Jian J. Duan

Population dynamics of an invasive forest insect and associated natural enemies in the aftermath of invasion: implications for biological control

Summary 1. Understanding the population dynamics of exotic pests and associated natural enemies is important in developing sound management strategies in invaded forest ecosystems. The emerald ash borer (EAB) Agrilus planipennis Fairmaire is an invasive phloem-feeding beetle that has killed tens of millions of ash Fraxinus trees in North America since first detected in 2002. 2. We evaluated populations of immature EAB life stages and associated natural enemies over a 7-year period (2008–2014) in six stands of eastern deciduous forest in southern Michigan, where Tetrastichus planipennisi Yang and two other Asian-origin EAB parasitoids were released for biological control between 2007 and 2010. 3. We observed 90% decline in densities of live EAB larvae in infested ash trees at both parasitoid-release and control plots from 2009 to 2014 and found no significant differences in EAB density or mortality rates by parasitoids, avian predators or other undetermined factors between parasitoid-release and control plots. The decline in EAB larval density in our study sites was correlated with significant increases in EAB larval parasitism, first by native parasitoids, then by T. planipennisi. 4. Life table analyses further indicated that parasitism by the introduced biocontrol agent and the North American native parasitoids contributed significantly to the reduction of net EAB population growth rates in our study sites from 2010 to 2014. 5. Synthesis and applications. Our findings indicate that successful biocontrol of emerald ash borer (EAB) may involve suppression of EAB abundance both by local, generalist natural enemies (such as Atanycolus spp.) and by introduced specialist parasitoids (such as T. planipennisi). Biological control programmes against EAB in the aftermath of invasion should focus on establishing stable populations of T. planipennisi and other introduced specialist parasitoids for sustained suppression of low-density EAB populations. Moreover, we recommend releasing the introduced specialist biocontrol agents as soon as possible to prevent the outbreak of EAB populations in both newly infested and aftermath forests when EAB densities are still low.

Quantifying the Impact of Woodpecker Predation on Population Dynamics of the Emerald Ash Borer (Agrilus planipennis)

The emerald ash borer (EAB), Agrilus planipennis, is an invasive beetle that has killed millions of ash trees (Fraxinus spp.) since it was accidentally introduced to North America in the 1990s. Understanding how predators such as woodpeckers (Picidae) affect the population dynamics of EAB should enable us to more effectively manage the spread of this beetle, and toward this end we combined two experimental approaches to elucidate the relative importance of woodpecker predation on EAB populations. First, we examined wild populations of EAB in ash trees in New York, with each tree having a section screened to exclude woodpeckers. Second, we established experimental cohorts of EAB in ash trees in Maryland, and the cohorts on half of these trees were caged to exclude woodpeckers. The following spring these trees were debarked and the fates of the EAB larvae were determined. We found that trees from which woodpeckers were excluded consistently had significantly lower levels of predation, and that woodpecker predation comprised a greater source of mortality at sites with a more established wild infestation of EAB. Additionally, there was a considerable difference between New York and Maryland in the effect that woodpecker predation had on EAB population growth, suggesting that predation alone may not be a substantial factor in controlling EAB. In our experimental cohorts we also observed that trees from which woodpeckers were excluded had a significantly higher level of parasitism. The lower level of parasitism on EAB larvae found when exposed to woodpeckers has implications for EAB biological control, suggesting that it might be prudent to exclude woodpeckers from trees when attempting to establish parasitoid populations. Future studies may include utilizing EAB larval cohorts with a range of densities to explore the functional response of woodpeckers.

Biology, Life History, and Laboratory Rearing of Spathius galinae (Hymenoptera: Braconidae), a Larval Parasitoid of the Invasive Emerald Ash Borer (Coleoptera: Buprestidae)

ABSTRACT Spathius galinae Belokobylskij & Strazanac is a recently described parasitoid of the emerald ash borer, Agrilus planipennis Fairmaire, in the Russian Far East, and is currently being considered for biocontrol introduction in the United States. Using A. planipennis larvae reared with freshly cut ash (Fraxinus spp.) sticks, we investigated the biology, life cycle, and rearing of S. galinae in the laboratory under normal rearing conditions (25 ± 1°C, 65 ± 10% relative humidity, and a photoperiod of 16:8 [L:D] h). Our study showed that S. galinae took approximately 1 mo (29 d) to complete a single generation (from egg to adult) under the laboratory rearing conditions. After éclosion from eggs, larvae of S. galinae molted four times to reach the fifth instar, which then spun cocoons for pupation and development to adults. Adult female wasps had a median survival time of 7 wk with fecundity peaking 3 wk after emergence when reared in groups (of five females and five males) and 2 wk in single pairs. Throughout the life span, a single female S. galinae produced a mean (±SE) of 31 (±3.0) progeny when reared in groups, and a mean (±SE) of 47 (±5.3) progeny when reared in single pairs. Results from our study also showed that S. galinae could be effectively reared with A. planipennis larvae reared in both green (Fraxinus pennsylvanica Marshall) and tropical [Fraxinus uhdei (Wenzig) Lingelsh] ash sticks. However, the abortion (unemergence) rate of S. galinae progeny was much higher (20%) when reared with host larvae in green ash sticks than that (2.1%) in tropical ash sticks.

