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ECOLOGY AND BEHAVIOR

Effect of Host Tree Seasonal Phenology on Substrate Suitability for the Pine Engraver (Coleoptera: Scolytidae): Implications for Population Dynamics and Enemy Free Space JACQUELINE S. REDMER, KIMBERLY F. WALLIN,

AND

KENNETH F. RAFFA1

Department of Entomology, 345 Russell Laboratories, 1630 Linden Drive, University of Wisconsin, Madison, WI 53706

J. Econ. Entomol. 94(4): 844Ð849 (2001)

ABSTRACT This study evaluated the effects of seasonal phenology on the substrate quality of susceptible hosts to the pine engraver, Ips pini (Say). We also determined the effects of the duration and method of storage on host quality for purposes of laboratory rearing. Live red pine trees were felled at various times during the season, and I. pini adults from a laboratory colony were established on the logs. Subsamples of logs were stored for various intervals, and then provided to beetles. Subsamples of stored logs were waxed at both ends to prevent water loss before being submitted to the same assays. Suitability of red pine phloem tissue in susceptible hosts declined for I. pini throughout the growing season. As the season progressed, the number of beetle progeny that emerged from colonized hosts dropped substantially. This decline was associated with simultaneous reductions in phloem moisture content. Reduction in host suitability may partially offset any advantage I. pini may gain from colonizing trees after the major predators have become less abundant. Bark beetle brood production decreased signiÞcantly with length of storage, regardless of the month of tree felling or the method of storing. Implications for bark beetle population dynamics and laboratory rearing systems are discussed. KEY WORDS Ips pini, Coleoptera, Scolytidae, Pinus resinosa, enemy free space, phloem quality

BARK BEETLES (COLEOPTERA: Scolytidae) are characterized by their ability to feed and develop within the subcortical tissue of host trees. Their ability to use this resource is facilitated by aggregation pheromones, symbiotic fungi, and chemosensory-based orientation to stressed hosts (Whitney 1982, Wood 1982, Raffa and Berryman 1987, Borden 1989). Most bark beetles are restricted to dead or dying trees, although some can colonize and kill healthy trees (Rudinsky 1962). Bark beetles are generally recognized as the most damaging insect group affecting North American forests (Wood 1982). As in many plant-herbivore interactions (Rhoades 1985, Langor et al. 1990, Price 1991, Ohgushi and Price 1992, Power 1992, Lundberg et al. 1994), the availability and quality of hosts greatly affect bark beetle reproductive success. Bark beetle survival is affected by both host susceptibility, which determines whether tree defenses can be overcome during colonization attempts, and host suitability, which affects the number of brood that can be produced in a susceptible tree (Raffa 1988a, 1988b; Reid and Robb 1999). Host susceptibility has been shown to vary among trees due to both environmental and genetic factors (Mitton and Sturgeon 1982, Raffa 1991a). Susceptibility also varies within individual trees as they age (Safranyik et al. 1975), and during the course of a single growing season (Lorio 1986, Lorio and Summers 1986, 1

To whom reprint requests should be addressed.

Raffa and Smalley 1988). Host suitability can also vary among trees. For example, the thickness, nutritional quality, and moisture of phloem can affect the production, longevity, fecundity, dispersal ability, and heterogeneity of emerging beetles (Amman 1972; Haack et al. 1984a, 1984b, 1987a, 1987b; Slansky and Haack 1986; Haack and Slansky 1987; Amman and Stock 1995; Reid and Robb, 1999). Little is known about how host suitability varies throughout a season, and how such changes affect the population dynamics of bark beetles. Although withinseason patterns of host susceptibility have been quantiÞed (Lorio 1986, Lorio and Summers 1986, Raffa and Smalley 1988), potential phenological effects on host suitability have received less attention. An improved understanding of the phenological changes that affect host suitability could improve our general understanding of bark beetle biology. For example, many bark beetle species have relatively brief periods during which they disperse and colonize new hosts, yet their cold hardiness and developmental plasticity suggest that they could colonize additional trees over a more extended period (Safranyik et al. 1975, Bentz et al. 1991, Reynolds and Holsten 1994, Bentz and Mullins 1999). The extent to which seasonal patterns in host suitability may limit voltinism and population growth is unknown. Moreover, some predators of bark beetles require longer periods to develop and undergo fewer generations per season than do their prey (Reeve et al. 1996). This raises the potential opportunity of pred-

