A review on the invasion ecology of Amur honeysuckle (Lonicera maackii, Caprifoliaceae) a case study of ecological impacts at multiple scales Author(s): Rachel E. McNeish and Ryan W. McEwan Source: The Journal of the Torrey Botanical Society, 143(4):367-385. Published By: Torrey Botanical Society DOI: http://dx.doi.org/10.3159/TORREY-D-15-00049.1 URL: http://www.bioone.org/doi/full/10.3159/TORREY-D-15-00049.1

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A review on the invasion ecology of Amur honeysuckle (Lonicera maackii, Caprifoliaceae) a case study of ecological impacts at multiple scales1 Rachel E. McNeish2 and Ryan W. McEwan Department of Biology, University of Dayton, Dayton, OH 45469-2320

Abstract. Invasive species are of global importance because of their impacts on ecological communities, habitat structure, native community dynamics, and ecosystem processes and function. Scientists and conservation managers are increasingly focusing on the biological impacts of invasive species and on devising management practices that emphasize the health of ecosystems based on measured biological processes. Amur honeysuckle (Lonicera maackii (Rupr.) Herder) is a highly successful invasive shrub in forests of eastern North America. The scientific literature surrounding this species has grown in the past several decades as researchers have investigated L. maackii impacts across multiple ecological scales. In this review we synthesized literature on (a) the key traits related to this species’ invasion success, (b) the impacts this invasive species has at various ecological scales, (c) the outcomes of restoration efforts for this species, and (d) the connections of this weed to invasion ecology theories. Lonicera maackii impacts are complex and vary across ecosystems and spatial scales; we report findings from studies demonstrating a wide range of effects on species composition, community structure, ecosystem function, and successional trajectories. We end by providing a working ecological framework that may help guide future research and conservation efforts. Key words: Ecosystem processes, invasion ecology, invasion theory, restoration impacts, terrestrial-aquatic linkages

Invasive species are considered to be one of the cooperative weed management areas and invasive most important threats to biodiversity and ecosys- plant boards. tem function across the globe (Ruesink et al. 1995, From both a management and scientific per- Wilcove et al. 1998), with the economic costs spective, there is a clear need to identify invasive estimated to be as high as approximately $120 US species and ensure they are thoroughly studied and billion/yr (Pimentel et al. 2005). Invasive plants have well-established, empirical evidence of eco- have prompted a great deal of interest with systems effects (Gurevitch and Padilla 2004, particular focus on quantifying the effects invaders Sagoff 2005). For example, tamarisk has been have on plant communities (other articles in this classified as an invasive in southwestern USA and special issue, Levine 2000, Collier et al. 2002, previous research suggested this plant reduced Crooks 2002, Callaway and Ridenour 2004). water availability through increased evapotranspi- Effects ascribed to invasive plants include modi- ration rates (ETR; Thomas 1963). More-recent fication of habitat structure, changing ecosystem studies have indicated that the ETR of riparian, processes, and decreasing native biodiversity invaded forests with tamarisk is the same, (Hejda et al. 2009). Many states in the USA have regardless of tamarisk density, and the impacts of rules about invasive plants, and efforts to manage tamarisk varies among sites (Stromberg and Chew activities for invasives are widespread and include 2002, Stromberg et al. 2009). Invasion implies high abundance of a particular problematic spe- 1 The authors thank Anastasia Stolz for her confocal cies, and although this can be easily measured in photos of L. maackii and her P. serotina images and to the field (and is visually obvious), some have Meg Maloney and Erin Rowekamp for their photos of argued that exotic species have been too quickly Anaxyrus americanus and T. migratorius. This work was ‘‘demonized’’ or ‘‘vilified’’ as ‘‘invasive’’ before supported in part by the Office for Graduate Academic Affairs, University of Dayton, through the Graduate their effects on ecosystems are fully understood Student Summer Fellowship Program, and by the (Stromberg and Chew 2002, Gurevitch and Padilla National Science Foundation (DEB 1352995). 2004, Borrell 2009, Stromberg et al. 2009, Davis 2 Author for correspondence: rachel.e.mcneish@ 2011). The native vs. exotic paradigm has started gmail.com shifting, and scientists continue to focus on doi: 10.3159/TORREY-D-15-00049.1 quantifying the biological impacts of particular ÓCopyright 2016 by The Torrey Botanical Society Received for publication September 1, 2015, and in species (Chew and Hamilton 2010, Thompson and revised form December 28, 2015; first published August Davis 2011) to inform management practices that 1, 2016. positively influence the ecosystem’s health, based 367 368 JOURNAL OF THE TORREY BOTANICAL SOCIETY [VOL. 143 on measured biological processes (Borrell 2009, during the industrial revolution and globalization Stromberg et al. 2009). eras—have been the most effective dispersal Amur honeysuckle (Lonicera maackii (Rupr.) agents, spreading invasive weeds across oceans Herder.) is a highly successful invasive shrub in and continents (Meyerson and Mooney 2007). The the eastern deciduous forest. Concern over this initial introduction of common reed (Phragmites species is widespread and, in fact, legal limitations australis (Cav.) Trin. ex Steud.) to the USA is exist in some states (USDA 1999). Initial research believed to have occurred at coastal ports along the on this species provided an outstanding back- Atlantic ocean, with dispersal of this invasive ground on the invasion biology of L. maackii promoted by the use of ship ballast to fill marsh (Luken 1988, Luken and Goessling 1995, Luken et sites used for railroad development (Saltonstall al. 1995, Hutchinson and Vankat 1998, Deering 2002). High propagule pressure combined with and Vankat 1999, Gould and Gorchov 2000). Since long-distance dispersal vectors and anthropogenic then, an extensive body of empirical evidence has activities are a potent combination for the success been developed that documents this plant’s (a) of invasive plants. suite of invasive traits, (b) success as regulated by Lonicera maackii is a good model of long- landscape characteristics, and (c) significant im- distance dispersal and abundant propagule produc- pacts at multiple ecological scales. This burgeon- tion in invasive plants. These shrubs have large ing scientific literature makes L. maackii an ideal fruiting events (Fig. 1a) and produce seeds that can species to serve as a model of invasion impact; germinate in various light, temperature stratifica- however, no recent consolidation of the empirical tion, and soil conditions (Luken and Goessling evidence has, to our knowledge, been made. 1995, Hidayati et al. 2000). We have also In this article, we synthesize the