Oviposition biology of Acanthocinus nodosus was examined on southern pine beetle (SPB), Dendroctonus frontalis, infested loblolly pine trees in Alabama, U.S.A. Components of oviposition biology, including oviposition pit description, colonization period, average number of eggs laid per oviposition pit, use of bark beetle entrance or ventilation holes as oviposition sites, and pit density were described. Acanthocinus nodosus oviposition pits were easily differentiated from Monochamus titillator, another cerambycid species that also inhabits SPB-killed trees. Colonization of trees by A. nodosus began within 2 days of initial SPB attack and lasted for 8 to 14 days. Females laid an average of 3.33 (SE ± 0.48) eggs per oviposition pit and 99% of the pits occurred on SPB entrance and ventilation holes. All pits were on the lower bole between 18 and 163 cm above the ground. Oviposition pit density ranged from 0.22 to 0.45 pits per cm2 of bark surface. Potential interactions with other phloem inhabiting species were noted.
Acanthocinus nodosus (F.), (Coleoptera: Cerambycidae) is a frequent associate of the southern pine beetle (SPB), Dendroctonus frontalis Zimmermann (Coleoptera: Scolytidae) in southern U.S. forests (Overgaard 1968; Moser et al. 1971; Dixon & Payne 1979). By attacking and killing living pine trees, SPB provides extensive phloem resources that can be utilized for reproduction by A. nodosus. Upon arrival at host trees, adult A. nodosus chew pits in the bark or enlarge bark beetle ventilation holes for use as oviposition sites (Beal 1952; USDA 1985). While mining in the phloem, A. nodosus larvae often compete with and/or destroy bark beetle brood (Beal 1952). Acanthocinus nodosus is usually found in the thick-barked lower portion of the tree bole (Savely 1939) and is reported to complete one generation per year (USDA 1985). Acanthocinus nodosus is found throughout the eastern United States in dead and dying pines (Yanega 1996).
Little research has been conducted on A. nodosus, however, Schroeder (1997) investigated the reproductive biology of A. aedilis (L.) on pine bolts in a Swedish forest. He found that 55% of A. aedilis oviposition on cut bolts occurred in bark beetle holes and reported a mean egg density of 3.7 eggs per pit.
The objectives of this study were to describe the oviposition pit of A. nodosus and aspects of its oviposition biology including egg density, area of infestation on tree boles, duration of oviposition, and some interactions with SPB.
Materials and Methods
Research was conducted between July 28 and August 16, 1998, in a mixed hardwood-pine forest on the Oakmulgee Ranger District of the Talladega National Forest, Alabama. Several species of pine were present including loblolly, Pinus taeda (L.), longleaf, Pinus palustris (Mill.), and shortleaf, Pinus echinata (Mill.). Three loblolly pines, trees A, B, and C, were used to investigate A. nodosus oviposition biology. Additional egg samples were removed from two P. taeda in the same SPB infestation.
Oviposition Pit Description
Oviposition of three female A. nodosus was observed. After oviposition was completed, pits were removed with a 2.54 cm arch punch and egg placement and egg characteristics were noted. These oviposition pits were compared to known Monochamus titillator (Fab.) pits to establish differences between the two species.
Trees were examined for evidence of oviposition pit construction over a 20-day period. After detecting a new SPB attack, trees were checked to determine presence of existing A. nodosus ovipositional pits. If no pits were detected, sampling commenced. The first day of SPB attack was the beginning of our first sample interval. Every other day (one sample interval) sample trees were checked for new oviposition pits. Pits were either marked with a permanent felt tip pen, or removed to determine egg densities. Trees were checked until no new pits were located for two successive sample intervals. Previous observations of A. nodosus oviposition indicate that once oviposition ceased for more than 3 days, trees were not further colonized.
Egg Densities and SPB Interactions
Egg density was determined by removing bark and phloem immediately surrounding an oviposition pit. A 2.54 cm arch punch was hammered through the bark and phloem, stopping at sapwood, and pits were removed. Bark samples (n = 97) were then dissected by peeling the phloem back from the bark and locating the eggs. Total number of eggs was recorded for each pit. Each sample was then examined to determine if a SPB ventilation or entrance hole had been used for oviposition by A. nodosus. If the ventilation or entrance hole was the only hole present in the pit and ended in an SPB gallery, then it was concluded that A. nodosus was using an SPB hole for an oviposition site.
Acanthocinus nodosus oviposition pits are elliptical to round with steeper walls than M. titillator and contain a noticeably round hole at the bottom of the pit (Fig. 1). Eggs of A. nodosus were oviposited as a group at one margin of the pit, apparently chosen at random, as if the ovipositor had been inserted once and all eggs deposited. Eggs were found directly in SPB galleries as well as in the phloem surrounding the SPB hole.
