Research Article |
Corresponding author: Ann E. Hajek ( aeh4@cornell.edu ) Academic editor: Jianghua Sun
© 2023 Saskya van Nouhuys, David C. Harris, Ann E. Hajek.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
van Nouhuys S, Harris DC, Hajek AE (2023) Population level interactions between an invasive woodwasp, an invasive nematode and a community of native parasitoids. NeoBiota 82: 67-88. https://doi.org/10.3897/neobiota.82.96599
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Parasitic nematodes and hymenopteran parasitoids have been introduced and used extensively to control invasive Eurasian Sirex noctilio woodwasps in pine plantations in the Southern Hemisphere where no members of this community are native. Sirex noctilio has more recently invaded North America where Sirex-associated communities are native. Sirex noctilio and its parasitic nematode, Deladenus siricidicola, plus six native hymenopteran woodwasp parasitoids in New York and Pennsylvania, were sampled from 204 pines in 2011–2019. Sirex noctilio had become the most common woodwasp in this region and the native parasitoids associated with the native woodwasps had expanded their host ranges to use this invader. We investigated the distributions of these species among occupied trees and the interactions between S. noctilio and natural enemies as well as among the natural enemies. Sirex noctilio were strongly aggregated, with a few of the occupied trees hosting hundreds of woodwasps. Nematode parasitism was positively associated with S. noctilio density, and negatively associated with the density of rhyssine parasitoids. Parasitism by the parasitoid Ibalia leucospoides was positively associated with host (S. noctilio) density, while parasitism by the rhyssine parasitoids was negatively associated with density of S. noctilio. Thus, most S. noctilio come from a few attacked trees in a forest, and S. noctilio from those high-density trees experienced high parasitism by both the invasive nematode and the most abundant native parasitoid, I. l. ensiger. There is little evidence for direct competition between the nematodes and parasitoids. The negative association occurring between rhyssine parasitoids and I. l. ensiger suggests rhyssines may suffer from competition with I. l. ensiger which parasitize the host at an earlier life stage. In addition to direct competition with the native woodwasp Sirex nigricornis for suitable larval habitat within weakened trees, the large S. noctilio population increases the parasitoid and nematode populations, which may increase parasitism of S. nigricornis.
Aggregation, co-infection, competition, Deladenus, density dependence, forest pest, Ibalia, parasite community, pine, Rhyssa, Sirex noctilio, spillback
In any community there are multiple parasite species simultaneously associated with any host species (
Invasive species may act as consumers, competitors, hosts to existing parasites, and as parasites of existing hosts. The introduced species may have a greater prevalence than in their native range (
Larvae of the Eurasian woodwasp Sirex noctilio (Siricidae) develop in the xylem of pine trees in association with a symbiotic white rot fungus, Amylostereum areolatum, that assists in slowly killing attacked trees and acting as an external rumen for larvae (
Members of the North American Sirex community associated with Pinus in this study, made up of invasive and native species and their origins. Invasives are listed in bold.
Species | Origin |
---|---|
Woodwasps (Siricidae) | |
Sirex noctilio | Eurasia |
Sirex nigricornis | Eastern North America |
Parasitoids (Hymenoptera) | |
Ibaliidae | |
Ibalia leucospoides ensiger | Eastern North America |
Ichneumonidae | |
Rhyssa lineolata | Eastern North America |
Rhyssa persuasoria | Eastern North America |
Rhyssa crevieri | Eastern North America |
Megarhyssa nortoni | Eastern North America |
Pseudorhyssa nigricornis | Eastern North America |
Parasite (Nematoda) | |
Neotylenchidae | |
Deladenus siricidicola INA | Eurasia (not North America) |
Sirex symbiont/Deladenus food (Fungus) | |
Russulales | |
Amylostereum areolatum | North America + Eurasia |
The community of parasitoids associated with S. noctilio and S. nigricornis in eastern North America is composed of up to six native hymenopteran species. Ibalia leucospoides ensiger (Ibaliidae) parasitizes eggs/early instars and is almost always the most common species. Four species of rhyssines (Ichneumonidae) parasitize later larval instars, and Pseudorhyssa nigricornis (also Ichneumonidae) is a kleptoparasitoid attacking the rhyssines (
The dimorphic nematode, Deladenus siricidicola, is also a parasite of S. noctilio. The impact of nematodes on host woodwasps is determined by both nematode and woodwasp species and genotypes (
Invasive S. noctilio in northeastern North America is therefore attacked by numerous species of native parasitoids as well as an introduced parasitic nematode (Table
Our overall goal in this study was to investigate relations among the parasitic nematode, the native parasitoid community, and the invasive host woodwasp in naturally occurring attacked trees. We evaluated emergence from 204 S. noctilio-infested trees from multiple forested areas in northeastern North America between 2011 and 2019. We tested the hypotheses that S. noctilio aggregate within a few of the infested trees in a stand, and that the natural enemies would each respond positively to host density. Further, since the natural enemies co-occur but cannot all successfully infect the same host individuals, there would be negative associations among them where their densities were high enough for competition to occur. Given the patterns of tree infestation and parasitism that we found, we discuss likely consequences to populations of the native woodwasp S. nigricornis from invasion of this community by S. noctilio. Results from this study will improve our understanding of population level interactions in mixed invasive and native communities, as well as the ecology of this host/parasite community, as the invasive host continues to expand its range in North America.
