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tanoak stand development and response to tanoak mortality caused by Phytophthora ramorum
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Forest Ecology and Management 255 (2008) 2650–2658 www.elsevier.com/locate/foreco
Redwood/tanoak stand development and response to tanoak mortality caused by Phytophthora ramorum Kristen M. Waring *, Kevin L. O’Hara Department of Environmental Science, Policy & Management, University of California, Berkeley, CA 94720-3114, United States Received 23 July 2007; received in revised form 9 January 2008; accepted 10 January 2008
Abstract Coast redwood (Sequoia sempervirens) and tanoak (Lithocarpus densiflorus) form mixed-evergreen forests along the northern California coast. In the mid-1990s, an introduced pathogen (Phytophthora ramorum) began causing extensive mortality of tanoak in these forests. This research reconstructed stand development patterns occurring in stands with and without the pathogen, measured stand responses to tanoak mortality, and developed projections of future stand development and structure in the presence of P. ramorum. Redwood forms an upper canopy layer while tanoak forms a multicohort lower canopy, resulting in distinct vertical stratification patterns. Individual redwood tree response patterns to tanoak mortality included crown expansion, increased basal sprouting, and increased basal area growth. Future stand structures will likely have greater proportions of redwood relative to tanoak. # 2008 Elsevier B.V. All rights reserved. Keywords: Stand dynamics; Sudden oak death; Tree response; Invasive species
1. Introduction Introduced forest pests have become increasingly common in the past century and include such well-known examples as chestnut blight (caused by Cryphonectria parasitica (Murrill) Barr.) and Dutch elm disease (caused by Ophiostoma spp.). These pests frequently result in widespread tree decline and mortality and may have cascading ecological effects (Liebhold et al., 1995). Unusually high mortality of hardwood trees along the California coast has been attributed to a newly described pathogen, Phytophthora ramorum (S. Werres, A.W.A.M. de Cock) (Rizzo et al., 2002). P. ramorum spores are spread through infected soil and plant material in addition to movement by air, water, humans, and domestic pets. The disease caused by P. ramorum has been particularly devastating to tanoak (Lithocarpus densiflora (Hook&Arn.)Rehd.) trees and generally results in rapid death of most infected tanoak stems (Rizzo and Garbelotto, 2003). Shade-tolerant tanoak trees commonly form mixed species stands with coast redwood (Sequoia sempervirens (D. * Corresponding author at: School of Forestry, Northern Arizona University, PO Box 15018, Flagstaff, AZ 86011-5018, United States. Tel.: +1 928 523 4920; fax: +1 928 523 1080. E-mail address: [email protected] (K.M. Waring). 0378-1127/$ – see front matter # 2008 Elsevier B.V. All rights reserved. doi:10.1016/j.foreco.2008.01.025
Don.)Endl.) along the north-central California coast. These second growth stands also include coast Douglas-fir (Pseudotsuga menziesii (Mirb.) Franco var. menziesii), and minor components of California bay (Umbellaria californica (Hook&Arn.)Nutt.) and Pacific madrone (Arbutus menzeisii Pursh). Light severity fire probably occurred frequently in these forests prior to 1900, removing mostly small stems (Hunter, 1997; Brown and Baxter, 2003). Previous work in Douglas-fir/mixed hardwood dominated stands has shown gap phase development patterns in the absence of fire (Hunter and Parker, 1993; Hunter et al., 1999). Gaps form as the result of one or more disturbance events such as windthrow or slope failure and tanoak is a common colonizer of new gaps (Hunter et al., 1999). However, these studies did not include a detailed retrospective view of past height development or typical patterns of tree ring growth and response nor does similar information exist for stands composed primarily of redwood and tanoak. In redwood/tanoak stands, increased mortality of tanoak due to P. ramorum may result in increased growth rates in surviving trees of both species. The competition for resources and stand development patterns may be altered, including height growth patterns over time. For example, redwood may capture newly available resources on the site and leave few resources available for surviving or regenerating tanoak; one method of assessing these changes is through stand reconstruction (Oliver, 1982) to
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describe pre- and post-tanoak mortality height growth patterns. Height growth patterns provide a key descriptive process of competitive positions of tree crowns in light-limited environments and are therefore an important aspect of stand development patterns (Oliver and Larson, 1996). Increased light availability may result in a sprout response, as both redwood and tanoak are prolific sprouters capable of producing vegetative sprouts from the stem or base. These sprouts originate from dormant and adventitious buds following the stimulation from increased light or heat, or from injury to the tree. This sprouting ability makes redwood rare among conifers because of its ability to produce stump sprouts. A separate response is the formation of basal sprouts at the base of uncut trees. These basal sprouts form new stems and are a typical response to disturbance (Tappeiner et al., 1990; Olson et al., 1990). Several studies have detailed changes in stand structure and development following pest introductions in other forests. Growing evidence suggests that major factors directing future stand development will be shade tolerance and a species’ presence on the site (Fajvan and Wood, 1996; Orwig and Foster, 1998; Waring and O’Hara, 2005). Changes in species composition, changes in age structure, and loss of the affected species are some commonly documented effects of introduced pests (Korstian and Stickel, 1927; Fajvan and Wood, 1996; Abrams et al., 1997; Forrester et al., 2003). In a southern Appalachian forest, Lorimer (1980) found that during the period of high chestnut blight mortality (1928–1938), understory tree release from suppression was higher than expected and certain species were more likely to benefit than others. In forest ecosystems vulnerable to introduced pests, management activities are likely to include preventative, mitigative or restorative objectives (Waring and O’Hara, 2005). An understanding of stand development patterns can serve as a guide to managers in predicting future stand development and response to treatments for any of these objectives. The present study documented effects of P. ramorum on mixed redwood/tanoak stand structures and projected potential future changes in these structures. We hypothesized that (1) tanoak density has been greatly reduced; (2) surviving tanoak have increased growth; (3) redwood has increased both sprouting and overall growth; and (4) future species composition will be dominated by redwood. Specific research objectives were to (1) confirm the comparability of the two research sites; (2) reconstruct patterns of stand development in these mixtures prior to and following P. ramorum invasion; (3) measure effects of P. ramorum-related mortality on tanoak and redwood tree growth and stem density; (4) measure the basal sprout response of redwood and tanoak to P. ramorum mortality; and (5) project changes in stand development following tanoak mortality.
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winter and spring followed by warm, dry summers. The two study sites used in this work are located approximately 190 km apart north-south, in the central zone of coast redwood forests (Noss, 2000). Three stands were selected within Jackson State Demonstration Forest (JDSF), Mendocino County, California (39.218N, 123.368W) to represent redwood/tanoak forests developing without P. ramorum infection. These stands originated from timber harvest about 80-years prior to sampling. Average annual temperature near the study stands is 12.6 8C, with an average of 1052 mm rainfall per year falling primarily during the wet winter months (WRCC, 2007). Soils underlying the study sites are primarily Vandamme loam, which are deep, well drained soils derived from sandstone (Rittiman and Thorson, 2002). Average site index of the JDSF study stands was 31 m (base 100 year). Four stands were selected within the Marin Municipal Water District (MMWD), Marin County, California (38.018N, 122.418W), which encompasses 38,074 ha set aside for management of water resources. Mortality of tanoak due to P. ramorum has been high within the MMWD since the mid1990s (Rizzo et al., 2002). Timber harvesting occurred approximately 80 years ago, with current stands characterized by an overstory conifer layer of primarily second-growth redwood and Douglas-fir with the occasional remnant oldgrowth redwood. Average annual temperature in the area is 13.7 8C with corresponding average annual precipitation of 1023 mm (WRCC, 2007). Soils in the area are formed from Franciscan Formation parent material, and are in the Dipsea soil series. The Dipsea series is characterized by deep, well-drained very gravelly loam (Kashiwagi, 1985). Average site index of the Marin Municipal Water District (MMWD) study stands was 33 m (base 100 year). Because of irregularities in ring formation, which can significantly affect accurately aging trees (Waring and O’Hara, 2006), site index numbers may not be reliable but provide an approximate comparison of site productivity between the two study sites. Study stands at both sites were selected based on approximate age (80 years) and species composition: redwood comprised at least 75% of the conifer component and tanoak comprised at least 75% of the broadleaved component. Stands were primarily even-aged based upon available stand history information, with initiation following early 20th Century timber harvesting. Three plots were located within a predefined 1 ha area within each stand. Each plot was subjectively located to include mature redwood and tanoak trees growing in close proximity and assumed to be in direct competition for available resources. These interactions were observed to be typical for the sampled stands. Although redwood and tanoak were the most abundant species, Douglas-fir, Pacific madrone, grand fir (Abies grandis (Dougl.) Lindl.), and California bay were also found in the study stands.
