Open Access This article is
- freely available
Forests 2018, 9(2), 69; https://doi.org/10.3390/f9020069
Coleopteran Communities Associated with Forests Invaded by Emerald Ash Borer
Department of Entomology, University of Kentucky, S-225 Ag North, Lexington, KY 40546, USA
Author to whom correspondence should be addressed.
Received: 19 December 2017 / Accepted: 25 January 2018 / Published: 30 January 2018
Extensive ash mortality caused by the non-native emerald ash borer alters canopy structure and creates inputs of coarse woody debris as dead and dying ash fall to the forest floor; this affects habitat heterogeneity; resource availability; and exposure to predation and parasitism. As EAB-induced (emerald ash borer-induced) disturbance progresses the native arthropod associates of these forests may be irreversibly altered through loss of habitat; changing abiotic conditions and altered trophic interactions. We documented coleopteran communities associated with EAB-disturbed forests in a one-year study to evaluate the nature of these changes. Arthropods were collected via ethanol-baited traps on five sites with varying levels of EAB-induced ash mortality from May to September; captured beetles were identified to the family level and assigned to feeding guilds (herbivore; fungivore; xylophage; saprophage; predator; or parasite). Over 11,700 Coleoptera were identified in 57 families. In spite of their abundance; herbivores comprised a relatively small portion of coleopteran family richness (8 of 57 families). Conversely, coleopteran fungivore richness was high (23 families), and fungivore abundance was low. Herbivores and fungivores were more abundant at sites where ash decline was most evident. The predatory Trogossitidae and Cleridae were positively correlated with ash decline, suggesting a positive numerical response to the increased prey base associated with EAB invasion. Ash forests are changing, and a deeper understanding of arthropod community responses will facilitate restoration.
Keywords:Fraxinus; invasive species; trophic guild; natural enemies
Invasions by non-native invasive species pose significant threats to forest ecosystem function  and native biodiversity [2,3], and have widespread economic impacts [4,5]. Ash (Fraxinus spp.) are a consistent component of hardwood forests throughout the United States [6,7]; their prevalence and persistence is threatened by the emerald ash borer (EAB, Agrilus planipennis Fairmaire, Coleoptera: Buprestidae). Since its discovery near Detroit, MI in 2002 , EAB has spread rapidly through much of the eastern contiguous United States and southeastern Canada  inflicting extensive ash mortality in invaded regions. Larvae feed on phloem beneath the bark, forming serpentine galleries and destroying the vascular tissue, disrupting translocation of water and nutrients to the canopy, ultimately girdling the tree [10,11]. The majority of EAB-induced ash mortality (>85%) occurs within 3–5 years of the initial invasion [12,13]. All North American Fraxinus species are susceptible to attack and EAB readily colonizes healthy trees .
The direct effects of EAB invasion include altered forest structure due to rapid ash mortality, with subsequent alterations in ash-associated communities [14,15,16,17,18]. The indirect effects of rapid and broad scale tree mortality include increased gap formation which alters light penetration to the forest floor, accumulation of coarse woody debris, and qualitative and quantitative alterations in litter inputs causing shifting temperature and moisture regimes on the forest floor [19,20]. Such changes associated with EAB-induced ash mortality is affecting arthropod community associates of these invaded forests. In particular, changes at the soil-surface interface via increased leaf litter and coarse woody debris inputs can influence the abundance and distribution of soil biota [21,22]. Coleopterans, in particular the Carabidae, are well documented indicators of disturbance [23,24], and have been shown to respond to EAB-induced changes [25,26].
We sought to gain a broader understanding of the extent to which EAB-induced ash mortality might affect arthropod community associates, and focus here on aerial Coleoptera. We evaluated the extent to which coleopteran abundance and richness are affected by widespread changes in forest structure associated with the EAB invasion, and further considered these changes in relation to trophic guilds. We hypothesized that EAB-induced changes in forest composition and structure will lead to guild-specific changes in coleopteran communities. Specifically, we expected that xylophage, saprophage, and fungivore abundance and overall richness would increase in response to increases in habitat caused by inputs due to EAB disturbance.
2. Materials and Methods
2.1. Study Sites
Five study sites were established in mixed mesophytic forests in north-central Kentucky along the forefront of the expanding EAB invasion , in Anderson, Fayette, Henry, Shelby, and Spencer counties. Ash thrive on the moist and fertile soils that predominate in this region [28,29], and were historically a significant component of these forests . At the onset of the study EAB was present at the Anderson, Henry, and Shelby sites (initially reported in November 2011, October 2009, and May 2009, respectively). EAB was first detected at the Fayette and Spencer sites in 2014, but there were little to no signs of EAB-induced stress.