0022-0493/01/0844Ð0849$02.00/0 䉷 2001 Entomological Society of America

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REDMER ET AL.: HOST PHENOLOGY AND SUBSTRATE SUITABILITY FOR I. pini

ator-free windows (Denno et al. 1990) for those beetles that undergo additional generations. An understanding of how host phenology affects substrate suitability is also useful for laboratory production of beetles, which can augment investigations on new control tactics or basic ecology. For example, bark beetles have recently received increased attention as models of insect behavioral genetics (Hager and Teale 1996), mating systems (Kirkendall et al. 1997), responses to climate and global change (Bentz 1995, Logan and Bentz 1999), predator-prey interactions (Raffa and Dahlsten 1995, Reeve 1997, Aukema et al. 2000, Erbilgin and Raffa 2000), and competition (Weslien 1992). The ability to maintain adequate and consistent laboratory colonies throughout the year is valuable to such studies. The pine engraver, Ips pini (Say), is distributed transcontinentally in North America. It has a relatively broad range of host trees, which includes almost all species of Pinus within its geographic range (Wood 1982). It is associated with stressed or killed trees, although it can cause signiÞcant economic damage under speciÞc conditions (Schenk and Benjamin 1969, Miller et al. 1989, Klepzig et al. 1991). Red pine, Pinus resinosa Ait., is the most common host of I. pini within the Great Lakes region. Males select suitable host substrate and emit aggregation pheromones that attract subsequent males and females. The males are polygamous, and mate with an average of three females each. After copulation, females oviposit along galleries. The larvae develop and feed for 3Ð 4 wk within phloem tissue and then pupate. Adults eclose approximately 1 wk later, emerge from host trees, and ßy in search of a new host. In Wisconsin, adult I. pini are active from mid-April until mid-October, with most ßight occurring from mid-May until late August. They have three to four generations per year (Schenk and Benjamin 1969, Raffa 1991b). The three objectives of this study were as follows: (1) characterize seasonal trends in the suitability of host tissue for I. pini brood production, (2) determine the relationship between storage interval and host quality, and (3) determine whether waxing the ends of stored logs to prevent moisture loss can reduce the effects of storage interval on brood production. Materials and Methods Our overall approach was to fell live trees at various times during the year, store them for varying intervals ranging from immediate use to several months, introduce constant numbers of parental beetles into these logs, and quantify the emergence of progeny. Subsamples of the stored logs were waxed at both ends. Phloem moisture was quantiÞed at the times of tree felling and beetle introduction. Field Sites and Treatment of Logs. All trees used in this experiment were 34-yr-old P. resinosa trees growing in a plantation in Sauk County, WI. This site is characterized by sandy soil and level terrain (Klepzig et al. 1991). These trees originated from local seed sources collected from the Wisconsin Department of