2. Materials and methods 2.2. Data collection and analysis 2.1. Study area The north-central California coast has a Mediterranean climate characterized by cool, wet conditions during fall,
Three circular fixed radius plots were installed in each stand at each site resulting in 9 plots at JDSF and 12 at MMWD. However, two MMWD plots were later excluded from analysis
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due to lack of tanoak mortality. Plots ranged in size from 0.01 to 0.05 ha, with each plot designed to include 8–12 overstory trees that were near-neighbors and presumed to be in direct competition with each other (or had recently been in direct competition in the case of dead tanoak). After locating the center point of each plot, the position of each tree greater than 1.37 m tall (breast height) within the plot radius was mapped, and tree species and diameter at breast height (DBH) were recorded. Redwood and tanoak basal sprout presence or absence was noted for each tree. Trees originating from common sprout clumps or clones were also noted, as were trees of seed origin. Between 5 and 10 representative trees/plot were selected for more intensive sampling; these trees are hereafter referred to as ‘sample trees’. Crown radii were measured at eight radii in cardinal directions around the circumference of all sample tree crowns using a clinometer to locate the drip line. Total sample tree height and height to the base of the live crown were measured. Main-canopy trees were assumed to be the ones most likely to respond quickly to tanoak mortality. A small number of trees greater than 100 cm DBH in the MMWD stands were removed from the analysis because they were remnant old-growth trees that were present on only one of the study sites. Relative height was then computed as the ratio of each tree’s height to the height of the tallest remaining tree measured at that site. Trees were placed into one of three categories with respect to canopy position: <0.25, 0.25–0.85, and >0.85 relative height. The analysis then focused upon only the main-canopy or central group that was the largest group of trees and comprised the primary canopy. The group of shortest trees comprised a total sample of only eleven trees primarily located in the suppressed subcanopy. The tallest trees also had a small sample size (n = 9) and included two old-growth trees in Marin that were not large enough to be excluded (e.g., <100 cm DBH). Non-parametric statistical analyses were performed where the assumptions of normality were not met within the sample data. Comparability of the two research sites was assessed using stocking (trees/ha and basal area), relative proportions of sprout-origin trees, site quality, and species composition. However, some differences were expected because of high levels of tanoak mortality in the MMWD. Species other than tanoak and redwood were combined into a single species group for assessment of stocking and species composition for the two study sites. Means between density for each species/species group were compared with t-tests. The two study sites were similar in pre-infection characteristics despite their geographic separation, therefore providing justification for comparison despite the distance between the sites. Both redwood and tanoak produce basal sprouts with the potential of forming tree stems. Comparative sprouting between study sites was assessed by evaluating the probability of a tree stem having a basal sprout present at the time of sampling. Sprout presence at the two research sites was compared using a Mann–Whitney non-parametric test for both tanoak and redwood. In each of the three stands within JDSF, two of the three plots were destructively sampled by felling each sample tree for stem
analysis and stand reconstruction (sensu Oliver, 1982). Stem analysis took place between May and October 2002. Sample trees on the third plot were not felled, but increment cores were removed at the base, breast height and 3 m from each tree for age and tree ring analysis. Immediately after tree felling, total tree length and length to the lowest live branch were recorded for each sample tree. Cross-sectional disks were removed from each tree at the base, breast height, and at variable locations along the tree bole. Distance between cross-sections was based upon merchantable log lengths for each species (5.0 m for redwood, 3.8 m for tanoak) for trees of merchantable size. Sections were removed every 1–3 m on non-merchantable trees. Sapwood area and 5-year radial growth were measured at two randomly located positions on each breast height crosssection shortly after felling. Cross-sections were sealed in large plastic bags for transport to the laboratory, where they were autoclaved. They were then planed and sanded with progressively finer sand paper until the rings were clearly visible. Individual redwood rings were not always present due to discontinuous and missing rings (Waring and O’Hara, 2006) so age was based on the maximum age of eight radii per crosssection. Due to constraints on tree felling in the MMWD, only nondestructive sampling procedures were implemented to reconstruct past stand development. Plot and sample tree selection was the same as at JDSF. All plots were installed in 2002. Increment cores were removed from each sample tree on the south and east sides within 0.3 m of the ground at the tree base on the uphill side of tree, at breast height, and at a height of 3 m. This limited sampling followed previous stand reconstruction protocols where trees were not felled (Oliver, 1978; O’Hara, 1995). Sapwood length was recorded in the field for each breast height and 3-m core. All cores were autoclaved to prevent spread of P. ramorum, glued to boards, and sanded with progressively finer sand paper until rings were clearly visible. To verify tanoak mortality due to P. ramorum, two dead tanoaks were selected on each plot in the MMWD for sampling. Wood samples were then removed from the base, breast height, and from any visible bleeding along the tree bole. The minimum number of samples per tree varied based on tree diameter and ranged from 2 to 8. Precautions were taken to avoid contamination between samples, which were then sealed and placed in cold storage for up to a week. The Forest Pathology Laboratory at UC Berkeley conducted PCR analysis on the samples, which confirmed the presence of P. ramorum DNA in dead tanoak at all MMWD stands. Cross-sections and cores were aged with the aid of a dissecting microscope or scanned into a computer and analyzed using the tree ring analysis software WinDendro (Regent Inst., 2004). All breast height samples were scanned to obtain precise ring width data. Only growth rings from 1997 to 2001 were used in subsequent growth ring width analysis. When multiple increment cores were available from a given height on the same tree, the cores were averaged prior to analysis. Redwood trees that were destructively sampled had up to eight individual radial measurements on a cross-section that were averaged for ring width analysis. Cross-dating at breast height was attempted
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in redwood but was not successful due to the growth ring anomalies (Brown and Baxter, 2003; Waring and O’Hara, 2006). However, basic height growth patterns should be relatively unaffected by this pattern due to the decrease in ring count variation higher along the tree bole (Waring and O’Hara, 2006). Reconstructed height growth patterns were then used as a basis for describing historical stand development patterns (Oliver, 1982). To assess the effects of P. ramorum on tree growth and crown characteristics, differences in cumulative 5-year basal area growth (1997–2001), crown surface area, and leaf area (redwood only) were used to assess post-infection change. Generally, changes in crown characteristics are expected to be a feature of a released tree that precede effects on bole increment (Oliver and Larson, 1996). Crown surface area (CSA) was calculated assuming a paraboloid shape for redwood and an ellipsoid shape for tanoak. The following equations were used: Paraboloid (modified from Zarnoch et al., 2004): CSArw
4pCL ¼ 3CW2
CW4 CW þ 4CL2 2
1:5
CW4 4CL2
1:5 (1)
where CSArw is redwood crown surface area (m2), CL is live crown length (m), and CW is mean crown width (m) at the widest point of the crown. Ellipsoid: 2 1 þ ðHCL=CWÞ arcsinðEÞ CSAto ¼ 2pCW (2) E
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Table 1 Mean summary characteristics for sampled redwood/tanoak plots at Jackson Demonstration State Forest (JDSF) and Marin Municipal Water District (MMWD) Species
Measure
JDSF
MMWD
Redwood
Trees/ha BA (m2/ha)
898 (195) 104.6 (18.1)
883 (182) 106.1 (19.0)
Tanoak
Trees/ha BA (m2/ha)
884 (101) 53.9 (5.3)
995 (210) 15.8 (3.0)
0.653 <0.001
Dead tanoak
Trees/ha BA (m2/ha)
100 (33) 2.3 (0.8)
605 (74) 16.9 (2.7)
<0.001 <0.001
Other species
Trees/ha BA (m2/ha)
38 (23) 9.6 (8.6)
75 (44) 8.9 (4.2)
0.481 0.943
n
9
p-Value 0.955 0.957
10
Standard errors are given in parentheses. Other species included California bay, Pacific madrone and Douglas-fir.
trees/ha and dead basal area were significantly different between study areas indicating the P. ramorum mortality greatly exceeded background mortality levels (Table 1). Stand reconstruction revealed a stratification of redwood over tanoak in these stands. Following stand initiation after post-1900 timber harvesting, redwood trees began growing
where CSAto is tanoak crown surface area (m2), HCL is one half pffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi 2 CW2 live crown length (m), CW is as above and E ¼ HCL . HCL Redwood leaf area was predicted using breast height sapwood area (Stancioiu and O’Hara, 2005). Analysis of covariance was used to examine the relationship between site and tree characteristics in instances where there were no significant interactions between study site and the variable of interest. Such interactions were tested for using between subjects effects tests. All statistics were performed using SPSS statistical software (SPSS, 2002). 3. Results Prior to the arrival of P. ramorum, redwood stocking was nearly identical and tanoak stocking was apparently similar (Table 1). Mean redwood basal area and trees/ha were nearly identical between study sites (Table 1). There were greater trees/ha in MMWD for the ‘‘other species’’ but no significant differences. Pre-infection tanoak basal area was greater at JDSF but trees/ha were greater at MMWD. Tanoak comprised about 32% of stand basal area at JDSF but was only 12% at MMWD after infection. Inclusion of recent mortality in tanoak basal area increased the tanoak total to approximately 22%. Additional mortality due to P. ramorum that was too decayed to measure would have probably increased these basal area numbers at MMWD. Although post-infection live trees/ha was not significantly different, differences in basal area, and dead
Fig. 1. Height growth development occurring over 80 years of stand development in redwood/tanoak stands, Jackson Demonstration State Forest. Similar patterns occurred on all study stands. Each line represents the development of a single tree.
