Research Article |
Corresponding author: Flora E. Krivak-Tetley ( flora.estella.krivak-tetley@dartmouth.edu ) Academic editor: Deepa Pureswaran
© 2022 Flora E. Krivak-Tetley, Jenna Sullivan-Stack, Jeff R. Garnas, Kelley E. Zylstra, Lars-Olaf Höger, María J. Lombardero, Andrew M. Liebhold, Matthew P. Ayres.
This is an open access article distributed under the terms of the CC0 Public Domain Dedication.
Citation:
Krivak-Tetley FE, Sullivan-Stack J, Garnas JR, Zylstra KE, Höger L-O, Lombardero MJ, Liebhold AM, Ayres MP (2022) Demography of an invading forest insect reunited with hosts and parasitoids from its native range. NeoBiota 72: 81-107. https://doi.org/10.3897/neobiota.72.75392
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The Sirex woodwasp Sirex noctilio Fabricius (Hymenoptera: Siricidae), a widespread invasive pest of pines in the Southern Hemisphere, was first detected in North America in 2004. This study assessed the impacts of life history traits, host resistance and species interactions on the demography of S. noctilio in New York, Pennsylvania and Vermont, then compared key metrics to those found in the native range in Galicia, Spain. Many trees naturally attacked by S. noctilio in North America produced no adult woodwasps, with 5 of 38 infested trees (13%) sampled across six sites yielding 64% of emerging insects. Reproductive success was highest in the introduced host scots pine, Pinus sylvestris, but native red pine, Pinus resinosa, produced larger insects. Sirex noctilio required one or sometimes two years to develop and sex ratios were male biased, 1:2.98 ♀:♂. Body size and fecundity were highly variable, but generally lower than observed in non-native populations in the Southern Hemisphere. Hymenopteran parasitoids killed approximately 20% of S. noctilio larvae and 63% of emerging adults were colonized by the parasitic nematode Deladenus siricidicola, although no nematodes entered eggs. Demographic models suggested that S. noctilio in the northeastern USA have a higher potential for population growth than populations in the native range: estimated finite factor of increase, λ, was 4.17–4.52 (depending on tree species colonized), compared to λ = 1.57 in Spain.
Forest pest, invasive species, population ecology, Sirex noctilio, woodwasp
Non-native insects are among the greatest current threats to global forest resources (
One approach for identifying key drivers of impacts caused by alien species is to compare important demographic parameters across native and invaded ranges (
The Sirex woodwasp, Sirex noctilio Fabricius (Hymenoptera: Siricidae), provides an ideal system for the comparison of invasive behavior across a range of contexts, with native populations in Eurasia and widely-studied non-native populations in both the Northern and Southern Hemispheres (
Sirex noctilio was first detected in North America in a survey trap in Fulton, NY near Lake Ontario in 2004 (
Female S. noctilio oviposit in suppressed or weakened pine trees (
A similar natural enemy complex is found in both the native range of S. noctilio and in North America. In North America, several native parasitoid species utilize both S. noctilio and native siricid species, such as S. nigricornis (
One possible explanation for differences in the behavior and impacts of invasive species populations is variability in important life history traits that impact potential population growth via fitness and fecundity. Perhaps the most important of these are insect body size and sex ratio (
Another potential explanation for variation in S. noctilio impacts is tree resistance or variation in the suitability of host trees, which has been hypothesized as a key factor controlling populations in North America (
A third potential explanation for frequent S. noctilio outbreaks in certain environments is the lack of controls by natural enemies in some non-native populations (
Our study was driven by the motivation to better understand current and potential future S. noctilio population dynamics in the eastern USA. Comprehensive research efforts to date in the USA and Canada have generated a range of estimates for important demographic parameters in these expanding populations and we have summarized these estimates in Table
Life history parameters reported in previous studies in North America. Summary of findings to date from all North American studies that have assessed aspects of Sirex noctilio life history. Variables include timing of emergence, voltinism, sex ratio, body size, fecundity, parasitism and larval survivorship.