At each site, 0.04 ha circular whole plots, situated ≥50 m apart, were placed in contiguous forests in blocks of three, with three blocks at each site, for a total of 45 plots across all five sites . Ash canopy dieback was visually assessed by a single observer and each tree assigned a crown dieback value from 0% (healthy) to 100% (dead). When split or sloughing bark, larval galleries, or adult exit holes were evident, dieback was attributed to EAB. Our sites represented the full spectrum of forest disturbance associated with the EAB invasion, including pre-invasion at Fayette and Spencer (newly detected; <17% ash canopy dieback, <2% ash mortality), peak invasion at Shelby (EAB populations high; 25–30% ash canopy dieback, ~10% ash mortality), and post-invasion forests at Henry and Anderson (EAB populations low; >55% canopy dieback, 19–50% ash mortality) .
2.2. Arthropod Monitoring
Native coleopteran communities in the sub-canopy strata were monitored using 12-unit Lindgren multi-funnel traps (one per plot, N = 45) from 20 May to 12 September 2014. Traps were suspended over an ash branch (~4 m) and fitted with two 50 mL vials of 70% ethanol, a commonly used lure for xylophagous insects [30,31,32], hung from the funnel edge, and with a dichlorvos strip (2 × 5 cm2) (American Vanguard Corporation Chemical Corp., Los Angeles, CA, USA) placed in each trap bottom. Traps were monitored every 7–14 days; contents were removed and stored in 70% EtOH in resealable plastic bags, and lures were replenished. In the laboratory samples were sorted to order ; Coleoptera were sorted and identified to family using available keys [33,34,35,36], counted, and assigned to trophic guilds based on larval feeding habits, including herbivore, saprophage, fungivore, xylophage, predator, or parasite . We used family-level identifications, which are deemed taxonomically sufficient when undertaking a study of this nature [38,39]. This approach provides a good estimate of invertebrate populations within a given community when using a given sampling method, and has been utilized in a number of invertebrate studies [39,40,41,42,43]. Ordinally the Coleoptera are trophically diverse, but more or less trophically uniform within families [37,44], which allows classifying families into feeding guilds that exploit resources in a similar manner . In our study, the carrion feeders, including the Silphidae, some Staphylinidae (e.g., Aleochara spp.), some Histeridae, some Nitidulidae (e.g., Nitidulia spp.), and some Leiodidae, were responding to the decaying trap contents rather than the ethanol lure, which resulted in excessive fluctuations in abundance, and so were excluded from additional analyses.
We used assessments of ash mortality from Davidson and Rieske  and also evaluated ash canopies for decline, ranging from low (Fayette) to high (Henry), to assess the influence of ash decline on coleopteran abundance and richness. The abundance of aerial coleopterans was evaluated with funnel traps (total no. trapped). Richness (total no. families captured) and evenness (Evar)  was derived by site. Diversity indices were not derived because of data gaps caused by intermittent difficulties in accessing monitoring sites. Data were tested for normality (PROC UNIVARIATE) and transformed when necessary. Significance was determined at α = 0.05 unless stated otherwise. All analyses were performed using SAS (v9.3, SAS Campus Drive Cary, NC, USA) .
Overall coleopteran abundance and cumulative richness by site were analyzed using a repeated measure mixed linear model (PROC MIXED), with sample interval as the repeated measure and individual plots (traps) as subjects. The difference of least squares (Least Squares Means) was used to separate means for these population parameters. Coleopteran feeding guild abundance and richness summed over the 16-week sampling period were analyzed using a generalized linear mixed model (PROC GLM) to compare guild × site interactions. Feeding guild abundance was transformed using a square root transformation for total counts and arcsine transformation for percent abundance. Feeding guild abundance (absolute and percent) was compared across all sites where the difference of least squares was used to separate means and post-hoc analysis was performed using pairwise T-Comparisons if differences arose. A chi squared analysis was used to determine differences in trophic guild abundance across sites. Correlations between the predator guild and ash canopy decline were evaluated (PROC CORR).
3.1. Study Sites
Across our study sites, ash composition ranged from 12–26% for stems >2.5 cm diameter. EAB-induced ash mortality ranged from 0–50% and was highly correlated with EAB abundance . Ash canopy dieback ranged from a low of ~7% at our least-disturbed, most recently invaded site to a high of 74% at our most degraded site (Table 1).
Funnel traps yielded 16,455 arthropods, including 11,786 coleopterans (>71%) representing 57 families, excluding carrion feeders (Table A1). Elateridae was the most abundant family (Figure 1), with 16% of the total, followed by the Curculionidae and Staphylinidae (13 and 12%, respectively); these three families comprised nearly 41% of the coleopterans captured. The next most abundant families were the Ptilodactylidae (9%), the Latridiidae (9%), and the Histeridae (8%); collectively they comprised almost 27% of the total coleopterans.