Between 2010 and 2018, 204 S. noctilio-infested pines were identified at sites where active infestations of S. noctilio were known or hypothesized to be present in pine forests at 21 sites in New York and Pennsylvania, USA (Table
Localities of collections of Sirex-infested trees in New York state and Pennsylvania.
Year | State | County | Site* | Pinus species | GPS | No. trees |
---|---|---|---|---|---|---|
2011 | New York | Schuyler | Arnot Forest | P. sylvestris | 42.26445, -76.62757 | 2 |
2011 | Pennsylvania | Tioga | TSF: Government Rd | P. resinosa | 41.65038, -76.92572 | 9 |
2011 | Pennsylvania | Tioga | TSF: Mountain Ridge Rd | P. resinosa | 41.74501, -76.94507 | 6 |
2011 | New York | Cortland | Heiberg Forest | P. resinosa | 42.76094, -76.08341 | 2 |
2011 | New York | Tompkins | Waterburg Rd | P. resinosa | 42.49939, -76.67325 | 3 |
2011 | New York | Broome | Triangle | P. resinosa | 42.34022, -75.88022 | 1 |
2012 | New York | Schuyler | Arnot Forest | P. resinosa | 42.26445, -76.62757 | 9 |
2012 | New York | Tompkins | Danby | P. sylvestris | 42.37903, -76.47251 | 1 |
2012 | New York | Steuben | Cameron State Forest | P. resinosa | 42.26578, -77.41622 | 1 |
2012 | New York | Schuyler | Finger Lakes National Forest | P. resinosa | 42.47374, -76.77994 | 3 |
2012 | New York | Warren | Nr. Pack Forest | P. resinosa | 43.51550, -73.81478 | 6 |
2012 | Pennsylvania | Tioga | TSF: Government Rd | P. resinosa | 41.65038, -76.92572 | 14 |
2012 | Pennsylvania | Tioga | Hills Creek State Park | P. resinosa | 41.85348, -77.19989 | 11 |
2012 | Pennsylvania | Tioga | TSF: Hypocrite Trail | P. resinosa | 41.67096, -76.92317 | 18 |
2012 | Pennsylvania | Tioga | Leonard Harrison State Park | P. resinosa | 41.69646, -77.45460 | 5 |
2013 | Pennsylvania | Tioga | TSF: Hypocrite Trail | P. resinosa | 41.67096, -76.92317 | 12 |
2013 | Pennsylvania | Tioga | Hills Creek State Park | P. resinosa | 41.85348, -77.19989 | 5 |
2013 | Pennsylvania | Tioga | Leonard Harrison State Park | P. resinosa | 41.69646, -77.45460 | 2 |
2014 | New York | Schuyler | Arnot Forest | P. resinosa | 42.28194, -76.63138 | 2 |
2014 | Pennsylvania | Tioga | Hills Creek State Park | P. resinosa | 41.85348, -77.19989 | 26 |
2014 | New York | Cortland | Hewitt State Forest | P. resinosa | 42.74353, -76.22174 | 2 |
2015 | Pennsylvania | Tioga | TSF: Arnot Forest | P. resinosa | 41.67380, -77.14184 | 4 |
2015 | New York | Schuyler | Arnot Forest | P. resinosa | 42.28194, -76.63138 | 1 |
2015 | Pennsylvania | Tioga | TSF: Fellows Creek | P. resinosa | 41.69965, -76.96671 | 5 |
2015 | Pennsylvania | Tioga | Hills Creek State Park | P. resinosa | 41.85348, -77.19989 | 13 |
2015 | Pennsylvania | Tioga | Ridge Road | P. resinosa | 41.67589,-76.95881 | 1 |
2015 | New York | Oneida | Sand Flats State Forest | P. sylvestris | 43.55212, -75.27708 | 3 |
2015 | Pennsylvania | Tioga | TSF: Tanglewood | P. resinosa | 41.71145, -76.98356 | 4 |
2016 | Pennsylvania | Tioga | TSF: Hypocrite Trail | P. resinosa | 41.67096, -76.92317 | 3 |
2017 | Pennsylvania | Clarion | Corsica | P. sylvestris | 41.17809, -79.22653 | 10 |
2017 | Pennsylvania | Indiana | Hillsdale | P. resinosa | 40.75009, -78.88494 | 10 |
2017 | Pennsylvania | Tioga | TSF: Hypocrite Trail | P. resinosa | 41.67096, -76.92317 | 3 |
2019 | Pennsylvania | Tioga | TSF: Government Rd. | P. resinosa | 41.65038, -76.92572 | 3 |
2019 | Pennsylvania | Tioga | TSF: Hypocrite Trail | P. resinosa | 41.67096, -76.92317 | 4 |
Sirex and parasitoid adults that emerged were kept individually in vials at 4 °C. Sirex noctilio and S. nigricornis were identified using
To evaluate nematode parasitism, subsamples of S. noctilio from each site and year were dissected as described in