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Fig. 2. Examples of height development in redwood/tanoak forest stands on the Marin Municipal Water District. (a) Tanoak mortality present but some live tanoak remain in 2002 and (b) tanoak mortality extensive and no live tanoak remain within plot. Note differing axis scales that highlight inter-tree relationships. Each line represents the development of a single tree.
faster in height than tanoak while also showing within-species differentiation (Figs. 1 and 2). All canopy trees were likely sprout origin given their rapid initial height growth rates and clumpy spatial patterns (Fig. 3). For redwood, the parent stumps were generally still present. Height differentiation continued to occur through the next several decades. A few tanoak entered the stand, likely as young sprouts, after stand initiation, forming multiple strata within the tanoak component. By 2002, the stands had stratified into an upper stratum dominated by redwood, a midstratum dominated by tanoak, and an understory of tanoak with some redwood and other species. A few residual trees (over 80 cm DBH, not harvested in the early 1900s) in Marin County formed an even higher stratum of sparsely distributed emergent trees. Pacific madrone followed similar height growth patterns as tanoak (data not shown). At JDSF 84% of redwood and 82% of tanoak were of clonal origin whereas at MMWD the clonal origin trees were 89% for redwood and 76% for tanoak. Recent seedling regeneration of all species was generally absent from all study sites. The probability of redwood trees producing basal sprouts was higher ( p = 0.038) at the MMWD study sites than at JDSF (Table 2). For tanoak, the probability of sprout production was greater at JDSF, however, this difference was not significant ( p = 0.062). Among the main-canopy redwood sample trees, basal area growth and leaf area were significantly greater in MMWD, while live crown ratio was significantly greater in JDSF
Fig. 3. Example spatial distribution of live and dead stems, including stumps, on second-growth redwood/tanoak plots of California. (a) Jackson Demonstration State Forest, no sudden oak death and (b) Marin Municipal Water District, mortality of tanoak due to sudden oak death. Each plot has a radius of 8 m.
(Table 3). Total tree height and DBH were not significantly different between study sites for redwood (Table 3). Redwood basal area growth crown surface area, and leaf area all tended to be larger for a given tree diameter on MMWD plots than on JDSF plots but analysis of covariance was only possible for leaf area, which was significant (Fig. 4, p < 0.001). Main-canopy tanoak sample trees showed different and often opposing patterns: total height and DBH were significantly greater at JDSF than MMWD, with no significant differences found between basal area growth, crown surface area or live crown Table 2 Percent probability of basal sprouts on redwood and tanoak stems for Jackson Demonstration State Forest (JDSF) and Marin Municipal Water District (MMWD) Species
JDSF
MMWD
p-value
Redwood Probability of trees with sprouts (%) n
74.4 (3.5) 156
85.1 (3.5) 107
0.038
Tanoak Probability of trees with sprouts (%) n
61.2 (4.4) 121
49.7 (4.2) 143
0.062
Probabilities were compared with non-parametric Mann–Whitney tests. Standard errors are given in parentheses.
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Table 3 Summary characteristics of main-canopy sample trees by species and site Species
JDSF
MMWD
Redwood DBH Height Live crown ratio Crown surface area Basal area growth Leaf area n
41.6 25.7 0.6 40.3 39.0 128.5 20
(3.7) (1.8) (0.03) (5.5) (7.7) (21.2)
43.5 25.2 0.4 97.1 91.5 179.3 22
Tanoak DBH Height Live crown ratio Crown surface area Basal area growth n
34.4 26.2 0.5 116.1 41.3 30
(2.4) (0.8) (0.04) (19.5) (6.9)
25 (1.5) 21.0 (1.0) 0.6 (0.03) 112.5 (13.2) 28.1 (3.9) 20
(4.3) (1.7) (0.03) (15.0) (14.4) (29.3)
p-value 0.71 0.822 0.001 0.001 0.003 0.176
0.001 <0.0001 0.123 0.877 0.548
JDSF: Jackson Demonstration State Forest and MMWD: Marin Municipal Water District. Comparisons were made using t-tests. Standard errors are given in parentheses.
ratio (Table 3). Tanoak crown surface area at MMWD was significantly greater at a given diameter that crown surface area at JDSF (ANCOVA, Fig. 5a). Basal area growth tended to increase in surviving tanoak trees on infected sites following P. ramorum-caused mortality, however, these differences were not significant (data not shown, p > 0.100). Similar trends can be seen in basal area growth, with greater growth for a given diameter occurring in MMWD (Fig. 5b); however, analysis of covariance was not performed because of a significant interaction between study site and basal area growth. 4. Discussion Following the infection of P. ramorum, there has been a significant decline in tanoak basal area in these stands and a similar but not significant trend in number of tanoak stems. This decline affects tanoak trees of all sizes and age classes/cohorts. At time of sampling, or about 8 years following initial infection, tanoak basal area and trees/ha were reduced 40–50%. Because tanoak was largely stump sprout origin with a very clumpy spatial pattern, this mortality is likely to leave large gaps and change the spatial patterns in these stands. In the absence of P. ramorum, stand development pattern in these second-growth sprout-origin forests was the formation of a redwood stratum over multiple lower strata of tanoak. Within 10 years of the stand replacement disturbance that initiated these stands, the redwood had outgrown the tanoak, relegating the tanoak to a lower canopy stratum that was maintained throughout the first 80 years of stand development. This height growth advantage over tanoak will probably continue to exist for hundreds of years, given the longevity of redwood trees and the absence of disturbance or management. Because the typical spatial patterns of these stands are large clumps of sprout-origin tanoak or redwood, redwood and tanoak trees are limited to specific small patches within the stand. This feature often allows tanoak to receive some direct sunlight although its height position implies a subordinate canopy position. On less
Fig. 4. Redwood relationship between diameter at breast height and (a) crown surface area; (b) leaf area; and (c) 5-year basal area growth. JDSF: Jackson Demonstration State Forest and MMWD: Marin Municipal Water District.
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Fig. 5. Tanoak relationship between diameter at breast height and (a) crown surface area and (b) 5-year basal area growth. JDSF: Jackson Demonstration State Forest and MMWD: Marin Municipal Water District.
productive sites, the redwood may not outgrow the tanoak in height as quickly. Following the development of the lower tanoak stratum, tanoak continues to enter the stands as seedlings or clonal sprouts. These tanoaks ultimately form a multiaged and multistrata component. Tappeiner and McDonald (1984) reported that both large and small tanoak growing in Douglas-fir dominated stands grew slowly and did not need disturbance to sprout. Tanoak mortality caused by P. ramorum infection has triggered a sprout response in the redwood trees, creating a new cohort that is beginning to reach breast height and can be seen in this data set primarily as a higher percentage of trees with basal sprouts. This trend will probably become more pronounced with continued tanoak mortality. However, the long-term growth of these sprouts is limited by their proximity to existing redwood sprout clumps that include overstory trees.
Increased mortality of tanoak in these stands is likely to benefit three categories of redwood trees: those upper-stratum trees beginning to slow in height growth, redwoods occupying the middle stratum, and possibly the regenerating cohort of redwood sprouts. Upper-stratum trees are likely to expand crowns into areas vacated by tanoak and experience increased or sustained diameter growth rates. Middle stratum and understory sprouts will only benefit if their spatial position allows them adequate resources to compete within their sprout clump competitors. Few trees other than redwood and tanoak were sampled, however, the few Douglas-fir sampled tended to follow a ‘‘through-growth’’ pattern where they grew rapidly in height growth and were able to grow through an overstory canopy (i.e. Fig. 2b). This pattern is similar to that observed in other research in coastal mixed-evergreen forests (Hunter and Barbour, 2001) and other western North American conifer forests (Larson, 1986). Redwood trees growing on infected sites near clumps of tanoak mortality had greater basal area growth, crown surface area and leaf area than trees on uninfected sites; these same parameters (basal area growth, crown surface area, leaf area) were also greater when compared at a given diameter. Crown surface area is a function of the assumed shape and crown width/length. Redwood trees on infected sites also had significantly greater crown width (data not shown) and this is likely the parameter driving the greater crown surface area. It is possible that these trees are beginning to respond to increased resources available due to high levels of tanoak mortality. However, tanoak mortality alone probably does not adequately explain the increased growth and crown size of these trees. The distinct spatial heterogeneity and clumping patterns may affect patterns of tree response, as redwood tends to be further removed from the dead tanoak than surviving tanoak. Surviving tanoak trees also showed a significantly greater crown surface area at a given diameter in MMWD. Although tanoak basal area growth showed a similar trend, the results may be confounded by the significant differences in tree size found between the two sites. These differences are likely driven by the high levels of mortality at MMWD. Surviving tanoaks were competing directly with dead tanoak for resources; the death of neighboring tanoak increases resources available for those remaining alive. Location of individual trees in relation to mortality may play a role in response pattern and rates. DiGregorio et al. (1999) found that subcanopy sugar maple increased in radial growth following decline of beech from beech bark disease, whereas canopy sugar maple did not show a similar response (although trees in and near gaps all increased radial growth). A similar situation could be presenting itself in redwood/tanoak forests. Additionally, Prestemon (1966) noted a trend of decreasing radial growth in tanoak with increasing site index in northern California (Mendocino and Humboldt counties), potentially due to increased conifer competitiveness on more productive sites. While site index was very similar between sites (31 m JDSF vs 33 m MMWD), slightly higher productivity at MMWD may affect tanoak radial growth enough to mask effects of P. ramorum. Site index may not be an accurate method of assessing site productivity on these sites due
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Fig. 6. Hypothetical height development of redwood trees following tanoak mortality, assumed to occur in 2002.
