Research Article |
Corresponding author: Alexandre P. Caouette ( alexandre.caouette@nrcan-rncan.gc.ca ) Academic editor: Alain Roques
© 2024 Alexandre P. Caouette, Claire E. Rutledge, Stephen B. Heard, Deepa S. Pureswaran.
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:
Caouette AP, Rutledge CE, Heard SB, Pureswaran DS (2024) No evidence for pronounced mate-finding Allee effects in the emerald ash borer (Agrilus planipennis Fairmaire). NeoBiota 95: 165-179. https://doi.org/10.3897/neobiota.95.127287
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Allee effects are density-dependent barriers that can impact species establishment and population growth, such as through reduced mating success at low population densities. The emerald ash borer, Agrilus planipennis Fairmaire, has been extremely successful at rapidly expanding its North American range. The impact of mate-finding Allee effects (an important type of component Allee effect) early in the invasion period of the emerald ash borer remains unknown. We measured mating success in females as a function of beetle abundance in Halifax, Canada, where the emerald ash borer was recently discovered, and in Connecticut USA, where it has been established for over a decade. We measured relative population abundance and sampled beetles using different strategies. In Halifax, we placed clusters of prism traps along an invasion gradient of emerald ash borer abundance, and in Connecticut, we collected beetles from foraging Cerceris fumipennis females. We dissected female reproductive tracts to measure mating success. We fit a linear regression to the mating success of females as a function of beetle abundance. We found that emerald ash borer did not present a pronounced mate-finding Allee effect as there was no positive relationship between female mating success and abundance. Lack of pronounced component Allee effects that impede population growth may explain rapid range expansion in species that are highly invasive, such as the emerald ash borer.
Allee effects, emerald ash borer, invasion biology, invasion dynamics, mating success, population ecology
Introduced species must overcome several ecological barriers before establishment and population growth can occur. Such barriers include Allee effects, density-dependent mechanisms that prevent low-density populations from increasing (
An introduced species that has caused widespread ecological and economic damage throughout North America in a relatively short period is the emerald ash borer (hereafter referred to as EAB), Agrilus planipennis Fairmaire (Coleoptera, Buprestidae). It has been introduced from eastern Asia to North America and eastern Europe (
The rapid expansion of EAB in its North American range can be attributed to the movement of ash materials such as saplings, wood chips, and untreated firewood (
Population modelling has shown that EAB could be managed if invading populations were under a strong demographic Allee effect (
We examined the mating success of EAB as a function of beetle abundance in two distinct geographical locations. First, we studied a recently established satellite population in Atlantic Canada. In 2018, EAB were detected in a city park in the northeastern edge of the Halifax Regional Municipality of Nova Scotia. We measured female EAB mating success as a function of male abundance in scattered ash tree clusters along the current EAB range in Halifax, collecting beetles in pheromone-baited traps. Second, we studied a population in Connecticut, USA, about 800 km SW of Halifax. In this case, we measured female EAB mating success in individuals collected as prey by a native wasp and used the proportion of EAB captured by wasps among all beetle prey as a proxy measurement of abundance (
EAB can be distinguished from native North American wood borers (Coleoptera, Buprestidae) by its metallic green coloration and metallic red on the dorsal portion of the abdomen (
We conducted the Nova Scotia study in 2022 using urban street trees and parks in the Halifax regional municipality (44°40'N, 63°36'W). The Bedford Basin, a large, enclosed bay, bisects the Halifax regional municipality. EAB was first detected at Harry DeWolf Park in 2018, at the interior tip of this basin. Halifax is a mid-sized city with a population of approximately 440,000 people and an area of 5,500 km2. Halifax manages approximately 49,000 public trees (
To measure EAB populations, we arranged green (Andermatt Canada Inc., Fredericton, New Brunswick) and purple (WestGreen Global Technologies Inc., Langley, British Columbia) prism traps in clusters of at least four ash trees (Fig.
Emerald ash borer collection in the Halifax Regional Municipality, Nova Scotia. Green circles represent sampled clusters of ash trees. Red star represents the location of the first ash borer detection in the Halifax Regional Municipality. Grey tree icons represent ash trees identified during street tree surveys.