Sirex density was quantified as all of the emerged Sirex plus each emerging Sirex parasitoid, as each parasitoid is solitary, representing one host individual. The native woodwasp S. nigricornis emerged from 25 of the 204 trees in five of the eight years. From 22 of these trees, S. noctilio emerged as well, usually in much higher quantities than S. nigricornis. From the remaining three trees only S. nigricornis emerged. As S. noctilio had emerged from other trees from those sites sampled throughout the same years and the parasitoids use both Sirex species as hosts (
All statistical analyses were done using JMP (
For the analysis of the association of nematode infection with per tree Sirex density and rate of parasitism by parasitoids we used logistic regression. The response variable was the presence/absence of nematodes in each of the 3154 S. noctilio dissected to detect nematodes. The samples collected from 2012 were not included because very few S. noctilio were dissected that year. The explanatory variables were year, site nested in year where sites were sampled across multiple years, the log of the number of Sirex in the tree the sample came from, the fraction of hosts parasitized by I. l. ensiger and by the combined rhyssine parasitoids in that tree, and interactions between the host and each parasitoid, and between I. l. ensiger and the combined rhyssines. Interactions that did not contribute to the model were removed. Because the number of wasps (Sirex + parasitoids) per tree ranged widely (from 1 to 864), with many trees occupied by few wasps, the number of wasps was log-transformed. Because the different parasitoids may have different patterns of parasitism and potential associations with the nematode, we separated I. l. ensiger and the combined rhyssine parasitoids.
For the analysis of association of parasitism by parasitoids with woodwasp density at the tree level, we used logistic regression with the full data set of all 204 trees that wasps emerged from over all eight years. Three separate models were tested. The binomial response variable in the first was whether a sample was a parasitoid or Sirex. In the second model the response variable was whether the sample was I. l. ensiger or not (if not I. l. ensiger it could be a Sirex or a rhyssine). In the third model the response variable was whether the sample was a rhyssine or not (if not a rhyssine it could be Sirex or I. l. ensiger). The explanatory variables in all three models included year, site nested in year, and the log of the number of Sirex in the tree the sample came from (host density). Since each parasitoid can have an independent relationship to host density, in the model for total parasitism the per tree rates of parasitism by I. l. ensiger and rhyssines, as well as their interactions with host density, were included as explanatory variables. The model for I. l. ensiger included the per tree rate of parasitism by rhyssines, and its interaction with host density as response variables. The model for rhyssines included per tree rate of parasitism by I. l. ensiger, as well as the interaction of I. l. ensiger parasitism and host density as response variables.
Between 2011 and 2019, S. noctilio and their parasitoids were reared from 204 S. noctilio-infested trees from Pennsylvania and New York State (Table
The distribution of Sirex equivalents (Sirex adults + parasitoid adults) emerging from trees in the whole data set. The inset shows the distribution of Sirex equivalents among the same number of trees if the Sirex were distributed randomly among trees (a Poisson distribution). The * indicates the mean number of wasps per tree (48.3). The number of wasps along the x-axis is shown in a modified log scale in order to make both small and large numbers of wasps per tree visible.