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Natural Resources. The diameter at 1.4 m height of test trees was restricted to a range of 15.8 Ð16.7 cm to ensure uniformity. Trees were felled at Þve different times beginning in July 1997. Trees were felled every 33 d from July to September, and then every 48 d from September 1997 to January 1998. At each felling date, three 0.3 m long log sections from the 2-m bottoms of two trees were provided immediately to beetles, and the remainder was discarded. Two-meter sections from the remaining felled trees were subjected to varying storage intervals and then sectioned and colonized for beetle assays. Storage treatments were assigned randomly among the felled trees. Log sections were stored at 10⬚C, 72% RH, and a photoperiod of 0:24 (L:D) h. In July, 12 trees were felled. One 2 m long section from each of two trees was provided to beetles within 72 h. Each of these 2-m sections was divided into three 0.3-m bolts, and the remainder was discarded. The 2-m bottoms of two trees each were stored for 30 Ð 45, 65Ð 80, 120 Ð135, and 175Ð190 d. The ends of two additional 2 m long sections were covered with 1-cm layers of wax using a paint brush, and stored for 175Ð 190 d. In August, 12 trees were felled. Two, 2 m long tree sections were used within 72 h, and two of each were stored for 30 Ð 45, 90 Ð105, and 150 Ð165 d. The ends of the remaining four sections were covered with 1-cm layers of wax: two were stored for 90 Ð105 and two were stored for 150 Ð165 d. Six trees were felled in September. Two, 2 m long sections were used within 72 h, and two each were stored for 65Ð 80 and 120 Ð135 d. In November, four trees were felled. Two, 2 m long sections were used within 72 h, and two were stored for 65Ð 80 d. In January, two trees were felled and used within 7 d. Colony Maintenance for Beetle Assays. Beetles were reared in 0.3-m log sections of P. resinosa using previously described methods (Raffa and Smalley 1995). Brießy, a 1.3-cm hole is drilled to expose the phloem, and one male is placed in a gelatin capsule, which is then secured over the hole with tape. At 72 h, three females are added to each male that entered the log. Rearing logs are placed in metal cans (50 cm high by 40 cm diameter) that are lined with screening on the inside. Two transparent jars are attached to the outside wall. Ips pini that ßy or climb toward the light source are collected in the jars. Rearing cans were held at 27⬚C and 70% RH. Beetle Assays. Beetle assays were conducted under the same conditions as colony rearing. Ten I. pini males from the colony were introduced into separate holes in each log. After 72 h, three females were added to each male that entered the log. If a male beetle died or did not enter the log, a new male was added with the females. All male and female beetles used in this assay had emerged within 72 h of introduction to the logs. All beetles, including beetles that did not reach the collection jars, were collected, counted and sorted according to gender. Phloem Moisture. Phloem samples were collected in the Þeld from trees immediately after felling, and

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55⬚C for 24 h and dry weights were recorded. Moisture content was calculated based on (wet weightÐ dry weight)/dry weight. Statistical Analysis. Statistical analyses were performed using analysis of variance (ANOVA) (SAS Institute 1996). One-way ANOVA was used to determine separately the effects of the date of tree felling and storage interval on brood production, and on phloem moisture content. Phloem moisture readings were pooled for each 0.3-m log section. Total brood emergence was regressed against length of storage within month of felling (SAS Institute 1996). Results Fig. 1. Brood production of I. pini in red pine logs in relation to month during which trees were felled. Ten males and 30 females were established in each log bolt. Means and standard errors are given. Beetles were applied at 1.29 males and 3.87 females per 100 cm2. Different letters indicate signiÞcant difference at P ⬍ 0.05 by Fisher protected least signiÞcant difference (LSD).

from stored logs just before beetle assays. A cork borer (10 mm diameter) was used to remove the phloem and bark from the tree. Phloem tissue was separated from outer bark. Three samples were taken at equal distances around the circumference of each 0.3 m long bolt. Samples collected in the Þeld were placed on ice in glass vials and returned to the laboratory where their wet weights were recorded. From July through September, six samples were collected from each 0.3-m log section into which beetles were introduced: after September, six samples were collected from one of the three 0.3-m sections taken from a particular tree. In addition, three samples were collected from each 2.0-m log section that was subjected to storage. Phloem samples were also collected at the times beetles were introduced. Phloem samples were dried at Table 1.