available documented the presence of L. maackii berries literature to provide a framework for understand- submerged in streams with and without L. maackii ing the ecological effects of L. maackii and to help in the riparian forest (Fig. 1b; R.E.M. and R.W.M., direct future research and management practices. personal observation)—suggesting stream corri- We begin by describing how anthropogenic dors are vectors for the spread of L. maackii activities and the life-history traits of L. maackii propagules. Bartuszevige and Gorchov (2006) contributed to its invasion success in the USA. We found some native birds (e.g., Turdus migratorius; then summarize findings from empirical studies American robin) eat and disperse viable L. maackii that identify key traits that regulate the invasion of seeds via defecation. Castellano and Gorchov L. maackii into vulnerable habitats and describe (2013) found that 68% of L. maackii seeds were the effects this invasive plant has at various still viable after passing through the intestinal system of Odocoileus virginianus (white-tailed ecological scales. We end by connecting L. deer). Although the fruits of this species are a poor maackii to invasion ecology theories and identify source of nutrition for wildlife (Ingold and Cray- directions for future research that will strengthen craft 1983), these animals contribute to the long- and advance plant invasion biology. distance dispersal of L. maackii and may specif- Lonicera maackii Advantageous Life-History ically support dispersal to edge habitats (Bartusze- vige and Gorchov 2006, Castellano and Gorchov Traits. DISPERSAL MECHANISMS. Long-distance dispersal and propagule pressure are key charac- 2013). teristics that contribute to the success of invasive RAPID GROWTH AND ENVIRONMENTAL PLASTICITY. plant populations (Gosper et al. 2005, Davies and Rapid growth and plasticity in response to Sheley 2007). For example, Japanese stilt grass changing environmental conditions are character- (Microstegium vimineum (Trin.) A. Camus) prop- istic traits of successful invasive species. For agule pressure was found to be 556.6 and 144.5 instance, mile-a-minute (Polygonum perfoliatum plants/m2 in riparian and upland forests, respec- L.) is an invasive Asian vine well known to grow tively (Eschtruth and Battles 2011). Camphorweed quickly, as indicated by its common name (Oliver (Heterotheca latifolia Buckey) dispersal was found 1996). Fogarty and Facelli (1999) demonstrated to be related to wind patterns in the Georgia the invasive European shrub Scotch broom piedmont area (USA), with expansion increasing at (Cytisus scoparius (L.) Link) grows faster than, a rate of 4.8 km/yr (Plummer and Keever 1963). and successfully outcompetes, South Australian Arguably, anthropogenic activities—especially natives varnish wattle (Acacia verniciflua A. MCNEISH AND MCEWAN: A REVIEW ON THE INVASION ECOLOGY OF AMUR 2016] HONEYSUCKLE 369

FIG.1. Lonicera maackii fall fruit production in (a) terrestrial, and (b) stream-run habitats. (c) Freeze- resistant leaves in mid-December 2009, and (d) senesced leaf litter in a headwater stream in southwestern Ohio, USA. Photos taken by R.E.M.

Cunn), myrtle wattle (Acacia myrtifolia (Sm.) (Deering and Vankat 1999). When upright stems Willd.), and beaked pincushion tree (Hakea are clipped, they resprout readily (Luken and rostrata F. Muell. Ex Meisn.). A Hawaiian study Mattimiro 1991, Deering and Vankat 1999), which that surveyed more than 60 invasive and native adds to this plant’s already ‘‘bushy’’ appearance plants found that invasives spent less energy and contributes to a dense L. maackii canopy that producing leaves and had greater specific leaf decreases light availability to the herb layer. This area, CO2 assimilation, and N and P levels than plant is also known to exhibit growth plasticity in natives did (Baruch and Goldstein 1999). These different habitats (Luken et al. 1995, 1997b). results also indicate that invasive plants have Compared with spicebush (Lindera benzoin (L.) phenotypic plasticity, which, in turn, may facilitate Blume), L. maackii was found to successfully use a their success in novel habitats. Invasive plants are range of light levels (1, 25, and 100% of full-sun commonly thought to grow faster than native photosynthetic photon flux density) more effec- weeds do, this trait is usually accompanied by the tively for growth and photosynthesis and to exhibit plant’s ability to use resources well, with greater higher branch plasticity and stomatal density phenotypic and genetic plasticity than natives have (Luken et al. 1997b). Seedling establishment can (Daehler 2003). occur in a variety of light conditions, and shrubs Lonicera maackii has a highly competitive located in open habitats produce significantly growth pattern, which is an important phenotypic greater numbers of fruits than do those in shaded characteristic that helps facilitate its success in new habitats (Luken and Goessling 1995, Luken and habitats. This woody shrub produces numerous Thieret 1996, Lieurance 2004). The net primary stem shoots and grows rapidly as an immature productivity and aboveground biomass of L. stem, then shifts resource allocation toward height maackii in open, high-sunlit habitats are substan- growth and reproduction in its mature stage tially greater compared with shrubs located in low- 370 JOURNAL OF THE TORREY BOTANICAL SOCIETY [VOL. 143 light woodland communities (Luken 1988, Lieur- and Dukes 2007). These chemicals are secondary ance 2004). The unique growth plasticity of L. plant compounds that typically suppress the maackii leaves and branches across light environ- growth, survivorship, and reproductive capabilities ments provides this shrub a competitive edge in a of competitors (Hierro and Callaway 2003). A variety of habitats. meta-analysis of common invasive plants in China found 75% of the most noxious invasive weeds PHENOLOGY. Invasive plant species’ phenologies displayed evidence of allelopathic effects (Ni et al. have been shown to vary, compared with natives in 2012). Stinson et al. (2006) found evidence that the invaded habitat. Japanese barberry (Berberis the antifungal phytochemistry of A. petiolata can thunbergii DC.), an invasive in the eastern indirectly disrupt the mutualistic relationship deciduous forest, leafs out nearly 1 mo earlier between hardwood trees and mycorrhizal fungi, than do native shrubs and demonstrates signifi- which can result in a reduction of tree-seedling cantly greater photosynthetic capacity than native regeneration in forest communities. Allelochem- plant species do (Xu et al. 2007). An invasive icals also affect microbial communities (Callaway biennial herb, garlic mustard (Alliaria petiolata and Ridenour 2004), suggesting invasive plants (Bieb.) Cavara & Grande), has a competitive edge may alter those communities and nutrient cycling in early spring because its leaves emerge earlier in terrestrial and aquatic systems. than native herbs do and because it achieves high A series of studies were conducted that photosynthetic rates (Myers and Anderson 2003). established evidence of the L. maackii allelopathic Tree-of-heaven (Ailanthus altissima (P. Mill.) effects on