8 Invasive Root-feeding in Natural Forest Ecosystems of North America

D.R. COYLE,1 W.J. MATTSON2 AND K.F. RAFFA1 1University of Wisconsin, Department of Entomology, Madison, Wisconsin, USA; 2USDA Forest Service, Rhinelander, Wisconsin, USA

8.1. Introduction

8.1.1. Importance of belowground herbivory

Many studies have examined aboveground herbivory as it relates to primary production and nutrient dynamics (Mattson and Addy, 1975; Ritchie, 1998; Hunter, 2001a). However, studies of belowground herbivory are largely lack- ing (Hunter, 2001b) even though belowground productivity, albeit much less conspicuous, is comparable to aboveground productivity (Newman et al., 2006). In forests, conservative estimates indicate that fine roots (≤2 mm in diameter) alone represent 33% of global annual net primary productivity (NPP) (Jackson et al., 1997), and as much as 73% of total NPP may occur belowground in some systems (Fogel, 1985). Fine-root NPP was estimated at >2 Mg ha−1 year−1 in a deciduous hardwood stand in the Adirondack Mountains (Burke and Raynal, 1994), and exceeded 4 Mg ha−1 year−1 in sugar maple, Acer saccharum, stands in Wisconsin (Aber et al., 1985). Average below- ground NPP is 7 Mg ha−1 year−1 in temperate forest systems (Burrows et al., 2003). Belowground herbivory can have numerous effects at scales of individ- ual plant roots and shoots, plant communities and ecosystems (see Blackshaw and Kerry, Seastedt and Murray, Hunter and Johnson et al., Chapters 3, 4, 5 and 9, respectively, this volume). Root feeders often decrease the below- ground biomass and alter the physiology of their host plant, and may exert a significant influence on primary production (Detling et al., 1980). Stevens et al. (2002) proposed root herbivory as the leading explanation for 37% fine- root mortality in a longleaf pine, Pinus palustris Miller, stand. Consistent with this hypothesis, an insecticidal soil drench increased fine-root longevity by up to 125 days, and decreased fine-root mortality by as much as 41% in peach, Prunus persica Batsch, trees (Wells et al., 2002). ©CAB International 2008. Root Feeders: An Ecosystem Perspective 134 (eds Johnson and Murray) Invasive Root-feeding Insects of North America 135

Root density and surface area are correlated with a plant’s competitive ability to gather water and nutrients (Casper and Jackson, 1997). Belowground herbivory can reduce competitive abilities, which can be particularly import- ant at high plant densities. The relationship between root herbivory and com- petitive ability was demonstrated in purple loosestrife, Lythrum salicaria L. (Nötzold et al., 1998), where Hylobius transversovittatus Goeze (Coleoptea: ) delayed flowering and reduced plant height, shoot weight and total biomass. In addition, fine-root feeders can greatly alter the carbon and nutrient flow throughout a habitat (Blossey and Hunt-Joshi, 2003), as fine roots generally have the highest nitrogen concentration, an essential element for development (Scriber and Slansky, 1981). Despite the importance of belowground herbivory, little is known about native species in natural systems. The majority of our knowledge of below- ground herbivores is from studies of pests of turf, agriculture and planta- tion forests. Of these, the corn rootworm, Diabrotica spp. (Coleoptera: Chrysomelidae), complex is probably the most damaging root feeder in agricultural systems worldwide, costing North American farmers over US$1 billion annually (ARS, 2001). Another well-studied example involves red pine, P. resinosa Solander, decline and Christmas tree mortality in the mid-western USA (Rieske and Raffa, 1993; Erbilgin and Raffa, 2002). There are few well-studied rhizophagous pests in natural systems in North America, with cicadas (Hemiptera: Cicadidae) being one exception (see Hunter, Chapter 5, this volume).