to the growth-ring anomalies found in redwood (Waring and O’Hara, 2006). Fig. 6 shows hypothetical height development patterns for redwood over the next 20 years. Most tanoaks are presumed dead in 2001; upper-stratum redwood trees would increase height growth but maintain current canopy positions relative to each other. The forest in 2020 would presumably be composed of three canopy layers: the upper canopy redwood, a middle stratum of released redwood, and suppressed young redwood sprouts and any surviving tanoak in the lowest canopy layer. In the future, redwood will show more dominance on P. ramorum infected sites as tanoak mortality continues. Tanoak may have become more prevalent over the past century due to preferential cutting of redwood, even-aged management, and fire exclusion. In particular, fire exclusion allows tanoak to dominate over other species in the understory because of its ability to regenerate in shaded conditions (Hunter, 1997; Hunter et al., 1999). Several possible scenarios may result from the current tanoak decline that is dependent on the size of the resultant canopy gaps. One scenario of small or discreet gaps will lead to existing redwood trees expanding into the available growing space, leaving few opportunities for a new cohort of any species. A second scenario may arise if large groups of tanoak die and leave a large gap. Light resources may be enough to promote establishment of a new cohort of redwoods from either seedling or sprout origin resulting in a multiaged stand. Tanoak resistant to P. ramorum, other hardwood species, or exotic species are other possible components of a new cohort. Finally, a third scenario may occur where large gaps are formed but redwoods are unable to expand into these gaps because they reproduce primarily through sprout production. In these situations other tree species or brush species may have an initial advantage that results in a mixed species stand with a highly variable structure. In stands like those sampled in this study, the first scenario of increased redwood dominance is most likely. Managers have few options in these forests to avert the dramatic change in stand structure and species composition.
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Landowners managing for commercial harvest of redwood may experience an increase in the speed at which these forests revert to single species, multicohort redwood forests. These structures may have been more abundant in the past due to the occurrence of fire and less management activity. Since tanoak is not a commercial timber species, many managers expend resources attempting to control its growth early in stand development; in such cases, P. ramorum caused mortality may have welcome effects. Additionally, thinning along uninfected boundaries may be analogous to the ‘‘Slow the Spread’’ campaign undertaken to slow the spread of gypsy moth (Lymantria dispar L.) in the eastern United States (Tobin et al., 2004). Although thinning these stands for P. ramorum management is untested and may or may not slow the spread of the pathogen, it would almost certainly alleviate fuel accumulation if harvested trees are removed from the stands. Old-growth forests are less likely to show a similar response to tanoak canopy gaps due to both their large size and old age. In areas that have reverted to tanoak following extensive harvest, planting may be necessary to regenerate the site following tanoak mortality to fill gaps with redwood. Finally, tanoak mortality may have cascading impacts throughout the ecosystem because it is the only mast producing species in the mixed-evergreen forest type. Effects range from impacts on wildlife (Apigian and Allen-Diaz, 2006; Apigian et al., 2006; Monahan and Koenig, 2006) to loss of biodiversity and have not been fully investigated. 5. Conclusions The infection of redwood/tanoak stands by P. ramorum has major effects on current stand structure and subsequent stand growth. In sampled stands, tanoak mortality was approaching 50% with mortality expected to continue. The effects of this mortality are greater basal sprouting of redwood trees and crown expansion of surviving tanoaks. Other expected outcomes are greater growth rates in both the redwood component and other minor species that are not affected by P. ramorum. The result will be a tendency of these stands to form multiaged structures with a higher proportion of redwood. The tanoak component in these stand structures will generally be lacking. Because of the aggregated spatial patterns of these sprout-origin stands, larger canopy gaps following tanoak mortality may remain unfilled by redwood. Acknowledgements This research was supported, in part, by the USDA Forest Service, Pacific Southwest Research Station, through Research Agreement Number 01-JV-11272164-165. Cooperation and assistance from Fay Yee, William Baxter, Robert Horvat, the Jackson Demonstration State Forest and the Marin Municipal Water District is greatly appreciated. The authors thank Paul Lilly, Kyla Sabo and Bruce Hammock and the UC Berkeley Forest Pathology Laboratory for field and laboratory assistance.
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References Abrams, M.D., Orwig, D.A., Dockry, M.J., 1997. Dendroecology and successional status of two contrasting old-growth oak forests in the Blue Ridge Mountains, USA. Can. J. For. Res. 27, 994–1002. Apigian, K., Allen-Diaz, B., 2006. SOD-induced changes in foraging and nesting behavior of insectivorous, cavity-nesting birds. In: Frankel, S.J., Shea, P.J., Haverty, M.I. (Technical Compilers), Proceedings of the Sudden Oak Death Science Symposium: The State of Our Knowledge. USDA Forest Service, Gen. Tech. Rep. PSW-GTR-196, pp. 191–192. Apigian, K., Brown, L., Loda, J., Toas, S., Allen-Diaz, B., 2006. Small mammal and herpetofauna abundance and diversity along a gradient of Sudden Oak Death infection. In: Frankel, S.J., Shea, P.J., Haverty, M.I. (Technical Compilers), Proceedings of the Sudden Oak Death Science Symposium: The State of Our Knowledge. USDA Forest Service, Gen. Tech. Rep. PSWGTR-196, p. 494. Brown, P.M., Baxter, W.T., 2003. Fire history in coast redwood forests of the Mendocino Coast, California. Northwest Sci. 77, 147–158. DiGregorio, L.M., Krasny, M.E., Fahey, T.J., 1999. Radial growth trends of sugar maple (Acer saccharum) in an Allegheny northern hardwood forest affected by beech bark disease. J. Torrey Bot. Soc. 126, 245–254. Fajvan, M.A., Wood, J.M., 1996. Stand structure and development after gypsy moth defoliation in the Appalachian Plateau. For. Ecol. Manage. 89, 79–88. Forrester, J.A., McGee, G.G., Mitchell, M.J., 2003. Effects of beech bark disease on aboveground biomass and species composition in a mature northern hardwood forest 1985–2000. J. Torrey Bot. Soc. 130, 70–78. Hunter, J.C., 1997. Fourteen years of mortality in two old-growth Pseudotsuga– Lithocarpus forests in Northern California. J. Torrey Bot. Soc. 124, 273–279. Hunter, J.C., Barbour, M.G., 2001. Through-growth by Pseudotsuga menziesii: a mechanism for change in forest composition without canopy gaps. J. Veg. Sci. 12, 445–452. Hunter, J.C., Parker, V.T., 1993. The disturbance regime of an old-growth forest in coastal California. J. Veg. Sci. 4, 19–24. Hunter, J.C., Parker, V.T., Barbour, M.G., 1999. Understory light and gap dynamics in an old-growth forested watershed in coastal California. Madrono 46, 1–6. Kashiwagi, J.H., 1985. Soil Survey of Marin County California. United States Department of Agriculture, USDA Soil Conservation Service, p. 131. Korstian, C.F., Stickel, P.W., 1927. The natural replacement of blight-killed chestnut in the hardwood forests of the Northeast. J. Agric. Res. 34, 631–648. Larson, B.C., 1986. Development and growth of even-aged stands of Douglasfir and grand fir. Can. J. For. Res. 16, 367–372. Liebhold, A.M., MacDonald, W.L., Bergdahl, D., Mastro, V.C., 1995. Invasion by exotic forest pests: a threat to forest ecosystems. For. Sci. (Monograph 30) 41 (2), 49. Lorimer, C.G., 1980. Age structure and disturbance history of a southern Appalachian virgin forest. Ecology 60, 139–142. Monahan, W.B., Koenig, W.D., 2006. Estimating the potential effects of sudden oak death on oak-dependent birds. Biol. Cons. 127, 146–157. Noss, R.F. (Ed.), 2000. The Redwood Forest: History, Ecology and Conservation of the Coast Redwoods. Island Press, Washington, DC. O’Hara, K.L., 1995. Early height development and species stratification across five climax series in the eastern Washington Cascade range. New Forests 9, 53–60.