The distribution of Sirex equivalents (Sirex adults + parasitoid adults) emerging from the 6 sites with the most data (each had 398 or more Sirex equivalents and nine or more trees). The wasps were strongly aggregated in these and the other 6 sites tested (see text). * denotes the mean number of Sirex equivalents per tree. The horizontal gray bars represent the 95% CI range of wasps per tree if the Sirex were distributed randomly among the trees, which would be a Poisson distribution (as shown in the inset in Fig.
Overall, 39% of the Sirex were parasitized by parasitoids. The most abundant parasitoid species was I. l. ensiger, which comprised 81% of the parasitoids reared and was found at every site. Next most abundant was Rhyssa lineolata, which made up 63% of the rhyssines (leaving out samples from 2012 when rhyssine species were not separated, Suppl. material
Nematodes were found in 11% of the dissected S. noctilio. The proportion of nematode-parasitized hosts in a tree was positively associated with host density (χ2 = 4.92; P = 0.0265; Table
Results of the logistic regression analyses of a) nematode parasitism, and parasitism by b) all parasitoids, c) I. l. ensiger, and d) rhyssines. See text for details of models.
Parameter | df | Estimate(SE) | χ2 | P > χ2 | Odds ratio | Effects likelihood ratio χ2 | P > χ2 |
---|---|---|---|---|---|---|---|
a) Nematodes | |||||||
Year | 6 | multiple | 166.04 | <0.0001 | |||
Site (Year) | 20 | multiple | 329.13 | <0.0001 | |||
Host density* | 1 | 0.23(0.10) | 4.72 | 0.0298 | 1.26 | 4.92 | 0.0265 |
Rhyssines rate** | 1 | -5.81(1.14) | 26.15 | <0.0001 | 0.01 | 31.57 | <0.0001 |
Rhyssines rate × host density | 1 | 5.05(1.20) | 17.66 | <0.0001 | 21.67 | <0.0001 | |
I. l. ensiger rate | 1 | -0.04(0.58) | 0.00 | 0.9460 | 0.97 | 0.004 | 0.9460 |
b) All parasitoid wasps | |||||||
Year | 7 | multiple | 1.25 | 0.9898 | |||
Site (Year) | 26 | multiple | 13.48 | 0.9793 | |||
Host density | 1 | -0.002(0.03) | 0.00 | 0.9522 | 0.99 | 0.003 | 0.9522 |
I. l. ensiger rate | 1 | 4.62(0.26) | 321.88 | <0.0001 | 101.72 | 348.39 | <0.0001 |
I. l. ensiger rate × host density | 1 | -0.29(0.16) | 3.21 | 0.0734 | 3.34 | 0.0674 | |
Rhyssines rate | 1 | 4.65(0.26) | 283.23 | <0.0001 | 105.37 | 316.39 | <0.0001 |
Rhyssines rate × I. l. ensiger rate | 1 | -3.29(1.31) | 6.30 | 0.0121 | 6.46 | 0.0110 | |
c) I. l. ensiger | |||||||
Year | 7 | multiple | 17.68 | 0.0135 | |||
Site (Year) | 26 | multiple | 211.78 | <0.0001 | |||
Host density | 1 | 0.18(0.03) | 30.51 | <0.0001 | 1.19 | 31.88 | <0.0001 |
Rhyssines rate | 1 | 0.42(0.24) | 3.07 | 0.0797 | 1.51 | 3.04 | 0.0813 |
Rhyssines rate × host density | 1 | 1.16(0.16) | 53.44 | <0.0001 | 62.39 | <0.0001 | |
d) Rhyssines | |||||||
Year | 7 | multiple | 422.98 | <0.0001 | |||
Site (Year) | 26 | multiple | 256.20 | <0.0001 | |||
Host density | 1 | -0.22(0.59) | 13.52 | 0.0002 | 0.80 | 12.60 | 0.0004 |
I. l. ensiger rate | 1 | 0.71(0.41) | 3.00 | 0.0830 | 2.04 | 3.00 | 0.0832 |
I. l. ensiger rate × host density | 1 | 1.92(0.23) | 72.32 | <0.0001 | 82.44 | <0.0001 |
The association of parasitism by the nematode Deladenus siricidicola with a per tree Sirex density (Logistic regression model coefficient P < 0.026; Table
The proportions of dissected S. noctilio parasitized by D. siricidicola at each site between 2011 and 2019. Sites with fewer than 10 dissected S. noctilio are excluded as well as all sites from 2012.
