Low growth resilience to drought is related to future mortality risk in trees.

Severe droughts have the potential to reduce forest productivity and trigger tree mortality. Most trees face several drought events during their life and therefore resilience to dry conditions may be crucial to long-term survival. We assessed how growth resilience to severe droughts, including its components resistance and recovery, is related to the ability to survive future droughts by using a tree-ring database of surviving and now-dead trees from 118 sites (22 species, >3,500 trees). We found that, across the variety of regions and species sampled, trees that died during water shortages were less resilient to previous non-lethal droughts, relative to coexisting surviving trees of the same species. In angiosperms, drought-related mortality risk is associated with lower resistance (low capacity to reduce impact of the initial drought), while it is related to reduced recovery (low capacity to attain pre-drought growth rates) in gymnosperms. The different resilience strategies in these two taxonomic groups open new avenues to improve our understanding and prediction of drought-induced mortality.

Early-Warning Signals of Individual Tree Mortality Based on Annual Radial Growth.

Tree mortality is a key driver of forest dynamics and its occurrence is projected to increase in the future due to climate change. Despite recent advances in our understanding of the physiological mechanisms leading to death, we still lack robust indicators of mortality risk that could be applied at the individual tree scale. Here, we build on a previous contribution exploring the differences in growth level between trees that died and survived a given mortality event to assess whether changes in temporal autocorrelation, variance, and synchrony in time-series of annual radial growth data can be used as early warning signals of mortality risk. Taking advantage of a unique global ring-width database of 3065 dead trees and 4389 living trees growing together at 198 sites (belonging to 36 gymnosperm and angiosperm species), we analyzed temporal changes in autocorrelation, variance, and synchrony before tree death (diachronic analysis), and also compared these metrics between trees that died and trees that survived a given mortality event (synchronic analysis). Changes in autocorrelation were a poor indicator of mortality risk. However, we found a gradual increase in inter-annual growth variability and a decrease in growth synchrony in the last ∼20 years before mortality of gymnosperms, irrespective of the cause of mortality. These changes could be associated with drought-induced alterations in carbon economy and allocation patterns. In angiosperms, we did not find any consistent changes in any metric. Such lack of any signal might be explained by the relatively high capacity of angiosperms to recover after a stress-induced growth decline. Our analysis provides a robust method for estimating early-warning signals of tree mortality based on annual growth data. In addition to the frequently reported decrease in growth rates, an increase in inter-annual growth variability and a decrease in growth synchrony may be powerful predictors of gymnosperm mortality risk, but not necessarily so for angiosperms.

Suitability of eastern pines for oviposition and survival of Sirex noctilio F.

The European woodwasp, Sirex noctilio F., is a pest of pines in many areas around the world. Since its introduction to North America, the distribution of S. noctilio overlaps with a known host (Pinus sylvestris) and hosts native to North America. Direct comparisons of suitability for oviposition and larval survival among these pines have not been made. We tested the relative suitability of four common pine species in northeastern North America (P. sylvestris, P. resinosa, P. banksiana, and P. strobus) as hosts for S. noctilio in a controlled, but in situ experiment. In a mixed pine forest in northern Ontario, we caged S. noctilio mating pairs on 10 freshly cut pine logs of each species, and estimated oviposition, counted adult S. noctilio (F1 generation) that emerged from logs, and calculated survivorship from egg to adult. Pinus sylvestris and P. resinosa were optimal hosts according to all three metrics of S. noctilio performance. Pinus strobus was a suitable larval host, but was not perceived as such by females, as evidenced by lower oviposition. Pinus banksiana was perceived as a suitable host by females, but was the least suitable larval host. Our results suggest that P. sylvestris and P. resinosa are more suitable hosts, at least in cut logs, than P. strobus and P. banksiana for S. noctilio in eastern North America.

A synthesis of radial growth patterns preceding tree mortality.