Mean brood production varied signiÞcantly with felling date (F ⫽ 5.88, df ⫽ 4, P ⬍ 0.003). The number of progeny decreased as the season progressed (Fig. 1). The decline was relatively constant from July to September. The total number of progeny from logs that became available in September was only 68% of the progeny from logs that were colonized in July. The progeny from trees felled in November and January was only 55% of the progeny from logs felled and colonized in July. Brood production decreased with the duration of storage, for all the felling dates (F ⫽ 4.556, df ⫽ 6, P ⫽ 0.004). Beetle emergence declined with storage time in a linear fashion, with a relatively consistent slope (Table 1). Whether logs were waxed or unwaxed during storage did not signiÞcantly inßuence the total number of progeny per male (F ⫽ 1.228, df ⫽ 1, P ⫽ 0.2705). The sex ratio of emerging beetles did not vary with the month of tree felling (F ⫽ 0.4, df ⫽ 4, P ⫽ 0.805), duration of storage (F ⫽ 1.05, df ⫽ 6, P ⫽ 0.39) or waxing treatment (F ⫽ 1.21, df ⫽ 1, P ⫽ 0.27). Overall sex ratio was 1:10 female:male, among the 1,435 beetles sampled.

Effect of storage time on production of adult I. pini progeny from P. resinosa log bolts

Date felled

Storage interval, da

Progeny/Bolt (mean ⫾ SE)

n

Y-Intercept

Slope

r2

24Ð30 July

0Ð7 30Ð45 65Ð80 120Ð135 175Ð190 0Ð7 30Ð45 90Ð105 150Ð165 0Ð7 65Ð80 120Ð135 0Ð7 65Ð80 0Ð7

146.0 ⫾ 5.07 102.3 ⫾ 4.79 104.0 ⫾ 5.12 119.8 ⫾ 8.78 83.6 ⫾ 7.79 127.0 ⫾ 8.34 87.3 ⫾ 5.08 98.9 ⫾ 5.03 72.1 ⫾ 6.91 99.2 ⫾ 4.40 101.7 ⫾ 4.06 69.0 ⫾ 0 78.7 ⫾ 3.31 63.3 ⫾ 4.05 82.8 ⫾ 9.94

6 6 6 6 11 6 6 12 8 6 6 1 6 6 6

133.3

⫺0.33

0.62

115.1

⫺0.26

0.63

107.1

⫺0.25

0.67

25Ð28 Aug

26 Sept 21 Nov 9 Jan

July: F ⫽ 3.25, df ⫽ 4, P ⫽ 0.01; Aug: F ⫽ 4.2, df ⫽ 3, P ⫽ 0.023; Sept: F ⫽ 4.5, df ⫽ 2, P ⫽ 0.042; Nov: F ⫽ 2.3, df ⫽ 1, P ⫽ 0.035 Data represent regression values from linear Þts for separate months of establishment Because the process of establishing beetles required several days, intervals are given. Means of each interval are as follows: 0 Ð7: July (0), Aug. (0), September (4), Nov. (3), January (5); 30 Ð 45: July (33.5), August (32); 65Ð 80: July (68.5), September (80), Nov. (71.5); 90 Ð105: August (99.2); 120 Ð135: July (126.5), September (122); 150 Ð165: August (159.5); 175Ð190: July (188.1). a

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Fig. 3. Conßicting roles of seasonal patterns on the relative effects of predators versus host quality on I. pini. Brood production data from Fig. 1 (JulyÐSeptember) and from B. Aukema and K.F.R. (unpublished data) (May); predator data from Raffa (1991b).

Fig. 2. (A) Seasonal changes in phloem moisture content (%) of red pine. Phloem samples were measured within 48 h of tree felling. (B) Effect of storage time on reduction in percentage moisture content of red pine phloem. Phloem moisture was calculated as percentage moisture lost on a per tree basis. Different letters indicate signiÞcant difference at P ⬍ 0.05 by Fisher protected LSD.

