The biology of Canadian weeds. 135. Lonicera japonica Thunb.

Brendon M. H. Larson1, Paul M. Catling2, and Gerald E. Waldron3

1Department of Environment and Resource Studies, University of Waterloo, Waterloo, Ontario, Canada N2L3G1; 2Biodiversity, National Program on Environmental Health, Agriculture and Agri-Food Canada, Research Branch, Saunders Bldg., Central Experimental Farm, Ottawa, Ontario, Canada K1A 0C6; 37641 County Road 20, R. R. #1, Amherstburg, Ontario, Canada N9V 2Y7. Received 18 April 2006, accepted 14 December 2006.

Larson, B. M. H., Catling, P. M. and Waldron, G. E. 2007. The biology of Canadian weeds. 135. Lonicera japonica Thunb. Can. J. Plant Sci. 87: 423–438. Japanese honeysuckle (Lonicera japonica Thunb.) is a twining semi-evergreen vine native to Japan, Korea and eastern China. Over the past 150 yr it has been introduced as an ornamental and become established in temperate and tropical regions worldwide. It was first discovered in Canada in 1976 in southwestern Ontario woodlands and has since been found growing without cultivation in 15 localities. While L. japonica does not occur very frequently in southern Ontario, climate change models suggest that it may become more abundant in this region. Its predominance elsewhere derives from morphological and physiological characteristics that allow it to be particularly successful in the edge habitats of fragmented landscapes. Through extensive vegetative propagation and competitive ability it occupies space which may otherwise host a diverse native flora. The plant has many uses in Asian medicine and is a popular ornamental, but has been prohibited in some regions due to its displace- ment of other species. A combination of cutting and foliar application of glyphosate has proven to be an effective control method in some circumstances. Planting of L. japonica should be discouraged and horticulturalists should consider alternative attractive vines. The spread of L. japonica should be monitored in Ontario and control of newly established populations should be consid- ered to avoid costly large scale control in the future.

Key words: Invasive species, Lonicera japonica, weed biology, climate change

Larson, B. M. H., Catling, P. M. et Waldron, G. E. 2007. La biologie des mauvaises herbes au Canada. 135. Lonicera japon- ica Thunb. Can. J. Plant Sci. 87: 423–438. Le chèvrefeuille du Japon (Lonicera japonica Thunb.) est une vigne volubile mi-sem- pervirente originaire du Japon, de la Corée et de l’est de la Chine. Introduite il y a 150 ans comme plante ornementale, elle s’est implantée dans toutes les régions tempérées et tropicales de la planète. L’espèce a été découverte pour la première fois au Canada en 1976, dans des boisés du sud-ouest de l’Ontario. Depuis, on la retrouvée à 15 endroits sans qu’elle y ait été plantée. Bien que L. japonica ne se rencontre pas souvent dans le sud de l’Ontario, les modèles du changement climatique laissent croire qu’elle pourrait devenir plus abondante dans cette région. Ailleurs, on doit sa prédominance à ses caractéristiques morphologiques et phys- iologiques qui lui permettent de prospérer dans les habitats à la lisière des reliefs morcelés. Une forte multiplication végétative et une bonne compétitivité lui permettent d’occuper les espaces où se développerait normalement une flore indigène plus diversifiée. Cette plante a maints usages dans la pharmacopée asiatique et est populaire en horticulture, mais on en a interdit la culture dans certaines régions à cause de sa propension à supplanter d’autres espèces. La coupe combinée à l’application de glyphosate s’avère efficace comme méthode de lutte dans certaines circonstances. On déconseille aux horticulteurs de planter L. japonica en leur sug- gérant d’opter pour d’autres vignes aussi attrayantes. Il conviendrait de surveiller la propagation de L. japonica en Ontario et de détruire les nouveaux peuplements si l’on veut s’épargner une lutte plus ardue et plus coûteuse dans l’avenir.

Mots clés: Espèce envahissante, Lonicera japonica, biologie des mauvaises herbes, changement climatique

1. Names - Aug.). Common synonyms include Nintooa japonica Lonicera japonica Thunb. – Japanese honeysuckle (Catling (Thun.) Sweet and Caprifolia japonicum (Thunb.) Kuntze. 1997; Nuzzo 1997), Chinese honeysuckle (often referring to The variety halliana (Dippel) G. Nicholson is a well-known var. chinensis), Hall’s honeysuckle (often referring to var. cultivated variety that has escaped in northeastern North halliana), woodbine (in older textbooks, Nuzzo 1997). America. This and other varieties, including chinensis (P. Chèvrefeuille du Japon (Erhaeghe 2004), clématite du Japon Watson) Baker, repens (Hort Bogor. ex Seibold) Rehder, (USDA 2005), ren dong (Chinese, USDA 2005), nindo and aureo-reticulata (T. Moore) Jacob-McKoy) are treated (Japanese, USDA 2005), suikazura (Japanese, USDA 2005), as synonyms by most authors. madreselva (Spanish, USDA 2005), Caprifoliaceae, honey- The genus name Lonicera commemorates German natu- suckle family, Caprifoliacées. ralist Adam Lonitzer (1528–1586). The specific epithet Lonicera japonica Thunb. ex Murray (Systemat japonica refers to Japan, where it is native. The horticultur- Vegetabilium, ed. 14: 216. 1784 - May–June) has priority al variety name halliana refers to Dr. George Hall, who over Lonicera japonica Thunb. (Flora Japonica 89–90. 1784 introduced it to the United States in 1862 (Coombes 1991). 423 424 CANADIAN JOURNAL OF PLANT SCIENCE

Lonicera japonica is placed in subgenus Chamaecerasus cascade”, “mint crist”, “Interold Darts World” (the latter on the basis of twining growth and flowers in axillary pairs with purple-crimson flowers), are widely available. (Sax and Kribs 1930). Schierenbeck et al. (1995) compared allozyme variability of L. japonica with sympatric L. sempervirens L. in the 2. Description and Account of Variation southeastern United States. Among 10 populations in South (a) Description – Perennial, semi-evergreen (in Canada) Carolina and Georgia, L. japonica had 75% polymorphic twining and trailing vine (Fig. 1), ascending to 10 m, but in loci (Ps), 1.96 alleles per locus (As), 2.28 alleles per poly- Canada rarely more than 4 m high. Younger stems reddish- morphic locus (Aps), and a total genetic diversity (Ht) of brown or light brown and pubescent, becoming woody, hol- 0.216. This variation was consistently lower than L. sem- low, brownish and glabrous with age, and eventually pervirens, but genetic variation within both species was developing a bark that peels off in long strips. Leaves oppo- equivalent to that of other species with similar life