8.1.2. Invasive species

Biological invasions constitute one of the greatest threats to native biodiver- sity (Gurevitch and Padilla, 2004), being partially responsible for nearly 50% of extinct or imperiled species in the USA (Wilcove et al., 1998). They cost the US economy an estimated US$120 billion annually (Pimentel et al., 2005), and may persist undetected for years before discovery (Liebhold et al., 1995; Mattson et al., 2007). Invasive plants such as kudzu, Pueraria spp., cost the USA nearly US$500 million annually, and salt cedar, Tamarix spp., can out- compete native flora, reduce the available groundwater (Hoddenbach, 1987) and reduce resident nesting bird species by >97% (Anderson and Ohmart, 1977). Invasive pathogens cost the USA an estimated US$30 billion year−1. For example, the exotic fungi causing Dutch elm disease (Ophiostoma spp.), white pine blister rust (Cronartium ribicola J. C. Fisch. ex Rab) (Peterson and Jewell, 1968; Gibbs and Wainhouse, 1986), butternut canker (Sirococcus clavigigenti-juglandacaerum N. B. Nair, Kostichka and Kuntz) (SAMAB, 1996), chestnut blight fungus (Cryphonectria parasitica [Murrill] M. E. Barr) (Liebhold et al., 1995) and sudden oak death (Phytophthora ramorum S. Werres, A. W. A. M. De Cock) (Rizzo et al., 2002) have dramatically and irrevocably altered ecosystem structure, composition and function. are one of the major groups of invasive species in North America, and have had enormous economic and ecological effects. Forests 136 D.R. Coyle et al.

are particularly susceptible to exotic insect invasions, partially because of the vast area and diverse ecosystems they cover. There are many well- documented cases of invasive insects in US forests (Mattson et al., 1994), but, nearly all published examples are aboveground feeders. Folivores such as the gypsy moth, Lymantria dispar L. (Lepidoptera: Lymantriidae), can alter species com- position of mature forests under heavy, repeated defoliation, and reduce aes- thetic values of parks and urban areas (Liebhold et al., 1995). The hemlock wooly adelgid, Adelges tsugae Annand (Homoptera: Adelgidae), threatens to eliminate hemlocks from eastern US forests (Orwig and Foster, 1998). Recently, the woodwasp, Sirex noctilio Fabricius (Hymenoptera: Siricidae), was discovered in New York (Hoebeke et al., 2005), subjecting several Pinus spp. to potential infestation and mortality. Aboveground insects have received the vast majority of attention world- wide because they are more apparent, and their aboveground life histories make them easier to study. The number of known invasive aboveground insects dwarfs the number of invasive belowground insects. For example, www.invasive.org lists 223 invasive insect species – of which only six are belowground pests. Less than 10% of the 423 exotic phytophagous insects in North American forests are root feeders (Mattson et al., 1994, 2007). In Canada, Kimoto and Duthie-Holt (2006) list 41 exotic forest insect species, of which only four feed belowground. Just as belowground herbivory by native insects is largely underesti- mated (Blossey and Hunt-Joshi, 2003), the same is likely true for invasive species. Again, our knowledge is derived mainly from cultivated systems. In North America, the major invasive root-feeding agricultural pest is the clover root curculio, Sitona hispidulus Fabricius (Coleoptera: Curculionidae), causing yield losses of nearly 1 Mg ha−1 (Hower et al., 1995). The Japanese , Popillia japonica Newman (Coleoptera: Scarabaeidae), feeds on more than 300 plant species in the USA and costs over US$450 million each year for control and management (Mannion et al., 2001; Potter and Held, 2002). The black vine , Otiorhynchus sulcatus Fabricius (Coleoptera: Curculionidae), is a serious pest of many ornamental tree species and small fruits (Moorhouse et al., 1992). The sugarcane rootstalk borer, Diaprepes abbreviatus L. (Coleoptera: Curculionidae), has recently been found on the West Coast of North America (Grafton-Cardwell, 2005), and threatens to severely impact plant production. The sweet potato weevil, Cylas formicarius Fabricius (Coleoptera: Brentidae) (Chalfant et al., 1990), European crane fly, Tipula spp. (Diptera: Tipulidae) (Umble and Rao, 2004) and several scarabs (Coleoptera: Scarabaeidae) (Jackson and Klein, 2006) are also economically important invasive belowground pests in North America. Although an insect’s economic impact often drives the research, its envir- onmental impact can be equally important. For example, a suite of invasive root-feeding (Coleoptera: Curculionidae) has established in the north- ern hardwood forests of eastern North America, and research has just begun to determine their range and impact. In this chapter, we summarize what is known so far about these insects, discuss their impacts on the northern forest ecosystems and suggest future research strategies and directions. Invasive Root-feeding Insects of North America 137

