Biol Invasions (2012) 14:863–873 DOI 10.1007/s10530-011-0123-7 ORIGINAL PAPER Damage levels from arthropod herbivores on Lonicera maackii suggest enemy release in its introduced range Deah Lieurance • Don Cipollini Received: 21 March 2011 / Accepted: 17 October 2011 / Published online: 1 November 2011 Ó Springer Science+Business Media B.V. 2011 Abstract The ‘enemy release hypothesis’ argues indicate that levels of herbivory experienced by when a species is introduced to a novel habitat, release L. maackii are relatively consistent across sites, vary from regulation by herbivores results in increased slightly with habitat and branch identity, but are likely vigor, abundance, and distribution. The invasive Asian too low to impact fitness of shrubs. These findings shrub Lonicera maackii appears to benefit from an indicate that low amounts of arthropod herbivory absence of arthropod herbivores in North America. occur for L. maackii across its introduced range, which We assessed the incidence, amount, and type of may contribute to its invasive success. herbivory occurring on L. maackii in forest edge and interior habitats and investigated differences in timing Keywords Herbivory Á Lonicera maackii Á Amur of damage. In October 2008, leaves were sampled honeysuckle Á Enemy release hypothesis from shrubs in forest interior and edge habitat from 8 sites in Ohio. In 2009, sampling was repeated at 3 sites in spring, summer, and fall with a distinction made Introduction between long and short branches. Leaf area removed averaged 1.83% across the 8 populations in 2008 and There are many studies that have tried to determine 3.09% across the 3 populations in 2009, with forest what characteristics (i.e. efficient resource utilization, edge plants receiving slightly more damage than forest high relative growth rates, and phenotypic plasticity) interior plants in 2008. Additionally, long shoots make an invasive species successful (e.g. Bazzaz received more damage than short shoots in 2009. 1986; Feng et al. 2007; Osunkoya et al. 2010a, b). One Damage incidence was also higher in the edge habitat prominent hypothesis explaining the success of inva- and on long shoots compared to short shoots. As sive plants in their new habitats is the ‘enemy release measured in 2009, damage accumulated steadily hypothesis’ (ERH) which suggests that when a plant throughout the season. Chewing was the most invader is introduced to a new habitat it will experi- prevalent type of damage (76. 8%) and low level of ence a reduction in regulation by specialist herbivores pathogen infection was observed (4.81%). Results or pathogens that are present in the native range, which can result in an increase in distribution and abundance (Keane and Crawley 2002). Research has suggested D. Lieurance (&) Á D. Cipollini that enemy release has provided a competitive Department of Biological Sciences and Environmental advantage to such invaders as Norway maple (Acer Sciences PhD Program, Wright State University, 3640 Colonel Glenn Highway, Dayton, OH 4543, USA platanoides) in northeastern United States, butter- e-mail: [email protected] fly bush (Buddleja davidii) in Europe, soapbush 123 864 D. Lieurance, D. Cipollini (Clidemia hirta) in Hawaii, and whitetop (Lepidium of L. maackii allows the plant to capitalize on such draba) in western United States (Adams et al. 2009; conditions presented in edge habitat including Cincotta et al. 2009; Cripps et al. 2006; DeWalt et al. increased light availability (Hutchinson and Vankat 2004; Ebeling et al. 2008; Morrison and Mauck 2007). 1997; Luken et al. 1995b). However, edge habitats can Results supporting this hypothesis commonly report exhibit increased arthropod abundance and diversity increased growth and reproduction of plants in the relative to understory habitats, and presumably invasive range compared to the native range (e.g. increased herbivore incidence and damage potential Colautti et al. 2004; Ebeling et al. 2008). (Barbosa et al. 2005; Ozanne et al. 2000). The extent to Lonicera maackii (Rupr.) Maxim (Amur honey- which the ERH may explain the success of L. maackii suckle), is one of the most important and prominent in North America has not been determined, and a first invasive plant species in the Midwestern United step requires estimates of herbivory levels on this States. Lonicera maackii, a deciduous woody shrub species in its invasive range. Anecdotal observations native to China, Japan, Korea, and southeastern indicate that L. maackii escapes meaningful levels of Russia, was originally introduced in the late 1880s herbivore and pathogen attack in its invasive range for habitat improvement, erosion control, and horti- (D. Lieurance and D. Cipollini, personal observa- cultural landscaping (Luken and Thieret 