher in Virginia pine than in loblolly or shortleaf pines.

The diseases of SPB have also been intensively studied in Mississippi and Alabama (Sikorowski, Pabst, and Tomson 1979). Average SPB mortality resulting from diseases over a 2-year period (1975-77) was about 22 percent. The organisms responsible for this mortality are listed in the Appendix at table 6. The

most common pathogens were a microsporidian, Unikaryon minutum, and another unidentified microsporidian. Together they accounted for 30 percent of all disease-related mortality. Other important pathogens included the funi Paecilomyces sp. And P. viridis, and two parasitic nematodes, Contortylenchus sp. and C. brevicomi. Infectivity tests in the laboratory showed that SPB larvae were most susceptible to the fungi Metarhizium anisophilae and P. viridis. The infection rate was 50 percent. Different pathogens were more prevalent at different times of the year (fig. 3-24). Fungi and bacteria were common during cool weather, while protozoans were prevalent during hot weather. Overall mortality was also highest during low-temperature periods (fig. 3-25). There was no apparent correlation of diseases with rainfall.

Figure 3-24 – Relative seasonal abundance of SPB pathogens in Mississippi and Alabama 1975-1977. (From Sikorowski et al. 1979).

Figure 3-25 – Incidence of SPB disease and yearly temperature. (From Sikorowski et al. 1979).

Entomophagous Fungi

Pabst and Sikorowski (1980) found that under laboratory conditions, three entomophagous fungi — Beauvaria bassiana, Metarhizium anisophilae, and Paecilomyces viridis — were pathogenic to SPB larvae. B. bassiana was most virulent.

Nematodes

Nematodes are common associates of the southern pine beetle (Joye and Perry 1976). Massey (1974) extensively reviewed the biology and taxonomy of nematode parasites and associates of bark beetles in the United States.

Recent studies by MacGuidwin (1979) showed that SPB females infected with the nematode Contortylenchus brevicomi produced fewer eggs and constructed shorter galleries than healthy females during the 3-week period after attack. No differences were evident during the first week. Parasitism of either male or female SPB by C. brevicomi did not affect survival of progeny, even though number of eggs was reduced.

SPB emerging from the lower and middle portions of tree boles have a higher incidence of endoparasitism by C. brevicomi than those emerging from the upper part of the tree (Kinn and Stephen 1980). However, these investigators found no differences in infection among attacking beetles flying at different heights as they arrived at the trees. Females emerging from trees were more heavily infected by C. brevicomi than males, but more males were infected among the beetles flying to new host trees. These findings may be due to more pronounced effects of the endoparasitism on the females, especially reduced flight capabilities. The number of SPB infected with C. brevicomi decreased through the summer, perhaps due to predation on the free-living forms of the nematode by the phoretic mites (Kinn 1980).

MacGuidwin (1979) also reported that a recently described microsporidian parasite, Unikaryon minutum (Knell and Allen 1978), was present in 65 percent of the beetles examined. However, microsporidian infection in female SPB — either alone or in combination with the nematode — did not affect egg production or gallery length during the 3-week period after attack.

Sampling SPB Pathogens

Atkinson and Wilkinson (1979) developed a frontalure-baited trap to secure large numbers of SPB for pathogen studies. It permits SPB to enter but excludes the clerid predator Thanasimus dubius. Though the trap caught only male SPB in Florida studies, results from laboratory investigations showed that the incidence of nematode and microsporidian infection was the same for male and female beetles. The incidence of the microsporidian U. minutum was similar for beetles caught in traps and reared from bolts infested with field-collected beetles. But trapped SPB had significantly fewer C. brevicomi nematodes than beetles reared from logs. This fact suggests that infested beetles may have reduced ability to fly, or to respond to baited traps.

Symbiotic Organisms

Among SPB associates, there are several organisms that benefit the beetle and also receive some benefits in return. These symbiotic organisms, primarily fungi and bacteria, may alter the phloem (inner bark) of pines under SPB attack, making nutrients more readily available to the beetles. Other symbiotic organisms may be involved in the production or enhancement of aggregating pheromones (Brand et al. 1976 and 1977).

Several bark beetles, including the SPB, have specialized body structures — mycangia — in which symbiotic organisms, mainly fungi, are carried. During SPB attack the fungi are introduced into the tree. Barras and Perry (1975) published an annotated bibliography on symbiotic organisms associated with bark beetles.