Variable | Value | Location | Source |
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Emergence timing | early July to early September | Ontario |
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July to September | Ontario |
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early July to early September | NY & PA |
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June to October | NY & PA |
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July to October | NY, PA, VT | This study | |
Development time | 4.1% required more than 1 year | Ontario |
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0.8% larvae remaining after year 1 | central NY |
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4% larvae remaining after year 1 | NY & PA |
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1.5–26.7% required > 1 year | NY & PA |
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10.4% required 2 years | NY, PA, VT | This study | |
Sex ratio | 20.6% ♀ | central NY |
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~ 25% ♀ | Ontario |
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27% ♀ | central NY |
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variable; 13.7% - > 60% ♀ | Ontario |
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25% ♀ | NY, PA, VT | This study | |
Body Size | pronotum width 3.2 mm (parasitized), 3.5 mm (non-parasitized) | NY & PA |
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pronotum width ♀ 3.2 mm, ♂ 2.2 mm | Ontario |
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♀ prothorax 3.9 mm (non-parasitized) | NY & PA |
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♀ body 19.7 mm; prothorax 2.6 mm; head capsule 2.8 mm | NY, PA, VT | This study | |
Fecundity | Average No. eggs: 79.6 (parasitized), 108.3 (non-parasitized) | NY&PA |
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No. eggs = 69∙(pronotum width in mm)-96 | Ontario |
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No. eggs = 0.17∙(body length in mm)2.072 | NY, PA, VT | This study | |
Ibalia leucospoides parasitism | 21% | central NY |
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10.6% P. sylvestris, 10.8% P. resinosa | NY |
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20.8% | Ontario |
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18% | central NY |
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3.4–17% | Ontario |
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13% | NY & PA |
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0–46% | Ontario |
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20% | NY, PA, VT | This study | |
Rhyssine parasitism | 1% | central NY |
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4.4% P. resinosa, 8.3% P. sylvestris | NY |
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3% | Ontario |
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10% | central NY |
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12% | NY & PA |
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0–6% | Ontario |
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3.5% | NY, PA, VT | This study | |
Total hymenopteran parasitism | 21.8% | Central NY |
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16.4% | NY |
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23.4% | Ontario |
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41.2% | NY & PA |
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1–50% range | Ontario |
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23.4% | NY, PA, VT | This study | |
Deladenus parasitism | 38% of ♀, no sterilization | Ontario |
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0.2–3% in larvae | central NY |
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27.9% all individuals | NY & PA |
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23.7% all individuals | NY & PA |
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32–64% of ♀, 23–62% of ♂ | Ontario |
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23.6% of ♀; higher in P. sylvestris than P. resinosa | NY |
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62% | NY, PA, VT | This study | |
Survivorship (egg to adult) | ~ 1–14% larval survivorship | Ontario |
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30% larval mortality within tree | NY |
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~ 5% | Ontario |
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28% | NY, PA, VT | This study |
We collected S. noctilio in New York, Pennsylvania and Vermont in 2013, 2014 and 2015. We searched for stands of hard pines (P. resinosa and P. sylvestris) during spring and summer, noting the locations of trees with emergence holes and resin drippings indicating S. noctilio attack in the previous season. Trees attacked by S. noctilio were difficult to find, with > 80% of stands showing no signs of woodwasp presence. In total, we located active S. noctilio populations in six locations in New York (MF: Montour Falls, Schuyler County, 42.3354°N, 76.8138°W), Pennsylvania (DE: Delmar, Tioga County, 41.7209°N, 77.3772°W; MI: Middlebury, Tioga County, 41.8416°N, 77.4072°W, BL: State Game Lands 276 in Blacklick, Indiana County, 40.4886°N, 79.1070°W; CL: Clarion County, 41.1777°N, 79.2269°W) and Vermont (UN: Underhill, Chittenden County, 44.4847°N, 72.9656°W) across three years. As is common in the region, most sites primarily contained one tree species: three stands contained P. sylvestris only (MF, DE, MI), two stands contained P. resinosa only (BL, CL) and one stand contained both (UN), though P. resinosa was more abundant (Table
Summary of trees and emerging insects sampled in each year of study. Number of trees sampled and number of native Sirex nigricornis, non-native S. noctilio and Sirex spp. parasitoids (Ibalia leucospoides and the rhyssines) collected from each tree species, at each site, across sampling years.