history site, ovate or oblong, acute or obtuse and apiculate, entire or characters. early leaves more or less lobed, pubescent but becoming More recently, Peng et al. (2005) found differing concen- glabrous above, relatively thick, 3–8 cm long and 1–3.5 cm trations of two polyphenolic compounds (hyperoside and wide, with pubescent petioles 0.4–1 cm long. Flowers white, chlorogenic acid) among samples of L. japonica from three sometimes with some external purple (or red in var. chinen- Chinese populations, whereas the concentrations of two oth- sis), becoming yellowish on the second day after opening, ers (luteolin and caffeic acid) were similar among popula- 3–4 cm long, glandular-pubescent externally, with a slender tions. tube and with two spreading and recurved lips at the apex, fragrant, produced all summer in axillary pairs on branches 3. Economic Importance 5–15 mm long on young shoots, often crowded at the shoot (a) Detrimental – Lonicera japonica is considered a prob- tips, with calyx glandular-pubescent or smooth, 1–2 mm lematic invader around the world because it displaces native long, the individual flowers sessile and attached at the sum- species and competes with cultivated plants. For example, it mit of a pedicillate ovary 2–3 mm long, subtended by a pair is considered a serious threat to the flora of the Juan of ovate bracts 1–2 cm long. Stamens 5, attached to and Fernandez Islands, Chile (Swenson et al. 1997) and to native about as long as the corolla. Style about as long as the corol- vegetation in southern Australia (Carr et al. 1992), where it la. Ovary inferior, developing into a globose or oval, black occurs in diverse plant associations including heathlands, or purple-black, pulpy berry 6–7 mm long (Fig. 2), which sclerophyllous forest, riparian scrub and temperate rainfor- matures from September (in Ontario) to November (in est. In Hawaii it contributes to the decline of the endangered southeastern US). Seeds 1–16 (average 6) in each fruit, endemic naenaè, Dubautia latifolia (A. Gray) Keck (Starr et brown or brownish-black, ovate or oblong, flat, 2–3 mm al. 2003). In many parts of the world where it has estab- long, each ca. 3.6 mg. See Fig. 3 for illustration of a lished, further planting of L. japonica is discouraged and its seedling. Description from Bailey (1949), Fernald (1950), spread is monitored so that new populations can be rapidly Schierenbeck (2004) and examination of living and herbari- um specimens. controlled, thus avoiding more expensive control later. The normal chromosome number for L. japonica is 2n = More than 50 yr ago, Fernald (1950) described L. japoni- 18. Wang and Wang (2005) provide details on its karyotype. ca in the United States as “a most pernicious and dangerous weed, overwhelming and strangling the native flora and (b) Distinguishing features – Lonicera japonica is easily most difficult to eradicate … [it is] extensively planted and distinguished from other northeastern North American encouraged by those who do not value the rapidly destroyed Lonicera because it is a twining vine with separate leaves indigenous vegetation (Fernald 1950).” In Michigan, adja- and flowers in pairs on axillary peduncles (Fig. 1). Other cent to its area of occurrence in southwestern Ontario, it has Lonicera vines are either rare escapes (L. sempervirens L.) been considered “an aggressive vine that defies eradication, or infrequent natives (L. hirsuta Eat. and L. dioica L.) with forming dense tangles that overwhelm the native vegeta- leaves below the inflorescence encircling the stem and flow- tion” (Voss 1996). ers in clusters at the end of branches. Lonicera japonica outcompetes native vegetation for both light (Bruner 1967; Thomas 1980) and below-ground (c) Intraspecific variation – The form with yellow-veined resources (Whigham 1984; Dillenburg 1993a, b), and there- leaves, generally referred to as var. aureoreticulata, is a by changes the structure of woodlands. Because it is ever- result of infection by honeysuckle yellow vein virus. green it has a capacity to photosynthesize and grow during Lonicera japonica var. chinensis, with purple, mostly the early spring and late fall (Carter and Teramura 1988a), glabrous leaves, and red flowers, has also escaped in North thereby excluding light from spring ephemerals and other America but does not occur north of New Jersey and woodland vegetation at these times of maximum light avail- Pennsylvania (Fernald 1950). Most of the North American ability. By overtopping pre-existing vegetation, the vines plants and those of Canada are referable to var. halliana, topple shrubs and smaller trees (Slezak 1976; Thomas 1980; which has green leaves and white flowers that turn yellow. McLenmore 1981), producing a more open habitat The variety repens has green leaves and white flowers with favourable to their growth. Any disruption of the tree a purple tinge. canopy was found to hasten development of L. japonica At least 12 horticultural varieties are known and many of cover, resulting in further loss of trees (Thomas 1980). these, such as “elegant creeper”, Hall’s prolific”, “cream Similarly, Webb et al. (2000) found that large-scale removal LARSON ET AL. — LONICERA JAPONICA THUNB. 425

Fig. 1. Flowering branch of Lonicera japonica (modified by P. M. Catling from Fig. 137 on p. 216 in Dippel, L. 1889. Handbuch der Laubholzkinde. Verlag von Paul Parey, Berlin. 449 pp.). of Acer platanoides L. resulted in significant release of non- species are at risk (Catling and Cayouette 1996). None- native species, including L. japonica. Yurkonis and Meiners theless, its potential harmfulness has been recognized only (2004) speculated that L. japonica affects local species rich- recently. It was not identified in the 1996 national survey of ness by appropriation of resources available for colonizing significant invasive species (Haber 1996). In a recent detailed species rather than through more direct competitive interac- evaluation developed for North America, L. japonica was not tions emphasized in other studies. among the top 81 invasive species (Catling and Mitrow In southwestern Ontario, L. japonica overgrows and 2005), but using more updated information it ranked within shades native vegetation in a region where numerous Canada’s national prioritized list (Catling et al. 2006). 426 CANADIAN JOURNAL OF PLANT SCIENCE

Fig. 2. Fruit and seeds of Lonicera japonica. A, Section of a fruiting branch. B, Berries showing position on branch. C, Seeds after removal of pulp. Photos by P. M. Catling from material collected in a ravine at Colchester Harbour, Ontario, on 2006 Oct. 21 by G. E. Waldron.