Mycangial Fungi

Some work has been done to determine the role of associated microorganisms in SPB development. Barras and Bridges (1976 unpublished) found that in the laboratory, SPB without mycangial fungi were more successful in initiating attacks in bolts, but their egg galleries averaged only a little over half as long as galleries cut by beetles with mycangial fungi (table 3-2). The difference in production of progeny was even more striking. Beetles with fungi produced 36 progeny per gallery and those without fungi, only 2. The same pattern continued through a second generation, suggesting that populations of SPB without mycangial fungi cannot survive for long.

Table 3—2. – Progeny (F₁) produced by southern pine beetle adults with and without mycangial fungi. (From Barras and Bridges 1976 unpublished.)

Phloem lipids were analyzed to help explain why SPB brood development was inhibited in the absence of mycangial fungi. Results showed that lipids in phloem lacking mycangial fungi decreased over time, while lipids increased in phloem colonized by the fungi.

The blue-stain fungus Ceratocystis minor (fig. 3-26), which is always associated with the SPB, was included in inoculations along with two mycangial fungi. C. minor is not always carried in the mycangium of SPB but can be carried on the outer surface of the body (Barras and Perry 1975). Inner bark colonized with the blue-stain fungus had the highest amounts of total lipids. But earlier findings have shown that SPB broods fail to develop in phloem infected with the fungus (Barras 1970, Franklin 1970b). Therefore, at this time the exact relationship between C. minor and the SPB appears contradictory if lipids are critical to the development and survival of SPB broods. Brown and Michael (1978 unpublished) suggested that beetle attacks favor successful invasion of the wood by the blue-stain fungus. Moist inner bark/outer wood conditions associated with newly

Figure 3-26 – Cross section of a tree attacked by SPB which shows extensive staining by Ceratocystis minor. Photo by C.W. Berisford.

excavated egg galleries probably allow the fungus to become well established before invading the wood. Brown and Michael concluded that blue-stain fungi are the primary cause of tree death since water stress results from the rapid drying of infected xylem associated with blockage of the water-conducting tracheids by fungal hyphae.

Natural Enemies’ Impact

Sufficient information has been accumulated that we can begin to evaluate the impact of a complex of natural enemies on the southern pine beetle.

SPB Brood Mortality Mortality of SPB broods caused by parasitoids and predators was determined by excluding them from SPB-infested trees during specific periods of SPB brood development (Linit and Stephen 1980). More than half of the total numbers of these natural enemies, mostly predators, arrived during the first week of SPB development. Since predators were thought to consume more than one host, highest SPB mortality probably occurred due to their activities. Total mortality caused by parasitoids and predators during SPB brood development was estimated to be about 15 percent. Obviously, studies on SPB population dynamics should consider the role and impact of parasitoids and predators. Stephen (1980) has developed SPB population dynamics models that allow testing of the role of natural enemies in the regulation of SPB populations. These models make it possible to simulate the impact of natural enemies on SPB population growth as affected by factors such as host tree species and season of the year. Figure 3-27A and B shows a simulation of SPB population growth in loblolly and shortleaf pine stands. The growth of SPB populations in the absence of natural enemies is rapid with either tree host but substantially faster in shortleaf pine.

Figure 3-27 – The effect of SPB natural enemies on loblolly (A) and shortleaf (B) pine mortality.

Impact on SPB Spot Growth Simulations of SPB spot growth, starting at different times of the year, show that natural enemies are important in regulating SPB spot growth in early summer (June) (fig. 3-28). Natural enemies appear to be less significant in late summer and early fall, when spot trend is similar with or without natural enemies. Contributions of ESPBRAP Research Program-supported studies have substantially increased our understanding of southern pine beetle associates. We can, for the first time, easily identify many associates using new keys and identification guides, quantify the impacts of some natural enemies, and determine how some associates work together to regulate SPB populations.

Figure 3-28 – The effect of season and natural enemies on predicted tree mortality through time.

Research in ESPBRAP has provided a cornerstone for further investigations into the complex interactions among the southern pine beetle and its associates. Future studies will ultimately generate the data required for development and implementation of SPB management plans that recognize and/or augment existing control by natural enemies.

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