8.2. Invasive Root-feeding Weevils in Eastern North American Deciduous Forests

8.2.1. Species composition

A complex of nine invasive rhizophagous weevils has been found by various trapping methods in northern hardwood forests in the north-eastern and Great Lakes Regions of North America. Two of these, sericeus Schaller and oblongus L., are generally the most abundant, comprising >80% of the total weevil population (Pinski et al., 2005b; D.R. Coyle, 2008, unpublished data). The other species, in order of relative abundance, include Sciaphilis asper- atus Bonsdorff, pellucidus Boheman, Trachyphloeus aristatus Gyllenhal and O. ovatus L. (Pinski et al., 2005b; D.R. Coyle, 2008, MI, unpublished data). Pitfall trapping recently yielded two additional invasive species, Calomycterus setarius Roelofs and Pachyrhinus elegans Schoenherr (Werner and Raffa, 2000), and sticky traps yielded the most recently discovered species, Strophosoma mel- anogrammum Forster (Shields et al., 2008). Only two native species have been found so far: H. warreni Wood via pitfall trapping (Werner and Raffa, 2000) and Hormorus undulates Uhier via sweepnetting. While there is some variation in phenology, the life cycles of these spe- cies are very similar. Adults emerge in late spring and early summer. They have an obligatory pre-oviposition feeding period on the developing buds and leaves of various understory deciduous woody plants, especially seed- lings and saplings of sugar maple, hop hornbeam, Ostrya virginiana Koch, yellow birch, Betula alleghaniensis Britton, basswood, Tilia americana L. and various shrubs including raspberry (Rubus spp.). Their impact on the leaf surface area of these plants can be severe, at times approaching 100% defolia- tion. Mating takes place soon after emergence and oviposition occurs approx- imately 2 weeks later, when eggs are deposited near or into the soil. Larvae hatch in approximately 1 month and begin feeding on root tissue. Larvae overwinter in the soil, and resume feeding the following spring until they pupate in May. Larval feeding habits and host preferences are, for the most part, unknown. However, we do know that some larvae do not enter a winter diapause, particularly if snowpack prevents a deep soil freeze. Preliminary data show that even over winter, some new fine roots are pro- duced by trees and larvae recovered during the winter months were active and increasing in weight, suggesting growth even during the winter months. Yet overall, little is known about the larval ecology and their feeding impacts on the invaded ecosystems.

8.2.2. Adult host range

Like many invasive coleopterans that feed on woody plants, including scarabs (Reding and Klein, 2007) and Otiorhynchus root weevils (Van Tol et al., 2004; Fisher, 2006), this suite of nine European weevils is polyphagous, feed- ing on many species of trees and shrubs. is known to feed 138 D.R. Coyle et al.

