Kristopher J. Abell

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.

Natural enemies implicated in the regulation of an invasive pest: a life table analysis of the population dynamics of the emerald ash borer

The emerald ash borer Agrilus planipennis Fairmaire is a serious invasive forest pest of ash (Fraxinus) trees in North America. Life tables were constructed for both experimentally established cohorts and wild populations of A. planipennis on healthy host trees from 2008 to 2011 in six forests in central Michigan. Life table analysis showed that the net population growth rates (R0) for the experimental cohorts (16.0 ± 2.9) and associated wild A. planipennis (19.4 ± 1.9) were the highest for the first study period (2008–2009) at three Ingham Co. sites but decreased to 4.7 ± 0.9 and 4.6 ± 0.4, respectively, for the second (2009–2010) study period at the same sites. By contrast, R0 values of both experimental cohorts (5.7 ± 2.2) and associated wild A. planipennis populations (11.3 ± 2.5) were intermediate in the third (2010–2011) study period at different sites in the Gratiot and Shiawassee Cos. The sudden decrease in R0 of both experimental and wild A. planipennis cohorts in the Ingham Co. sites corresponded with increases in parasitism by hymenopteran parasitoids Atanycolus spp. (native) and Tetrastichus planipennisi Yang (introduced), as well as an increase in woodpecker predation, indicating the role of these natural enemies in regulation of the pests population dynamics.

Evolution of increased cold tolerance during range expansion of the elongate hemlock scale Fiorinia externa Ferris (Hemiptera: Diaspididae)

Abstract 1. Alien species often face novel challenges to their spread and population growth. One critical hurdle often involves an organism’s ability to tolerate environmental extremes characteristic of their invaded range. Although abiotic factors often determine range limits, there is less evidence for local adaptation in invasive organisms whose initial arrival and rapid population growth is separated by a lengthy lag period.

Responses of an Idiobiont Ectoparasitoid, Spathius galinae (Hymenoptera: Braconidae), to Host Larvae Parasitized by the Koinobiont Endoparasitoid Tetrastichus planipennisi (Hymenoptera: Eulophidae): Implications for Biological Control of Emerald Ash Borer (Coleoptera: Buprestidae)

ABSTRACT Understanding interspecific competition among insect parasitoids is important in designing classical biological control programs that involve multiple species introductions. Spathius galinae Belokobylskij and Strazenac, a new idiobiont ectoparasitoid from the Russian Far East, currently is being considered for introduction to the United States for biological control of the emerald ash borer, Agrilus planipennis Fairmaire, whereas Tetrastichus planipennisi Yang, a koinobiont endoparasitoid native to China, is another natural enemy that already has been introduced in the same program. In a laboratory study, we examined the potential interactions between these two parasitoids when they compete for the same emerald ash borer host larvae. In multiple-choice assays where healthy emerald ash borer larvae were presented along with emerald ash borer larvae previously parasitized by T. planipennisi at different times, S. galinae attacked host larvae already parasitized by T. planipennisi for up to 4 d, but not 8 d. However, parasitism rates were significantly lower in previously parasitized hosts as compared with healthy host larvae. In no-choice tests where S. galinae females were presented either with healthy emerald ash borer larvae or emerald ash borer larvae parasitized by T. planipennisi at several earlier time points, S. galinae again parasitized significantly more healthy host larvae than T. planipennisi-parasitized larvae. These results suggest that the ectoparasitoid S. galinae can discriminate between healthy host larvae and T. planipennisi-parasitized larvae, and competitive interactions between the two parasitoids are likely to be minimal if coreleased by the emerald ash borer biological control program.

Monitoring the establishment and flight phenology of parasitoids of emerald ash borer (Coleoptera: Buprestidae) in Michigan by using sentinel eggs and larvae