Oliver, C.D., 1978. The development of northern red oak in mixed stands in central New England. Yale Univ. School of Forestry and Environmental Studies, Bulletin No. 91, p. 63. Oliver, C.D., 1982. Stand development—its uses and methods of study. In: Means, J.E. (Ed.), Forest Succession and Stand Development Research in the Northwest. Oregon State University, Forest Res. Lab., pp. 100–112. Oliver, C.D., Larson, B.C., 1996. Forest Stand Dynamics, Update Edition. John Wiley & Sons, Inc., New York. Olson Jr., D.F., Roy, D.F., Walters, G.A., 1990. Sequoia sempervirens (D. Don) Endl. Redwood. In: Burns, R.M., Honkala, B.H. (Technical Coordinators), Silvics of North America, Vol. 1. Conifers. USDA Forest Service Agricultural Handbook, Vol. 654, pp. 541–551. Orwig, D.A., Foster, D.R., 1998. Forest response to the introduced hemlock woolly adelgid in southern New England, USA. J. Torrey Bot. Soc. 125, 60–73. Prestemon, D.R., 1966. The variation of heart stain and wood density in tanoak (Lithocarpus densiflorus (Hook&Arn.)Rehd.). Dissertation. University of California, Berkeley, CA. Regent Instruments Inc., 2004. WinDENDRO: Tree Ring, Stem, Wood Density Analysis and Measurement. Quebec City, Canada. Rittiman, C.A., Thorson, T., 2002. Soil Survey of Mendocino County, California Western Part. USDA Natural Resources Conservation Service; in cooperation with the Regents of the University of California (Agricultural Experiment Station) and the United States Department of the Interior, Bureau of Land Management, Washington, DC, p. 459. Rizzo, D.M., Garbelotto, M., 2003. Sudden oak death: endangering California and Oregon forest ecosystems. Frontiers Ecol. 1, 197–205. Rizzo, D.M., Garbelotto, M., Davidson, J.M., Slaughter, G.W., Koike, S.T., 2002. Phytophthora ramorum as the cause of extensive mortality of Quercus spp. and Lithocarpus densiflorus in California. Plant Dis. 86, 205–214. SPSS for Windows, 2002. 11.5.0, SPSS, Inc., Chicago, IL. Stancioiu, P.T., O’Hara, K.L., 2005. Sapwood area–leaf area relationships for coast redwood. Can. J. For. Res. 35, 1250–1255. Tappeiner II, J.C., McDonald, P.M., 1984. Development of tanoak understories in conifer stands. Can. J. For. Res. 14, 271–277. Tappeiner II, J.C., McDonald, P.M., Roy, D.F., 1990. Lithocarpus densiflorus (Hook&Arn.)Rehd. Tanoak. In: Burns, R.M., Honkala, B.H. (Technical Coordinators), Silvics of North America, Vol. 2. Hardwoods. USDA Forest Service Agricultural Handbook, Vol. 654, pp. 417–425. Tobin, P.C., Sharov, A.A., Liebhold, A.A., Leonard, D.S., Roberts, E.A., Learn, M.R., 2004. Management of the gypsy moth through a decision algorithm under the STS project. Am. Entomol. 50, 200–209. Waring, K.M., O’Hara, K.L., 2005. Silvicultural strategies in forest ecosystems affected by introduced pests. For. Ecol. Manage. 209, 27–41. Waring, K.M., O’Hara, K.L., 2006. Estimating relative error in growth ring analyses of second growth coast redwood (Sequoia sempervirens). Can. J. For. Res. 36, 2216–2222. Western Regional Climate Center, 2007. Historical climate information: Western United States individual weather station data. National Oceanic and Atmospheric Administration. Retrieved April 2, 2007 from http:// www.wrcc.dri.edu/. Zarnoch, S.J., Bechtold, W.A., Stoke, K.W., 2004. Using crown condition variables as indicators of forest health. Can. J. For. Res. 34, 1057–1070.
Forest Ecology and Management 255 (2008) 2650–2658 www.elsevier.com/locate/foreco
Redwood/tanoak stand development and response to tanoak mortality caused by Phytophthora ramorum Kristen M. Waring *, Kevin L. O’Hara Department of Environmental Science, Policy & Management, University of California, Berkeley, CA 94720-3114, United States Received 23 July 2007; received in revised form 9 January 2008; accepted 10 January 2008
Abstract Coast redwood (Sequoia sempervirens) and tanoak (Lithocarpus densiflorus) form mixed-evergreen forests along the northern California coast. In the mid-1990s, an introduced pathogen (Phytophthora ramorum) began causing extensive mortality of tanoak in these forests. This research reconstructed stand development patterns occurring in stands with and without the pathogen, measured stand responses to tanoak mortality, and developed projections of future stand development and structure in the presence of P. ramorum. Redwood forms an upper canopy layer while tanoak forms a multicohort lower canopy, resulting in distinct vertical stratification patterns. Individual redwood tree response patterns to tanoak mortality included crown expansion, increased basal sprouting, and increased basal area growth. Future stand structures will likely have greater proportions of redwood relative to tanoak. # 2008 Elsevier B.V. All rights reserved. Keywords: Stand dynamics; Sudden oak death; Tree response; Invasive species
1. Introduction Introduced forest pests have become increasingly common in the past century and include such well-known examples as chestnut blight (caused by Cryphonectria parasitica (Murrill) Barr.) and Dutch elm disease (caused by Ophiostoma spp.). These pests frequently result in widespread tree decline and mortality and may have cascading ecological effects (Liebhold et al., 1995). Unusually high mortality of hardwood trees along the California coast has been attributed to a newly described pathogen, Phytophthora ramorum (S. Werres, A.W.A.M. de Cock) (Rizzo et al., 2002). P. ramorum spores are spread through infected soil and plant material in addition to movement by air, water, humans, and domestic pets. The disease caused by P. ramorum has been particularly devastating to tanoak (Lithocarpus densiflora (Hook&Arn.)Rehd.) trees and generally results in rapid death of most infected tanoak stems (Rizzo and Garbelotto, 2003). Shade-tolerant tanoak trees commonly form mixed species stands with coast redwood (Sequoia sempervirens (D. * Corresponding author at: School of Forestry, Northern Arizona University, PO Box 15018, Flagstaff, AZ 86011-5018, United States. Tel.: +1 928 523 4920; fax: +1 928 523 1080. E-mail address: [email protected] (K.M. Waring). 0378-1127/$ – see front matter # 2008 Elsevier B.V. All rights reserved. doi:10.1016/j.foreco.2008.01.025
Don.)Endl.) along the north-central California coast. These second growth stands also include coast Douglas-fir (Pseudotsuga menziesii (Mirb.) Franco var. menziesii), and minor components of California bay (Umbellaria californica (Hook&Arn.)Nutt.) and Pacific madrone (Arbutus menzeisii Pursh). Light severity fire probably occurred frequently in these forests prior to 1900, removing mostly small stems (Hunter, 1997; Brown and Baxter, 2003). Previous work in Douglas-fir/mixed hardwood dominated stands has shown gap phase development patterns in the absence of fire (Hunter and Parker, 1993; Hunter et al., 1999). Gaps form as the result of one or more disturbance events such as windthrow or slope failure and tanoak is a common colonizer of new gaps (Hunter et al., 1999). However, these studies did not include a detailed retrospective view of past height development or typical patterns of tree ring growth and response nor does similar information exist for stands composed primarily of redwood and tanoak. In redwood/tanoak stands, increased mortality of tanoak due to P. ramorum may result in increased growth rates in surviving trees of both species. The competition for resources and stand development patterns may be altered, including height growth patterns over time. For example, redwood may capture newly available resources on the site and leave few resources available for surviving or regenerating tanoak; one method of assessing these changes is through stand reconstruction (Oliver, 1982) to
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describe pre- and post-tanoak mortality height growth patterns. Height growth patterns provide a key descriptive process of competitive positions of tree crowns in light-limited environments and are therefore an important aspect of stand development patterns (Oliver and Larson, 1996). Increased light availability may result in a sprout response, as both redwood and tanoak are prolific sprouters capable of producing vegetative sprouts from the stem or base. These sprouts originate from dormant and adventitious buds following the stimulation from increased light or heat, or from injury to the tree. This sprouting ability makes redwood rare among conifers because of its ability to produce stump sprouts. A separate response is the formation of basal sprouts at the base of uncut trees. These basal sprouts form new stems and are a typical response to disturbance (Tappeiner et al., 1990; Olson et al., 1990). Several studies have detailed changes in stand structure and development following pest introductions in other forests. Growing evidence suggests that major factors directing future stand development will be shade tolerance and a species’ presence on the site (Fajvan and Wood, 1996; Orwig and Foster, 1998; Waring and O’Hara, 2005). Changes in species composition, changes in age structure, and loss of the affected species are some commonly documented effects of introduced pests (Korstian and Stickel, 1927; Fajvan and Wood, 1996; Abrams et al., 1997; Forrester et al., 2003). In a southern Appalachian forest, Lorimer (1980) found that during the period of high chestnut blight mortality (1928–1938), understory tree release from suppression was higher than expected and certain species were more likely to benefit than others. In forest ecosystems vulnerable to introduced pests, management activities are likely to include preventative, mitigative or restorative objectives (Waring and O’Hara, 2005). An understanding of stand development patterns can serve as a guide to managers in predicting future stand development and response to treatments for any of these objectives. The present study documented effects of P. ramorum on mixed redwood/tanoak stand structures and projected potential future changes in these structures. We hypothesized that (1) tanoak density has been greatly reduced; (2) surviving tanoak have increased growth; (3) redwood has increased both sprouting and overall growth; and (4) future species composition will be dominated by redwood. Specific research objectives were to (1) confirm the comparability of the two research sites; (2) reconstruct patterns of stand development in these mixtures prior to and following P. ramorum invasion; (3) measure effects of P. ramorum-related mortality on tanoak and redwood tree growth and stem density; (4) measure the basal sprout response of redwood and tanoak to P. ramorum mortality; and (5) project changes in stand development following tanoak mortality.