on elm (Ulmus spp.), maple (Acer spp.), birch (Betula spp.), hop hornbeam, aspen (Populus tremuloides), willow (Salix spp.), basswood, pear (Pyrus spp.), apple (Malus spp.), various shrubs and strawberries (Fragaria spp.) (Felt, 1928; Massee, 1932; Caruth, 1936; Fields, 1974; Helsen and Blommers, 1988). Hop hornbeam and mountain maple (A. spicatum Lamarck) were preferred in laboratory trials, followed by basswood, white birch (Betula papyrifera Marshall), sugar maple, red maple (A. rubrum), aspen, poplar (Populus) and yellow birch (Pinski et al., 2005a). P. sericeus feeds not only on many of the same aforementioned hosts, but also on oak (Quercus spp.), hazel (Corylus spp.) and alder (Alnus spp.) (Parrott and Glasgow, 1916; Frost, 1946; Simmons and Knight, 1973; Morris, 1978; Casteels and De Clercq, 1988; Gharadjedaghi, 1997). In laboratory feeding trials, yellow birch and basswood were the most preferred host species, fol- lowed by hop hornbeam, white birch, red oak (Quercus rubra), poplar, aspen, sugar maple, mountain maple and red maple (Pinski et al., 2005a). The generalist B. pellucidus feeds on strawberry (Bomford and Vernon, 2005), raspberry (Levesque and Levesque, 1994) and grapes (Vitis spp.) (Bouchard et al., 2005). This is a widely distributed invasive weevil, and is known to feed on hosts from the plant families Anacardiaceae, Asteraceae, Fagaceae, Rosaceae, Ulmaceae, Vitaceae (Bouchard et al., 2005) and Cucurbita- ceae (Barrett and Agrawal, 2004). Interestingly, B. pellucidus is an important component of salamander diets in the north-eastern USA (Maerz et al., 2005). Sciaphilis asperatus feeds primarily on sugar maple, birch, raspberry and other trees and shrubs (Henshaw, 1888; Witter and Fields, 1977; Levesque and Levesque, 1994; Maerz et al., 2005), as well as plants in the family Apiaceae (Šerá et al., 2005). In addition, we have captured S. asperatus on hop horn- beam and basswood. Hosts commonly consumed by both P. oblongus and P. sericeus (and pre- sumably by S. asperatus) in the northern hardwood forest include sugar maple, red maple, hop hornbeam, elm, basswood and wild raspberry. Leatherwood, Dirca palustris L., is almost never eaten even though it is rela- tively common. Few records of T. aristatus exist, but these weevils are occasionally found in northern hardwood forests (Pinski et al., 2005a). Trachyphloeus bifoveolatus, a close relative, is reported to be a common pest of grasslands (Barstow and Getzin, 1985), raspberries (Levesque and Levesque, 1994) and vineyards (Bouchard et al., 2005).

8.2.3. Geographic distribution

Without aggressive and systematic sampling, determining an accurate geo- graphic range for any insect species is extremely difficult. None the less, with the help of many insect museum curators across the north-eastern and mid- western USA, and eastern Canada, we have compiled what we believe is an accurate picture of the current distribution of this suite of invasive weevils (Table 8.1). Due to the low numbers of T. aristatus and O. ovatus captured, we Invasive Root-feeding Insects of North America 139

Table 8.1. Confirmed collection locations of invasive root-feeding weevils in North America. See text for references.

Species USA Canada

Phyllobius oblongus Connecticut, Michigan, New Brunswick, Nova Minnesota, New Hampshire, Scotia, Prince Edward New York, Ohio, Pennsylvania, Island, Quebec Wisconsin, West Virginia Polydrusus sericeus Connecticut, Illinois, Indiana, New Brunswick, Nova Massachusetts, Michigan, Scotia, Ontario, Prince Minnesota, New Hampshire, Edward Island, Quebec Ohio, Pennsylvania, Wisconsin Barypeithes pellucidus California, Connecticut, District British Columbia, New of Columbia, Idaho, Illinois, Brunswick, Newfoundland, Indiana, Massachusetts, Nova Scotia, Ontario, Maryland, Maine, Michigan, Prince Edward Island, Minnesota, North Carolina, Quebec New Hampshire, New Jersey, New York, Ohio, Oklahoma, Oregon, Pennsylvania, Rhode Island, Utah, Virginia, Vermont, Washington, Wisconsin, West Virginia Sciaphilis asperatus Colorado, Connecticut, Idaho, Alberta, British Columbia, Massachusetts, Maryland, New Brunswick, Nova Maine, Michigan, Minnesota, Scotia, Ontario, Quebec North Carolina, New Hampshire, New Jersey, New York, Ohio, Oklahoma, South Dakota, Vermont, Wisconsin