Year | State | County | No. trees | Tree Species | No. Sirex noctilio | No. Sirex nigricornis | No. Ibalia leucospoides | No. rhyssines |
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2013 | NY | MF | 3 | P. sylvestris | 1 | 0 | 0 | 0 |
PA | DE | 8 | P. sylvestris | 170 | 0 | 74 | 4 | |
PA | MI | 3 | P. sylvestris | 0 | 0 | 0 | 0 | |
VT | UN | 4 | P. resinosa | 71 | 68 | 0 | 30 | |
2014 | PA | DE | 8 | P. sylvestris | 499 | 0 | 96 | 12 |
VT | UN | 1 | P. sylvestris | 2 | 9 | 0 | 1 | |
VT | UN | 2 | P. resinosa | 77 | 66 | 2 | 16 | |
2015 | PA | BL | 4 | P. resinosa | 41 | 0 | 0 | 0 |
PA | CL | 5 | P. resinosa | 130 | 0 | 67 | 3 | |
Total | 38 | 991 | 143 | 239 | 66 |
During late June or early July 2014–2016, we visited previously-identified sites to cut trees attacked in the prior season. All trees were dead or dying at the time of cutting. Over three years, we felled 38 attacked trees, recording GPS locations and diameter at breast height (dbh) for each. After felling, we cut each stem into ~ 1 m-long bolts, discarding the top of the tree (diameter < ~ 2 cm). Bolts were labeled individually to record their position relative to the ground and transported to emergence containers at Dartmouth College, Hanover, NH.
Wasp-infested logs were placed in 55-gallon laminated cardboard emergence drums and stored indoors (ambient laboratory temperature ~ 21 °C). Drum openings were covered with fine mesh to prevent insect escape. Drums were checked every 1–3 days during peak emergence (mid-July to September) and at least twice a week thereafter until several weeks had passed with no new emergences (late October or early November). At the end of the first emergence season, we removed dead insects, then stored bolts in the laboratory until the following May, at which point we resumed regular checks. All emerging insects were collected, including S. noctilio, the native S. nigricornis and hymenopteran parasitoids. Due to low overall numbers, rhyssine parasitoids (R. persuasoria and R. lineolata) and kleptoparasitoids Pseudorhyssa spp. were combined for analysis and referred to as “rhyssines”. For S. noctilio and S. nigricornis, we measured body length (excluding the ovipositor), then dissected each individual to check for nematodes. Nematodes from a subset of wasps were cultured and confirmed as D. siricidicola when they were sequenced as part of a study by
Collected bolts were weighed and measured for length and diameter at each end. For each bolt, we calculated the surface area and volume from length and diameter. Before we placed them in emergence drums, we measured wood moisture content at five locations along each bolt (~ 0.8 cm depth) using a Delmhorst RDM-3 moisture meter (Delmhorst Instrument Co., Towaco NJ) and averaged these measurements for analysis. Occasional measurements above or below the operating range of the device (6–60%) were recorded as 6% and 60%, respectively.