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winter and spring followed by warm, dry summers. The two study sites used in this work are located approximately 190 km apart north-south, in the central zone of coast redwood forests (Noss, 2000). Three stands were selected within Jackson State Demonstration Forest (JDSF), Mendocino County, California (39.218N, 123.368W) to represent redwood/tanoak forests developing without P. ramorum infection. These stands originated from timber harvest about 80-years prior to sampling. Average annual temperature near the study stands is 12.6 8C, with an average of 1052 mm rainfall per year falling primarily during the wet winter months (WRCC, 2007). Soils underlying the study sites are primarily Vandamme loam, which are deep, well drained soils derived from sandstone (Rittiman and Thorson, 2002). Average site index of the JDSF study stands was 31 m (base 100 year). Four stands were selected within the Marin Municipal Water District (MMWD), Marin County, California (38.018N, 122.418W), which encompasses 38,074 ha set aside for management of water resources. Mortality of tanoak due to P. ramorum has been high within the MMWD since the mid1990s (Rizzo et al., 2002). Timber harvesting occurred approximately 80 years ago, with current stands characterized by an overstory conifer layer of primarily second-growth redwood and Douglas-fir with the occasional remnant oldgrowth redwood. Average annual temperature in the area is 13.7 8C with corresponding average annual precipitation of 1023 mm (WRCC, 2007). Soils in the area are formed from Franciscan Formation parent material, and are in the Dipsea soil series. The Dipsea series is characterized by deep, well-drained very gravelly loam (Kashiwagi, 1985). Average site index of the Marin Municipal Water District (MMWD) study stands was 33 m (base 100 year). Because of irregularities in ring formation, which can significantly affect accurately aging trees (Waring and O’Hara, 2006), site index numbers may not be reliable but provide an approximate comparison of site productivity between the two study sites. Study stands at both sites were selected based on approximate age (80 years) and species composition: redwood comprised at least 75% of the conifer component and tanoak comprised at least 75% of the broadleaved component. Stands were primarily even-aged based upon available stand history information, with initiation following early 20th Century timber harvesting. Three plots were located within a predefined 1 ha area within each stand. Each plot was subjectively located to include mature redwood and tanoak trees growing in close proximity and assumed to be in direct competition for available resources. These interactions were observed to be typical for the sampled stands. Although redwood and tanoak were the most abundant species, Douglas-fir, Pacific madrone, grand fir (Abies grandis (Dougl.) Lindl.), and California bay were also found in the study stands.
2. Materials and methods 2.2. Data collection and analysis 2.1. Study area The north-central California coast has a Mediterranean climate characterized by cool, wet conditions during fall,
Three circular fixed radius plots were installed in each stand at each site resulting in 9 plots at JDSF and 12 at MMWD. However, two MMWD plots were later excluded from analysis
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due to lack of tanoak mortality. Plots ranged in size from 0.01 to 0.05 ha, with each plot designed to include 8–12 overstory trees that were near-neighbors and presumed to be in direct competition with each other (or had recently been in direct competition in the case of dead tanoak). After locating the center point of each plot, the position of each tree greater than 1.37 m tall (breast height) within the plot radius was mapped, and tree species and diameter at breast height (DBH) were recorded. Redwood and tanoak basal sprout presence or absence was noted for each tree. Trees originating from common sprout clumps or clones were also noted, as were trees of seed origin. Between 5 and 10 representative trees/plot were selected for more intensive sampling; these trees are hereafter referred to as ‘sample trees’. Crown radii were measured at eight radii in cardinal directions around the circumference of all sample tree crowns using a clinometer to locate the drip line. Total sample tree height and height to the base of the live crown were measured. Main-canopy trees were assumed to be the ones most likely to respond quickly to tanoak mortality. A small number of trees greater than 100 cm DBH in the MMWD stands were removed from the analysis because they were remnant old-growth trees that were present on only one of the study sites. Relative height was then computed as the ratio of each tree’s height to the height of the tallest remaining tree measured at that site. Trees were placed into one of three categories with respect to canopy position: <0.25, 0.25–0.85, and >0.85 relative height. The analysis then focused upon only the main-canopy or central group that was the largest group of trees and comprised the primary canopy. The group of shortest trees comprised a total sample of only eleven trees primarily located in the suppressed subcanopy. The tallest trees also had a small sample size (n = 9) and included two old-growth trees in Marin that were not large enough to be excluded (e.g., <100 cm DBH). Non-parametric statistical analyses were performed where the assumptions of normality were not met within the sample data. Comparability of the two research sites was assessed using stocking (trees/ha and basal area), relative proportions of sprout-origin trees, site quality, and species composition. However, some differences were expected because of high levels of tanoak mortality in the MMWD. Species other than tanoak and redwood were combined into a single species group for assessment of stocking and species composition for the two study sites. Means between density for each species/species group were compared with t-tests. The two study sites were similar in pre-infection characteristics despite their geographic separation, therefore providing justification for comparison despite the distance between the sites. Both redwood and tanoak produce basal sprouts with the potential of forming tree stems. Comparative sprouting between study sites was assessed by evaluating the probability of a tree stem having a basal sprout present at the time of sampling. Sprout presence at the two research sites was compared using a Mann–Whitney non-parametric test for both tanoak and redwood. In each of the three stands within JDSF, two of the three plots were destructively sampled by felling each sample tree for stem
analysis and stand reconstruction (sensu Oliver, 1982). Stem analysis took place between May and October 2002. Sample trees on the third plot were not felled, but increment cores were removed at the base, breast height and 3 m from each tree for age and tree ring analysis. Immediately after tree felling, total tree length and length to the lowest live branch were recorded for each sample tree. Cross-sectional disks were removed from each tree at the base, breast height, and at variable locations along the tree bole. Distance between cross-sections was based upon merchantable log lengths for each species (5.0 m for redwood, 3.8 m for tanoak) for trees of merchantable size. Sections were removed every 1–3 m on non-merchantable trees. Sapwood area and 5-year radial growth were measured at two randomly located positions on each breast height crosssection shortly after felling. Cross-sections were sealed in large plastic bags for transport to the laboratory, where they were autoclaved. They were then planed and sanded with progressively finer sand paper until the rings were clearly visible. Individual redwood rings were not always present due to discontinuous and missing rings (Waring and O’Hara, 2006) so age was based on the maximum age of eight radii per crosssection. Due to constraints on tree felling in the MMWD, only nondestructive sampling procedures were implemented to reconstruct past stand development. Plot and sample tree selection was the same as at JDSF. All plots were installed in 2002. Increment cores were removed from each sample tree on the south and east sides within 0.3 m of the ground at the tree base on the uphill side of tree, at breast height, and at a height of 3 m. This limited sampling followed previous stand reconstruction protocols where trees were not felled (Oliver, 1978; O’Hara, 1995). Sapwood length was recorded in the field for each breast height and 3-m core. All cores were autoclaved to prevent spread of P. ramorum, glued to boards, and sanded with progressively finer sand paper until rings were clearly visible. To verify tanoak mortality due to P. ramorum, two dead tanoaks were selected on each plot in the MMWD for sampling. Wood samples were then removed from the base, breast height, and from any visible bleeding along the tree bole. The minimum number of samples per tree varied based on tree diameter and ranged from 2 to 8. Precautions were taken to avoid contamination between samples, which were then sealed and placed in cold storage for up to a week. The Forest Pathology Laboratory at UC Berkeley conducted PCR analysis on the samples, which confirmed the presence of P. ramorum DNA in dead tanoak at all MMWD stands. Cross-sections and cores were aged with the aid of a dissecting microscope or scanned into a computer and analyzed using the tree ring analysis software WinDendro (Regent Inst., 2004). All breast height samples were scanned to obtain precise ring width data. Only growth rings from 1997 to 2001 were used in subsequent growth ring width analysis. When multiple increment cores were available from a given height on the same tree, the cores were averaged prior to analysis. Redwood trees that were destructively sampled had up to eight individual radial measurements on a cross-section that were averaged for ring width analysis. Cross-dating at breast height was attempted
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in redwood but was not successful due to the growth ring anomalies (Brown and Baxter, 2003; Waring and O’Hara, 2006). However, basic height growth patterns should be relatively unaffected by this pattern due to the decrease in ring count variation higher along the tree bole (Waring and O’Hara, 2006). Reconstructed height growth patterns were then used as a basis for describing historical stand development patterns (Oliver, 1982). To assess the effects of P. ramorum on tree growth and crown characteristics, differences in cumulative 5-year basal area growth (1997–2001), crown surface area, and leaf area (redwood only) were used to assess post-infection change. Generally, changes in crown characteristics are expected to be a feature of a released tree that precede effects on bole increment (Oliver and Larson, 1996). Crown surface area (CSA) was calculated assuming a paraboloid shape for redwood and an ellipsoid shape for tanoak. The following equations were used: Paraboloid (modified from Zarnoch et al., 2004): CSArw
4pCL ¼ 3CW2
CW4 CW þ 4CL2 2
1:5
CW4 4CL2
1:5 (1)
where CSArw is redwood crown surface area (m2), CL is live crown length (m), and CW is mean crown width (m) at the widest point of the crown. Ellipsoid: 2 1 þ ðHCL=CWÞ arcsinðEÞ CSAto ¼ 2pCW (2) E
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Table 1 Mean summary characteristics for sampled redwood/tanoak plots at Jackson Demonstration State Forest (JDSF) and Marin Municipal Water District (MMWD) Species
Measure
JDSF
MMWD
Redwood
Trees/ha BA (m2/ha)
898 (195) 104.6 (18.1)
883 (182) 106.1 (19.0)
Tanoak
Trees/ha BA (m2/ha)
884 (101) 53.9 (5.3)
995 (210) 15.8 (3.0)
0.653 <0.001
Dead tanoak
Trees/ha BA (m2/ha)
100 (33) 2.3 (0.8)
605 (74) 16.9 (2.7)
<0.001 <0.001
Other species
Trees/ha BA (m2/ha)
38 (23) 9.6 (8.6)
75 (44) 8.9 (4.2)
0.481 0.943
n
9
p-Value 0.955 0.957
10
Standard errors are given in parentheses. Other species included California bay, Pacific madrone and Douglas-fir.