will focus on P. sericeus, P. oblongus, B. pellucidus and S. asperatus. Several ref- erences were also used in constructing these ranges (Arnett, 1973; O’Brien and Wibmer, 1982; Wibmer and O’Brien, 1989; Majka et al., 2007a,b) as well as the generous help from nearly 20 public and University museum curators. P. oblongus was first recorded in New York, USA, in 1923 (Felt, 1928). It has been captured in eastern Canada, throughout the north-eastern USA, south to West Virginia and west to Minnesota, where it was first collected in 1990. P. sericeus, first discovered in Connecticut in 1934 (Britton, 1934), has been captured in every state and province bordering the Great Lakes, sev- eral north-eastern US states and in the Maritime Provinces of Canada. S. asperatus was first captured in Nova Scotia in 1884 (Harrington, 1891). Currently, it is well established in the north-eastern USA, and there are scat- tered records of its occurrence across much of southern Canada and the northern USA, including as far south as Oklahoma and North Carolina. B. pellucidus has the most cosmopolitan distribution of this group, having 140 D.R. Coyle et al.

been collected in all the Maritime Provinces of Canada and Quebec, Ontario and British Columbia. Blatchley and Leng (1916) first reported this weevil in several north-eastern states in the early 1900s. Barypeithes pellucidus has been recorded from nearly all states in the north-east and bordering the Great Lakes, and as far south as North Carolina and Oklahoma, and in several states west of the Rocky Mountains.

8.2.4. Population dynamics

We annually monitored larval abundance of the soil-inhabiting invasive weevil complex in the Ottawa National Forest in Gogebic County of the western Upper Peninsula of Michigan from 1998 to 2007. Each November we extracted 30–40 randomly placed soil cores (6.45 cm diameter × 16 cm length) from the same 100 × 40 m quadrat of a northern hardwood forest dominated by a dense canopy of mature sugar maple (Pinski et al., 2005a). Soil cores were stored in plastic bags and returned to the laboratory, where we sieved them to recover all meso-macro invertebrates, but especially weevil larvae. All larvae were counted and then saved to measure fresh and dry weights and retained in 80% ethanol for later sorting to species. Weevil larval populations varied yearly by nearly tenfold, and ranged from 112 to 972 m−2 (Fig. 8.1A). Their annual mean density was 571 m−2. Larval fresh mass per square metre varied yearly and ranged almost 14-fold, from 0.52 to 7.11 g m−2, with a 10-year mean of 3.62 g m−2 (Fig. 8.1B). If weevil lar- vae are randomly distributed within the forest, then the data from our soil cores should conform to the Poisson probability distribution where the sam- ple variance (v2) is equal to the sample mean (v2 = m) (Sokal and Rohlf, 1995). However, Fig. 8.2 reveals instead that sample variances were generally larger than the mean, and increased approximately as follows: v2 = m + m2/k, where k = 3, the variance equation for the negative binomial probability distribu- tion. The parameter k is an index of over-dispersion or aggregation due per- haps to the heterogeneous distribution of larval foods and to behaviour such as egg dumping by mothers. But, should the k values be very large or very small, then the underlying data would likely represent the Poisson or the logarithmic distributions, respectively.

8.3. Impacts on Forest Ecosystems

8.3.1. Soil processes

In order to determine the effects that root feeding is having on northern hard- wood forests we need to know how much root tissue the larvae are consum- ing. We can estimate this quantity using larval weights from our 10-year larval sampling data (Fig. 8.1A and B). The larvae were probably only two- thirds grown in November, having yet to finish their feeding and final growth in the ensuing spring after soil temperatures permitted feeding. Assuming Invasive Root-feeding Insects of North America 141

(A) 1200

1000 2 800

600

400 Numbers per m 200

(B) 10 9 8 2 7 6 5 4 3 Grams fwt per m 2 1 0 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 Year

Fig. 8.1. Annual estimates of (A) larval weevil density and (B) total weevil larval biomass at Taylor Lake, Gogebic Co., Michigan. The dashed line in (B) is the overall mean. Sampling was conducted in November of each year.