After insects finished emerging in the second year (at least two months with no further emergence), we dissected a subset of bolts (2–3 per tree). We counted resin drippings and emergence holes, then removed the bark and cambium to count oviposition sites (attacks) and the number of holes (drills) per attack using an illuminated tabletop magnifier (5×) and hand lens (10×–20×) as needed, following methods established by
For each bolt, we estimated the number of eggs laid, based on the number of attacks and drills per attack following
# eggs = 0.01∙single drills + 0.68∙double drills + 1.55∙triple drills + 2.22∙quadruple drills
After dissection, we cut each bolt into three equal lengths (avoiding knots) to expose fresh surfaces. We estimated the percentage of the cross-sectional area colonized by bluestain (ophiostomatoid) fungi by outlining visible bluestain on the cut surface of each bolt and photographing the surface (see Suppl. material
For analyses of S. noctilio body size, egg number and allometric equation development, we incorporated additional data from 1,511 emerging S. noctilio, collected from 53 trees sampled in central NY in 2008; hereafter referred to as the “Central NY data set” (see
To compare egg sizes between the USA and Spain, we also measured eggs from S. noctilio collected emerging from bolts in Galicia, Spain in 2013–2015, as described in
Data analysis was conducted in JMP Pro 13.0 (
We used Maximum Likelihood to estimate the number of wasps emerging per tree, number of insects emerging per bolt and the number of nematodes per parasitized S. noctilio adult. For each of these metrics, we evaluated four candidate distributions and compared them via log-likelihood: Poisson, zero-inflated Poisson, negative binomial and zero-inflated negative binomial (R package VGAM;
We used Chi-square statistics to test for differences in: voltinism between male and female wasps; sex ratio between pine species and across sites; and nematode parasitism among tree species, sites and wasps of different sexes. We used restricted Maximum Likelihood generalized linear mixed models (R package lme4;
We used simple linear regression to test for a relationship between emergence date and body size, analyzing insects emerging from the P. resinosa and P. sylvestris separately. The impacts of sex and tree species on insect body size were examined using 2-way ANOVA with an interaction term. To describe the relationship between body size and S. noctilio egg number, we used the nls function in the R base package to fit a power function to our egg count data from dissected females, then tested for effects of tree species and voltinism on egg number by analyzing the residuals.
Parasitism rates were estimated as the slope of the regression line (with forced intercept = 0) of numbers of emerging parasitoids versus numbers of all emerging insects (siricids plus parasitoids) (
To examine relationships between bolt traits and measures of insect attack and emergence, we generated a matrix of Pearson Correlation Coefficients using all complete pairwise observations, then visualized them with the R package corrplot (
We collected 1007 S. noctilio (253 females and 754 males) over three years from 38 trees harvested in New York, Pennsylvania and Vermont (Table
The sex ratio of emerging S. noctilio was male biased 1:2.98 ♀:♂. Voltinism influenced sex ratios, with insects emerging in one year having a sex ratio of 1:3.5 ♀:♂ and females dominating in year 2, with 1:0.90 ♀:♂. Sex ratio also varied across sites, with the lowest proportion of males in a P. resinosa stand (Blacklick, Pennsylvania) and the highest at a P. sylvestris stand (Delmar, Pennsylvania; 0.32 vs. 0.83; χ2 = 59.43, df = 4, p < 0.0001). Although both of these sites are in Pennsylvania, the time since the stands had first become infested appeared to differ: S. noctilio had likely recently arrived to Blacklick, while a population was established in the area around Delmar since at least 2008 (
Sirex noctilio body length ranged from 6–37 mm, with an average length of 15.66 ± 0.16 mm. Females (n = 251, 19.67 ± 0.31 mm) were larger than males (n = 752, 14.32 ± 0.15 mm) (t = 15.40, df = 369.63, p < 0.0001; Fig.
Number of eggs per female ranged from 5 to 284. Number of eggs was positively related to body size and well described by a power function where number of eggs = 0.17∙(BodyLength)2.072 (Fig.