There is much concern that L. japonica establishment 1994). The larvae were found in populations along roadsides after selective logging will prevent forest re-growth (Evans adjacent to agricultural fields in numerous sites, but whether 1984). It is particularly problematic in managed pine stands. L. japonica is a host outside of southern Georgia and north- For example, Cain (1984) reported that it causes severe ern Florida is unknown. Although heliothine larvae were regeneration problems in uneven-aged stands of loblolly and predominately found in crops rather than wild hosts (includ- shortleaf pines in southeastern Arkansas. Nelson (1953) ing L. japonica) during the growing season in Mississippi estimated that 1 million acres in the lower Piedmont had (Parker 2000), L. japonica could be a significant contributor heavy honeysuckle growth, and that perhaps 2.5 million to over-wintering populations of these larvae (Pair 1994). acres had some degree of coverage. The tendency of L. Similarly, L. japonica may be a winter food source for a tor- japonica to outcompete tree seedlings following site prepa- tricid moth in Brazil and Uruguay [Bonagota cranaodes ration by discing, burning and bush-hogging led forest com- (Meyrick)], thus augmenting its reduction of apple crops panies to conduct research on herbicide control methods (Bentancourt et al. 2004). In North Carolina, L. japonica (Prine and Starr 1971; McLenmore 1981). populations adjacent to crop fields are host to overwintering Lonicera japonica is also problematic along railway populations of two spotted spider mite (Tetranychus urticae rights-of-way (Regehr and Frey 1988) and in field borders Koch) that re-invade corn and peanut in the spring and hedges (Warbach 1953; Gunning 1964). Shankman (Margolies and Kennedy 1985). (1986) found that L. japonica covered abandoned fields Lonicera japonica may also impact agriculture as a shortly after the cessation of cultivation on loess bluffs in source of whitefly-transmitted viruses. For example, white- western Tennessee, yet it was replaced by continuous forest fly-transmitted begomoviruses have been introduced to canopy within three decades. Europe with L. japonica (Briddon 2001) and Osaki (1979) Some caution may be required in using and handling L. noted that a whitefly (Bemisia lonicerae Takahashi) may japonica for medicinal purposes (see below). There is a sin- transmit tobacco leaf curl virus (TLCV) (which attacks gle record of three patients incurring a contact dermatitis tomatoes and tobacco) from L. japonica to crops. similar to poison ivy (itchy raised blisters) after pruning Hall’s Japanese honeysuckle (L. japonica halliana), yet it (b) Beneficial – Lonicera japonica has long been used in was easily treated with topical steroids (Webster 1993). traditional Asian medicine, and related species of Lonicera When eaten in large quantities the fruit may be toxic, caus- are used in different parts of China (Bensky and Gamble ing diarrhea, vomiting, rapid heartbeat, respiratory failure, 1993). The Chinese Pharamacopoeia lists both its stem, Ren convulsion and coma (Russell 1997). Dong Teng or Caulis Lonicerae, and its flowers, J¯ın Y¯ın Hu¯a Lonicera japonica may also act as a host for insect pests or Flos Lonicerae (Tang and Eisenbrand 1992; Bensky and of crop plants. In Tift County, Georgia, it was a local host Gamble 1993). Ren Dong Teng is the dry cane of L. japon- for populations of two noctuid moths, the tobacco budworm ica collected in the fall and winter; it is used to treat fever, [Heliothis virescens (F.)] and the corn earworm dysentery, abscess and rheumatic swelling. J¯ın Y¯ın Hu¯a is [Helicoverpa zea (Boddie)], which feed on crop plants (Pair composed of the dry flower buds of L. japonica and other LARSON ET AL. — LONICERA JAPONICA THUNB. 427 influenza and other infectious diseases (Li 1974; Benksy and Gamble 1986). It has also been studied as a source of HIV-1 reverse transcriptase activity, although it has lower efficacy than other Chinese herbs (Chang et al. 1995). Finally, it is a popular, healthy cooling drink among Chinese people during the summer (Li 1974). Lonicera japonica is often combined with other Chinese medicinal herbs for maximum effect (Bensky and Gamble 1993), such as in the popular herbal product Quilinggao (Wong and Chan 2003). Recent studies have confirmed the effectiveness of some traditional uses of L. japonica (for example, Chang and Hsu 1992; Lee et al. 2001; Houghton et al. 1993; Kwak et al. 2003; Kwon et al. 2004), and given its medicinal activity there have been numerous recent attempts to isolate its active ingredients for pharmacological purpos- es (for example, Tang and Eisenbrand 1992; Peng et al. 2005). Three possible types of contraceptives may be developed from L. japonica: an anti-ovulatory contraceptive, a post- coital contraceptive, and a male contraceptive. The Central Drug Research Institute in Lucknow, India, in collaboration with the US National Institutes of Health, the World Health Organization, and the ICMR have confirmed anti-implanta- tion activity by L. japonica (Chaudhury 1993). Lonicera japonica was first introduced to North America as a garden ornamental. There are numerous early refer- ences to its attractiveness (Andrews 1919; Hardt 1986) and it is still popular due to its fragrant flowers and rapid growth (Bradshaw 1991). Lonicera japonica is easily grown and propagated but is not the only choice for the garden. Considering its detrimental aspects, a number of good sub- stitutes have been proposed (Swearingen 2006), including false jasmine [Gelsemium sempervirens (L.) Ait. f.], trumpet honeysuckle (Lonicera sempervirens L.), trumpet creeper [Campsis radicans (L.) Seem. ex Bureau], crossvine (Bignonia capreolata L.), native wisteria [Wisteria frutescens (L.) Poir.], and Jackman clematis (Clematis × jackmanii T. Moore). Fig. 3. Seedling of Lonicera japonica, 70 d after germination and Numerous studies have considered the benefits of L. 105 d after planting. From seed collected at Colchester Harbour, japonica as a food for economically important animals. Ontario on 2006 Oct. 15 (specimen voucher at DAO) and grown Livestock may feed on it, especially when other roughage is under unheated greenhouse conditions (+4 to +21°C) through limited, and preliminary experiments showed that it may be November, December and January (without cold treatment). acceptable as emergency roughage for dairy cattle (Noland Drawing by Gerald Waldron. and Morrison 1954). Although the boiled leaves are used as a vegetable and to make a tea, some caution is required because they contain toxic saponins (Facciola 1990). species of Lonicera collected in early summer before Lonicera japonica has often been recognized as a locally blooming (Zhang et al. 2004); it is used to treat abscess, preferred browse species of white-tailed deer, so wildlife dysentery, cold, and fever, generally acting to “clear heat managers have recommended transplanting it into old fields and poisons” (Bensky and Gamble 1993). and pine groves where deer are desired or even using fertil- Lonicera japonica has been used as an antibacterial, anti- izers to increase its growth (Handley 1945; Nixon et al. inflammatory, antispasmodic, antiviral, depurative, diuretic, 1970; Sheldon and Causey 1974; Segelquist and Rogers febrifuge, and as a cure for tuberculosis, venereal disease 1975; Stransky 1984; Dyess et al. 1993). With increasing and skin disorders (Yeung 1985; Foster and Duke 1998). recognition of its invasive properties, however, this is prob- Lee et al. (1998) noted the general efficacy of L. japonica ably ill-advised. In the southeastern US, L. japonica is part extracts in the treatment of urinary disorders, fever and of the winter diet of bobwhite quail and turkey (Handley headache, and as an anti-inflammatory agent for upper-res- 1945; Brazil 1993). piratory tract infections, diabetes mellitus and rheumatoid Tangles of L. japonica provide nesting sites, feeding sta- arthritis. It is an antimicrobial and antiviral agent against tions, and general cover (Handley 1945), particularly in the 428 CANADIAN JOURNAL OF PLANT SCIENCE