Tree mortality is a key factor influencing forest functions and dynamics, but our understanding of the mechanisms leading to mortality and the associated changes in tree growth rates are still limited. We compiled a new pan-continental tree-ring width database from sites where both dead and living trees were sampled (2970 dead and 4224 living trees from 190 sites, including 36 species), and compared early and recent growth rates between trees that died and those that survived a given mortality event. We observed a decrease in radial growth before death in ca. 84% of the mortality events. The extent and duration of these reductions were highly variable (1-100 years in 96% of events) due to the complex interactions among study species and the source(s) of mortality. Strong and long-lasting declines were found for gymnosperms, shade- and drought-tolerant species, and trees that died from competition. Angiosperms and trees that died due to biotic attacks (especially bark-beetles) typically showed relatively small and short-term growth reductions. Our analysis did not highlight any universal trade-off between early growth and tree longevity within a species, although this result may also reflect high variability in sampling design among sites. The intersite and interspecific variability in growth patterns before mortality provides valuable information on the nature of the mortality process, which is consistent with our understanding of the physiological mechanisms leading to mortality. Abrupt changes in growth immediately before death can be associated with generalized hydraulic failure and/or bark-beetle attack, while long-term decrease in growth may be associated with a gradual decline in hydraulic performance coupled with depletion in carbon reserves. Our results imply that growth-based mortality algorithms may be a powerful tool for predicting gymnosperm mortality induced by chronic stress, but not necessarily so for angiosperms and in case of intense drought or bark-beetle outbreaks.

Nonlethal Effects of Nematode Infection on Sirex noctilio and Sirex nigricornis (Hymenoptera: Siricidae).

A nonnative woodwasp, Sirex noctilio F., has established in pine forests in eastern North America. To facilitate prediction of the full range of impacts S. noctilio could have as it continues to spread in North American forest ecosystems, we studied the effects of infection by a nonsterilizing parasitic nematode on S. noctilio size, fecundity, and flight capacity and on the native woodwasp, S. nigricornis, size and fecundity. We also developed predictive models relating size to fecundity for both species. On average, S. noctilio (3.18 ± 0.05 mm) were larger than S. nigricornis (2.19 ± 0.04 mm). For wasps of similar size, S. nigricornis was more fecund. Nematode infection negatively affected potential fecundity by a mean difference of 36 and 49 eggs in S. noctilio and S. nigricornis, respectively. Nematode-infected males of S. noctilio, however, were larger than uninfected individuals. Nematode infection showed inconsistent results on mean speed and total distance flown by S. noctilio males and females. Nematode infection did not affect total distance flown by females, and so is unlikley to have a direct, or strong influence on S. noctilio flight capacity. Models developed to predict fecundity of Sirex spp. from body size, based on the close relationship between pronotum width and potential fecundity for both species (R(2) ≥ 0.69), had low measures of error when compared with true values of fecundity (± 25-26 eggs).

Do Native Insects and Associated Fungi Limit Non-Native Woodwasp, Sirex noctilio, Survival in a Newly Invaded Environment?

Sirex noctilio F. (Hymenoptera: Siricidae) is an introduced pest of pines (Pinus spp.) in several countries in the Southern Hemisphere. Although S. noctilio is established in North America (first discovered in 2004), it has not been a destructive pest there so far, where forest communities more closely resemble those in its native Eurasian range­where it is not a pest. To investigate the influence of the existing community of associated insects (competitors + natural enemies) and fungi (vectored by insects) on S. noctilio survival in North America, we examined stage-specific mortality factors and their relative importance, generating life tables drawn from experimentally-manipulated and natural cohorts of Sirex spp. (mostly S. noctilio, but some native S. nigricornis F.). For both natural and experimentally-manipulated cohorts, factors which acted during the earliest Sirex life stages, most likely tree resistance and/or competition among fungal associates, were paramount in dictating woodwasp survival. Experimentally-manipulated life tables revealed that protection from the community of associates resulted in a significantly, and substantially larger (>15x) S. noctilio F1 generation than exposure to it. Seventy percent of generation mortality in the exposed cohort was due to tree resistance or unknown causes early in larval development, which could have included competition among other bark- or wood-inhabiting insects and/or their fungal associates. Only 46% of generation mortality in the protected cohort was due to tree resistance and/or unknown causes. Parasitoids, particularly endoparasitoids (Ibalia spp.), showed limited ability to control S. noctilio, and reduced the experimentally-established cohort by only 11%, and natural cohorts an average of 3.4%. The relative importance of tree resistance vs. competition with bark- and wood-borers in reducing S. noctilio survival remains unclear. Tree resistance and/or competition likely contribute more than natural enemies in maintaining the S. noctilio population in North America below damaging levels.