Coleopteran abundance (Table 1), but not cumulative family richness (Figure 2) differed significantly among study sites; both tended to be lowest in pre-(Fayette) and post-disturbed (Henry) sites, and greatest at the site typifying peak invasion (Shelby). Henry, Anderson, and Shelby had the highest coleopteran evenness, and Spencer had the lowest (Table 1).
Coleopteran abundance was greatest among herbivores (4207 individuals, 36%) (Table 2), comprised primarily of the Elateridae, which feed on flowers, nectar, pollen, and rotting fruit .
However, in spite of their abundance, herbivores comprised only 14% of total family richness (8 families). In contrast, coleopteran fungivore richness was highest at 40% (23 families), in spite of the fact that abundance was relatively low (2082 individuals, 17%) (Table 2; Figure 3).
Fungivores were dominated by the Latridiidae (Figure 1), which typically feed on the reproductive structures of fungi and are commonly found in plant debris . Predators comprised 26% of the total (3050 individuals) and 19% of the coleopteran family richness (11 families) (Table 2). Predators consisted primarily of the Staphylinidae (Figure 1), which are generalists, and the Histeridae, which has one subfamily associated with bark beetle (Curculionidae) galleries, and another subfamily that feeds principally on fly and beetle larvae associated with dung . Saprophages and xylophages made up ~10% of the abundance, and similarly 10 and 12% of coleopteran family richness, and consisted primarily of Ptilodactylidae and Scolytines (Figure 1; Table 2).
Trophic guild abundance across sites varied (x2 = 1045.6; df = 20; p < 0.0001) (Figure 4). Herbivore and saprophage abundance was greatest at Shelby (Figure 4a,b), which represented the greatest EAB activity, reflected in EAB intercept trap catch , among the five sites. Fungivore abundance (Figure 4c) was positively correlated with ash decline and was greatest at Shelby, Anderson, and Henry, where disturbance caused by the EAB invasion was more advanced, and lowest at Fayette and Spencer, where EAB-related disturbance was minimal. Xylophages were most abundant at Spencer (Figure 4d), again representing relatively early stages of EAB invasion. Predator abundance (Figure 4e) was lowest at Fayette and Henry, representing both pre- and post-EAB invasion and highest at the sites where the invasion is nearer its peak. Parasite abundance (Figure 4f) was similar across all sites.
Among the predators, Trogossitidae and Cleridae abundance (7% and 5% of total predator abundance, respectively) were positively correlated (α < 0.1) with ash decline (Figure 5).
Changes in structure, composition, and succession [14,15,16,17,18], alterations in light availability to the forest floor [19,20], and inputs of coarse woody debris associated with forest disturbance create and eliminate habitats [14,15,16,17,21,22,25], and affect resource availability and trophic relationships. Ash-dominated forests in the wake of the EAB invasion are expecting a loss of overall arthropod richness and are facing cascading ecological impacts and altered ecosystem processes. Of the 282 native arthropods associated with ash, 43 are monophagous; nine of these monophages are coleopterans . Undoubtedly, these ash specialists will be negatively affected and may experience localized extirpation. We found discernible differences in aerial coleopteran communities associated with EAB-disturbed forests. The increase in abundance and cumulative richness of coleopteran associates where EAB activity density was at its greatest may be attributable to increases in habitat availability due to newly forming snags and coarse woody debris, and to volatile emissions from dying trees [30,31,48,49]. These resources are relatively transient, and as they decline we can anticipate a corresponding decline in coleopteran taxa reliant on their persistence. Contrary to expectations, coleopteran family evenness was highest in sites more heavily disturbed by EAB, where these transient resources would be most plentiful.
We found coleopteran abundance to be greatest among herbivores, comprised primarily of the Elateridae, which feed on flowers, nectar, pollen, and rotting fruit . The Latridiidae, which feed on fungal reproductive structures and are common in plant debris , were the dominant fungivore family. The increase in fungivore richness that we observed may be a response to an increase in availability of these types of resources as ash decline progresses. Predators comprised 26% of the total trap catch, and consisted primarily of the Staphylinidae, which are generalist predators, and the Histeridae, which has one subfamily most commonly associated with bark beetle (Curculionidae) galleries [35,36]. Among the predators, Trogossitidae and Cleridae were positively correlated with ash decline. Trogossitids consisted of 228 individuals of primarily Tenebroides sp.; these are bark-gnawing beetles found beneath the bark of dead trees and are associated with wood-boring beetles . Clerids (144 individuals) consisted primarily of Enoclerus sp.; these checkered beetles are associated with dead wood, and are often found predating larval Curculionidae, Cerambycidae, and Buprestidae .