plants. Cipollini et al. (2008c) identified Swingle) is another invasive plant that leafs out 13 secondary metabolites present in L. maackii in early spring, stores high concentrations of leaves and demonstrated that luteolin and apigenin photosynthate in its leaves and stems, and is derivatives were the main allelopathic chemicals efficient at photosynthesis, making this plant present in leaf extracts. Lonicera maackii root and highly competitive early in the growing season shoot extracts have been shown to reduce (Fryer 2010). A combination of early leaf germination of several native herbaceous plants, emergence and efficient photosynthetic processes including jewelweed (Impatiens capensis Meerb.), are important characteristics that promote the and tall thimbleweed (Anemone virginiana L.) success and spread of invasive plant species. (Dorning and Cipollini 2005, McEwan et al. 2010, Lonicera maackii has an extended growing Cipollini and Flint 2013). McEwan et al. (2010) season in comparison with other plants. Leaf also demonstrated L. maackii leaf and fruit extracts development and expansion occurs 2 to 3 wk had differential effects on four grass and forb earlier, and the final leaf abscission is later than species. Lonicera maackii fruit extracts suppressed native species (McEwan et al. 2009a). Another all forb and grass seed germination in tall fescue competitive edge is that the leaves are freeze (Festuca arundinacea Schreb, known synonym, resistant and are still present on shrubs during early Schedonorus arundinaceus), a dwarf white impa- winter (Fig. 1c; McEwan et al. 2009a). As stated tiens hybrid (Impatiens walleriana Hook. f. known earlier, L. maackii propagule production is copious synonym buzzy lizzy), garden coreopsis (Coreop- in the fall, and berry formation begins in early fall sis lanceolata L.), and Kentucky bluegrass (Poa and will stay attached well into winter (R.E.M. and pratensis L.), whereas leaf extracts only sup- R.W.M., personal observation; Fig 1a). Massive pressed seed germination of I. walleriana. Other flower production occurs in midspring (Luken and experimental studies have focused on the effects of Thieret 1996), and these flowers are a resource for L. maackii extracts on the morphology, fecundity, pollinators (Goodell et al. 2010, McKinney and reproduction, and growth on Arabidopsis (Arabi- Goodell 2011). The combination of previously dopsis thaliana (L.) Heynh.) (Cipollini and Dorn- described growth characteristics and phenology ing 2008, Cipollini et al. 2012). Mouse-ear cress gives L. maackii a competitive edge that increases grown in L. maackii–conditioned soils exhibited its ability to outcompete native flora. decreased survivorship and an 11-day delay in ALLELOPATHY AND RESISTANCE TO HERBIVORY. flower production; however, seed production and Some invasive plant species have been shown to mature leaves were larger and more abundant exhibit biochemical effects on predators through compared with those grown in unconditioned soils the production of allelochemicals (Theoharides (Cipollini and Dorning 2008). Schradin and MCNEISH AND MCEWAN: A REVIEW ON THE INVASION ECOLOGY OF AMUR 2016] HONEYSUCKLE 371

Cipollini (2012) conducted a study to identify extracts compared with control food. Lieurance positive or negative feedbacks on L. maackii and Cipollini (2013a) conducted a study to identify growth compared with the native northern bush how juvenile L. maackii shrubs responded to honeysuckle (Diervilla lonicera Mill.) grown in herbivory under conditions of environmental different soil types and to determine whether stress. They found that, at low light and nitrogen growth patterns were due to soil abiotic or biotic levels, L. maackii tolerance and resistance to conditions. Soil type (sandy and loamy) and herbivory was still high. These findings suggest conditioning and soil biota influenced the sign L. maackii has strong resistance to natural and strength plant-soil feedbacks. For example, L. predators, which may be another competitive maackii grew approximately two times more in its strategy for this invasive species. own conditioned, sandy soil (L. maackii–condi- tioned) compared with unconditioned soil, result- Lonicera maackii Invasion Effects at Various ing in a positive feedback. Soil sterilization Ecological Scales. EFFECTS ON PLANT COMMUNITIES. resulted in negative feedback, decreasing L. As invasive species encroach and proliferate in maackii growth in sandy soil. Alternatively, there habitats, they modify substrate, resources, and was negative feedback on D. lonicera growth ecosystem processes, which can result in substan- when grown in its own soil, with feedback effects tial changes in plant and animal communities neutralized when the soil was sterilized. Cipollini taxonomically and functionally (Randall 1996, et al. (2012) also conducted a study to determine Shea and Chesson 2002, Vila` et al.2011). whether L. maackii and the invasive herb A. Empirical evidence suggests L. maackii invasion petiolata had similar allelopathic effects on A. has substantial negative impacts on native plants. thaliana. Results indicated that L. maackii leaf Forests with this invasive shrub have significantly extracts reduced reproduction and growth of A. less herb fecundity, fitness, and growth (Gould and thaliana, whereas there were few effects from A. Gorchov 2000, Miller and Gorchov 2004). Collier petiolata. Bauer et al. (2012) cautioned that et al. (2002) found that herb abundance and allelopathic impacts are dependent on context, richness significantly decreased under L. maackii based on their field study, which suggested soil shrubs compared with away locations and with microorganisms and different native species are stands that had longer L. maackii residence times. important factors that influence net allelopathic Lonicera maackii exhibited strong aboveground effects. These collective findings suggest the competition, where removal of its shoots increased chemistry of L. maackii can have an effect on seedling and herbaceous growth (Gorchov and native plant communities, and strong evidence Trisel 2003), survivorship (Cipollini et al. 2008a, suggests it has allelopathic effects in some Gorchov and Trisel 2003), and species richness experimental settings; however, more research is (Musson and Mitsch 2003). The presence of L. needed to understand how allelopathic effects are maackii shrubs may also decrease recruitment of manifested in the invasion biology of L. maackii in secondary forests because native seedlings experi- the field. ence greater herbivory because of the lack of protective herbaceous cover under L. maackii Evidence suggests that L. maackii has some shrubs (Meiners 2007). White et al. (2014) found traits that confer resistance to herbivory in its when L. maackii abundance increased in riparian introduced range. McEwan et al. (2009b) investi- zones, native tree seedling and sapling densities gated the antiherbivory potential of L. maackii on decreased. Invaded forests are predicted to expe- the invasive generalist gypsy moth caterpillar rience alterations in species interactions and (Lymantria dispar; Erebidae). Caterpillar relative species composition, ultimately affecting