The percentage moisture contents of red pine phloem are shown in Fig. 2A. The moisture content of P. resinosa phloem decreased as the season progressed (F ⫽ 4.713, df ⫽ 4, P ⫽ 0.016). Phloem moisture content decreased with the length of storage (F ⫽ 4.936, df ⫽ 5, P ⫽ 0.022) (Fig. 2B). This decrease occurred regardless of felling date, storage or waxing. The total number of progeny was related to phloem moisture at the time of introduction of the parental generation (r2 ⫽ 0.194, F ⫽ 11.482, df ⫽ 1, P ⫽ 0.0013). Discussion Brood production was very similar to the production of I. pini brood observed by Robins and Reid (1997) in Pinus contorta variety latifolia Engelmann logs. In their study, equivalent densities yielded approximately Þve offspring per female and 18 offspring per male, compared with our July brood production of 4.9 offspring per female and 14.6 offspring per male. These results demonstrate that the suitability, i.e., substrate quality, of susceptible trees to I. pini rapidly decreases with seasonal phenology. Thus, any advantages that beetles may gain by undergoing additional

generations, for example reduced tree defenses (Safranyik et al. 1975, Raffa and Berryman 1987) or avoidance of predators (Raffa 1991b), are at least partially offset by declining moisture and nutritional quality of the subcortical resource. One component of this trade-off is illustrated in Fig. 3. Most of the predators of I. pini in Wisconsin are active early in the season, and the abundance of predators per I. pini becomes very dilute later in the season (Raffa 1991b, Aukema et al. 2000). This raises the possibility that those I. pini that colonize trees later in the season could gain some “enemy free space” (Denno et al. 1990). However, the corresponding decline in host quality greatly reduces any Þtness advantage that could be gained by colonizing trees after July. Likewise, trees might become increasingly susceptible as a season progresses (Safranyik et al. 1975), but the suitability of these hosts declines (Fig. 1). This reinforces the view (Raffa 1988a, 1988b; Reid and Robb 1999) that when considering the role of host plants in the population dynamics of bark beetles, a distinction must be made between host susceptibility (e.g., resin ßow, allelochemical content, induced reactions) and host suitability (e.g., phloem thickness, tree diameter, phloem nutritional content, phloem moisture). Our results are consistent with the views that phloem moisture is an important factor in host suitability to bark beetles, and that the role of seasonal phenology in bark beetle reproduction may relate to changes in phloem moisture content (Fig. 2). However, the absolute moisture contents we observed are lower than we expected. We are unable to Þnd equivalent data upon which to base comparisons. Ito (1955) reported that the sapwood moisture of Pinus densiflora S. and Z. dropped by 20% from May to August, and Clark and Gibbs (1957) reported that sapwood moisture in Betula dropped by 39% from April to July. Haack et al. (1984b) reported the phloem moisture of

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Pinus elliotti Engelmann in Florida at 68% in AprilÐ June. We observed P. resinosa phloem in May to be 35Ð 40%, with correspondingly high brood production by I. pini, using similar methods (E. Erbilgin, University of Wisconsin and K.F.R., unpublished data). Drying of phloem tissue is typical as trees undergo prewinter hardening (Kozlowski et al. 1990). Other factors besides moisture content, such as nutritional quality, are likely involved in the seasonal decline in brood production. For example, the decline in host suitability continues during some intervals when phloem moisture content remains stable (Fig. 1). The seasonal decline in host suitability has implications for the production of bark beetles in laboratory colonies. The equations in Table 1 provide a basis by which researchers can quantify the relative beneÞts of felling trees at various times of the year, versus storing them for various intervals. It is also useful to know that waxing the ends of P. resinosa logs does not improve I. pini brood production, at least under the conditions used in this study, and that the sex ratio of emerging beetles is not inßuenced by seasonal phenology, storage interval, or storage method. Acknowledgments Nadir Erbilgin and Brian Aukema (University of Wisconsin-Madison) generously allowed the use of unpublished data. Kevin Zei, Jason Ludden, Sara LaFontaine, and Kelly Boland (University of Wisconsin-Madison) assisted with Þeld and laboratory work. The critical review of an anonymous reviewer is greatly appreciated. The Wisconsin Department of Natural Resources kindly provided study trees. This study was supported by National Science Foundation grants DEB 9408264 and DEB 9629776, U.S. Department of Agriculture USDA NRI AMD 96 04317, McIntire Stennis, and the University of Wisconsin-Madison College of Agricultural and Life Sciences. This study was conducted as part of an undergraduate independent research project by J.S.R.

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