Interestingly, the parastic Passandridae, comprised entirely of Catogenus rufus (Fabricius), were consistently present in low numbers, regardless of the extent of forest disturbance (Figure 4f). Catogenus rufus has been found as both larvae and adults in EAB galleries from dead ash in EAB-invaded forests ; it was present in low numbers across sites and appeared unaffected by the stage of the EAB invasion or by the corresponding decline in ash canopies. Its presence at all sites in similar abundance suggests that it utilizes a variety of wood-boring hosts and is not demonstrating a numerical response to the EAB invasion in these forests, though it may still be utilizing EAB as a resource. Tenebroides, Enoclerus and Catogenus spp. have been documented in association with EAB larvae and pupae near the epicenter of the EAB invasion in North America , suggesting that they may be playing a role in population dynamics of this aggressive invader.
Our use of family level identifications in the evaluation of aerial coleopteran communities could be viewed as a limitation of this study. However, “taxonomic sufficiency” (sensu Ellis 1985 ) recognizes that, within a community, changes at the species level are often reflected at coarser taxonomic levels. The use of coarser taxonomic identifications reduces the inputs associated with large scale community level studies [40,41,42,51,52]. Family level richness is a good predictor of species richness for a variety of taxa, including butterflies . Family level identifications of benthic fauna are appropriate for calculating stream quality indices [53,54,55,56] and multivariate analyses of community data , and can reliably detect moderate ecosystem impacts . Identifications beyond the family level may not yield much more information and may not be cost effective . Targeting coarser taxonomic resolution, rather than insisting upon species level identification for woody plant surveys, significantly reduces costs of field work . Clearly, accepting coarser taxonomic sufficiency provides us with an effective approach to conduct rapid studies on ephemeral systems such as ours, as well as larger landscape scale studies over longer periods of time to answer broad questions regarding arthropod community responses to change. However, findings must be treated with caution, as not all members within a family are trophically equivalent (e.g., Formicidae) [58,59], leading to potentially misleading conclusions .
We compare the assemblage of aerial coleopterans in forest plots with no apparent EAB to the assemblage associated with the projected post-EAB community , which allows projections about long-term effects of ash loss on aerial coleopterans. Our comparative approach does not describe unforeseen alterations in successional trajectories independent of the EAB invasion, nor does it compare the ecological histories of the communities within these distinct forests, but it does provide a means of estimating potential long-term changes in arthropod community structure as a result of EAB-induced ash mortality (see [42,43]).
Endemic aerial coleopterans are readily utilizing the influx of resources provided by the EAB invasion. Collectively, our data suggest that native predators and parasites are being recruited to forests impacted by EAB, and that these native natural enemies may be a viable component of post-invasion EAB population dynamics in eastern North American forests.
Unprotected ash are devastated by the emerald ash borer. Following depletion of the ash resources, EAB populations sharply decline , greatly reducing the pest pressure on regenerating seedlings and saplings. The decline in pest pressure increases the chance of continued survival of young ash in North American forests , providing essential resources for ash specialists.
Ash forests are changing, and a deeper understanding of how arthropod communities and trophic guilds are responding will contribute to more proficient monitoring and protection.
The authors thank Bill Davidson, Eric Chapman, Ignazio Graziosi, Abe Nielsen, and Chris Strohm for assistance with field and laboratory work, and Sarah Witt and Edward Rouales for help with statistical analyses. Mary Arthur and Lee Townsend provided comments on an earlier version of this manuscript. We also thank Lee Crawfort, Bonnie Cecil, Taylorsville Lake State Park, Shelby County Parks and Recreation, and Lexington-Fayette Urban County Government for providing access to land for this project. This is publication number 17-08-120 of the Kentucky Agricultural Experiment Station paper and is published with the approval of the Director. This work is supported by the Kentucky Division of Forestry and the USDA Forest Service through a Landscape Scale Restoration Grant, and by McIntire Stennis Funds under 2351197000.
M.B.S. and L.K.R. conceived and designed this experiment; M.B.S. performed the experiments and analyzed the data as partial requirements for a master degree; M.B.S. and L.K.R. wrote the paper.
Conflicts of Interest
The authors declare no conflict of interest.