Fig. 4. Geographic distribution of naturalized Lonicera japonica in Canada. The herbarium records are based on specimens in DAO, MICH and TRT (acronyms from Holmgren 2005). southeastern US, where leaves are retained through the win- in any provincial weed and seed acts. It is not listed on the ter. For example, L. japonica thickets in Ohio were some- United States federal Noxious Weed or Seed lists, but there times used over extensive periods for bedding of deer is control in some states. For example, commercial sale is (Nixon et al. 1970). Peles et al. (1995) demonstrated that L. prohibited in Illinois by the Exotic Weed Act (Nyboer 1990; japonica was a preferred nest site and food source of gold- Nuzzo 1997). Although often recognized as a pest, L. japoni- en mice in Kentucky. ca is widely available in the US and Canada and even recom- Lonicera japonica may also support songbird popula- mended by some wildlife managers for planting for forage tions. Suthers et al. (2000) assessed fruit consumption by and cover (see Schierenbeck 2004). To assist with the control fall migratory songbirds in central New Jersey and found of L. japonica in North America, its importation, propagation, that fruits of L. japonica were favored. In particular, distribution and sale should be prohibited in Canada. 54–60% of the diet of neotropical Catharus thrushes feeding New Zealand has developed legislation that is apparently in panicled dogwood shrubland was comprised of L. japon- effective for dealing with invasive species, including L. ica (based on seed recovery from feces). Because the fruits japonica. The New Zealand National Pest Plant Accord, a remain on the vines during the winter, they may also be cooperative agreement between regional councils and gov- important for overwintering birds (White and Stiles 1992). ernment departments, enables the regional councils to There have been numerous reports that L. japonica thick- undertake surveillance to prevent the commercial sale ets reduce erosion and stabilize river banks (Stadtherr 1982; and/or distribution of an agreed upon list of pest plants Evans 1984; Hardt 1986). However, there is little evidence (Biosecurity New Zealand 2001). For example, L. japonica that erosion rates are lower with L. japonica than with other is no longer permitted to be sold, propagated, distributed or species. commercially displayed because it is on the Regional Jackson (1974) and Moerman (1998) reported that Surveillance Plant Pest List for Auckland region (Auckland Cherokee Indians used L. japonica stems to make baskets Regional Council 1997). This could provide a model for and trays. This is a recent phenomenon since it escaped from dealing with invasive species like L. japonica elsewhere. cultivation around 1900. 4. Geographical Distribution (c) Legislation – Lonicera japonica is not listed as a noxious Lonicera japonica is native and common in Japan, Korea weed in Canada’s Seeds Act (Agriculture Canada 1985) nor and eastern China, including Manchuria, where it grows as LARSON ET AL. — LONICERA JAPONICA THUNB. 429 a trailing or climbing vine in thickets on hills and moun- 8.9°C. Cold winter temperatures determine the extent of tainsides (Ohwi 1965; Schweitzer and Larson 1999). It has stem die-back and at their extreme may kill plants been introduced and naturalized in temperate and subtropi- (Leatherman 1955). The westward limit of L. japonica in cal regions around the world. Currently it occurs in much of North America relates to insufficient moisture and drought southern North America including most of the United during seedling establishment. These factors limit its natu- States. It is particularly well established in eastern North ralization in the western United States to local areas with America north to Missouri, Michigan, southern Ontario, irrigation, even though it is still a popular ornamental. New York and Massachusetts (Hardt 1986; Kartesz and Lonicera japonica is also limited to warmer and moister Meachum 1999). It is also established in the Caribbean parts of its native Japan (Sasek and Strain 1990). region, Central and South America, Europe including Leatherman (1955) noted that the type locality of L. japoni- England, Wales, Portugal and Corsica, northern Africa and ca in Japan is climatically similar to eastern North America, South Africa, Australia and New Zealand, the Philippines, consistent with Baker’s (1974) suggestion that climatic sim- the Hawaiian Islands, and the Pacific Islands (Nuzzo 1996; ilarities may account for the establishment of some weedy Starr et al. 2003; Schierenbeck 2004). Sasek and Strain species from eastern Asia in parts of eastern North America. (1990) and Evans (1984) provide maps that differentiate areas where it is ornamental, naturalized and invasive. (b) Substratum – Lonicera japonica grows best on well- Herbarium specimens documenting the distribution (Fig. drained soils (Leatherman 1955), but it also occurs in low, 4) of L. japonica are located at CAN, DAO, HAM, TRTE, wet bottomlands, clay soils with pH from 6 to 7.5, sand TRT, UWO and WAT (acronyms from Holmgren 2005). plains and mine spoils (Jackson 1974). However, it is With the exception of two literature reports that are not doc- noticeably absent on coarse sands and poorer peat soils umented with a specimen (Lockrey and Pegg 1993; Bree (Jackson 1974). In the Pennypack Wilderness located in a 2000), L. japonica is confined in Canada to the Carolinian suburban Pennsylvania landscape, Robertson et al. (1994) region of extreme southwestern Ontario, also known as the found slightly higher frequency and density of L. japonica Lake Erie Lowland ecoregion of the Mixedwood Plain eco- in mixed mesophytic forest than in mixed oak forest. They zone (Ecological Stratification Working Group 1995). This suggested that the slightly better drainage, greater acidity, region is part of the 5b hardiness zone (National Land and and lower fertility of the latter, because of its origin on sand- Water Information Service 2000), which also extends into stone, could be a factor contributing to lower densities. much of Nova Scotia and southern British Columbia and therefore L. japonica could occur in these regions. (c) Communities in which the species occurs – Lonicera Herbarium and sight records indicate that L. japonica is japonica is found in a variety of habitats, ranging from old frequent in parts of mainland Essex County and on Pelee fields, thickets, roadsides, fencerows, and open woodlands, Island (Fig. 4). It also occurs as a cluster of populations in to mature woodlands, where it is especially prominent in the London area of Middlesex County and in part of the canopy gaps (Evans 1984), bottomlands (Oosting 1942) and Niagara Peninsula. Single populations are known in Elgin, edge habitats (Yates et al. 2004). Lonicera japonica sur- Kent and Hamilton-Wentworth counties. vives in most associations into which it is introduced, except Sasek and Strain (1990) predicted that a doubling of for spruce and fir-dominated communities and coastal pine atmospheric carbon dioxide could allow L. japonica to barrens (Jackson 1974). Webb et al. (2000) reported that L. spread northward up to 400 km. The effects of L. japonica japonica occurred in forests dominated by either Acer sac- could be exacerbated throughout its range with further glob- charum Marsh., Acer platanoides L. or Fagus grandifolia al warming, both because of growth enhancement at low Ehrh., but densities were much lower in the latter type. temperatures (especially important because it is semi-ever- Robertson et al. (1994) found L. japonica more frequently in green and produces leaves in the spring before other woodlands than in old fields, thickets, mature forests and species) and greater water use efficiency with increasing riparian plots, but density was highest in the thickets and old CO2. More recent studies at Oak Ridge National fields. In North Carolina, L. japonica extended further