trees/ha and dead basal area were significantly different between study areas indicating the P. ramorum mortality greatly exceeded background mortality levels (Table 1). Stand reconstruction revealed a stratification of redwood over tanoak in these stands. Following stand initiation after post-1900 timber harvesting, redwood trees began growing
where CSAto is tanoak crown surface area (m2), HCL is one half pffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi 2 CW2 live crown length (m), CW is as above and E ¼ HCL . HCL Redwood leaf area was predicted using breast height sapwood area (Stancioiu and O’Hara, 2005). Analysis of covariance was used to examine the relationship between site and tree characteristics in instances where there were no significant interactions between study site and the variable of interest. Such interactions were tested for using between subjects effects tests. All statistics were performed using SPSS statistical software (SPSS, 2002). 3. Results Prior to the arrival of P. ramorum, redwood stocking was nearly identical and tanoak stocking was apparently similar (Table 1). Mean redwood basal area and trees/ha were nearly identical between study sites (Table 1). There were greater trees/ha in MMWD for the ‘‘other species’’ but no significant differences. Pre-infection tanoak basal area was greater at JDSF but trees/ha were greater at MMWD. Tanoak comprised about 32% of stand basal area at JDSF but was only 12% at MMWD after infection. Inclusion of recent mortality in tanoak basal area increased the tanoak total to approximately 22%. Additional mortality due to P. ramorum that was too decayed to measure would have probably increased these basal area numbers at MMWD. Although post-infection live trees/ha was not significantly different, differences in basal area, and dead
Fig. 1. Height growth development occurring over 80 years of stand development in redwood/tanoak stands, Jackson Demonstration State Forest. Similar patterns occurred on all study stands. Each line represents the development of a single tree.
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Fig. 2. Examples of height development in redwood/tanoak forest stands on the Marin Municipal Water District. (a) Tanoak mortality present but some live tanoak remain in 2002 and (b) tanoak mortality extensive and no live tanoak remain within plot. Note differing axis scales that highlight inter-tree relationships. Each line represents the development of a single tree.
faster in height than tanoak while also showing within-species differentiation (Figs. 1 and 2). All canopy trees were likely sprout origin given their rapid initial height growth rates and clumpy spatial patterns (Fig. 3). For redwood, the parent stumps were generally still present. Height differentiation continued to occur through the next several decades. A few tanoak entered the stand, likely as young sprouts, after stand initiation, forming multiple strata within the tanoak component. By 2002, the stands had stratified into an upper stratum dominated by redwood, a midstratum dominated by tanoak, and an understory of tanoak with some redwood and other species. A few residual trees (over 80 cm DBH, not harvested in the early 1900s) in Marin County formed an even higher stratum of sparsely distributed emergent trees. Pacific madrone followed similar height growth patterns as tanoak (data not shown). At JDSF 84% of redwood and 82% of tanoak were of clonal origin whereas at MMWD the clonal origin trees were 89% for redwood and 76% for tanoak. Recent seedling regeneration of all species was generally absent from all study sites. The probability of redwood trees producing basal sprouts was higher ( p = 0.038) at the MMWD study sites than at JDSF (Table 2). For tanoak, the probability of sprout production was greater at JDSF, however, this difference was not significant ( p = 0.062). Among the main-canopy redwood sample trees, basal area growth and leaf area were significantly greater in MMWD, while live crown ratio was significantly greater in JDSF
Fig. 3. Example spatial distribution of live and dead stems, including stumps, on second-growth redwood/tanoak plots of California. (a) Jackson Demonstration State Forest, no sudden oak death and (b) Marin Municipal Water District, mortality of tanoak due to sudden oak death. Each plot has a radius of 8 m.
(Table 3). Total tree height and DBH were not significantly different between study sites for redwood (Table 3). Redwood basal area growth crown surface area, and leaf area all tended to be larger for a given tree diameter on MMWD plots than on JDSF plots but analysis of covariance was only possible for leaf area, which was significant (Fig. 4, p < 0.001). Main-canopy tanoak sample trees showed different and often opposing patterns: total height and DBH were significantly greater at JDSF than MMWD, with no significant differences found between basal area growth, crown surface area or live crown Table 2 Percent probability of basal sprouts on redwood and tanoak stems for Jackson Demonstration State Forest (JDSF) and Marin Municipal Water District (MMWD) Species
JDSF
MMWD
p-value
Redwood Probability of trees with sprouts (%) n
74.4 (3.5) 156
85.1 (3.5) 107
0.038
Tanoak Probability of trees with sprouts (%) n
61.2 (4.4) 121
49.7 (4.2) 143
0.062
Probabilities were compared with non-parametric Mann–Whitney tests. Standard errors are given in parentheses.
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Table 3 Summary characteristics of main-canopy sample trees by species and site Species
JDSF
MMWD
Redwood DBH Height Live crown ratio Crown surface area Basal area growth Leaf area n
41.6 25.7 0.6 40.3 39.0 128.5 20
(3.7) (1.8) (0.03) (5.5) (7.7) (21.2)
43.5 25.2 0.4 97.1 91.5 179.3 22
Tanoak DBH Height Live crown ratio Crown surface area Basal area growth n
34.4 26.2 0.5 116.1 41.3 30
(2.4) (0.8) (0.04) (19.5) (6.9)
25 (1.5) 21.0 (1.0) 0.6 (0.03) 112.5 (13.2) 28.1 (3.9) 20
(4.3) (1.7) (0.03) (15.0) (14.4) (29.3)
p-value 0.71 0.822 0.001 0.001 0.003 0.176
0.001 <0.0001 0.123 0.877 0.548
JDSF: Jackson Demonstration State Forest and MMWD: Marin Municipal Water District. Comparisons were made using t-tests. Standard errors are given in parentheses.
ratio (Table 3). Tanoak crown surface area at MMWD was significantly greater at a given diameter that crown surface area at JDSF (ANCOVA, Fig. 5a). Basal area growth tended to increase in surviving tanoak trees on infected sites following P. ramorum-caused mortality, however, these differences were not significant (data not shown, p > 0.100). Similar trends can be seen in basal area growth, with greater growth for a given diameter occurring in MMWD (Fig. 5b); however, analysis of covariance was not performed because of a significant interaction between study site and basal area growth. 4. Discussion Following the infection of P. ramorum, there has been a significant decline in tanoak basal area in these stands and a similar but not significant trend in number of tanoak stems. This decline affects tanoak trees of all sizes and age classes/cohorts. At time of sampling, or about 8 years following initial infection, tanoak basal area and trees/ha were reduced 40–50%. Because tanoak was largely stump sprout origin with a very clumpy spatial pattern, this mortality is likely to leave large gaps and change the spatial patterns in these stands. In the absence of P. ramorum, stand development pattern in these second-growth sprout-origin forests was the formation of a redwood stratum over multiple lower strata of tanoak. Within 10 years of the stand replacement disturbance that initiated these stands, the redwood had outgrown the tanoak, relegating the tanoak to a lower canopy stratum that was maintained throughout the first 80 years of stand development. This height growth advantage over tanoak will probably continue to exist for hundreds of years, given the longevity of redwood trees and the absence of disturbance or management. Because the typical spatial patterns of these stands are large clumps of sprout-origin tanoak or redwood, redwood and tanoak trees are limited to specific small patches within the stand. This feature often allows tanoak to receive some direct sunlight although its height position implies a subordinate canopy position. On less
Fig. 4. Redwood relationship between diameter at breast height and (a) crown surface area; (b) leaf area; and (c) 5-year basal area growth. JDSF: Jackson Demonstration State Forest and MMWD: Marin Municipal Water District.