Table A1. Coleopteran family abundance at five forested sites in north central Kentucky with trophic guild designations including; herbivores (H), fungivores (F), predators (P), saprophages (S), xylophages (X), and parasitoids (Pa).
|Coleopteran Families||Trophic Guilds||Abundance|
- Ehrenfeld, J.G. Ecosystem consequences of biological invasions. Annu. Rev. Ecol. Syst. 2010, 41, 59–80. [Google Scholar] [CrossRef]
- Wilcove, D.S.; Rothstein, D.; Dubow, J.; Phillips, A.; Losos, E. Quantifying threats to imperiled species in the United States: Assessing the relative importance of habitat destruction, alien species, pollution, overexploitation, and disease. Bioscience 1998, 48, 607–615. [Google Scholar] [CrossRef]
- Byers, J.E.; Reichard, S.; Randall, J.M.; Parker, I.M.; Smith, C.S.; Lonsdale, W.M.; Atkinson, I.A.; Seastedt, T.R.; Williamson, M.; Chornesky, E. Directing research to reduce the impacts of nonindigenous species. Conserv. Biol. 2002, 16, 630–640. [Google Scholar] [CrossRef]
- Pimentel, D.; Zuniga, R.; Morrison, D. Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecol. Econ. 2005, 52, 273–288. [Google Scholar] [CrossRef]
- Aukema, J.E.; Leung, B.; Kovacs, K.; Chivers, C.; Britton, K.O.; Englin, J.; Frankel, S.J.; Haight, R.G.; Holmes, T.P.; Liebhold, A.M. Economic impacts of non-native forest insects in the continental United States. PLoS ONE 2011, 6, e24587. [Google Scholar] [CrossRef] [PubMed]
- Kennedy, H.E., Jr. Fraxinus pennsylvanica Marsh. Green ash. In Silvics of North America: Volume 2, Hardwoods; Burns, R.M., Honkala, B.H., Eds.; Agricultural Handbook 654; USDA Forest Service: Washington, DC, USA, 1990; pp. 348–354. [Google Scholar]
- Schlesinger, R.C. Fraxinus americana L. white ash. In Silvics of North America: Volume 2, Hardwoods; Burns, R.M., Honkala, B.H., Eds.; Agricultural Handbook 654; USDA Forest Service: Washington, DC, USA, 1990; pp. 654–665. [Google Scholar]
- Haack, R.A.; Jendak, E.; Houping, L.; Marchant, K.R.; Petrice, T.R.; Poland, T.M.; Ye, H. The emerald ash borer: A new exotic pest in North America. Newsl. Mich. Entomol. Soc. 2002, 47, 1–5. [Google Scholar]
- USDA APHIS. USDA Animal and Plant Health Inspection Service Cooperative Emerald Ash Borer Project: Initial County EAB Detections in North America. 2017. Available online: http://www.emeraldashborer.info/files/MultiState_EABpos.pdf (accessed on 12 December 2017).
- Cappaert, D.D.; McCullough, D.G.; Poland, T.M.; Siegert, N.W. Emerald ash borer in North America: A research and regulatory challenge. Am. Entomol. 2005, 51, 152–165. [Google Scholar] [CrossRef]
- Flower, C.E.; Knight, K.S.; Rebbeck, J.; Gonzalez-Meler, M.A. The relationship between the emerald ash borer (Agrilus planipennis) and ash (Fraxinus spp.) tree decline: Using visual canopy condition assessments and leaf isotope measurements to assess pest damage. For. Ecol. Manag. 2013, 303, 143–147. [Google Scholar] [CrossRef]
- Poland, T.M.; McCullough, D.G. Emerald ash borer: Invasion of the urban forest and the threat to North America’s ash resource. J. For. 2006, 104, 118–124. [Google Scholar]
- Kashian, D.M.; Witter, J.A. Assessing the potential for ash canopy tree replacement via current regeneration following emerald ash borer-caused mortality on southeastern Michigan landscapes. For. Ecol. Manag. 2011, 261, 480–488. [Google Scholar] [CrossRef]
- Gandhi, K.J.K.; Herms, D.A. Direct and indirect effects of alien insect herbivores on ecological processes and interactions in forests of eastern North America. Biol. Invasions 2010, 12, 389–405. [Google Scholar] [CrossRef]
- Gandhi, K.J.K.; Herms, D.A. North American arthropods at risk due to widespread Fraxinus mortality caused by the alien emerald ash borer. Biol. Invasions 2010, 12, 1839–1846. [Google Scholar] [CrossRef]
- Flower, C.E.; Knight, K.S.; Gonzalez-Meler, M.A. Impacts of the emerald ash borer (Agrilus planipennis Fairmaire) induced ash (Fraxinus spp.) mortality on forest carbon cycling and successional dynamics in the eastern United States. Biol. Invasions 2013, 5, 931–944. [Google Scholar] [CrossRef]
- Levin-Nielsen, A.; Rieske, L.K. Evaluating Short Term Simulations of a Forest Stand Invaded by Emerald Ash Borer. iForest 2014, e1–e6. [Google Scholar] [CrossRef]