20

10 V 2 = m + m 2 k

Variance / where k = 3

0 0123456 Mean larval density/soil core

Fig. 8.2. Relationship between sample variance and mean of larval root-feeding weevil abundance. Sampling was conducted at Taylor Lake, Gogebic Co., Michigan, each November during 1998–2007. 142 D.R. Coyle et al.

that the gross efficiency of food conversion for larvae feeding on fine roots is about 5–10% (Slansky and Scriber, 1985), then average total plant consump- tion by November is roughly 10–20 times fresh larval mass, or 36–72 g m−2 fresh root weight. Furthermore, assuming that fine-root net primary produc- tion averages about 200 g m−2 dry weight in northern hardwood forests (Burke and Raynal, 1994), then weevils may be consuming up to 15% of fine- root mass after accounting for their spring feeding. Little information is available on how root herbivory affects soil micro- bial communities. One approach for measuring soil microbes is phospholipid fatty acid analysis, where lipids of the microbe cell walls are removed and measured, giving an indication of the relative abundance and types of microbes present in the sample (Kao-Kniffin and Balser, 2007). As root herbi- vory increases, the amount of dead root tissue may increase, as roots may be severed or only partially eaten. An increased number of herbivores will result in an increased amount of frass in the soil, and Hunter (2001a) showed that elevated frass inputs to the soil can drastically alter soil microbiota. The soil microbial community is expected to respond positively to changes in amount and quantity of available organic matter. Herbivory reduces the amount of plant material in the soil, therefore reducing the amount of plant material that will eventually die (e.g. fine-root turnover). This can induce a chain reaction of lower carbon accumulation and reduced carbon flow in an ecosystem (Cebrián and Duarte, 1995), unless graz- ing stimulates compensatory plant growth. Most carbon balance and nitrogen cycling models do not take root herbivory into account even though it may greatly alter the flux of carbon from naturally dying plant material into the ecosystem. In addition, few soil respiration studies include and identify inputs from soil dwelling fauna, even though this guild is an important contributor to overall soil respiration (Hanson et al., 2000). Fine-root turnover represents a large source of soil carbon accumulation, and is often nearly as high as fine- root production (McClaugherty et al., 1982). Root herbivory by weevil larvae could drastically alter this balance by accelerating root turnover, decreasing aboveground productivity and altering soil carbon fractionization pools. Högberg et al. (2001) showed that a high proportion of plant carbon allo- cation is belowground, suggesting that nutrient cycling and energy fluxes through terrestrial ecosystems are larger than previously thought. Estimates of global root turnover and primary production may also be greatly under- estimated (Chapin and Ruess, 2001), in part due to the paucity of data on the impact of root herbivores. More detailed, intensive and systematic measure- ment of the impact of root herbivores could lead to a fundamental paradigm shift in our understanding of their roles in root turnover and nutrient cycling.

8.3.2. Displacement of native fauna

In the Lake States, invasive curculionid larvae comprise between 75% and 82% of the belowground insect mesofauna (Pinski et al., 2005a, Invasive Root-feeding Insects of North America 143

D.R. Coyle, 2008, unpublished data). Less than 1% of the larval curculionids were from native species. Invasive weevil adults likewise dominate above- ground fauna in the understory. Considering the overwhelming proportion of larval curculionids to total fauna, and the ratio of invasive to native root weevils, we can confidently say this suite of invasive weevils is the dominant belowground and aboveground fauna in this system. This raises the question: before the weevils’ introduction to North America, what organisms dominated the belowground ecological niche? While it is possible that prior to the introduction of these invasive weevils there was no root-feeding guild in this ecosystem, this seems unlikely. A more probable scenario is that a native complex of root feeders was replaced by a complex of invasive species that were more efficient competitors. Some evidence sup- ports this idea, namely the rare capture of native weevil species. Curculionid collections in insect museums throughout the range of the northern hard- wood forests may hold the answer to this question. If displacement of native species occurred, we would expect the ratio of native to exotic weevils to decline precipitously with collection date. This shows the need for biological surveys that yield baseline data and studies that utilize the resources avail- able in insect museums across North America and worldwide.