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Fig. 5. Tanoak relationship between diameter at breast height and (a) crown surface area and (b) 5-year basal area growth. JDSF: Jackson Demonstration State Forest and MMWD: Marin Municipal Water District.
productive sites, the redwood may not outgrow the tanoak in height as quickly. Following the development of the lower tanoak stratum, tanoak continues to enter the stands as seedlings or clonal sprouts. These tanoaks ultimately form a multiaged and multistrata component. Tappeiner and McDonald (1984) reported that both large and small tanoak growing in Douglas-fir dominated stands grew slowly and did not need disturbance to sprout. Tanoak mortality caused by P. ramorum infection has triggered a sprout response in the redwood trees, creating a new cohort that is beginning to reach breast height and can be seen in this data set primarily as a higher percentage of trees with basal sprouts. This trend will probably become more pronounced with continued tanoak mortality. However, the long-term growth of these sprouts is limited by their proximity to existing redwood sprout clumps that include overstory trees.
Increased mortality of tanoak in these stands is likely to benefit three categories of redwood trees: those upper-stratum trees beginning to slow in height growth, redwoods occupying the middle stratum, and possibly the regenerating cohort of redwood sprouts. Upper-stratum trees are likely to expand crowns into areas vacated by tanoak and experience increased or sustained diameter growth rates. Middle stratum and understory sprouts will only benefit if their spatial position allows them adequate resources to compete within their sprout clump competitors. Few trees other than redwood and tanoak were sampled, however, the few Douglas-fir sampled tended to follow a ‘‘through-growth’’ pattern where they grew rapidly in height growth and were able to grow through an overstory canopy (i.e. Fig. 2b). This pattern is similar to that observed in other research in coastal mixed-evergreen forests (Hunter and Barbour, 2001) and other western North American conifer forests (Larson, 1986). Redwood trees growing on infected sites near clumps of tanoak mortality had greater basal area growth, crown surface area and leaf area than trees on uninfected sites; these same parameters (basal area growth, crown surface area, leaf area) were also greater when compared at a given diameter. Crown surface area is a function of the assumed shape and crown width/length. Redwood trees on infected sites also had significantly greater crown width (data not shown) and this is likely the parameter driving the greater crown surface area. It is possible that these trees are beginning to respond to increased resources available due to high levels of tanoak mortality. However, tanoak mortality alone probably does not adequately explain the increased growth and crown size of these trees. The distinct spatial heterogeneity and clumping patterns may affect patterns of tree response, as redwood tends to be further removed from the dead tanoak than surviving tanoak. Surviving tanoak trees also showed a significantly greater crown surface area at a given diameter in MMWD. Although tanoak basal area growth showed a similar trend, the results may be confounded by the significant differences in tree size found between the two sites. These differences are likely driven by the high levels of mortality at MMWD. Surviving tanoaks were competing directly with dead tanoak for resources; the death of neighboring tanoak increases resources available for those remaining alive. Location of individual trees in relation to mortality may play a role in response pattern and rates. DiGregorio et al. (1999) found that subcanopy sugar maple increased in radial growth following decline of beech from beech bark disease, whereas canopy sugar maple did not show a similar response (although trees in and near gaps all increased radial growth). A similar situation could be presenting itself in redwood/tanoak forests. Additionally, Prestemon (1966) noted a trend of decreasing radial growth in tanoak with increasing site index in northern California (Mendocino and Humboldt counties), potentially due to increased conifer competitiveness on more productive sites. While site index was very similar between sites (31 m JDSF vs 33 m MMWD), slightly higher productivity at MMWD may affect tanoak radial growth enough to mask effects of P. ramorum. Site index may not be an accurate method of assessing site productivity on these sites due
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Fig. 6. Hypothetical height development of redwood trees following tanoak mortality, assumed to occur in 2002.
to the growth-ring anomalies found in redwood (Waring and O’Hara, 2006). Fig. 6 shows hypothetical height development patterns for redwood over the next 20 years. Most tanoaks are presumed dead in 2001; upper-stratum redwood trees would increase height growth but maintain current canopy positions relative to each other. The forest in 2020 would presumably be composed of three canopy layers: the upper canopy redwood, a middle stratum of released redwood, and suppressed young redwood sprouts and any surviving tanoak in the lowest canopy layer. In the future, redwood will show more dominance on P. ramorum infected sites as tanoak mortality continues. Tanoak may have become more prevalent over the past century due to preferential cutting of redwood, even-aged management, and fire exclusion. In particular, fire exclusion allows tanoak to dominate over other species in the understory because of its ability to regenerate in shaded conditions (Hunter, 1997; Hunter et al., 1999). Several possible scenarios may result from the current tanoak decline that is dependent on the size of the resultant canopy gaps. One scenario of small or discreet gaps will lead to existing redwood trees expanding into the available growing space, leaving few opportunities for a new cohort of any species. A second scenario may arise if large groups of tanoak die and leave a large gap. Light resources may be enough to promote establishment of a new cohort of redwoods from either seedling or sprout origin resulting in a multiaged stand. Tanoak resistant to P. ramorum, other hardwood species, or exotic species are other possible components of a new cohort. Finally, a third scenario may occur where large gaps are formed but redwoods are unable to expand into these gaps because they reproduce primarily through sprout production. In these situations other tree species or brush species may have an initial advantage that results in a mixed species stand with a highly variable structure. In stands like those sampled in this study, the first scenario of increased redwood dominance is most likely. Managers have few options in these forests to avert the dramatic change in stand structure and species composition.
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Landowners managing for commercial harvest of redwood may experience an increase in the speed at which these forests revert to single species, multicohort redwood forests. These structures may have been more abundant in the past due to the occurrence of fire and less management activity. Since tanoak is not a commercial timber species, many managers expend resources attempting to control its growth early in stand development; in such cases, P. ramorum caused mortality may have welcome effects. Additionally, thinning along uninfected boundaries may be analogous to the ‘‘Slow the Spread’’ campaign undertaken to slow the spread of gypsy moth (Lymantria dispar L.) in the eastern United States (Tobin et al., 2004). Although thinning these stands for P. ramorum management is untested and may or may not slow the spread of the pathogen, it would almost certainly alleviate fuel accumulation if harvested trees are removed from the stands. Old-growth forests are less likely to show a similar response to tanoak canopy gaps due to both their large size and old age. In areas that have reverted to tanoak following extensive harvest, planting may be necessary to regenerate the site following tanoak mortality to fill gaps with redwood. Finally, tanoak mortality may have cascading impacts throughout the ecosystem because it is the only mast producing species in the mixed-evergreen forest type. Effects range from impacts on wildlife (Apigian and Allen-Diaz, 2006; Apigian et al., 2006; Monahan and Koenig, 2006) to loss of biodiversity and have not been fully investigated. 5. Conclusions The infection of redwood/tanoak stands by P. ramorum has major effects on current stand structure and subsequent stand growth. In sampled stands, tanoak mortality was approaching 50% with mortality expected to continue. The effects of this mortality are greater basal sprouting of redwood trees and crown expansion of surviving tanoaks. Other expected outcomes are greater growth rates in both the redwood component and other minor species that are not affected by P. ramorum. The result will be a tendency of these stands to form multiaged structures with a higher proportion of redwood. The tanoak component in these stand structures will generally be lacking. Because of the aggregated spatial patterns of these sprout-origin stands, larger canopy gaps following tanoak mortality may remain unfilled by redwood. Acknowledgements This research was supported, in part, by the USDA Forest Service, Pacific Southwest Research Station, through Research Agreement Number 01-JV-11272164-165. Cooperation and assistance from Fay Yee, William Baxter, Robert Horvat, the Jackson Demonstration State Forest and the Marin Municipal Water District is greatly appreciated. The authors thank Paul Lilly, Kyla Sabo and Bruce Hammock and the UC Berkeley Forest Pathology Laboratory for field and laboratory assistance.
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