- Klooster, W.S.; Herms, D.A.; Knight, K.S.; Herms, C.P.; McCullough, D.G.; Smith, A.; Gandhi, K.J.K.; Cardina, J. Ash (Fraxinus spp.) mortality, regeneration, and seed bank dynamics in mixed hardwood forests following invasion by emerald ash borer (Agrilus planipennis). Biol. Invasions 2014, 16, 859–873. [Google Scholar] [CrossRef]
- Perkins, T.D.; Vogelmann, H.W.; Klein, R.M. Changes in light intensity and soil temperature as a result of forest decline on Camels Hump, Vermont. Can. J. For. Res. 1987, 17, 565–568. [Google Scholar] [CrossRef]
- Zhang, Q.; Liang, Y. Effects of gap size on nutrient release from plant litter decomposition in a natural forest ecosystem. Can. J. For. Res. 1995, 25, 1627–1638. [Google Scholar] [CrossRef]
- Ulyshen, M.D.; Klooster, W.S.; Barrington, W.T.; Herms, D.A. Impacts of emerald ash borer-induced tree mortality on leaf litter arthropods and exotic earthworms. Pedobiologia 2011, 54, 261–265. [Google Scholar] [CrossRef]
- Perry, K.I.; Herms, D.A. Effects of late stages of emerald ash borer (Coleoptera: Buprestidae)-induced ash mortality on forest floor invertebrate communities. J. Insect Sci. 2017, 119, 1–10. [Google Scholar] [CrossRef]
- Rainio, J.; Niemelä, J. Ground beetles (Coleoptera: Carabidae) as bioindicators. Biodivers. Conserv. 2003, 12, 487–506. [Google Scholar] [CrossRef]
- Pearce, J.L.; Venier, L.A. The use of ground beetles (Coleoptera: Carabida) and spiders (Araneae) as biodindicators of sustainable forest management: A review. Ecol. Indic. 2006, 6, 780–793. [Google Scholar] [CrossRef]
- Gandhi, K.J.K.; Smith, A.; Hartzler, D.M.; Herms, D.A. Indirect effects of emerald ash borer-induced ash mortality and canopy gap formation on epigaeic beetles. Environ. Entomol. 2014, 43, 546–555. [Google Scholar] [CrossRef] [PubMed]
- Perry, K.I.; Herms, D.A. Short-term responses of ground beetles to forest changes caused by early stages of emerald ash borer (Coleoptera: Buprestidae)-induced ash mortality. Environ. Entomol. 2016, 45, 616–626. [Google Scholar] [CrossRef] [PubMed]
- Davidson, W.; Rieske, L.K. Native parasitoid response to emerald ash borer (Coleoptera: Buprestidae) and ash decline in recently invaded forests of the central United States. Ann. Entomol. Soc. Am. 2015, 108, 777–784. [Google Scholar] [CrossRef]
- Wharton, M.E.; Barbour, R.W. Trees and Shrubs of Kentucky; University Press of Kentucky: Lexington, KY, USA, 1973. [Google Scholar]
- Campbell, J.J. Historical evidence of forest composition in the Bluegrass Region of Kentucky. In Proceedings of the Seventh Central Hardwood Forest Conference, Carbondale, IL, USA, 5–8 March 1989; Rink, G., Budelsky, C., Eds.; General Technical Report, NC-135. Department of Agriculture, Forest Service, North Central Forest Experiment Station: St. Paul, MN, USA, 1989; pp. 231–246. [Google Scholar]
- Montgomery, M.E.; Wargo, P.M. Ethanol and other host-derived volatiles as attractants to beetles that bore into hardwoods. J. Chem. Ecol. 1983, 9, 181–190. [Google Scholar] [CrossRef] [PubMed]
- Lindelöw, Å.; Risberg, B.; Sjödin, K. Attraction during flight of scolytids and other bark- and wood-dwelling beetles to volatiles from fresh and stored spruce wood. Can. J. For. Res. 1992, 22, 224–228. [Google Scholar] [CrossRef]
- Bouget, C.; Brustel, H.; Brin, A.; Valladares, L. Evaluation of window flight traps for effectiveness at monitoring dead wood-associated beetles: The effect of ethanol lure under contrasting environmental conditions. Agric. For. Entomol. 2009, 11, 143–152. [Google Scholar] [CrossRef]
- Triplehorn, C.A.; Johnson, N.F. Borror and DeLong’s Introduction to the Study of Insects; Brooks/Cole: Belmont, CA, USA, 2005; p. 888. [Google Scholar]
- Marshall, S.A. Insects: Their Natural History and Diversity—With a Photographic Guide to Insects of Eastern North America; Firefly Books: Buffalo, NY, USA, 2006; p. 736. [Google Scholar]
- Evans, A.V. Beetles of Eastern North America; Princeton University Press: Princeton, NJ, USA, 2014; p. 560. [Google Scholar]
- BugGuide. Order Coleoptera: Beetles. Available online: http://bugguide.net/node/view/60/tree (accessed on 1 March 2017).
