1. Introduction
Invasive species have caused dramatic economic damage and loss of biodiversity worldwide and non-native species continue to invade forest ecosystems in the United States at an accelerating rate [
1]. Despite general consensus on the risks posed by alien species, the exact economic and ecological impact of invasions is an active area of debate and, in some cases, certain potential benefits are pointed out, depending on particular species, scenario, and perspective (reviewed in [
2]). Nevertheless, there are an estimated 50,000 non-native species on U.S. soil [
3]. According to Wilcove
et al. [
4], 57% of the 1055 imperiled plant species in the U.S., for which they managed to collect threat data, were negatively impacted by alien species. Based on the same data, Gurevitch and Padilla [
5], estimated that out of 602 plant species in the U.S. imperiled by invaders, 410 (about 68%) could be linked to competition and indirect habitat effects caused by alien plants, but highlighted that invasive plants often act in parallel with other factors, such as habitat loss. Invasive plants reduce forest productivity [
6] and degrade forest health [
2], and pose a particularly severe threat to the economically and ecologically important forestlands in the southeastern U.S. Southeastern forests contain about 201 million acres of timberland, corresponding to about 58% of U.S. timber production and about 16% of timber production world-wide [
7], and also support a high level of biodiversity, with over 3000 native plant species [
8]. However, invasive plants threaten both the productivity of timber species essential to economic sustainability of the region [
9] and the biodiversity equilibrium essential to the provision of ecosystem services, such as erosion control [
10].
Japanese honeysuckle (
Lonicera japonica Thunb.), which was introduced into the U.S. from China and Japan in the early 1800s [
11], is one of the most aggressive invasive species in North America. It has become naturalized in 45 states of the U.S., and the Canadian province of Ontario [
11,
12]. Its attractive and fragrant flowers made it a valued cultivar, but its long flowering period and hardy growth characteristics allowed it to escape cultivation [
11], probably during the 1890s, and spread to most of its present range within about 30 years [
13]. Japanese honeysuckle prefers moist woodlands, often growing in tangled clumps along slopes, but is able to tolerate most forest conditions [
14]. It grows rapidly, flowers early and for long durations [
15], reproduces via animal-dispersed seeds or vegetatively [
16], possesses phenotypic plasticity which reduces herbivore damage [
17], and has no known predators or pathogens within its invaded range [
11]. It negatively affects native vegetation [
18], modifying vegetation structure [
19], decreasing biodiversity [
20,
21], and inhibiting natural regeneration of native species, including loblolly pine [
22], a predominant tree species in both artificially and naturally regenerated forests of the southeast. While natural pine forest range has been gradually declining, the acreage of pine plantations has been steadily expanding since 1950s, reaching 32 million acres in 1999 with further expected increase up to 54 million acres in 2040 [
23]. The expanding plantations and increased timber yield additionally highlight economic potential of the southeastern forests. Approximately 84% of the seedlings planted annually throughout the South are loblolly pine [
24]. In the forestlands of eastern Texas, largely corresponding to the western part of the Piney Woods ecoregion, where loblolly pine is of both commercial and ecological importance, Japanese honeysuckle is the most prevalent invasive vine [
25].
A recent study identified areas vulnerable to invasion by Japanese honeysuckle throughout Mississippi, stretching northward across western Tennessee and western Kentucky, westward across southern Arkansas, eastward across north-central Alabama, and also in several counties scattered within Virginia [
26]. These authors used logistic regression to correlate land characteristics and climatic conditions with presence/absence of Japanese honeysuckle based primarily on analysis of data collected prior to 2006.
In the present study, we calculated the recent range expansion of Japanese honeysuckle within the forestlands of eastern Texas based on analyses of an extensive set of field data collected by the U.S. Forest Service on fixed plots during the period from 2007 to 2011. We then used boosted regression trees to analyze an extensive data set collected as part of the Forest Inventory and Analysis (FIA) program of the United States Department of Agriculture (USDA) Forest Service to identify areas within the forestlands of eastern Texas that were invaded by Japanese honeysuckle during the FIA inventory period that extended from 2007 to 2011. We quantitatively assessed a suite of landscape features, climatic conditions, forest conditions, forest management activities, and disturbances as potential factors affecting the likelihood of invasion. Based on identification of the potentially most influential factors, we predicted likelihoods of future invasions by Japanese honeysuckle under a common management strategy (artificial regeneration of loblolly pine).