8.3.3. How are community processes and forest structure affected?

In northern hardwood forests, root feeding by weevils may reduce seedling vigour and increase mortality, reducing regeneration and eventually chang- ing forest structure. Larval weevil feeding on fine roots may indirectly select for more grazing-tolerant plant species or genotypes, as plant tolerance likely varies among individuals. It is unknown if larval weevils feed selectively on the roots of seedlings or mature trees, or show no preference. Given few reports of physiological differences between the fine roots of mature versus young trees, it seems unlikely that larvae have major preferences between them. Wounds caused by root feeding may result in elevated susceptibility or access to pathogens. The soil is rich in microorganisms, and part of a tree’s defences is the protective epidermis on fine roots. Root feeding damages this tissue, creating infection courts. Root feeding by larvae may weaken plants, and reduce their competitive ability to compete with other invasive species, such as pathogens or other species of plant. Invasive root-feeding weevils could potentially predispose northern for- est ecosystems to subsequent biological invasions. For example, several spe- cies of invasive plants are known to aggressively colonize forest gaps. Similarly, root-feeding curculionids could potentially predispose stands to invasive earthworms. Our sampling during 2001–2002 indicated low dens- ities of earthworms, only 61 m−2 (R.A. Pinski, 2002, unpublished data), com- pared to areas in which they have become well established, with densities of >565 m−2 (Eisenhauer et al., 2007). More studies are needed to examine inter- actions between exotic earthworms and arthropod fauna (Bohlen et al., 144 D.R. Coyle et al.

2004a,b). It is also possible that as earthworms become more established at these sites they could increase activities by established invasive weevils. For example, plants in areas with exotic earthworms have exhibited increased foliage nitrogen levels (Scheu, 2003) – which could increase food quality for adult weevils. Exotic earthworms can decrease fine-root biomass (Fisk et al., 2004), which could negatively impact root-feeding weevil larvae.

8.4. Conclusions

A complex of root-feeding weevils is established in North America, ranging throughout south-eastern Canada and the north-eastern USA. Rhizophagous larvae comprise a large portion of the belowground biomass and mesofauna abundance in the northern hardwood forests. They appear to have displaced much of the native fauna. We do not know how they are affecting plant ecology or nutrient cycles, and we have little information regarding their interactions with other native or invasive organisms. Additional research is needed to deter- mine the impacts on ecosystem function, production and overall health.

Acknowledgements

We are indebted to the many systematists who provided data for this project: C. Bartlett (University of Delaware), R. Bell (University of Vermont), S. Boucher (McGill University), D. Chandler (University of New Hampshire), G. Fauske (North Dakota State University), C. Freeman (The Ohio State University), P. Johnson (South Dakota State University), S. Krauth (University of Wisconsin), D. Larson (Memorial University), C. Majka (Nova Scotia Museum of Natural History), C. O’Brien (retired, Florida A&M University), G. Parsons (Michigan State University), K. Pickett (University of Vermont), G. Setliff (University of Minnesota), L. Shapiro and K. Kim (Penn State University). This work could not have been completed without the assist- ance of many dedicated technicians from UW-Madison and the USDA Forest Service. Funding has been provided for this research and publication from the USDA Cooperative State Research, Education and Extension Service (CSREES Proj WI50 and WIS04969), an EPA STAR Fellowship and grant from Applied Ecological Services, Inc., to DRC, and the USDA Forest Service and UW-Madison College of Agriculture and Life Sciences.

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