into Laboratory’s free-air carbon dioxide enrichment (FACE) forest interior compared with other non-native species and facility confirmed that L. japonica responds to CO2 enrich- more so on south-facing edges (Fraver 1994). It occurs com- ment in situ (Belote et al. 2004). monly in old fields that are regenerating to woody vegeta- tion (Keever 1979; Myster and Pickett 1992; Meiners et al. 5. Habitat 2001). (a) Climatic requirements – Sasek and Strain (1990) con- Near Amherstburg in Essex County, L. japonica occurs cluded that the area in which L. japonica is considered a on slopes in mature forest dominated by American elm serious weed is limited by low temperature sensitivity of (Ulmus americanus L.), black walnut (Juglans nigra L.), overwintering stems. The northern limit of this area corre- black cherry (Prunus serotina Ehrh.), and green ash sponds to the –20°C isocline of the 30-yr mean lowest win- (Fraxinus pennsylvanica Marsh). In this area, it was dis- ter temperature in the eastern United States. Lonicera placing native species of Geum, Parthenocissus, and japonica is naturalized in regions with more than 100 cm of Circaea and was overgrowing bladdernut shrubs (Staphylea annual precipitation and mean January temperatures above trifolia L.). On Pelee Island in southwestern Ontario, it –1°C (that is, below about 36°N latitude), with growth in occurs in the Nature Conservancy’s Shaughnessy Cohen New Jersey beginning with temperatures between 1.1 and Nature Reserve in moist green ash forest that has developed 430 CANADIAN JOURNAL OF PLANT SCIENCE on previously cultivated land, and in open woodlands dom- lished in parts of Essex County and had been found escaped inated by hackberry (Celtis occidentalis L.). At Big Creek in near London in Middlesex County (MICH, TRTE), Port Essex County the plants are widespread in hawthorn Bruce Provincial Park in Elgin County (Oldham et al. 1993, (Crataegus spp.) thickets. At several southern Ontario sites, UWO), and in Kent County (MICH). it is climbing over dogwoods (Cornus spp.). In general, the abundance of L. japonica tends to increase 7. Growth and Development with disturbance and edge effects, as with other lianas (a) Morphology – Lonicera japonica is a twiner, a vine (Teramura et al. 1991; Merriam 2003; Yates et al. 2004). In whose shoots spirally twine around a support (Carter and mature mixed-oak woodland in New Jersey, Davison and Teramura 1988a; Chiu and Ewers 1992). It also produces Forman (1982) found a positive correlation between percent prostrate shoots that root when they contact the ground and cover of L. japonica and light levels. After debris avalanch- allow lateral spread (Larson 2000). Sasek and Strain (1990) es in Nelson County, Virginia, L. japonica was an important reported that individual stems of L. japonica rarely exceed component of vegetative recolonization (Hull and Scott 2–3 m in length, but extensive vegetative growth and 1982). Since L. japonica may increase light penetration branching allow it to form tangled patches. Teramura et al. through its effects on vegetation structure and composition, (1991) observed that L. japonica consistently maintains its its abundance may be self-perpetuating through positive leaf temperatures above ambient by arraying its leaves near- feedback (Thomas 1980). ly horizontal, which forms a large absorbing surface. The rate of growth from seedlings is not documented 6. History because propagation, particularly of the invasive form, is Lonicera japonica was introduced in the United States from from stem cuttings. Seedling growth may be slow for the Japan in 1806 as an ornamental, and was later used for ero- first few years (Little and Somes 1967) and water availabil- sion control and highway landscaping (Leatherman 1955). ity may strongly influence growth rate during this period (Sasek and Strain 1990). Once established, the growth rate Mack (2003) noted that it had not escaped cultivation by –1 1860, and there is minimal evidence that it did so before the may exceed 1.5 m yr (Leatherman 1955), with vines 1890s because it was not included in floras until 1898 when sometimes overtopping 4.5 m trees in a single year (Bruner Britton and Brown reported it as freely escaping from south- 1967; Bell et al. 1988), though its success is not attributable ern New York and Pennsylvania to North Carolina and West simply to high growth rates (see below). Virginia. The first record of escape from cultivation was Schweitzer and Larson (1999) claimed that the success of along the Potomac River in 1882 (Schierenbeck 2004). It L. japonica compared with the native coral honeysuckle (L. sempervirens) might result from greater morphological plas- was reported as far as Florida in 1903 and Texas in 1918 ticity. Schierenbeck et al. (1994) demonstrated greater mor- (Hardt 1986). Leatherman (1955) reported its occurrence in phological plasticity of L. japonica in terms of southwest Virginia in 1892, Florida in 1897 and Athens, compensation to herbivore damage, and Sasek and Strain Georgia in 1900. At the same time that L. japonica was (1990, 1991) showed greater allocation to leaf biomass with increasing its range as an escape from cultivation in North CO2 enhancement. In addition, L. japonica allocates more America it was spreading around the world. For example, it photosynthetic surface area per unit support tissue than L. was reported as naturalized in Australia between 1820 and sempervirens, leading to greater competitive ability (Sasek 1840 (Schierenbeck 2004), in New Zealand in 1926 and Strain 1991; Teramura et al. 1991; Schierenbeck and (Williams et al. 2001), and in South America in the 1940s Marshall 1993). (Schierenbeck 2004). The stem anatomy of L. japonica may enhance its ability Although the earliest records for adjacent Michigan are to spread. In a study comparing xylem structure in three 1894 and 1902 (Voss 1996), L. japonica appears to have Lonicera species with different growth forms, L. japonica arrived in Ontario much later. It was reported neither for was the only one with maximum vessel diameter above 50 Ontario by Soper and Heimburger (1982) nor for Canada by µm (Chiu and Ewers 1992). These wide vessels could facil- Scoggan (1979). Although well established now at Point itate long-distance water transport by compensating for its Pelee and on Pelee Island, it was not reported from these narrow stems. Nonetheless, vessel diameter in L. japonica is regions during the much earlier surveys of Dodge (1914) at the low end for vines in general, and much lower than and Core (1948), respectively. It was first mentioned in the cohabitant vines of eastern North America, such as Vitis unpublished reports of Maycock et al. (1976 unpublished, vulpina L. and Parthenocissus quinquefolia (L.) Planch. Point Pelee dryland vegetation resource analysis, Point These narrow vessels may protect against freezing-induced Pelee National Park) and Johnson and Wannick (1977), and cavitation and xylem embolism, which facilitates water then in the published list for Essex County by Botham transport in winter, when the semi-evergreen L. japonica is (1981). The earliest collection that we have seen is from still photosynthesizing (Bell et al. 1988). Cedar Creek in Essex County in 1981 (TRTE; for an expla- nation of this and following acronyms see Holmgren 2005). (b) Perennation – Lonicera japonica may perennate vegeta- Considering that the most distinctive plants of the tively by above ground runners and below ground rhizomes Carolinian region of Ontario were extensively surveyed by (Larson, Catling and Waldron, personal observation). Soper and others in the 1940s, 1950s and 1960s, it seems likely that L. japonica established only recently as suggest- (c) Physiological data – There have been numerous studies ed by the collections. By the early 1990s it was well estab- of the role of physiological factors in the spread of L. japon- LARSON ET AL. — LONICERA JAPONICA THUNB. 