4. Discussion
The number of sites invaded by Japanese honeysuckle almost doubled within only five years. Clearly, northern sites are far more frequently invaded than those in the south (
Figure 1), and the species was identified in, what seems moderate, 25.7% of the sampled sites. However, for a better understanding of the species presence one should perhaps consider that in 2011 less than 5% of the forested counties in eastern Texas remained uninvaded. The species abundance throughout the region seems uneven, but given its ability to spread rapidly, as evidenced by comparison of 2006
vs. 2011 presence-absence records, and its current distribution, there is potential for further invasion into other currently uninvaded sites. The change in spatial patterns, as shown by our results, agrees with the earlier work by Wang
et al. [
26] who estimated probabilities of invasion of Japanese honeysuckle throughout the Southern US forestlands based primarily on analysis of data collected during the FIA inventory period that ended in 2006. In particular, they identified areas vulnerable to invasion in eastern Texas, with northeastern sites showing higher probability of invasion. Our index of potential rate of spread, assuming a mean interval of five years between samples on any given plot, suggests a mean potential dispersal velocity of 3200 m/year (16 km/5 years), which is faster than the rates used in the models of Morales and Carlo [
41] and Clark
et al. [
42]. Morales and Carlo [
41] used a spatially-explicit simulation model to estimate a dispersal velocity of approximately 800 m per year for plants dispersed by frugivores. Clark
et al. [
42] used a stochastic model based on information from a variety of sources to estimate a range of annual velocities of seed dispersal by birds: 90% of the seeds were dispersed 0–100 m from the parent tree, 8% were dispersed 100–500 m, 1.7% were dispersed 500–5000 m and 0.3% were >5000 m. Our index was almost surely biased by exclusion of propagule sources in relatively close, un-sampled areas; the FIA field data were collected from a lattice of 4047-m
2 hexagons, with only one sample plot located randomly within each hexagon [
29]. On the other hand, given that seeds of Japanese honeysuckle are dispersed by wide-ranging animals, such as white-tailed deer, a relatively high dispersal velocity is not surprising.
While several factors affect a site’s susceptibility to Japanese honeysuckle invasion, forest features and climate conditions seem to play predominant roles. The majority of the species occurrences have been noted on sites with very low basal area, although the exact impact of basal area is somewhat ambiguous considering the interlacing positive and negative effects upon the fitted function along the variable’s distribution. A clear and consistent effect, however, may be observed in the case of other major contributors from the forest features group of variables. In particular, the youngest stands are most invasion-prone, and the susceptibility gradually decreases with age. High site productivity appears to favor invasions, as well. Logically, relatively young and highly-productive sites provide favorable conditions for any species, native and invasive ones alike [
43]. The main factor identified as a limitation to mature forest stand invasions by Japanese honeysuckle was limited light availability, even though the species can tolerate a relatively low light environment [
44,
45]. Relatively open habitats facilitate early age flowering and prolific seed production. Halls [
46] showed that Japanese honeysuckle in eastern Texas reproduced fruit at three years of age when plants were grown in the open, but at age five when grown in the shade. In addition, signs of stress developed after two years of growth under 8% of ambient light [
47]. Even though new growth was initiated each spring, leaders would subsequently die back and a portion of the current leaf crop would abscise following maturation of the flush [
47].
Japanese honeysuckle invasions were more abundant on sites with medium-high biodiversity index values. Although it seems counterintuitive that a new species would successfully establish itself in a diverse and likely balanced community (a classic view by Elton; [
48]), post-invasion dynamics within this community as well as fate of the invader remain unknown. Debate is ongoing with arguments and evidence both supporting and opposing the classic perspective, however [
48,
49,
50,
51]. This disagreement also was noted between theoretical analyses and field studies (reviewed in [
52]). In a recent case study, Wang and Grant [
53] noted that sites with dominant loblolly pine overstory were less diverse than mixed evergreen-deciduous and mostly-deciduous stands. They suggested that the evergreen canopy was the likely factor diminishing risk of encroachment by invasive shrubs due to the decreased amount of light reaching the understory. On the contrary, the mixed canopy partially opens up from fall to early spring allowing for more light to reach the understory during that period. Indeed, the interspecies feedback loops [
54,
55] that characterize ecological communities challenge us to focus on the processes by which resident species affect the availability of physical resources, such as light, with which the likelihood of species invasions often are correlated.
Apart from favorable forest features, climate conditions of eastern Texas forest stands also appear to facilitate Japanese honeysuckle invasions. Leatherman [
15] reported that Japanese honeysuckle in Eastern North America expands generally south of an isotherm where mean January temperature is −1 °C, north of an isotherm where only 5% of January daily low temperatures are <0 °C, and east of a mean annual precipitation of 1016 mm. Although Japanese honeysuckle may tolerate cool winter temperatures and regrow vigorously the following summer, late spring frosts that damage new growth and short growing seasons limit the northern distribution [
13,
56]. Sasek and Strain [
57] suggested that projected future climate change may allow Japanese honeysuckle to expand its northern range; however, its southern distribution may be limited by mild winter temperatures that are insufficient for seed stratification. Our simulated intensity of invasion generally decreased with increasing mean annual temperature and decreasing annual precipitation.