Dissection of 76 bolts from 24 trees (10 P. radiata and 14 P. sylvestris) yielded 11,253 attacks comprising 16,604 oviposition drill holes. Attack density was higher in P. sylvestris than in P. resinosa (8.83 ± 1.29 vs. 5.28 ± 1.72 attacks/dm2; F1,51.72 = 4.43, p = 0.04). The number of drills per attack ranged from 1 to 6, distributed as follows: 64% were single drills, 27% doubles, 8% triples and 1% four or more. The number of drills per attack was slightly higher on average for P. resinosa (1.62 ± 0.01) than for P. sylvestris (1.38 ± 0.01) (Fig.
Emergence of adult wasps was concentrated in a relatively small number of bolts and was best described by a zero-inflated negative binomial (ZINB) distribution with parameters Φ = 0.24, µ = 20.43 and k = 0.85. For both tree species, emergence was — as expected — positively correlated (r = 0.36 - 0.79) with attacks, attack density, drills, drill density, drills per attack, estimated number of eggs laid and the estimated density of eggs laid, most of which were correlated with each other (Suppl. material
Emergence per attack was higher for P. sylvestris (0.11 ± 0.01) than P. resinosa (0.08 ± 0.01) (Fig.
Sirex noctilio emergence success. Emergence per attack for Pinus resinosa (A slope = 0.08 ± 0.01) and P. sylvestris (B slope = 0.11 ± 0.01) and emergence per estimated number of eggs laid for P. resinosa (C slope = 0.16 ± 0.02) and P. sylvestris (D slope = 0.41 ± 0.04). Each point represents one bolt.
A total of 143 native S. nigricornis co-occurred with S. noctilio in our trees, but emergence of this native siricid was concentrated in three trees from one site (Table
Of the 806 S. noctilio assessed for nematode parasitism, 62% contained nematodes in gonadal tissue, with no difference between sexes (χ2 = 0.25, df = 1, p = 0.62). We found no instances of nematodes within S. noctilio eggs. Wasps emerging in the first year were more likely to be parasitized (63.52%) than those emerging in year two (13.64%) (χ2 = 22.64, df = 1, p < 0.0001). Among wasps emerging in year one, non-parasitized females were larger than parasitized females (22.03 ± 0.62 mm vs. 17.60 ± 0.49 mm; t = 5.58, df = 158, p < 0.0001) with the same pattern seen in males (t = 4.75, df = 644, p < 0.0001). Females also had smaller eggs in the presence of nematodes (t = 3.17, df = 21.98, p = 0.004). Adult woodwasps that emerged from P. sylvestris were much more likely to be parasitized by D. siricidicola than those that emerged from P. resinosa (81.3% vs. 5.15%; χ2 = 363.85, df = 1, p < 0.0001), but species and location were confounded (Table
We constructed simple demographic models of S. noctilio in the northeastern USA, reporting study-wide values in addition to separate values for insects colonizing the two pine species in the study, P. resinosa and P. sylvestris (Table
Demographic parameters for Sirex noctilio in Spain and the USA. Overall values for North America are shown, as well as separate values for Pinus resinosa and P. sylvestris. All data from Spain come from P. pinaster. Percent change in lambda (% Δ λ) is the percent change in USA λ when the Spain value for each row is substituted for the USA value. It indicates the relative impact of each of demographic factor on λ. Spanish values are adapted from Table
Spain | North America | North America by Species | |||||
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P. resinosa | P. sylvestris | ||||||
Parameter | Parameter | % Δ λ | Parameter | % Δ λ | Parameter | % Δ λ | |
Eggs/♀1 | 58 | 78 | -26 | 102 | -43 | 66 | -12 |
Nematode escape | 0.64 | 1 | -36 | 1 | -36 | 1 | -36 |
Emergence/viable egg2 | 0.2 | 0.28 | -28 | 0.16 | 27 | 0.41 | -51 |
Hymenopteran escape | 0.8 | 0.77 | 4 | 0.77 | 4 | 0.77 | 4 |
Proportion female | 0.26 | 0.25 | 4 | 0.36 | -28 | 0.2 | 30 |
♀/♀ (λ) | 1.57 | 4.20 | -63 | 4.52 | -65 | 4.17 | -62 |
Non-native S. noctilio populations in North America showed a higher potential for population growth than native populations in Galicia, Spain (Table
Our results broaden the evidence of remarkably high body size variation for S. noctilio, consistent with reports of an 8–38 mm range in length from the native range (