- Hammond, P.M. Insect abundance and diversity in the Dumoga-Bone National Park, N. Sulawesi, with special reference to the beetle fauna of lowland rain forest in the Toraut region. In Insects and the Rain Forests of South East Asia (Wallacea); Knight, W.J., Holloway, J.D., Eds.; Royal Entomological Society of London: London, UK, 1990; pp. 197–254. [Google Scholar]
- Ellis, D. Taxonomic sufficiency in pollution assessment. Marine Poll. Bull. 1985, 16, 459. [Google Scholar] [CrossRef]
- Birkhofer, K.; Bezemer, T.; Hedlund, K.; Setälä, H. Community composition of soil organisms under different wheat-farming systems. In Microbial Ecology in Sustainable Agroecosystems; Cheeke, T., Coleman, D., Wall, D., Eds.; CRC Press: Boca Raton, FL, USA, 2012; pp. 89–111. [Google Scholar]
- Hoback, W.W.; Svatos, T.M.; Spomer, S.M.; Higley, L.G. Trap color and placement effects estimates of insect family-level abundance and diversity in a Nebraska salt marsh. Entomol. Exp. Appl. 1999, 91, 393–402. [Google Scholar] [CrossRef]
- Riggins, J.J.; Davis, C.A.; Hoback, W.W. Biodiversity of belowground invertebrates as an indicator of wet meadow restoration success (Platte River, Nebraska). Restor. Ecol. 2009, 17, 495–505. [Google Scholar] [CrossRef]
- Rohr, J.R.; Mahan, C.G.; Kim, K.C. Response of arthropod biodiversity to foundation species declines: The case of the eastern hemlock. For. Ecol. Manag. 2009, 258, 1503–1510. [Google Scholar] [CrossRef]
- Adkins, J.K.; Rieske, L.K. Loss of a foundation forest species due to an exotic invader impacts terrestrial arthropod communities. For Ecol. Manag. 2013, 295, 126–135. [Google Scholar] [CrossRef]
- Hammond, P.M. Species Inventory. In Global Biodiversity: Status of the Earth’s Living Resources; Groombridge, B., Ed.; Chapman and Hall: London, UK, 1992; pp. 17–39. [Google Scholar]
- Root, R.B. The niche exploitation pattern of the blue-gray gnatcatcher. Ecol. Monogr. 1967, 37, 317–350. [Google Scholar] [CrossRef]
- Smith, B.; Wilson, J.B. A consumer’s guide to evenness indices. Oikos 1996, 76, 70–82. [Google Scholar] [CrossRef]
- SAS Institute. SAS/IML 9.3 User’s Guide; SAS Institute: Cary, NC, USA, 2011. [Google Scholar]
- Kimmerer, T.W.; Kozlowski, T.T. Ethylene, ethane, acetaldehyde, and ethanol production by plants under stress. Plant Physiol. 1982, 69, 840–847. [Google Scholar] [CrossRef] [PubMed]
- Harmon, M.E.; Franklin, J.F.; Swanson, F.J.; Sollins, P.; Gregory, S.V.; Lattin, J.D.; Anderson, N.H.; Cline, S.P.; Aumen, N.G.; Sedell, J.R. Ecology of coarse woody debris in temperate ecosystems. Adv. Ecol. Res. 1986, 15, 302. [Google Scholar]
- Bauer, L.S.; Liu, H.; Haack, R.A.; Petrice, T.R.; Miller, D.L. Natural enemies of emerald ash borer in southeastern Michigan. In Proceedings of the Emerald Ash Borer Research and Technology Development Meeting, Port Huron, MI, USA, 30 September–1 October 2003; Mastro, V., Reardon, R., Eds.; Comps. USDA Forest Service, Forest Health Technology Enterprise Team: Morgantown, WV, USA, 2004; pp. 33–34. [Google Scholar]
- Williams, P.H.; Gaston, K.J. Measuring more of biodiversity: Can higher-taxon richness predict wholesale species richness? Biol. Conserv. 1994, 67, 211–217. [Google Scholar] [CrossRef]
- Balmford, A.; Jayasuriya, A.H.M.; Green, M.J.B. Using higher-taxon richness as a surrogate for species richness: II. Local applications. Proc. Biol. Sci. 1996, 263, 1571–1575. [Google Scholar] [CrossRef]
- Hilsenhoff, W.L. Rapid field assessment of organic pollution with a family level biotic index. J. N. Am. Benthol. Soc. 1988, 7, 65–68. [Google Scholar] [CrossRef]
- Barbour, M.T.; Gerritsen, J.; Snyder, B.D.; Stribling, J.B. Rapid Bioassessment Protocols for Use in Streams and Wadeable Rivers: Periphyton, Benthic Macroinvertebrates and Fish, 2nd ed.; U.S. Environmental Protection Agency, Office of Water: Washington, DC, USA, 1999.