We chose cluster locations based on the availability ash trees on public land and at increasing distances from the initial infestation point, which in other studies has been shown to correlate with decreasing populations sizes (
We measured degree days above 10 °C (DD10) from a weather station monitored by the Government of Canada in Halifax to know when to deploy and finish trap collection. We deployed traps at the beginning of EAB flight on June 3rd, 2022, at approximately 260 (DD10C), and collected them on August 15th, at approximately 745 (DD10C), when flight neared its end. We checked traps weekly, collected all the buprestid beetles into a cooler, then transferred them to a -18 °C freezer until dissection.
We conducted the Connecticut study in 2013–2016 and 2022–2023, using 48 sites across the state ranging from 41.43 to 41.88°N, and from-71.88–73.50°W. Emerald ash borer was first detected in New Haven County, Connecticut, USA in 2012 (
Biosurveillance exploits the buprestid-hunting habit of a native wasp, Cerceris fumipennis (Hymenoptera, Crabronidae). These solitary ground-nesting wasps use paralyzed, adult buprestid beetles to provision their brood cells. Wasps live in aggregations in sandy areas, from which they set out to hunt in the canopy of the surrounding forest. They will target a wide range of genera within the Buprestidae, limited only by prey weight and size relative to the individual female wasp, phenology, and arboreal habit. More than 100 species of beetles have been recorded as prey of C. fumipennis (
We (CER and colleagues) have been conducting biosurveillance across the state since 2010, and all beetles collected have been identified by site and date. Since 2016, all EAB have been frozen and stored after capture, and thus were available for dissection. We selected female EAB for dissection from site/year combinations for which at least 30 beetles had been collected. This ensures that the estimate of relative abundance of EAB at that site was robust.
For beetles captured in the prism traps, we cleaned glue residue from collected beetles using limonene. We identified and kept only EAB beetles. We identified females either based on their enlarged 1st abdominal segment and a lack of dense setae on the prosternum (
We dissected female reproductive systems by pulling the ovipositor with forceps, removing the reproductive tract, and mounting it onto a microscope slide. We cut the bulb of the spermatheca and gently squeezed it to push out any sperm. We stained the slide with Giemsa stain (
Estimating absolute abundance for EAB in an urban area with non-random ash tree distribution is difficult, and the appropriate sampling unit (such as area or number of ash trees) is not obvious. We chose instead to work with relative estimates of abundance: total male trap catch (per tree cluster) for Halifax and proportion of EAB collected from Cerceris wasps (per site) for Connecticut. For the remainder of the text, we use “abundance” to refer to this relative abundance estimate of beetles. Because we are using relative estimates, we cannot directly relate our Halifax and Connecticut abundance estimates. However, this does not matter, as we are only asking whether we can detect mating-abundance relationships within each region.
To test the hypothesis that mating success increases with beetle abundance, we fit weighted linear regressions of proportion mated females as a function of male abundance, separately for EAB collected from Halifax (by tree cluster) and Connecticut (by site). We weighted each data point by one divided by the square of the difference between the upper confidence interval (CI) and the lower confidence interval (CI) to account for the greater information contained in estimates from sites with more beetles. However, unweighted regressions supported identical conclusions (results not shown). An alternative analysis for Halifax with log transformation of male abundance yielded essentially identical results (not shown).
We used the Scipy (V.1.9.3) and Scikit Learn (V.1.0.2) packages in Python (V.3.9.16) to conduct all statistical analyses. We performed data visualization using the Matplotlib (V.3.6.2) and Seaborn (V.0.12.2) packages.
We collected 1673 adult EAB (1329 males and 356 females) over the course of the study. Of the 356 females, 174 had sperm present in their spermatheca leading to a mean female mating success rate of 0.59 (±0.072 SE). More than half (983 individuals) of the beetles were collected from a site nearest the invasion epicentre. The number of males significantly predicted the number of females collected within clusters (r2=0.98, p=2.5e-14). For every female EAB collected in traps approximately 3.7 males were collected. Male abundance was not a good predictor of female mating success (r2=0.015, p=0.63, 95% CI slope = [-1.2 e-03, 7.7 e-04], Fig.
Female mating success as a function of relative male abundance. Collected from prism traps in Halifax, Nova Scotia, Canada, in 2022. Dots represent clusters of trees where beetles were trapped. Error bars represent 95% confidence intervals of the proportion of mated females at each location. The dotted red line represents the slope of the weighted linear regression (not significant). The dashed blue line represent 95% confidence intervals of the linear regression.