commu- consumption and growth rates were significantly nity structure, function, and successional trajecto- reduced when provided with only L. maackii as a ries (Hutchinson and Vankat 1997, Luken et al. food resource. The development time of the 1997a, Hartman and McCarthy 2008). caterpillars was also inhibited when fed L. maackii, and all larva died before molting to the next stage. ANIMAL COMMUNITY IMPACTS. Effects of invasive Cipollini et al. (2008c) found indications that the plants on animals are an important motivating factor moth generalist beet armyworm (Spodoptera for managers of natural areas and for the public. exigua; Noctuidae) had reduced feeding when Pysekˇ et al. (2012) found nearly 70% of studies given food sources made with L. maackii leaf reported nonnative invasive species vegetation 372 JOURNAL OF THE TORREY BOTANICAL SOCIETY [VOL. 143 negatively affected animal communities. Most er, invaded plots supported greater Acari (mites invasive plants are pollinated by generalists, which and ticks) abundance than did noninvaded plots. can affect native plant-pollinator mutualistic rela- These studies demonstrate L. maackii has differ- tionships (Richardson et al. 2000, Traveset and ential effects on arthropod communities, influenc- Richardson 2006). For example, ornamental jewel- ing resources and habitat substrate for arthropod weed (Impatiens glandulifera Royle), an Asian use. invader in central Europe, attracts native bee Lonicera maackii can also have consequences pollinators because its nectar is more nutrient rich on human-related disease vectors. This shrub has than that of the native flowers, resulting in been demonstrated to affect Ochlerotatus triser- decreased fitness and abundance for the native iatus (known synonym: Aedes triseriatus; Culici- flowers (Chittka and Schu¨rkens 2001). Ballard et al. dae), which is the disease vector for the La Crosse (2013) found arthropod abundance, biomass, and encephalitis virus (Conley et al. 2011). In fact, richness was substantially reduced on nonnative Conley et al. (2011) found the oviposition of this plants compared with native plants, suggesting disease-vectoring mosquito decreased with L. nonnative plants may affect food resources (e.g., maackii density, suggesting L. maackii alters the arthropods) that support higher trophic levels. These landscape by decreasing the amount of habitat studies highlight the importance of research on (e.g., tree holes) available for oviposition. A invasive plant impacts on animal communities. different study found L. maackii may be a Lonicera maackii has substantial effects on food facilitator of the West Nile Virus mosquito vector resources for fauna, resulting in alterations in food- Culex pipiens (Culicidae; Shewhart et al. 2014). web dynamics and disease-vector population Mosquito eggs exposed to L. maackii leaf and dynamics. Goodell et al. (2010) found L. maackii flower leachates had the highest larval survivorship serves as a resource for pollinators and was related compared with native leaf leachates, and only to increased pollinator visits and pollen deposition larvae exposed to L. maackii leachates reached of the native herb largeleaf waterleaf (Hydro- adulthood (Shewhart et al. 2014). In a study phyllum macrophyllum Nutt.) despite L. maackii observing the effects of L. maackii on tick-borne shading effects (McKinney and Goodell 2011). diseases, it was found white-tailed deer visited L. Alternatively, McKinney and Goodell (2010) maackii–invaded areas more frequently, which found spotted geranium (Geranium maculatum supported a greater number of lone star ticks L.) pollination visits and seed set were reduced in (Amblyomma americanum) that were infected with the presence of L. maackii, suggesting L. maackii a bacterial pathogen from the ehrlichiosis group has differential impacts on pollinators. Loomis et (Ehrlichia spp.) compared with areas in which L. al. (2014) found spider taxa and guilds were more maackii was removed (Allan et al. 2010). These abundant in honeysuckle-present plots, with more studies suggest L. maackii may affect mosquito- than double the vertical colonization of spiders and tick-vector habitats and population dynamics, compared with honeysuckle-absent plots, suggest- ultimately affecting the incidence of human ing the complex branch architecture of L. maackii disease. is important for spider communities. However, Lonicera maackii invasion across the forest-to- Buddle et al. (2004) reported ground-dwelling urban gradient has substantially affected the predator spider communities were less diverse in survivorship of avian species fledglings and the narrow riparian forests and hedgerows compared nesting-habitat availability (Borgmann and Rode- with wider forests buffers because of decreased wald 2004, Rodewald 2009, McCusker et al. 2010, habitat complexity and ground cover, which the Rodewald et al. 2010). Forests with dense authors suggested may have been due to the Lonicera spp. invasion had increased densities of presence of L. maackii in these habitats. In a understory bird species (e.g., T. migratorius), similar study, Loomis et al. (2014) found other especially for overwintering birds, when Lonicera arthropod orders (e.g., Diptera, Hymenoptera, spp. fruit production was high; however, densities Coleoptera) were more diverse and vertically of upper-canopy birds (e.g., Contopus virens, covered more shrub area in honeysuckle-present eastern wood-pewees) decreased in these forests plots than honeysuckle-absent plots. Christopher (McCusker et al. 2010). Nest predation is one of and Cameron (2012) found L. maackii invasion did the most important threats to avian fledgling not affect arthropod community diversity; howev- success; therefore, it is important for birds to MCNEISH AND MCEWAN: A REVIEW ON THE INVASION ECOLOGY OF AMUR 2016] HONEYSUCKLE 373 select appropriate nesting habitats (Martin 1992). than they did native roughleaf dogwood (Cornus Borgmann and Rodewald (2004) found avian nest drummondii C.A. Mey.) during the spring (Mattos success of T. migratorius and Cardinalis cardinalis et al. 2013). These studies indicate some grani- (northern cardinal) was lower in invasive Lonicera vores and mesopredators may be positively spp. and multiflora rose (Rosa multiflora Thunb.) influenced by the presence of L. maackii; however, locations along an increased urban gradient more research is needed to identify how the compared with native woody species. Rodewald presence of this shrub may influence behavior. (2009) discovered an increase in Empidonax There has been some research related to how L. virescens (Acadian flycatcher) brood parasitism maackii may mediate amphibian communities. was positively related to the number of stems Watling et al. (2011c) investigated how invaded around the nest. Stems were associated with L. L. maackii plots in a deciduous forest altered the maackii invasion, suggesting its ‘‘bushy’’ growth understory microclimate (temperature and humid- pattern creates perching sites for brown-headed ity) and amphibian community. Plots invaded by L. cowbirds (Molothrus ater) to view nests, increas- maackii had a lower mean daily temperature and ing opportunities for brood