431 ica. Somewhat surprisingly, its success is attributable nei- linators were excluded set fruit (Miyake and Yahara 1998; ther to high growth rates nor to high photosynthetic rates. Its Larson et al. 2002). Preliminary allozyme analyses support rate of stem elongation is notably low (Bell et al. 1988; this interpretation (Schierenbeck et al. 1995). Although its Teramura et al. 1991), and its maximum net photosynthetic flowers have characteristics of the hawkmoth-pollination rate is similar to non-invasive species (Carter et al. 1989). syndrome (such as long, white tubes; sweet scent; anthers Teramura et al. (1991), however, showed that light-saturat- dehiscing at dusk; abundant nectar), bees are prevalent visi- ed rates of net photosynthesis are higher in L. japonica than tors in its native Japanese range (Miyake and Yahara 1998; for trees on which it grows. Furthermore, even its new win- Miyake et al. 1998), in England (Roberts 1979) and in ter leaves in January in South Carolina maintain substantial Arkansas, near the western edge of its North American photosynthetic rates (Schierenbeck and Marshall 1993). range (Larson et al. 2002). Miyake et al. (1998) observed Lonicera japonica biomass is positively related to irradi- visits to L. japonica by three different sphinx moths, an ance levels (Leatherman 1955; Thomas 1980; Blair 1982; anthophorid and an halictid bee species in Japan. Among the Baars and Kelly 1996). However, a few studies have shown bee and wasp genera listed as pollinators by Schierenbeck that L. japonica can survive at low light levels (Blair 1982; (2004) are Bombus, Apis, Vespa and Vespula. Syrphid flies Robertson et al. 1994; Baars and Kelly 1996). For example, are reported as pollinators by Leatherman (1955) and L. japonica can utilize sunflecks for photosynthesis even if Schierenbeck et al. (1994). it is unable to effectively climb at low light levels (Carter In Arkansas, primary shoots of L. japonica produce and Teramura 1988a). paired axillary flowers in early May, and about 3 wk later, Bell et al. (1988) found that L. japonica had a distinctive after these die, there is a second distinct flowering period, midday maxima of transpirational water loss compared with when secondary lateral shoots produce axillary flowers morning peaks in Vitis vulpina and Parthenocissus quinque- (Larson et al. 2002). Flowering is generally reduced in shad- folia. They concluded that reduced water availability would ed habitats (Robertson et al. 1994). Individual flowers open greatly curtail the activity of the latter species. and their anthers dehisce in the evening (Roberts 1979; Miyake and Yahara 1998; Larson et al. 2002). In a study (d) Phenology – The phenology of L. japonica is likely an conducted within a population in the native Japanese range important contributor to its weediness (Carter et al. 1989). of L. japonica, the flowers were still white and contained Its leaves may be evergreen or semi-evergreen depending on most of their pollen the next morning, but by the end of that location within its range (Evans 1984). In southern Ontario, day most pollen had been removed and floral color had leaves above the snowline are killed in cold weather, where- faded to yellow (Miyake and Yahara 1998). This flowering as those under the snow are green but flaccid (G. Waldron, pattern corresponded with high visitation, but limited pollen personal observation. 2003). In South Carolina, peak leaf removal, by a nocturnal hawkmoth, Theretra japonica de expansion occurs in September and again between January L’Orza, followed by diurnal visits by bee species and April (Schierenbeck et al. 1994). In southern locations (Tetralonia nipponensis Pérez and Lasioglossum sp.) that it retains its old leaves through the winter, and they contin- removed most of the pollen from flowers by the end of the ue to photosynthesize, even as a new leaf cohort begins in day, owing to extensive pollen removal during individual January (Schierenbeck and Marshall 1993). The ability to visits. Nocturnal flowering allows long-distance pollination maintain stomatal opening on mild winter days greatly with low pollen removal, followed by higher removal dur- increases its annual carbon budget, especially because max- ing a diurnal phase of short-distance pollen movement imum conductances on these days may be similar to late- (Miyake and Yahara 1998, 1999). spring and summer values (Carter and Teramura 1988b). Larson et al. (2002) postulated that pollen delivery limit- Schierenbeck and Marshall (1993) estimated that the much ed fertility in Arkansas populations of L. japonica because higher leaf area and photosynthetic rate of L. japonica in few floral visitors or ripe fruits were seen, and nectar was January resulted in five times higher carbon fixation than in observed dripping from the corolla tube. They confirmed L. sempervirens. pollen limitation by showing that naturally pollinated con- In the United States, L. japonica exhibits a bimodal flow- trol flowers set significantly fewer fruit (17.4% of flowers) ering period (Pair 1994; Larson et al. 2002). In the southern compared with those to which supplemental pollen was US, the peak bloom occurs in April and May, and there is a added by hand (78.7%). Fruit set for flowers on secondary subsequent blooming from September through November shoots (23%) was significantly greater than that on primary (Pair 1994). In central New Jersey, L. japonica fruits ripen shoots (13%). Hawkmoths were only observed on the flow- in October and persist into the winter (Suthers et al. 2000), ers during the second flowering period, and other insect vis- and in the southeastern U.S. they are present from itors appeared to be pollen and nectar robbers (see also September to November. Roberts 1979), so low visitation rates and low visitor quali- ty accounted for limited fertility. In particular, short distance (e) Mycorrhiza – There are no reports of mycorrhizal asso- pollen movement by bees could cause reduced fertility ciations with L. japonica. through geitonogamy in the large clones of L. japonica. Pair’s (1994) finding that traps baited with L. japonica 8. Reproduction flowers were attractive to a number of economically impor- (a) Floral biology – Lonicera japonica is thought to be tant adult Lepidoptera inspired two studies. Schlotzhauer et xenogamous because only 2.1% of flowers from which pol- al. (1996) reported that constituents derived from phenyl- 432 CANADIAN JOURNAL OF PLANT SCIENCE propanoid increased at night, whereas compounds from sonal observation). This is the first observation of germina- lipoxygenase activity increased during the day. Some con- tion of L. japonica seed in Canada. stituents were constant through the day, whereas others, par- Hidayati et al. (2000) showed that maximum germination ticularly the dominant terpenoids, peaked in fresh and occurs after cold stratification. These results are consistent 24-h-old flowers. Miyake et al. (1998) found that linalool, with earlier studies that concluded that moist L. japonica an isoprenoid, was the most prevalent volatile emitted by seeds germinate after 28–40 days stratification at 4°C flowers of L. japonica. This volatile showed maximal emis- (Leatherman 1955; Williams et al. 2000). Gibberellic acid sion during the night, when sphinx moths are active. (GA3) treatment is a successful substitute for cold stratifica- tion (Hidayati et al. 2000). (b) Seed production and dispersal – Fruit set takes place The requirements for embryo growth and dormancy break about 60 d after abscission of the corolla (Schierenbeck in L. japonica correspond to germination phenology under 2004). In New Zealand, L. japonica fruits had a mean diam- natural conditions (Hidayati et al. 2000). In Kentucky, seeds eter of 5.1 mm and contained an average of 6.1 seeds that began to germinate under leaf litter beginning in late weighed 1.10 mg each (Williams et al. 2001). Lonicera January 1998, but peak germination was between February japonica fruits in Arkansas had a mean weight of 186 mg 15 and 22. Since most seeds of L. japonica dispersed in the (wet) and 57 mg (dry), with 6.2 seeds per fruit that