1996). Traits tions). Trisel (1997) reported damage amounts from a that L. maackii shares with many other invasive plants combination of frost, deer browse, insect herbivory, include extended leaf phenology, rapid aboveground and drought on L. maackii at Miami University in growth rates, high fecundity, broad phenotypic plas- Oxford, Ohio from 1992 to 1994 that were well below ticity, and tolerance to a variety of habitats (Lieurance various native woody species. Damage levels have 2004; Luken et al. 1995a, b; 1997a, b; Trisel 1997; never been quantified on this species in its native McEwan et al. 2009b). Additionally, L. maackii range. However, observations of L. maackii in its responds to increases in light availability with a native versus introduced range indicate that the shrub plastic response in branch architecture, producing two grows more vigorously and abundantly in its intro- distinct branch types, ‘long’ and ‘short’ (Luken et al. duced range (Luken and Thieret 1996), while being 1995a, b). Long branches extend the crown height in much rarer in its native range in China (J. Ding, response to increased light and are presumably cheap personal communication), and endangered in Japan in construction, poorly defended, and expendable, (http://www.biodic.go.jp/english/rdb/red_plants.csv). while short branches have leaves that are thicker, In an effort to characterize the natural enemies of tougher, and more resistant to herbivory (Ballare Lonicera spp. in their native range and to identify 2009; Guerra et al. 2010; Herms and Mattson 1992; possible biocontrol candidates, 44 insect species and Ishii and Shoko 2010). 21 fungal species were reported on the genus in China Current land use patterns have resulted in disturbed including 4 arthropod species specifically attacking habitats, fragmentation of forests in rural areas, and L. maackii (Zheng et al. 2006). In contrast, observa- creation of suburban woodlots all of which provide tions of L. maackii growing alongside the native appropriate habitat for L. maackii to spread across the Lonicera reticulata in Ohio revealed native vines landscape. In Ohio and Kentucky, L. maackii shrubs suffering substantial early season damage from the comprise up to 50% of the understory species com- specialist honeysuckle sawfly (Zarea inflata)while position in some small woodlots, and near monocul- exotic shrubs remained undamaged by this insect tures along the edges of old fields and roadsides (D. Lieurance, personal observation). (Hartman and McCarthy 2008; Medley 1997; Enemy escape can result from a combination of this Pennington et al. 2010; Watling and Orrock 2010). apparent lack of specialist herbivores and resistance to As anthropogenic habitat fragmentation increases, the generalists that may be present in the invasive range. creation of edge habitat insures the persistence and Resistance strategies employed by plants include the spread of L. maackii in the landscape. The conditions production of secondary metabolites used to defend presented to organisms by edge habitats are often very against herbivores. Previous research has identified different than those of the understory with significant several phenolic metabolites in leaves of L. maackii, microenvironmental differences in temperature, light, including chlorogenic acid, several flavones and their and moisture (Matlack 1993). The adaptive plasticity glycoside derivatives, and iridoids (Cipollini et al. 123 Damage levels from arthropod herbivores 865 2008a, D. Bowers, personal communication). These short branches; and (5) because the early season compounds may act as deterrents to generalist herbiv- phenology of L. maackii provides an abundant food ory and be responsible for some of the allelopathic source for early spring herbivores, the majority of effects attributed to L. maackii (Cipollini et al. 2008a, damage would occur in the spring and then increase b; Dorning and Cipollini 2006; Cipollini and Dorning through time. Results of this study provide informa- 2008; McEwan et al. 2009a; Trisel 1997). It has been tion on the autecology of L. maackii in its introduced postulated that secondary metabolites effective in range and indicate whether enemy release may herbivore defense are a result of coevolution with contribute to the success of this woody invasive. herbivores present in their native habitat (Becerra 2003; Ehrlich and Raven 1964) and for non-native plants the separation from coevolved herbivores is Materials and methods integral to ERH (Keane and Crawley 2002). However these metabolites may be novel and/or effective Sample collection 2008 against generalist herbivores that may be present in the introduced range. Samples were collected in October, 2008 from eight Sometimes a non-native invader can experience sites