parasitism to occur. amphibian species richness and evenness and Rodewald et al. (2010) suggest L. maackii experienced a shift in the amphibian community presence results in an ecological trap for avian composition. In a study focused on the interaction species. Lonicera maackii is suspected to be an of predators and L. maackii chemistry on amphib- ephemeral ecological trap for C. cardinalis be- ian larvae, artificial pools were created in invaded cause of its unique leaf phenology. Birds may and noninvaded plots (Watling et al. 2011b). Pools preferentially build nests in L. maackii shrubs to were lined with soil that was or was not chemically hide nests from predators because of the early leaf influenced by L. maackii growth and allowed to fill out this plant exhibited in the spring compared up with natural rain water. It was found that with native plants; however, L. maackii shrubs lack Anaxyrus americanus (American toad) larvae the habitat complexity needed for nesting sites, development was significantly faster in pools which, in actuality, makes nests more susceptible containing leaf litter and soil from L. maackii. to predation and results in a decrease in overall Hickman and Watling (2014) also found A. bird annual production (Rodewald et al. 2010). americanus tadpoles exhibited increased risk- Research has yet to identify if L. maackii prone behaviors, such as increased surfacing and influences bird plumage color, an important trait swimming behavior in L. maackii leachate, for mate selection; however, a study conducted by regardless of the presence of predator chemical Witmer (1996) found that E. virescens tail bands cues. These findings indicate L. maackii chemi- change from yellow to orange when Morrow’s cally alters amphibian habitat, indirectly altering honeysuckle (Lonicera morrowii A. Gray) fruits risk-prone behavior and making these animals were consumed. These studies indicate L. maackii more susceptible to predators. shrubs provide poor habitat for avian fauna, Odocoileus virginianus is an important ungulate creating an ecological trap that reduces avian known to reduce tree seedling and herbaceous success. regeneration (Tilghman 1989, Rooney and Dress The invasion of L. maackii can also initiate 1997), forest habitat structure (McShea and Rap- behavioral changes in animals, resulting in alter- pole 1992, Fuller 2001), and food-web interactions ations in foraging behavior and predation risk. (Rooney and Waller 2003). Several studies have Peromyscus leucopus (white-footed mouse) was indicated there is an important relationship be- found to increase in risky behavior (e.g., foraging) tween L. maackii and O. virginianus. Deer are in L. maackii stands (contingent upon food known to eat L. maackii berries, and Castellano availability and moon light), most likely because and Gorchov (2013) found 68% of seeds were still of the high canopy cover L. maackii provides in viable after passing through the deer gut, suggest- the shrub layer (Mattos and Orrock 2010). Similar ing this ungulate can be an important dispersal findings were observed for other nocturnal mam- vector of L. maackii. Christopher et al. (2014) mals (e.g., opossums and raccoons), with mice demonstrated both L. maackii presence and O. preferring to forage under L. maackii shrubs on virginianus browsing decreased annual and spring cloudless nights (Dutra et al. 2011). Rodent perennial abundance. A L. maackii 3 O. virgin- granivores also preyed on L. maackii seeds more ianus interaction effect revealed O. virginianus 374 JOURNAL OF THE TORREY BOTANICAL SOCIETY [VOL. 143 reduced perennial abundance regardless of L. communities, affecting ecosystem function and maackii presence or absence. In a study examining processes. Further research is needed to fully the interactive effect of L. maackii and O. virgin- understand how these microbial effects may ianus on litter arthropod communities, no interac- manifest as alterations of ecosystem function. tive effect was found on arthropod diversity and total abundance, but there was a significant Lonicera maackii Invasion and Landscape interaction effect on the abundance of Acari Ecology. Plant species invasions have been (Christopher and Cameron 2012). Lonicera strongly linked to land use and characteristics of maackii led to a decrease in Aranea spp. (orb- the landscape matrix in which the potentially weaver spiders) abundance, whereas there was an invadable habitat is embedded (Hutchinson and increase in Acari abundance, suggesting L. maack- Vankat 1998, Bartuszevige et al. 2006, Johnson et ii and deer may have indirectly affected arthropod al. 2006). For instance, Johnson et al. (2006) communities (Christopher and Cameron 2012). reported a relationship between invasive species Future research is needed to understand how the colonization and site features such as soil pH. Edge interactive role of L. maackii and O. virginianus effects can also strongly influence resource can affect higher trophic levels and ecosystem availability within a given site. Bartuszevige et processes. al. (2006) and Yates et al. (2004) found the amount of edge in the landscape surrounding habitat MICROBIAL COMMUNITY IMPACTS. Invasive species patches was a strong determinant of invasion and affect soil and aquatic microbial communities, small forest patches are susceptible to edge effects which are crucial to organic matter processing and nutrient cycling, resulting in alterations in ecosys- well into their interiors. Intensive land use is well- tem processes and function (Kourtev et al. 2002, known to have a lasting influence on the Hawkes et al. 2005, Gessner et al. 2007, Claeson vegetation composition of forests (Bellemare et et al. 2014). Invasive plants tend to support al. 2002, Foster et al. 2003), including the different microbial communities, when compared facilitation of invasive species establishment with native plants, coupled with unique leaf (Johnson et al. 2006). Moreover, if the historical characteristics (e.g., increased nitrogen), which land use creates an ‘‘extinction debt’’ of native result in alterations in decomposition and nutrient species (Vellend et al. 2006), invasive species may transformation. Arthur et al. (2012) reported L. exploit the resources that were made available in maackii leaf-litter breakdown was five times faster, this ‘‘empty niche’’ (Hierro et al. 2005). had greater nitrogen, and less lignin concentrations Lonicera maackii is a good model species for than native white ash (Fraxinus americana L.) and understanding and demonstrating the landscape hickory Carya Nutt. spp. Through the decompo- ecology of plant invasion. Landscape features have sition process, L. maackii leaf litter maintained been shown to influence the invasion biology of microbial communities that were distinguishable this species, and anthropogenic features are from the community present on native species particularly important. For instance, Bartuszevige (Arthur et al. 2012). Ali et al. (2015) found that L. and Gorchov (2006) and Hutchinson and Vankat maackii leachate added to sterilized soil caused a (1997) both demonstrated this species’ presence in 1.5-fold increase in mycorrhizal infection of I. forest patches was