High variation in woodwasp body size could also reflect genetic differences among wasps and complex selective landscapes that favor large insects in some instances, but not in others. Long feeding galleries necessary to produce large adults may be more feasible in large trees than small trees. Large males may have difficulties mating with small females (
The fecundity of North American S. noctilio is higher than in Spain, but this is not driven by differences in body size. An average-sized female in our sample (19.67 mm long) had ~ 78 eggs. Although Spanish S. noctilio, measured by
At a population level, observed male-biased sex ratios were similar to those previously reported in North America (see Table
Host choice and oviposition behavior influence the success of S. noctilio in new landscapes. In our study, 64% of total attacks involved only a single drill. Single drills are thought to indicate rejection of the oviposition site (since eggs are rarely placed), perhaps as a consequence of the detection of suboptimal moisture levels and/or oleoresin pressure for fungal establishment, egg survival or larval success (
The fate of larvae inside host trees strongly influenced reproductive potential in both US and Spanish S. noctilio populations. This is consistent with past studies that have highlighted the role of host resistance in limiting S. noctilio reproduction and spread (
Spanish woodwasp populations experience consistent top-down control by nematodes via sterilization of ~ 90% of the eggs in 39% of females (
Our finding that nematode parasitism dropped to under 14% for larvae that took two years to develop supports the hypothesis that delayed development can help woodwasps evade parasitism (
Hymenopteran parasitoids exerted a moderate top-down influence on North America S. noctilio, reducing the number of progeny by ~ 20%, which is within the range of reports from other studies in North America (~ 1–50%; Table
The presence of native pines, native siricids and native siricid parasitoids in North America may confer some biotic resistance to invasion by S. noctilio (
All hard pine species in North America are potentially susceptible to S. noctilio (
More broadly, a comprehensive comparison of the population demography of Northern and Southern Hemisphere S. noctilio would help us better elucidate the importance of specific controls on S. noctilio populations and improve understanding of variable tree species susceptibility. Such studies would also help clarify the importance of landscape-level patterns in resource availability in determining woodwasp population growth rates. Current and future population models would also be improved by better understanding and incorporating density-dependent feedbacks in the demographics.
The authors thank USDA Forest Service International Programs for funding the project: International Comparison of Sirex. AML acknowledges funding from grant EVA4.0, No. CZ.02.1.01/0.0/0.0/16_019/0000803 from OP RDE.
Tables S1, S2, Figures S1–S4
Data type: Text, tables and figures (docx. file)
Explanation note: This file includes demographic data from native Sirex nigricornis woodwasps that were collected during our study. Table S1. Correlation matrix of bolt-level variables for P. resinosa and P. sylvestris. Table S2. Review of 10th and 90th percentile female body mass from insect species estimated from source paper cited, showing comparatively higher female S. noctilio body size variation. Figure S1. Examples of S. noctilio oviposition sites, lesion formation and emergence holes in the field. Figure S2. Top panels show a typical bolt from P. sylvestris with bark removed and S. noctilio emergence holes and oviposition sites identified. Figure S3. The number of S. noctilio emerging per tree was best described by a zero inflated negative binomial distribution (dotted line) with proportion of excess zeroes Φ = 0.32, µ = 75.39 and overdispersion parameter k = 0.35. Figure S4. Allometric relationships for S. noctilio in the Central NY data set: number of eggs and adult female mass (a; quantile regression), adult female mass and adult female length (b; fitted power function) and adult length and width of adult head capsule (c; linear regression).