Among the investigated disturbance factors, proximities of the nearest known propagule source and road were significantly correlated with the distribution of Japanese honeysuckle. Propagule pressure has been shown to affect the distribution and abundance of many invasive plants [
58,
59] and, like many other invasive plants, recruitment limitation tends to slow the range expansion of Japanese honeysuckle [
60,
61]. These results support the concept that invasions are best mitigated during the early stages of recruitment and establishment [
62,
63] or via control of outlier populations [
64]. The control of biological invasions has become a topic discussed at the highest scientific, policy and management levels [
65]. While long-term invasive plant management strategies are recognized as essential to reduce the ecological damage and economic costs associated with invasions, the development and implementation of such plans lags considerably behind [
66]. Most of invasive plant management strategies, including that of Japanese honeysuckle, have emphasized controlling highly infested areas, despite this knowledge.
Roads have been shown as invasion corridors that facilitate the spread of invasive plants [
67,
68]. This is especially likely for an invasive vine such as Japanese honeysuckle, capable of plastic responses to heterogeneous habitat and thus of rapid growth in light gaps such as road-sides [
69]. If there are no structures available for twining, Japanese honeysuckle can grow in a mat form along the ground, increasing the likelihood that roads could act as corridors for, rather than barriers to, spread. Spread of the species along roads may be additionally augmented by seed dispersal, also across the road, by wildlife. Japanese honeysuckle has been recognized as an important browse and forage species, especially for white-tailed deer, but also for other wildlife [
70,
71,
72] throughout much of the eastern and southern United States, particularly during poor mast years and during winter when other food sources are scarce or inaccessible [
73,
74]. For example, in areas of northern Alabama managed primarily for loblolly pine production, Japanese honeysuckle constituted 49.4% of the year-round diet of white-tailed deer, whereas no other single food item accounted for more than 6% [
75]. White-tailed deer can move over large distances [
76,
77,
78] and have been observed utilizing roadways [
79,
80] and, thus, may be important vectors of Japanese honeysuckle seed dispersal.
The roles of other studied factors, namely landscape conditions and forest management activities, were rather minor. About 75% of the plots in eastern Texas currently occupied by Japanese honeysuckle occur at the northern part of the area, and about 98% occur on lands with a slope ratio less than 8%, where favorable habitats are created on well-drained sites [
81]. In general, the species is noticeably absent on coarse sands and poor peat soils [
82]. Extensive areas of poorly drained soils have also been linked with the absence of Japanese honeysuckle in southern Florida [
15].
Anthropogenic effects on Japanese honeysuckle distribution are multifaceted. However, while roadways may facilitate the spread of the invader, artificial forest regeneration, one of the management practices we considered in this work, was shown effective in reducing the likelihood of Japanese honeysuckle invasions. A positive outcome of artificial regeneration, which generally involves some effort to control woody competition prior to planting, is that these types of sites are at least temporarily less susceptible to Japanese honeysuckle invasion. Approaches like herbicide application, mechanical treatment, or burning, aim to reduce interspecific competition and allow for successful establishment of the newly planted seedlings. However, as a side effect, this step may also reduce biodiversity on artificially regenerated sites in general (mean Hs = 0.69 vs. Hs = 1.06 on sites with and without history of artificial regeneration, respectively). The majority of the industrial plantations are located in southeastern Texas and, consequently, artificial regeneration is more common in this part of the state, with about 30% of the sites being classified in this category, as compared to about 21% of the sites in northeastern Texas, a region with less frequent human intervention and more favorable soil types.
We estimated invasion likelihood by applying boosted regression trees to data on landscape features, climatic conditions, forest conditions, disturbance factors, and forest management activities collected over a five-year period. Two valid criticisms of our approach are that our estimates of invasion likelihood are unique to our method of analysis [
83] and to our specification of the variables included in that analysis [
84]. These criticisms are generic problems related to structural uncertainty in the mathematical representation of natural systems [
85]. We identified most of our potential independent variables following a recent study focused on the invasion of Japanese honeysuckle in forestlands of the southern United States [
27]; however, we did not use exactly the same set of independent variables and we used a different modeling approach. The possibility remains that there might be a more powerful model [
83] and/or a more useful set of explanatory variables [
66]. Evaluation of the relative merits of the different methodological approaches to geographical distribution modeling currently is a topic of much debate [
83,
86,
87], but is beyond the scope of the present study.
In conclusion, our analyses suggest that the range of Japanese honeysuckle in forestlands of eastern Texas is expanding. Even though providing reliable predictions of habitats that are most at risk, distribution limits, and efficacy of management strategies for any invasive species remain a challenge, our model showed the positive impact of selected management practices upon reducing the likelihood of invasion. Our model may also guide forest managers in development of long term monitoring and control strategies for Japanese honeysuckle by facilitating detection and eradication of newly established invasions in eastern Texas.