positively related to the distance capensis compared with sterilized soil, generally to the nearest town. White et al. (2014) found L. increasing I. capensis growth; however, when leaf maackii was indicative of areas that were more extracts were added to live soil, there was a urbanized and less associated with forested areas. decrease in mycorrhizal infection of I. capensis Borgmann and Rodewald (2005) found that L. and overall growth. In a plant-soil feedback study maackii cover was best explained by an increase in that examined changes in arbuscular mycorrhizal urban land cover, and that L. maackii was more fungi abundance associated with invasive species, pervasive in urban forests compared with rural L. maackii reduced arbuscular mycorrhizal fungi ones. Flory and Clay (2005, 2009) demonstrated on native plant roots indirectly via soil legacy the density and germination success of L. maackii effects and directly when grown in conjunction increased closer to roadways and in forests at early with L. maackii (Shannon et al. 2014). These and midsuccessional stages in central and southern findings suggest L. maackii leaves support unique Indiana, USA. In a study conducted in Louisville, microbial communities and leachate alters soil KY, USA, L. maackii was shown to be less MCNEISH AND MCEWAN: A REVIEW ON THE INVASION ECOLOGY OF AMUR 2016] HONEYSUCKLE 375 successful in terms of stem density within forest described via five leaf breakdown experiments in patches located outside 10 km from the center of which L. maackii leaf breakdown was up to the city, compared with those within that distance approximately four times faster than that of several (Trammell and Carreiro 2011). Pennington et al. native leaf species (Arthur et al. 2012, McNeish et (2010) found L. maackii was a dominant species in al. 2012, Poulette and Arthur 2012, Trammell et urban riparian systems, and McNeish et al. (2012, al. 2012, Fargen et al. 2015). In an aquatic leaf- 2015) found that L. maackii–dominated riparian pack study, L. maackii leaves supported greater zones affected aquatic ecosystems, suggesting and a more-complex microbial growth, possibly accumulated impacts at the watershed scale may because of the increased number of trichomes, be more severe. which created a more-complex leaf-surface topog- raphy at the microscale, compared with black Lonicera maackii Effects on Ecosystem cherry (Prunus serotina leaves Ehrh.; Fig. 2; Processes. Ecosystems are open systems, suscep- R.W.M., unpublished data). Lonicera maackii leaf tible to subsidies and allochthonous flows of deposition into streams is quite high (Fig. 1d; resources from adjacent habitats (Baxter et al. McNeish et al. 2015); therefore, there may be 2005, Leroux and Loreau 2008). Invasive species impacts on the scaling of aquatic leaf processing can substantially alter ecosystem processes, such from the reach to the watershed level. as nutrient cycling, decomposition, and energy Lonicera maackii may also have substantial transformation, within and across ecosystems. effects on water and nutrient transformation and Kudzu (Pueraria montana (Lour.) Merr.) is an availability. In a terrestrial leaf-pack study, L. invasive, nitrogen-fixing legume found in the maackii released nitrogen faster compared with southeastern USA, which significantly increased sugar maple (Acer saccharum Marshall) leaf litter net N mineralization, nitrification, and nitric oxide (Trammell et al. 2012). Poulette and Arthur (2012) emissions from invaded soils by more than 100% found L. maackii increased N loss in mixed (Hickman et al. 2010). Mineau et al. (2012) found honeysuckle-hickory leaf packs up to approxi- the riparian invasive tree Russian olive (Elaeagnus mately two times more than any other honeysuck- angustifolia L.) substantially increased terrestrial le-native leaf-pack combination. A through-fall organic-matter subsidies and retention of leaf study demonstrated there was decreased through- organic matter in a stream system, resulting in an fall volume under L. maackii shrubs and cation estimated 14% decrease in stream ecosystem concentrations increased up to three times (Mc- efficiency (ratio of ecosystem respiration to Ewan et al. 2012). Lonicera maackii has been organic matter input). In a meta-analysis of 199 shown to have a higher transpiration rate compared articles presenting data related to invasive species with other shrubs, using an estimated 10% of effects, it was found that, although presence of ground and surface water (Boyce et al. 2011). invasive species tends to result in a decline of local Rapid uptake of surface water, coupled with high native species, many plant invasions result in leaf N concentration and loss during decomposi- increased ecosystem function (Vila` et al. 2011). tion, may support a positive nutrient feedback loop Several studies have demonstrated L. maackii for L. maackii shrubs, resulting in an impact on can affect a variety of terrestrial and aquatic forest production and water and nutrient transfor- ecosystem processes and functions. For example, mation and availability in terrestrial and aquatic Trammell et al. (2012) found total foliar biomass habitats. was 1.5 times lower in invaded L. maackii forests; however, L. maackii foliar biomass was 16 times Management and Restoration of Lonicera greater in those plots, compared with less-invaded maackii–Invaded Habitats. DETECTION AND forests. This study suggests L. maackii may MANAGEMENT. Early detection of invasive species negatively affect production of native tree and is an important proactive approach to manage- shrub species. In a tree-ring study, Hartman and ment (Moody and Mack 1988). The USA McCarthy (2007) found upper canopy trees had National Invasive Species Council developed reduced radial growth in forested sites with dense guidelines for early detection and rapid response L. maackii compared with noninvaded sites. of invasive species (USDOI 2015). Early detec- Lonicera maackii affects organic matter processing tion allows for preemptive eradication of nascent and availability in terrestrial and aquatic habitats as foci before these small populations combine into 376 JOURNAL OF THE TORREY BOTANICAL SOCIETY [VOL. 143