Relative abundance of EAB, as measured by proportion of EAB to other beetles collected, ranged from 0.020–0.935 with a median abundance total of 0.388 from 48 sites. The number of beetles collected at sites from which dissected beetles were chosen ranged from 31–288 with a median sample size of 63. We dissected 249 female EAB. Of the female EAB dissected, 168 had sperm present in their spermatheca indicating successful mating while 81 did not successfully mate as indicated by the lack of sperm.
Population abundance did not significantly predict female mating success (r2=0.000, p=0.9, 95% CI slope = [-0.38, 0.34], Fig.
Female mating success as a function of relative EAB abundance. Collected from Cerceris fumipennis wasps in Connecticut, United States, from 2014–2016 and 2022–2023. Dots represent geographically distinct communities within Connecticut. Error bars represent 95% confidence intervals of the proportion of mated females at each location. The dotted red line represents the slope of the weighted linear regression (not significant). The dashed blue line represents 95% confidence intervals of the linear regression.
Allee effects can have important influences on establishment success of non-native species, even determining whether populations continue to grow in the invaded habitat. Allee effects have been shown to influence population dynamics and suppress populations between outbreaks in both non-native forest insects such as the spongy moth (Lymantria dispar dispar Linnaeus) (
Mate-finding Allee effects have been demonstrated in very few forest insect systems because it is typically difficult both to observe individuals at low densities and to determine mating status of those individuals (e.g.,
Studying low-density populations, ones that are frequently affected by component Allee effects, remains challenging due to the difficulty of finding small enough populations but detecting enough individuals to derive meaningful statistical conclusions (
Our results suggest that EAB is not subject to pronounced mate-finding (component) Allee effects through the range of abundances we studied. We found approximately half of collected EAB females were mated even at our lowest populations. This contrasts with some studies of other introduced species such as the brown spruce longhorn beetle (
Even at our highest-abundance sites, a substantial fraction of females often remained unmated: mated fractions reached only 60–70% in Halifax, and 40–80% in Connecticut. For brown spruce longhorn beetle,
Mate-finding Allee effects in low-density populations generally exist when organisms are sparsely distributed in space and encounters among individuals are low. However, mate-finding difficulties can potentially be overcome if mate-finding is particularly efficient. This might be especially true in systems where mate-finding is multimodal, as it is for EAB. EAB uses multiple cues to identify host trees and find mates. Both males and females are attracted to volatiles of stressed ash trees, particularly 3Z-hexenol, a component of ash foliage (
Understanding the strength of Allee effects on invasive species remains important, as it can impact how management strategies are best implemented. Invasive species experiencing Allee effects may be better managed at low densities (
Risk modelling of long-distance dispersal of EAB has shown that Allee effects are likely to be an important determinant of its spread (
The authors have declared that no competing interests exist.
No ethical statement was reported.
This work was supported by Canadian Forest Service and Natural Sciences and Engineering Research Council of Canada.
Conceptualization: Alexandre P. Caouette, Claire E. Rutledge, Stephen B. Heard, Deepa S. Pureswaran. Data Curation: Alexandre P. Caouette. Formal Analysis: Alexandre P. Caouette. Funding Acquisition: Stephen B. Heard, Deepa S. Pureswaran, Claire E. Rutledge. Investigation: Alexandre P. Caouette, Claire E. Rutledge. Methodology: Alexandre P. Caouette, Claire E. Rutledge. Project Administration: Alexandre P. Caouette, Claire E. Rutledge. Resources: Stephen B. Heard, Deepa S. Pureswaran. Software: Alexandre P. Caouette. Supervision: Stephen B. Heard, Deepa S. Pureswaran. Validation: Alexandre P. Caouette. Visualization: Alexandre P. Caouette. Writing – Original Draft Preparation: Alexandre P. Caouette. Writing – Review & Editing: Alexandre P. Caouette, Stephen B. Heard, Deepa S. Pureswaran, Claire E. Rutledge
Alexandre P. Caouette https://orcid.org/0000-0001-9518-7338
Stephen B. Heard https://orcid.org/0000-0002-5976-1133
Deepa S. Pureswaran https://orcid.org/0000-0002-4040-7708
All of the data that support the findings of this study are available in the main text or Supplementary Information. We have submmited data to DRYAD at the following URL: https://doi.org/10.5061/dryad.000000097.
Number of beetles caught in a cluster based on the distance from the invasion epicentre
Data type: docx