Abstract The emerald ash borer, Agrilus planipennis Fairmaire (Coleoptera: Buprestidae), is an important invasive pest of ash (Fraxinus) trees in North America. Two larval parasitoid species, Tetrastichus planipennisi Yang (Hymenoptera: Eulophidae) and Spathius agrili Yang (Hymenoptera: Braconidae), and 1 egg parasitoid species, Oobius agrili Zhang and Huang (Hymenoptera: Encyrtidae), were introduced into the United States in 2007 as part of a classical biological control program. We conducted field studies to assess the flight phenology of introduced and native parasitoids of emerald ash borer in central Michigan from 2011 to 2013 by using sentinel logs. Parasitism rates of sentinel A. planipennis eggs by O. agrili fluctuated throughout the season from 0 to 22% in 2011 and 0 to 6% in 2012. Flight phenology of O. agrili adults varied between years, and discrete generations were not apparent. Rather, O. agrili adults were generally continually present over a 3 mo period each year. Parasitism rates of sentinel A. planipennis larvae by T. planipennisi and the North American native Atanycolus spp. (Hymenoptera: Braconidae), respectively, ranged from 0 to 5% and 33 to 77% in 2011, from 0 to 69% and 0 to 27% in 2012, and from 0 to 53% and 0 to 46% in 2013. Phenology of adult flight of both T. planipennisi and Atanycolus spp. was inconsistent between years. Development of nondestructive methods to determine when stages of A. planipennis suitable for parasitism are present in combination with the use of sentinel logs to observe parasitoid phenology as described here will enhance the ability to evaluate the impacts of parasitoids on emerald ash borer.

Aphelinid and Encyrtid (Hymenoptera: Chalcidoidea) Parasitoids of Armored Scales (Hemiptera: Diaspididae) Attacking Hemlocks (Tsuga spp.) in Japan and the United States, with Description of Eight New Species

ABSTRACT The complex of aphelinids and encyrtids (Hymenoptera: Chalcidoidea) parasitizing armored scales (Hemiptera: Diaspididae) on hemlock in Japan (Tsuga diversifolia Masters and Tsuga sieboldii Carrière) and in the eastern United States (Tsuga canadensis [L.] Carrière) was surveyed. Eight new species were discovered and are described here: Five species of Encarsia and one species each of Pteroptrix (Aphelinidae), Coccidencyrtus, and Thomsonisca (Encyrtidae). Two previously known species, Aphytis moldavicus Yasnosh and Encarsia brimblecombei Girault, are recorded for the first time from Japan. New host-parasitoid associations were found for five diaspidids: Fiorinia externa Ferris, Dynaspidiotus tsugae Marlatt, Pseudaulacaspis momi Kuwana, Lepidosaphes japonica Kuwana, and Lepidosaphes pseudotsugae Takahashi.

THE USE OF COHORTS TO EVALUATE THE IMPACT OF ENCARSIA CITRINA (HYMENOPTERA: APHELINIDAE) ON FIORINIA EXTERNA (HEMIPTERA: DIASPIDIDAE) IN THE EASTERN UNITED STATES

ABSTRACT Two years of natural enemy exclusion experiments with cohorts of the invasive scale Fiorinia externa Ferris were conducted in Connecticut, Pennsylvania, and North Carolina. The parasitoid Encarsia citrina Craw had a significant effect on the percentage of F. externa that reached reproductive maturity. For cohorts exposed to E. citrina, 11% reached maturity in 2006 and 8% in 2007 compared to cohorts protected from E. citrina, in which 29% reached maturity in 2006 and 18% in 2007 (averaged across all 3 states). While E. citrina exerted some control of F. externa density, it was insufficient to maintain F. externa density at the study sites at levels comparable to those of the scale in its native range in Japan.

Classical and Augmentative Biological Control

Parasitoids, predators, herbivorous arthropods, and plant pathogens may fail to follow an invasive species to new regions, allowing great increases in the invading species’ density. Introduction of the missing natural enemies, once their safey has been demonstrated to the local fauna or flora, is termed classical biological control. Classical biological control is a major tool in reducing impacts of invasive species, both in crops and natural areas, and has successfully control several hundred invasive species, completely and permanently in invaded countries. This form of restoration ecology is a basic tool in invasive species management and should be considered whenever the objective is to permanently reduce the density of an invasive species over a large area. In contrast, augmentative biological control seeks only to protect a crop during its period of production and permanent pest suppression is not intended or possible. Natural enemies used in augmentative biological control are reared in insectaries, often by commercial firms. This approach is used against insects and mites, but not weeds. The value of this approach depends on efficacy and cost of the natural enemy and augmentative biological control is most effective in greenhouse crops. Classical biological control is less polluting than use of pesticides and is often the only practical approach to suppression of invasive weeds or insects in wild lands. Both classical and augmentative biological control are harmless to people and vertebrates. Risks to nontarget plants or native insects may exist, depending on the host specificity of the agents use, and such risks can be managed to low levels by careful screening of the species employed.