FIG. 2. Scanning electron microscope images of fresh (a) L. maackii, and (b) P. serotina leaves depicting trichome density and aquatic microbial and fungal growth on (c) L. maackii, and (d) P. serotina leaves anchored in a headwater stream for three days. Pilot study was conducted summer of 2010 with L. maackii and P. serotina leaf packs anchored in a small headwater stream for 7 days. Photos were taken by Anastasia Stolz. larger populations and become more difficult to unique, seasonal timing of leaf abscission of control (Moody and Mack 1988). Simberloff many invasive plants compared with native (2003) discusses the importance of early detection species, can be used to facilitate detection of and rapid response of invasive species, highlight- invasive species. These studies highlight that ing several successes in the eradication of early detection methods and preemptive efforts invasives, such as Acacia karroo (Vachellia are pivotal in the quest for managing plant karroo (Hayne)Banfi&Galasso)inWestern invaders. Australia and tansy ragwort (Senecio jacobaea L.) A suite of studies have identified practical in New Zealand. For example, killer alga detection and treatment methods that are useful (Caulerpa taxifolia (Vahl) C. Agardh) is a tropical for management of L. maackii. Environmental alga that has invaded the coasts along several remote-sensing images can be used to detect and countries, including France, Italy, and Spain. This map locations of invasive species in a cost- invasive alga was first sighted in a small coastal effective manner (Huang and Asner 2009). The area outside Monaco in 1984; however, no extended leaf phenology of Lonicera maackii management efforts were made until the popula- allows for detection in early spring and late fall tion spread along thousands of hectares (Simberl- using image differencing of satellite photos off 2003). Wilfong et al. (2009) demonstrated that (Wilfong et al. 2009). A combination of images satellite Landsat 5 Thematic Mapper e and with fine spatial resolution, data from TM Landsat 7 ETMþ imagery, coupled with the satellites, and ground truthing (field observations) MCNEISH AND MCEWAN: A REVIEW ON THE INVASION ECOLOGY OF AMUR 2016] HONEYSUCKLE 377 can potentially be one of the most-effective eventually causing leaves to brown and premature methods for early detection of L. maackii (John- senescence (Riffle and Watkins 1986, Beales et al. ston et al. 2012, Shouse et al. 2013). 2004). In a recent survey of L. maackii shrubs Several eradication studies have been conducted conducted around Cincinnati, OH, USA, 61.8% of to identify the most effective way to manage L. L. maackii stems were dead, which was approx- maackii. Schulz et al. (2012) found seasonal stem imately 58% more than found in reports from 1989 cutting, followed by an application of 18% (3.2%; Boyce et al. 2014). Thus far, there has been glyphosate, resulted in a 75–85% reduction of L. no studies, to our knowledge, on biocontrol agents maackii individuals, whereas stem cutting, fol- for L. maackii; however, a study by Waipara et al. lowed by spraying of regrowth shoots with 1% (2007) demonstrated herbivore and pathogen glyphosate approximately 40 days later, was less damage was low on Japanese honeysuckle (Loni- effective, resulting in up to 56% of L. maackii cera japonica Thunb.) in New Zealand and individuals killed. Rathfon and Ruble (2007) tested suggested further research on natural enemies in four removal-treatment methods: foliar application, the native L. japonica range is necessary for the streamline basal bark application, full basal bark development of biocontrol agents. application, and stump cutting with a chemical Lonicera maackii populations may be suscepti- application. Foliar applications were effective in ble to forest litter and allelopathic effects from controlling 70–90%, whereas basal bark applica- native plant species. Wilson et al. (2013) conduct- tions did not give consistent results and were thus ed a study to identify forest characteristics related considered unreliable. Stump cutting coupled with to L. maackii invasion. Findings indicated in- chemical application was most effective against creased oak (Quercus L.) leaf-litter depth was larger L. maackii shrubs, which resulted in more negatively associated with the presence of L. than 90% control of L. maackii shrubs. In a study maackii. Rietveld (1983) found the allelochemical examining the rationale of 1 yr vs. annual juglone, commonly found in the walnut (Juglans treatment of L. maackii, annual treatment of L. L.) family, had negative effects on L. maackii.In maackii via stump cutting treated with glyphosate that study, varieties of herbaceous and woody plant coupled with pulling plants was up to approxi- species, including L. maackii, were exposed to 3 mately six times more effective than a one-event different juglone concentrations (0–10 M). There treatment (Loeb et al. 2010). Hartman and Mc- was a significant decrease in L. maackii seed Carthy (2004) found that stump cutting with a germination (92–43%), radical growth (8–0 mm), treatment of glyphosate and stem injection with and shoot elongation (20–1 cm) when exposed to EZ-Ject Lance (EZ-ject, Omaha, NE) were both increasing juglone concentrations. These studies highly effective at killing L. maackii shrubs (. are important because they identified forest 94%). These collective studies suggest that best- characteristics that may increase forest community management practices for L. maackii is an resistance to L. maackii invasion. application a chemical herbicide immediately after LONICERA MAACKII MANAGEMENT IMPACTS ON stump cutting and repeating the process on an FLORA AND FAUNA. Several studies have document- annual or semiannual basis; although, a more cost- ed the effects on removal and managing L. maackii effective method may be to use foliar applications. on plant and animal communities. Runkle et al. In addition to human-induced efforts, there has (2007) found that 7–8 yr after L. maackii removal, been some natural dieback of invasive honeysuck- plant cover, tree seedling density, and species le species reported in several states throughout the richness increased—suggesting removal of L. Midwest, USA (Boyce et al. 2014). In recent maackii can enhance plant ground cover and affect years, some L. maackii shrubs have exhibited ecosystem productivity and function. Hartman and dieback because of the presence of a honeysuckle McCarthy (2004) conducted a removal and non- leaf blight fungus (Insolibasidium deformans: removal study to identify how removal of L. Basidiomycete; Boyce et al. 2014). This fungus maackii affected native seedling survivorship. affects individuals of the Lonicera genus and is They found 3 yr after L. maackii removal, seedling widespread throughout northcentral and northeast- survivorship was greater compared with plots in ern USA and the UK (Riffle and Watkins 1986, which L. maackii was present; however, seedling Beales et al. 2004). Symptoms of I. deformans survivorship varied among genera. Removal of L. start in spring when lesions on new leaves develop, maackii shrubs also resulted in an increase in the 378 JOURNAL OF THE TORREY BOTANICAL SOCIETY [VOL. 143 abundance of P. leucopus, an important generalist Simberloff 2006). For example, the European rodent (Shields et al. 2014). McNeish et al. (2015) buckthorn (Rhamnus cathartica L.) and the found removal of L. maackii from the riparian zone Lumbricus terrestris (European earthworm) may of a stream significantly increased in-stream light have cofacilitated one another in North America, availability, terrestrial organic matter contribution and their coinvasion may have facilitated several to the stream, and aquatic macroinvertebrate other invasive pests and insects (Heimpel et al. density, compared with a nonremoval stream 2010). These theories are often studied and reach, indicating management of L. maackii in considered separately; however, there is evidence terrestrial habitats can affect adjacent aquatic that many of these theories may apply to single systems. In a similar study, Fargen et al. (2015) species, and the theories themselves are conceptu- found removal of riparian