weighed fall are not exposed to warm temperatures before germina- an average of 3.4 mg (air dried) (Shelton and Cain 2002). tion, only cold stratification is required for germination. The mean seed length within Kentucky populations was Physiological dormancy is broken in mid-winter, but 2.89 mm (Hidayati et al. 2000). Most plants from Point embryos do not grow until temperature increases later in the Pelee, Ontario had 6 seeds/fruit (G. Waldron, personal season. observation). There is limited potential for a persistent L. japonica seed Lonicera japonica fruits have been classified as “juicy bank since seeds germinate to high percentages under either fibrous,” based on a pulp water content of 80–85% leaf litter or soil (Hidayati et al. 2000; Fowler and Larson (Williams et al. 2000). Peles et al. (1995) reported a mean 2004). Shelton and Cain (2002) found that seed viability caloric content of 4.48 kcal g–1 dry weight, a mean percent was significantly reduced after 2 or 3 yr in the forest floor, crude protein of 9.75%, and total phenolics (percent gallic with only 1% of seeds germinating after 3 yr of field stor- acid equivalents) of 2.20%. The caloric and crude protein age. values were within the range normally required by mam- malian herbivores, and the phenolic content was considered (d) Vegetative reproduction – Once it colonizes a site, L. relatively low. Suthers et al. (2000) reported that their fruit japonica spreads extensively by vegetative means (Slezak were 1.6% lipid and 50.3% carbohydrate. Handley (1945) 1976), including rhizomes and prostrate shoots. Larson recorded 10.42% crude protein, 7.86% fat, and 6.65% crude (2000) compared circumnutation (rotation about a central fiber. White and Stiles (1992) considered the fruit pulp to be axis) behavior in L. japonica and L. sempervirens. She of low quality, since it contained less than 10% dry mass found that erect shoots behaved quite similarly (rotating lipid. about 31° clockwise per hour), but that their prostrate shoots Birds and small mammals have often been listed as dis- differed markedly. Shoots of L. japonica had reduced cir- persal agents for L. japonica (White and Stiles 1992; cumnutation (averaging 2.1° per hour) compared with those Suthers et al. 2000). Birds that have been observed to eat the of L. sempervirens. This behavior increased the rooting suc- fruits in North America include wild turkey, bobwhite, cess and dispersion of L. japonica, because its prostrate mockingbird, white-throated sparrow, white-crowned spar- shoots grow in a relatively constant compass direction com- row, dark-eyed junco, American robin, purple finch, pared with the more erratic growth (because of interference goldfinch, bluebird, pine grosbeak, hermit thrush and house with the ground) of L. sempervirens shoots. Consequently, finch (Martin et al. 1951; Handley 1945; Schierenbeck the maximum dispersion of L. japonica prostrate shoots was 2004). 39% greater than that of L. sempervirens, despite similar Dispersal may also result from transport and dumping of total shoot lengths. Furthermore, shoots of L. japonica garden waste, which may include both vegetative material remained closer to the ground, which resulted in much that roots readily as well as seeds (Larson, Catling and greater node rooting. All nodes of L. japonica that were less Waldron, personal observation). than 2 cm above the ground developed roots. Effectively, the lateral shoots of L. japonica give them a behavior much (c) Seed banks, seed viability and germination – Hidayati et like the stolons of clonal herbs, and this clonal mobility, al. (2000) found that seeds of L. japonica from Kentucky combined with its climbing success, allow it to exploit var- had underdeveloped spatulate embryos that were about 43% ied microclimates (Larson 2000). of seed length when dispersed. Embryo length increased very slowly with cold stratification (5°C) in the light, but 9. Hybrids more quickly with warm stratification (25/15°C). After 12 Hybrids are only known between species of the same sec- wk of warm stratification, embryo length had increased tion of Lonicera (Sax and Kribs 1930). Sax and Kribs about 67%, allowing the embryos to split their seed coats. (1930) assign L. japonica to subgenus Chamaecerasus, sec- Waldron collected L. japonica seeds from Point Pelee, tion Nintooa, with Chinese species such as L. henryi Hemsl. Ontario on 20 January, and obtained 50% germination (per- and L. alseuosmoides Graebn. Other species of section LARSON ET AL. — LONICERA JAPONICA THUNB. 433 Nintooa are not established in North America. Chiu (1998) ed in the winter when co-habitants are dormant (see also suggested that the variability in L. japonica in Taiwan could Nuzzo 1997). He recommended careful application of be related to the presence of hybrids and that L. shintenen- glyphosate or Crossbow (triclopyr and 2,4-D combination) sis Hayata may be a hybrid of L. japonica and L. hypoglau- at this time of the year, but the latter may be more persistent. ca Miq. Note, however, that Regehr and Frey (1988) reported that applications of glyphosate or dichlorprop plus 2,4-D were 10. Population Dynamics less effective when the leaves were senescing in December. Thomas (1980) hypothesized the following sequence of Cain (1984) found that hexazinone (Velpar L) was more events in L. japonica colonization of a forest on Theodore effective than amitrol (Amitrol T) or mechanical cutting Roosevelt Island (on the Potomac River in Washington, over a 3-yr study in all-aged loblolly-shortleaf pine stands in DC). First, he found reduced vertical structure in habitats Arkansas, but the trees had to be protected from the appli- with L. japonica, suggesting that disturbance of this struc- cation and multiple applications were required. Yeiser and ture allows it to colonize. It may be present in the understo- Howell (1997) reported that metsulfuron (Escort) and ry for long periods even in closed-canopy forest (Whigham glyphosate (Accord) provided the best control in young 1984; Robertson et al. 1994; Spyreas et al. 2004), but can clearcuts and in older bottomland hardwood stands. respond rapidly to disturbance (Leatherman 1955; Slezak Caiazza and Quinn (1980) found that lower leaf surface 1976; Davison and Forman 1982; Carter and Teramura stomatal density decreased and upper surface trichome den- 1988a; Teramura et al. 1991). The second major coloniza- sity increased in L. japonica populations closer to a zinc ore tion event hypothesized by Thomas (1980) was that exten- smelter in Pennsylvania. They suggested that lowered stom- sive growth of L. japonica in response to greater light atal density could reduce the penetration of gaseous particu- effectively allows it to form a new ground layer, which may lates into the mesophyll (e.g., along a gradient of SO2 air suppress the reproduction of overstory dominants and kill pollution), whereas increasing trichome density could lower small trees and shrubs. The rapid development of popula- metabolic rates and thereby reduce pollution damage. tions of L. japonica may also result from its allelopathic effects on trees (Skulman et al. 2004) and herbs (Thomas 12. Response to Other Human Manipulations 1980; Friedland and Smith 1982; Davison and Forman In a recent review, Schierenbeck (2004) noted that 1982). Suppression of dominant species may lead to positive “although L. japonica is naturalized in many areas where it feedback that converts the forest to an open vine-dominated has been introduced, there still may be hope for the control disclimax (Little 1961; Thomas 1980; Whigham 1984). of local infestations and of its further spread in areas that However, on Theodore Roosevelt Island, L. japonica is have a fairly recent introduction history.” This obviously gradually being replaced by the invasive alien Hedera helix applies to Canada. A number of mechanical methods are L. and is expected to decline with time (Thomas 1980). available, some to be used in combination with chemical Lonicera japonica and Liquidambar styraciflua L. have