- Bailey, R.C.; Norris, R.H.; Reynoldson, T.B. Taxonomic resolution of benthic macroinvertebrate communities. J. N. Am. Benthol. Soc. 2001, 20, 280–286. [Google Scholar] [CrossRef]
- Reynoldson, T.B.; Norris, R.H.; Resh, V.H.; Day, K.E.; Rosenberg, D.M. The reference-condition: A comparison of multimetric and multivariate approaches to assess water-quality impairment using benthic macroinvertebrates. J. N. Am. Benthol. Soc. 1997, 16, 833–852. [Google Scholar] [CrossRef]
- Ferraro, S.P.; Cole, F.A. Taxonomic level sufficient for assessing a moderate impact on macrobenthic communities in Puget Sound, Washington, USA. Can. J. Fish. Aquat. Sci. 1992, 49, 1184–1188. [Google Scholar] [CrossRef]
- Resh, V.H.; Unzicker, J.D. Water quality monitoring and aquatic organisms: The importance of species identification. J. Water Pollut. Control Fed. 1975, 47, 9–19. [Google Scholar] [PubMed]
- Hölldobler, B.; Wilson, E.O. The Ants; Harvard University Press: Cambridge, MA, USA, 1990. [Google Scholar]
- Longcore, T. Terrestrial arthropods as indicators of ecological restoration success in coastal sage scrub (California, USA). Restor. Ecol. 2003, 11, 397–409. [Google Scholar] [CrossRef]
- Herms, D.A.; McCullough, D.G. Emerald ash borer invasion of North America: History, biology, ecology, impacts, and management. Annu. Rev. Entomol. 2014, 59, 13–30. [Google Scholar] [CrossRef] [PubMed]
- Duan, J.J.; Bauer, L.S.; Abell, K.J.; Ulyshen, M.D.; Van Driesche, R.G. Population dynamics of an invasive forest insect and associated natural enemies in the aftermath of invasion: Implications for biological control. J. Appl. Ecol. 2015, 52, 1246–1254. [Google Scholar] [CrossRef]
Figure 1. Relative abundance of the 10 numerically dominant coleopteran families found in forests associated with emerald ash borer-induced ash mortality.
Figure 2. Cumulative coleopteran family richness at five forested sites in north central Kentucky varying in levels of EAB-induced (Emerald Ash Borer-induced) disturbance.
Figure 3. Relationship between relative herbivore ( ) and fungivore ( ) abundance and richness among coleopterans sampled from EAB-impacted (Emerald Ash Borer-impacted) forests.
Figure 4. Coleopteran feeding guild abundance at five forested sites in north central Kentucky, including (a) herbivores, (b) saprophages, (c) fungivores, (d) xylophages, (e) predators, and (f) parasitoids. Means followed by the same letter do not differ (α = 0.05).
Figure 5. Relationship between Fraxinus canopy decline and abundance of two coleopteran predators: the Trogossitidae (Trogossitid abundance = 8.7 × canopy decline (%) + 19.5, R2 = 0.71, p = 0.07) and the Cleridae (Clerid abundance = 8.6 × canopy decline (%) + 3, R2 = 0.74, p = 0.06).
Table 1. Ash canopy dieback and coleopteran abundance at five sites in north-central Kentucky used to evaluate the colopteran community associated emerald ash borer-induced ash decline. Means followed by the same letter do not differ (α = 0.05).
|Site||Location (Lat., Long.)||Sample Intervals (Site Visits)||Fraxinus spp. Canopy Dieback (Mean % (s.e.))||Coleoptera Abundance 1||Coleoptera Evenness 2|
|Henry||38.56572, 85.14665||14||73.9 (4.6) a||1.30 (0.07) b||0.27 (0.01) a|
|Anderson||32.00857, 84.95980||13||56.9 (1.9) b||1.53 (0.07) ab||0.23 (0.01) a|
|Shelby||38.27980, 85.36258||16||27.4 (3.9) c||1.64 (0.06) a||0.27 (0.01) a|
|Spencer||38.02163, 85.27577||6||16.2 (2.8) cd||1.49 (0.11) ab||0.11 (0.01) b|
|Fayette||37.89653, 84.39270||10||7.4 (3.0) d||1.27 (0.08) b||0.17 (0.02) ab|
|F3,350 = 58.6; p < 0.001||F4,527 = 2.1; p < 0.02||F4,14 = 35.0; p < 0.01|
1 Number of individuals per day (LS-means ± s.e.) captured in ethanol-baited funnel traps. Means separation on transformed data. 2 Evenness index: .
Table 2. Relative abundance and richness of Coleopteran feeding guilds sampled from five sites affected by emerald ash borer ash decline.
|Trophic Guild||Abundance (%)||Richness (%)|
© 2018 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).