Colonization of host trees by A. nodosus ranged from 8 to 14 days after initial SPB attack, with an average of 11.3 (SE ± 1.8). On average, 80% of oviposition pits on sample trees occurred during the first five sampling intervals following initial SPB attack. Average number of A. nodosus pits on host trees was 41.3 (SE ± 10.6) and ranged from 27 to 62 (Table 1). Average pit number per 100 cm2 of bark surface was 0.30 (SE ± 0.08).
Egg numbers per oviposition pit varied considerably. Mean number of eggs was 3.33 (SE ± 0.48), with a range of 0 to 33 (Fig. 2). Among 97 pits removed for sampling, over 35% contained 0 eggs, 11% contained 3 eggs, 10% contained 1 egg, and 9% contained 2 eggs. Almost all (96 of 97) A. nodosus oviposition pits were found at the site of SPB holes. The one pit that did not use a SPB hole was located within a M. titillator oviposition pit.
Infested bole length varied slightly between sample trees (Table 1). Average infested bole length was 135.3 cm (SE ± 4.8), with tree C having the longest infested bole (145 cm) and tree B the shortest (130 cm). On average, infestation ranged from 23 cm (SE ± 2.9) to 158.3 cm (SE ± 2.6) from the base of the tree. Tree B had the largest area of infestation (1.56 m2), followed by tree A (1.39 m2) and tree C (1.15 m2). For tree A, the greatest number (19%) of pits occurred between 100-120 cm, with 40% occurring between 100-160 cm (Fig. 3A). On tree B, 68% of oviposition pits occurred at heights above 80 cm, with 42% of the total pits concentrated in the 100-160 cm range (Fig. 3B). In contrast to the other sample trees, 63% of the oviposition pits on tree C were located below 100 cm (Fig. 3C). The highest density of pits on tree C occurred between 120-140 cm and 20-40 cm from the base of the tree.
Arrival of SPB associates, especially parasitoids and predators, has been investigated by several authors (Camors & Payne 1973; Dix & Franklin 1978; Dixon & Payne 1979). Unfortunately, fundamental knowledge concerning the basic biology of many associates, especially those that do not assume a direct beneficial role (i.e., parasitoids or predators) is lacking. This study explored the oviposition biology of A. nodosus, one of those poorly studied associated insect species.
We were able to easily differentiate the oviposition pits of A. nodosus from M. titillator. While M. titillator pits were elliptical with a small horizontal line at the bottom (Webb 1909), A. nodosus pits tended to be more rounded in shape and contained a distinct round hole at the bottom. In our study, the round hole at the bottom of the oviposition pit was most likely a result of the bark beetle entrance or ventilation hole. Another difference between A. nodosus and M. titillator oviposition pits was placement of the eggs. Acanthocinus nodosus eggs were placed as a single group, usually oriented in one direction. In comparison, M. titillator placed eggs in a distinct circular pattern around the center of its oviposition pits (Webb 1909). Eggs of A. nodosus were creamy-white in color compared to the yellowish color of M. titillator eggs.
Acanthocinus nodosus was common on the trees we sampled and had a close association with SPB. After successful initiation of SPB attack, A. nodosus arrived and began oviposition. Acanthocinus nodosus oviposition activity lasted from 8 to 14 days and occurred during the egg-oviposition stage of SPB activity. Interestingly, A. nodosus pits were found that had fresh resin flowing from them. It is reported that A. nodosus use bark beetle exit holes as oviposition sites (USDA 1985). The findings of our study, however, suggest that colonization occurs much sooner. We found A. nodosus ovipositing while SPB adults were making galleries and depositing eggs. Also, SPB entrance holes are typically filled with resin and frass and slant in relation to the bark surface, while ventilation holes are horizontal and filled with frass only (Stephen & Taha 1976). In our study, we did not differentiate between the types of bark beetle holes. However, it was noted on several occasions that fresh resin was in the SPB hole that was used as an oviposition site by A. nodosus. Due to the presence of SPB adults constructing galleries and resin in the egg samples, it can be assumed that A. nodosus were using SPB entrance holes and ventilation holes for oviposition sites. Discrepancies between A. nodosus usage of SPB hole types in our study and the previously recorded observations (USDA 1985) could be a factor of A. nodosus oviposition timing and SPB density. In our study, SPB mass attack density was low and rate of colonization appeared slow in our sample trees. For example, during the entire time A. nodosus were ovipositing, SPB were constructing galleries and depositing eggs.