Overall parasitism by parasitoids was unrelated to tree-level host density (χ2 = 0.003; P = 0.9522; Table
The association of parasitism by parasitoids with tree level host density. The curves show the logistic fit for a I. l. ensiger (P < 0.0001; Table
The invading S. noctilio exhibited very strong aggregation in specific trees within a stand, with up to 854 Sirex equivalents emerging from one tree and few S. noctilio emerging from the majority of infested trees (Figs
Generally, aggregated resource use can result from variation of resource quality (
The nematode D. siricidicola was present in 11% of the S. noctilio which is less than reports from many smaller studies in North America (see
Nematodes may parasitize a woodwasp before or after it has been parasitized by a wasp. Once within a shared host, nematodes could, in principle, move from the woodwasp larva to a parasitoid larva. However, the nematode D. siricidicola is specific to Sirex as well as parasitizing a wood-dwelling genus of beetle associated with siricids (Serropalpus) (
Further, the nematode D. siricidicola cannot successfully develop in or be vectored by a Sirex parasitized by a parasitoid because the host is killed by the parasitoid. While the nematodes would not succeed in such a shared host, parasitoids likely can develop in Sirex larvae that are also parasitized by nematodes. There may be a cost to parasitoids due to reduced host size since nematode-parasitized Sirex are somewhat smaller than unparasitized individuals (
The observed negative association of nematode parasitism with rhyssines may simply be because the nematodes are strongly positively host density dependent, so they are nearly absent from trees with low host density, which are the ones in which parasitism by rhyssines was highest. Alternatively, competition between nematodes and rhyssines at low host densities may decrease the number of nematode-infected Sirex, contributing to the pattern of host density dependence of the nematodes. While such competition may contribute to the pattern, it is not the full explanation because at low host density nematode parasitism is near 0 (Fig.
Both the nematode and the abundant parasitoid I. l. ensiger increase with host density within trees. Yet there is no evidence of direct competition, since even accounting for host density, high I. l. ensiger density was not associated with lower prevalence of nematodes. This suggests that there could be some spatial segregation of host use. For example, I. l. ensiger, which have short ovipositors, have been found to be most abundant high up in trees where bark is thinner (
The native community of parasitoids that were present in the northeastern US before invasion by S. noctilio readily use S. noctilio as a host. On average, 37% of the Sirex from a tree was parasitized, ranging from 0 to 100%. This overall parasitism is similar to what was found by
The rhyssine species showed higher parasitism at low host density. If parasitoids do not respond to host density the fraction parasitized can appear higher at very low host density than at high host density, simply reflecting the population size of foraging females (
As a caveat, the interactions between parasitoids and S. noctilio is complicated to evaluate due to variable voltinism of both rhyssines and S. noctilio (
In this study the native woodwasp, S. nigricornis occurred at much lower densities than S. noctilio, with the majority emerging early in the study, between 2011 and 2014 (Suppl. material
In summary, this study of invasive S. noctilio and its introduced and native natural enemies emerging from 204 naturally infested trees over eight years, allowed for a robust analysis of the distribution of S. noctilio among trees, and for an exploration of the complex association of host and natural enemies over a large range of natural host densities. We found a strong pattern of aggregation by the woodwasp in a subset of the trees it occupied. Parasitism by the nematode D. siricidicola increased with host density, making its distribution also aggregated. Parasitism by the native woodwasp parasitoid I. l. ensiger was high and also increased with host density, suggesting that this wasp may contribute to the control of the woodwasp. Additionally, though both the nematode and I. l. ensiger were positively host density dependent, there was little evidence of direct competition between the parasitoid and the nematode. The suite of native rhyssine parasitoids of Sirex were less abundant and occurred mostly where host densities were low. While our study indicates that they suffer from competition with I. l. ensiger, their population level relationship with the host and the other parasitoids may be complicated by a variation of voltinism.
We thank Brad Regester, Bill Laubscher, and Sarah Johnson of the Pennsylvania Division of Forest Health for assistance with searching for and felling trees. We thank Cornell’s Arnot Forest and Christopher Foelker, Dylan Parry, and Melissa Fierke of SUNY, ESF for assistance with finding and sampling infested pines. Stefan Long, Stefanie Kroll, Jake Henry, and Chad Keyser as well as many additional people in the Hajek Lab assisted with emergence from wood, identification of parasitoids, and detection of nematodes in Sirex. SvN thanks The Israeli Institute for Advanced Studies for support during writing.
The number of Sirex, nematodes, and parasitoids collected from each site, each year.
Data type: Occurance
Explanation note: Data table showing the number of individuals of each species collected as part of this study.