methods. been studied as a model system for the effect of vines on tree Hand-pulling is effective only for removing L. japonica growth. Whigham (1984) found that the growth rate of the seedlings, as older plants have extensive roots that will trees was significantly higher when vines were removed regenerate (Nuzzo 1997). Consequently, some managers from both the tree and the ground. This study suggested that have considered hand-pulling only practical for small areas an understory of vines alone can suppress the growth of to remove incipient patches of seedlings. Hand-pulling can canopy trees, likely as a result of root competition for nutri- reduce spraying requirements, however, and in some cases ents and water. Similarly, Dillenberg et al. (1993a) showed has been used to remove L. japonica over hundreds of acres. that below-ground competition with L. japonica significant- The roots are pulled out and tied up, but the plants are not ly decreased Liquidambar styraciflua sapling growth, and removed from the trees since this would simply provide that canopy competition was only effective when it occurred light for regrowth (M. Imray, personal communication). in concert with root competition. Mowing and grazing may reduce the spread of vegetative Meiners et al. (2001) found that L. japonica colonized runners (Handley 1945; Nelson 1953), but tend to increase fields within 5 yr of abandonment and reached its peak after the number of stems or produce a low mat (Stransky 1984; 15 yr, whereas Myster and Pickett (1992) suggested a some- Faulkner et al. 1989; Nyboer 1990). Repeated mows may what later peak. reduce recovery (Evans 1984). The efficacy of grazing has not been shown empirically, and its costs likely outweigh its 11. Response to Herbicides and Other Chemicals benefits in many sensitive habitats (Evans 1984). Unless it Evans (1984) reviewed early studies of herbicide treatments is repeated, grazing may simply stimulate resprouting, as on L. japonica and Nuzzo (1997) provided a later update. with mowing. Bush-hogging is ineffective since re-invasion Glyphosate (Round-up) treatment is often recommended, occurs within a year (McLenmore 1985). Discing has though L. japonica may be defoliated by high-volume proven to be effective, but it destroys native species and spring sprays of a variety of herbicides (Evans 1984). may stimulate germination of L. japonica seedlings (Nuzzo However, control is not dependable, and some individuals 1997). are nearly always present after treatment (Warbach 1953; Lonicera japonica is susceptible to fire (Handley 1945), Little 1961). Nyboer (1990) pointed out that the semi-ever- but resprouts from its roots after a single burn (Leatherman green habit of L. japonica allows it to be detected and treat- 1955; Faulkner et al. 1989). Pre-burn cover is re-established 434 CANADIAN JOURNAL OF PLANT SCIENCE within a few years (Oosting and Livingstone 1964; Barden (d) Nematodes and/or other non-vertebrates – In North and Mathews 1980). Burning may be most effective com- Carolina, two spotted spider mite (Tetranychus urticae) bined with foliar application of reduced amounts of occurs on L. japonica (Margolies and Kennedy 1985). herbicide, such as glyphosate (Nyboer 1992; Nuzzo 1997). Mid-summer cutting or fall grazing may also limit Diseases resprouting (Evans 1984). Stransky (1984) studied alternate (a) Fungi – Lonicera japonica is sometimes damaged by control methods within deer food lots and reported that powdery mildew, leaf spots and blights (Brickell and Zuk burning is an inexpensive way to confine honeysuckle to 1997). Some but not all populations are resistant to leaf food plots. blight caused by Insolibasidium deformans (C.J. Gould) Lonicera japonica may be a candidate for biocontrol (see Oberwinkler and Bandoni (Gould 1945). below), especially given that it has no close relatives in North America, but this requires the usual cautions about (b) Bacteria – No record has been found. potential unintended consequences of such action. (c) Viruses – Brunt et al. (1980) isolated a previously unde- 13. Response to Herbivory, Disease and Higher scribed carlavirus, honeysuckle latent virus, from plants in Plant Parasites southern England that had severe leaf chlorosis. Macintosh Lonicera japonica is sometimes described as “pest-free” et al. (1992) used monoclonal antibodies to confirm the (Dehgan 1998), and the absence of herbivory in North presence of whitefly-transmitted tobacco leaf curl virus in America has been used to explain its success (Leatherman two European populations of L. japonica var. aureo-reticu- 1955). Dillenberg et al. (1993b) noted that L. japonica had lata. This geminivirus could be spread from the ornamental much less leaf damage due to mildew and beetle grazing L. japonica by whiteflies, potentially infecting European than Parthenocissus quinquefolia. However, in young crops (Osaki 1979). Also, honeysuckle yellow vein mosaic woodland in South Carolina, Schierenbeck et al. (1994) begomovirus has been reported from Japanese and New found that L. japonica was more subject to herbivory than L. Zealand populations of L. japonica (Lyttle and Guy 2004; sempervirens. When subjected to insect and mammal her- Were et al. 2005). bivory, L. japonica showed a compensatory response that led to its greatest biomass and allocation to leaves. In con- Higher plant parasites – No record has been found. trast, L. sempervirens showed the opposite pattern, accumu- lating the most biomass in the absence of herbivory. In ACKNOWLEDGEMENTS short, the ability of L. japonica to compensate for relatively B. Larson acknowledges doctoral support from the low rates of herbivory gave it an additional advantage over University of California at Santa Barbara and postdoctoral its congener, as well as other species. The early season leaf funding from the Integrative Graduate Education and growth of L. japonica also allows it to better escape her- Research Traineeship (IGERT) program in Biological bivory before insect herbivores are active. Invasions at the University of California at Davis (NSF–DGE 0114432). Herbivory (a) Mammals, including both domestic and wild animals – Agriculture Canada. 1985. Seeds Act and Regulations. Queen’s Livestock feed on L. japonica, especially when other Printer, Ottawa, ON, Publs. RES-3153 and YX55-1985-S-8. roughage is limited (Noland and Morrison), and their feed- [Online] Available: http://laws.justice.gc.ca/en/S-8/SOR-2005- ing stimulates sprouting. Williams and Timmins (1997) 220/index.html. reported a rapid response to its browsing by goats, deer and Andrews, E. F. 1919. The L. japonica in the eastern United States. opossums. Lonicera japonica is a locally preferred species Torreya 19: 37–43. of white-tailed deer (Handley 1945; Stransky 1984). Auckland Regional Council. 1997. Pest facts # 43, Japanese hon- eysuckle, Lonicera japonica. Auckland, New Zealand. Baars, R. and Kelly, D. 1996. Survival and growth responses of (b) Birds and/or other vertebrates – Consumption of fruit by native and introduced vines in New Zealand to light availability. N. birds is beneficial for the dispersal of L. japonica seeds and Z. J. Bot. 34: 389–400. the foliage is consumed by bobwhite quail and turkey dur- Bailey, L. H. 1949. Manual of cultivated plants. MacMillan ing the winter, but it is a minor part of their diet (Handley Company, New York, NY. 1116 pp. 1945). No records of consumption by other vertebrates have Baker, H. G. 1974. The evolution of weeds. Annu. Rev. Ecol. been found. Syst. 5: 1–24. Barden, L. S. and Matthews, J. F. 1980. Change in abundance of (c) Insects – In China, L. japonica is host to aphids and a honeysuckle (Lonicera japonica) and other ground flora after pre- cicadellid [Empoasca biguttula (Ishida)] that are also pests scribed burning of a Piedmont-pine forest. Castanea 45: 257–260. of cotton (Chen et al. 1987; Li and Wen 1988). The ceram- Bell, D. J., Forseth, I. N. and Teramura, A. H. 1988. Field water relations of three temperate vines. 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