Type of intercept trap not important for capturing female Sirex noctilio and S. nigricornis (Hymenoptera: Siricidae) in North America.

Current detection tools for Sirex noctilio F. (Hymenoptera Siricidae) in North America are poor. To determine the importance of intercept trap type for capturing females of S. noctilio and its native congener, Sirex nigricornis F., in eastern North America, we report on seven trap comparison studies from different years and geographic locations. Among studies, total numbers of S. noctilio captured were low (mean of < or = 1 wasp per trap). Total numbers of S. nigricornis caught were generally greater, and ranged from a mean of 1-13 wasps per trap. Nearly all studies found no significant differences among intercept trap types in the number of woodwasps caught. For future studies, we recommend that either panel or 12-unit Lindgren funnel traps be used to catch S. noctilio or S. nigricornis in eastern North America.

Densities of Agrilus auroguttatus and Other Borers in California and Arizona Oaks.

We investigated within-tree population density of a new invasive species in southern California, the goldspotted oak borer, Agrilus auroguttatus Schaeffer (Coleoptera: Buprestidae), with respect to host species and the community of other borers present. We measured emergence hole densities of A. auroguttatus and other borers on the lower stem (bole) of naïve oaks at 18 sites in southern California and on co-evolved oaks at seven sites in southeastern Arizona. We sampled recently dead oaks in an effort to quantify the community of primary and secondary borers associated with mortality-species that were likely to interact with A. auroguttatus. Red oaks (Section Lobatae) produced greater densities of A. auroguttatus than white oaks (Section Quercus). On red oaks, A. auroguttatus significantly outnumbered native borers in California (mean ± SE of 9.6 ± 0.7 versus 4.5 ± 0.6 emergence holes per 0.09 m² of bark surface), yet this was not the case in Arizona (0.9 ± 0.2 versus 1.1 ± 0.2 emergence holes per 0.09 m²). In California, a species that is taxonomically intermediate between red and white oaks, Quercus chrysolepis (Section Protobalanus), exhibited similar A. auroguttatus emergence densities compared with a co-occurring red oak, Q. kelloggii. As an invasive species in California, A. auroguttatus may affect the community of native borers (mainly Buprestidae and Cerambycidae) that feed on the lower boles of oaks, although it remains unclear whether its impact will be positive or negative.

Partial life tables from three generations of Enaphalodes rufulus (Coleoptera: Cerambycidae).

We used life table analyses to investigate age specific mortality and to better understand the population dynamics of the red oak borer, Enaphalodes rufulus (Haldeman) (Coleoptera: Cerambycidae). We continually sampled populations within 177 trees at primarily two sites in the Ozark National Forest in Arkansas throughout three (2-yr) generations. The first cohort (adults emerged in 2003) was sampled during a severe population outbreak, whereas the second and third (2005 and 2007) were sampled during the population crash that followed. Generation mortality was 94% in 2003 and 99% in both 2005 and 2007. Estimates of apparent mortality indicated that the E. rufulus population crash likely occurred during or before the first overwintering period (2003-2004) of the generation that emerged as adults in 2005. We found limited evidence for density dependent mortality, which suggest that intraspecific competition after the first active feeding period was apparently not an important mortality factor during E. rufulus development. Life tables revealed that E. rufulus larvae generally experienced the greatest apparent mortality during the second summer of active feeding (80-94%) when larvae were feeding in, and moving between phloem and sapwood. The least apparent mortality was incurred during the following spring and early summer (26-67%) when late stage larvae and pupae were deepest and most protected within sapwood or heartwood tunnels. We found very little evidence for mortality from associated species. Scarring of vascular tissue in response to E. rufulus feeding occurred during early life stages and may be an important tree resistance mechanism and E. rufulus mortality factor.