L. maackii did not ally linked, which highlights the importance of influence in-stream leaf-litter decomposition; how- exploring these theories in tandem (Hierro et al. ever, L. maackii leaf-litter packs supported lower 2005, Joshi and Vrieling 2005). macroinvertebrate abundance compared with na- The invasion biology of L. maackii is a good tive A. saccharum litter packs. model for understanding the overlap and intercon- nection of some important invasion theories. For Connections to Invasion Theory. Several instance, the success of L. maackii has been linked theories have been developed to address how and to both the NWH and the ERH. Several studies why some nonnative species become overabun- presented in the Forest Community Impacts and dant, successfully outcompete natives, and even- Resistance to Herbivory sections above suggested tually become classified as invasive. For example, L. maackii may have allelopathic effects, inhibiting the empty niche hypothesis (ENH) presumes a native plant germination, growth, and development nonnative can become successful when there is and suppressing insect survivorship (Dorning and open habitat for the organism to colonize, Cipollini 2005; Cipollini et al. 2008b, c; McEwan proliferate, and spread outside its native range et al. 2009b, 2010). Lonicera maackii generally (Shea and Chesson 2002). The enemy release experiences low levels of arthropod herbivory hypothesis (ERH) details the idea a nonnative (Lieurance and Cipollini 2012) but has been becomes invasive when a natural enemy (e.g., commonly observed to be browsed by O. virgin- specialist consumer) is not present in the new ianus (Castellano and Gorchov 2013). Cipollini et range, and thus, the nonnative has essentially al. (2008c) identified secondary compounds in L. escaped from its natural enemy (Keane and maackii leachate that decreased insect herbivore Crawley 2002, Colautti et al. 2004). The novel consumption and native seed germination, sug- weapons hypothesis (NWH) states invasive plants gesting allelochemistry may in part explain why L. may bring with them, into ‘‘recipient’’ communi- maackii is so successful and lending support to the ties, new biochemistries that provides an advan- NWH. Lieurance and Cipollini (2013b) also tage, and through generations, this alteration may studied the herbivory effects of the specialist become selected for and increase in strength NorthAmericanhoneysucklesawfly(Zaraea (Callaway and Ridenour 2004). Some invasive inflata: Cimbicidae) and the generalist caterpillar plants are known to exhibit increased allelochem- Spodoptera frugiperda (fall armyworm: Noctui- ical production outside their native range, which dae) on L. maackii, grape honeysuckle (Lonicera may serve as a ‘‘novel weapon,’’ providing a reticulata Raf.), blackhaw (Viburnum prunifolium competitive edge against native species (Vivanco L.), and L. japonica (Japanese honeysuckle et al. 2004, Ni et al. 2012). The evolution of Thunb.) in field and laboratory settings. Lonicera increased competitive ability theory postulates maackii had significantly less foliage damage and that, with the removal of natural enemies, an was not affected by the sawfly specialist, which invasive plant will shift resources from defense to preferred L. reticulata over L. maackii when given growth to improve its competitive ability (Blossey a choice (Lieurance and Cipollini 2013b). The and Notzold 1995). Another major ecological generalist caterpillar fed equally on all Lonicera theory—invasional meltdown—predicts that the species, but, in laboratory assays, effects on L. success and establishment of one invasive species maackii were more strongly observed (Lieurance may facilitate and/or increase the establishment of and Cipollini 2013b). These findings lend support other invasive species (Simberloff and Holle 1999, to the NWH and ERH because (a) L. maackii MCNEISH AND MCEWAN: A REVIEW ON THE INVASION ECOLOGY OF AMUR 2016] HONEYSUCKLE 379

FIG. 3. Predictive framework for Lonicera maackii impacts across ecosystems at multiple ecological scales. produces allelochemicals that negatively affect communities. These findings lend support to the native plants and arthropods, (b) herbivory is quite hypothesis that L. maackii effects are complex and low on L. maackii, and (c) this invasive can escape vary across ecosystems and multiple ecological from specialist and generalist insect herbivores, scales (Fig. 3), suggesting this invasive has a which hinder native honeysuckle and confamiliars. diversity of impacts on species interactions and These findings also suggest strong potential for the composition, community structure and succession- evolution of increased competitive ability hypoth- al trajectories, and ecosystem function and pro- esis, particularly given the rapid growth rate and cesses. phenotypic plasticity of L. maackii. Observations Lonicera maackii transforms aquatic and terres- by the authors from forests in Ohio and Kentucky, trial ecosystems via alterations of terrestrial USA, suggest invasional meltdown may also be subsidies, habitat structure, community composi- occurring with L. maackii invasion because control tion, and ecosystem function (Fig. 3). The presence sites often display a profusion of A. petiolata of L. maackii along stream habitats (or potentially growth, and some areas of heavy invasion by L. along other water bodies) resulted in a substantial maackii are underlain by an invasion of winter change in the pool of resources in the aquatic creeper (Euonymus fortunei (Turcs.) Hand.-Maz.). system that support aquatic food webs and ecosystem processes (McNeish et al. 2015). Many Future Directions and Considerations. In this aquatic macroinvertebrates have a terrestrial adult review, we have synthesized empirical literature phase (e.g., mosquitoes and blackflies), and that demonstrated the effects of L. maackii across impacts on the population dynamics of aquatic- various ecological scales, ecosystem processes and insect life stages, which may result in a bottom-up function, and restoration efforts. Lonicera maackii effect on secondary production present in the has been shown to (a) suppress local plant species terrestrial habitat, and serves as an important food survivorship, growth, and reproduction; (b) de- resource for terrestrial vertebrates (Lounibos 2002, crease primary productivity and enhance the Baxter et al. 2005, Burdon and Harding 2008). Co- ecosystem processes of decomposition and nutrient occurring with L. maackii impacts in aquatic turnover; (c) increase risk-prone behavior and systems are similar effects in terrestrial systems. decrease reproductive success of certain animals; Lonicera maackii alters plant community compo- (d) provide needed protection from predators and sition and microbial communities, affecting the supply seeds as a food resource for granivores; (e) pool of resources available in terrestrial systems, provide support for human disease vectors; and (f) ultimately influencing amphibian, avian, and support high vertical diversity of certain arthropod arthropod communities (Gould and Gorchov 380 JOURNAL OF THE TORREY BOTANICAL SOCIETY [VOL. 143

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