Potential New Associations of North American Parasitoids With the Invasive Asian Longhorned Beetle (Coleoptera: Cerambycidae) for Biological Control.

Abstract The Asian longhorned beetle, Anoplophora glabripennis (Motschulsky), is a polyphagous wood-boring insect native to Asia. Since it invaded North America in the 1990s, the beetle has been continuously targeted by quarantines and eradication programs in the United States and Canada. We examined the potential for development of new species-associations between A. glabripennis and hymenopteran parasitoids collected from cerambycids and other wood-boring insects infesting red maple (Acer rubrum L.) trees in the mid-Atlantic region of the United States. Results of our study showed that five groups of braconid parasitoids (Ontsira mellipes Ashmead, Rhoptrocentrus piceus Marsh, Spathius laflammei Provancher, Heterospilus spp., and Atanycolus spp.) successfully attacked early instars of A. glabripennis larvae infesting red maple logs and produced both male and female progenies. One species, O. mellipes, was continuously reared on A. glabripennis larvae inserted inside small red maple sticks for over 50 generations, and produced female-biased progeny (∼6:1 female to male ratio) at each generation. Continuous rearing of O. mellipes on A. glabripennis larvae did not significantly increase the parasitism and mean number of progeny produced per parasitized host. Together, these findings demonstrate that some North American parasitoids may be able to develop new associations with A. glabripennis and thus should be further studied under semifield or field conditions for possible use in biocontrol.

Climate variation alters the synchrony of host–parasitoid interactions

Abstract Observed changes in mean temperature and increased frequency of extreme climate events have already impacted the distributions and phenologies of various organisms, including insects. Although some research has examined how parasitoids will respond to colder temperatures or experimental warming, we know relatively little about how increased variation in temperature and humidity could affect interactions between parasitoids and their hosts. Using a study system consisting of emerald ash borer (EAB), Agrilus planipennis, and its egg parasitoid Oobius agrili, we conducted environmentally controlled laboratory experiments to investigate how increased seasonal climate variation affected the synchrony of host–parasitoid interactions. We hypothesized that increased climate variation would lead to decreases in host and parasitoid survival, host fecundity, and percent parasitism (independent of host density), while also influencing percent diapause in parasitoids. EAB was reared in environmental chambers under four climate variation treatments (standard deviations in temperature of 1.24, 3.00, 3.60, and 4.79°C), while O. agrili experiments were conducted in the same environmental chambers using a 4 × 3 design (four climate variation treatments × 3 EAB egg densities). We found that EAB fecundity was negatively associated with temperature variation and that temperature variation altered the temporal egg laying distribution of EAB. Additionally, even moderate increases in temperature variation affected parasitoid emergence times, while decreasing percent parasitism and survival. Furthermore, percent diapause in parasitoids was positively associated with humidity variation. Our findings indicate that relatively small changes in the frequency and severity of extreme climate events have the potential to phenologically isolate emerging parasitoids from host eggs, which in the absence of alternative hosts could lead to localized extinctions. More broadly, these results indicate how climate change could affect various life history parameters in insects, and have implications for consumer–resource stability and biological control.

Life History, Reproductive Biology, and Larval Development of Ontsira mellipes (Hymenoptera: Braconidae), a Newly Associated Parasitoid of the Invasive Asian Longhorned Beetle (Coleoptera: Cerambycidae)

Abstract The invasive Asian longhorned beetle, Anoplophora glabripennis (Motschulsky), is a destructive xylophagous forest pest species originating from Asia. Several endemic North American hymenopteran (Braconidae) species in the mid-Atlantic region were capable of attacking and reproducing on A. glabripennis larvae in laboratory bioassays. Ontsira mellipes Ashmead (Hymenoptera: Braconidae) has been continually reared on A. glabripennis larvae at USDA-ARS BIIRU since 2010, and has been identified as a potential new-association biocontrol agent. Two experiments were conducted to investigate parasitism, paralysis, reproductive biology, larval development, and longevity of adult O. mellipes. In the first experiment, pairs of adult parasitoids were given single A. glabripennis larvae every 2 d (along with honey and water) over their lifetimes, while in the second experiment individual parasitoids were observed daily from egg to adult, and adults were subsequently starved. Adults in the first experiment parasitized ∼21% of beetle larvae presented to them throughout their life, and paralysis of larvae occurred 1–2 d after oviposition. More than half of the individual pairs parasitized A. glabripennis larvae, with each female producing around 26 offspring throughout her life. In the second experiment, median development time of O. mellipes from egg to adult was about 3 wk, with five larval instars. Adult O. mellipes that were provided with host larvae, honey, and water lived 9 d longer than host-deprived and starved adults. These findings indicate that mass-rearing procedures for O. mellipes may be developed using the new association host for development of effective biocontrol programs against A. glabripennis.