There are a number of possible explanations to account for the wide range of egg numbers found in A. nodosus pits (0-33). First, the large number of zero egg counts could be a result of predation by egg predators (e.g., Histeridae). Because SPB ventilation or entrance holes are used for oviposition by A. nodosus, predators have easy access to eggs. On several occasions, histerid beetles were found in the presence of A. nodosus eggs. Because histerids are known SPB egg predators (Moser et al. 1971), it seems probable that they would consume A. nodosus eggs. Second, some cerambycid species need a period of maturation before oviposition commences (Linsley 1961). Walsh and Linit (1985) found that some M. carolinensis (Olivier) females chewed oviposition pits before reaching sexual maturity. At the other extreme, the large numbers of eggs found in some oviposition pits could be explained as multiple oviposition events by female A. nodosus. Because A. nodosus displays opportunistic behavior by using SPB holes, it also seems possible that females may oviposit in existing pits created by their own species. A similar habit has been noted in female Eucalyptus borers, Phoracantha semipunctata F., where up to 100 eggs have been found in the same area under bark or in crevices of eucalyptus trees (L. M. Hanks, pers. comm.). Mean number of A. nodosus eggs was similar to estimates in Sweden by Schroeder (1997) who found an average of 3.7 A. aedilis eggs per pit.
No oviposition pits of A. nodosus occurred above 163 cm and only one tree contained pits below 20 cm. There could be several reasons for A. nodosus not ovipositing in areas higher on the tree bole. First, by ovipositing lower on the tree bole, A. nodosus avoids competing with high densities of other phloem inhabiting species (e.g., SPB, M. titillator). In addition, A. nodosus is reported to pupate in the bark of host trees (USDA 1985) and may be confined to the lower bole where thick bark provides adequate pupation sites. The highest density of pits per 100 cm2 occurred on tree A, which had the second highest infested bole area. The lowest density of pits occurred on tree B, which had the greatest infested bole area. However, on trees B and C pits were marked and removed for egg counts, while not removed on tree A. Release of host volatiles, combined with bark removal from tree B and C could have negatively impacted oviposition behavior of A. nodosus. The negative effect on A. nodosus oviposition behavior on trees B and C seems surprising since the removal of bark surface would likely increase host volatiles, perhaps increasing the attractiveness of the tree to cerambycids. Although there has been no work conducted on the effect of host volatiles on A. nodosus, Schroeder and Weslien (1994a) found A. aedilis was attracted to alpha-pinene and 95% ethanol. It is likely that A. nodosus exhibits a similar behavioral response to host volatiles.
Our study provides basic observations of A. nodosus oviposition behavior and its interactions with SPB. Because both SPB and A. nodosus coexist in time and space with other bark beetle and cerambycid species, competition or intraguild predation among these species is probable. Schroeder and Weslien (1994b) investigated interactions between A. aedilis and Tomicus piniperda (L.) (Coleoptera: Scolytidae) and found that the cerambycid species significantly impacted bark beetle reproduction. Coulson et al. (1980) reported that M. titillator competed for food resources with SPB, reducing SPB brood by 14% when the two species occurred concurrently in the same tree. Further, Dodds et al. (2001) concluded that Monochamus carolinensis larvae were facultative intraguild predators of Ips calligraphus larvae (Germar). Because A. nodosus feeds in the same manner as M. titillator, but in the lower portion of the bole, competition or intraguild predation between SPB and A. nodosus is probable in that area of the tree. However, the overall impact of A. nodosus foraging on SPB survival may be less than that caused by M. titillator since the latter inhabits much more tree surface area than A. nodosus.
Bark beetle species that share the same tree are typically partitioned along the length of the bole to minimize competition (Paine et al. 1981; Flamm et al. 1987). Like the stratification that occurs in bark beetle species, a similar type of resource division might occur among cerambycid species arriving on SPB infested trees. For example, it is known that M. titillator primarily inhabits the middle and upper portions of infested tree boles (Hennier 1983), while A. nodosus occurs in the lower portion. Arhopalus rusticus obsoletus (Randall), another cerambycid species occurring in SPB infestations, is limited to the base and roots of dead and dying pines (Knull 1946; Linit et al. 1983). Xylotrechus sagittatus sagittatus (Germar) occurs concurrently with the above cerambycids, but may avoid direct competition for phloem resources by feeding primarily in the sapwood (Gardiner 1957).
Further studies into cerambycid biology, including A. nodosus, and other SPB associates are needed. A more developed knowledge of interspecific interactions of the phloem inhabiting guild associated with SPB may lead to a more complete understanding of bark beetle population dynamics.
We thank Joe Fowler and Bobby Lee, USFS Talladega National Forest, for assistance locating study sites. M. J. Linit (University of Missouri), L. M. Schroeder (Swedish University of Agricultural Sciences), and R. L. McIntosh (Saskatchewan Environment and Resource Management) all provided valuable comments on an early draft of this paper. Also, D. C. Steinkraus and M. V. Meisch (University of Arkansas) provided additional comments on this work. Funding for this research was provided by the University of Arkansas Agricultural Experiment Station and the Arkansas Forest Resources Center. Published with the approval of the Director, Arkansas Agricultural Experiment Station, manuscript #99007.