Amur honeysuckle (Lonicera maackii (Rupr.) Maxim.), an introduced shrub native to lowland forests in eastern Asia, has emerged as perhaps the most widespread and problematic invader of forests throughout the eastern United States and adjacent Canada. The body of literature concerning this invasive is large and has been summarized/reviewed by Luken and Thieret (1996), Lieurance and Landisbergen (2016), and McNeish and McEwan (2016). The harm Amur honeysuckle inflicts on natural processes and native species populations is extensive, ranging from competitive exclusion of native plants (Collier and Vankat 2002, Loomis et al. 2015, Gorchov 2005, Sena et al. 2021), to modification of herbivory patterns (Meiners 2007, Orrock et al. 2015), facilitation of pathogen vectors (Allana et al. 2010), modifications of soil (McEwan et al. 2012, Trammell et al. 2012), and modification of stream communities (McNeish et al. 2015). Despite an abundance of study, no truly time/cost-effective and ecologically appropriate technique has been devised to eliminate Amur honeysuckle from natural areas. Land managers seem to be resigned to its continued presence.
Scope of honeysuckle invasion over the last 30 + years is to a large extent a consequence of forest fragmentation and the degraded nature of regional forests. Commonly honeysuckle establishes in forest edges and damaged stands where the canopy is relatively open (Bartuszevige et al. 2006, Henken et al. 2013). High light conditions support rapid growth and copious seed production (Luken et al. 1997, Schulz and Wright 2015), with ready populations of animal vectors to disperse seed (Ingold and Craycraft 1983, Vellend 2002, Bartuszevige and Gorchov 2006, Castellano and Gorchov 2013). Because honeysuckle has a reasonable level of shade tolerance, it can persist in the understory and capitalize on natural canopy openings for further growth and establishment opportunities (Henken et al. 2013).
On mesic sites in eastern North America established honeysuckle are now experiencing a changing understory environment. Canopy closure is occurring in many formerly open canopy stands, reducing light availability. Additionally, throughout much of the eastern United States the process of “mesophication” (sensu Nowaki and Abrams 2008, Alexander et al. 2021) is under way. This involves replacement of fire tolerant species (e.g., Quercus L. spp., Carya Nutt. spp.) with highly competitive and fire intolerant species, especially sugar maple (Acer saccharum Marshall.). Active fire suppression has eliminated this constraint on the growth and spread of fire intolerant species. Maple forest understories are exceedingly dark and limit forest floor shrubs to a few shade tolerant species. For this reason, the capacity to survive and prosper in the forest understory will play a larger role for honeysuckle in the future. Part of this scenario is that honeysuckle will compete with other shade tolerant woody species.
In southern Illinois we have noticed three woody species are abundant in dark understories where honeysuckle is present: sugar maple, pawpaw (Asimina triloba Adans.) and spicebush (Lindera benzoin Thunb.). Maple and pawpaw appear to ultimately overtop honeysuckle, while dense spicebush stands crowd it significantly. This pattern might occur because of shade tolerance in these species, or priority effects. In this study we hypothesized that pawpaw and spicebush had greater shade tolerance than honeysuckle. We focus only on these species because the extreme shade tolerance of maple is well known and has been more widely studied (e.g., Ellsworth and Reich 1992, Walters et al. 1993, Walters and Reich 1996, Sendall et al. 2015). Based on the ongoing expansion of pawpaw and spicebush we predicted higher rates of photosynthesis in shade, stronger manifestation of shade acclimation responses in leaf structure, and higher leaf area ratios (LAR, leaf area / plant mass) than in honeysuckle. To provide context for the performance of honeysuckle in shade, we also examined the photosynthetic performance of honeysuckle in edge habitats where it prevails. This was not possible for pawpaw and spicebush because they are absent from forest edges in our region.
Photosynthesis is a key aspect of shade tolerance. Early studies tended to treat acclimation or adaptation of photosynthesis to shade as the central element of shade tolerance (Bjorkman 1972, Boardman 1977, Chabot and Chabot 1977). Later work emphasizes patterns of resource allocation, respiratory load, and canopy architecture in conjunction with photosynthetic patterns as important determinants of shade tolerance (Givnish 1988, Lei and Lechowitz, 1990, Woodward 1990, Walters et al. 1993). Unfortunately, measuring, integrating, and interpreting these aspects is operationally challenging when studying seedlings in controlled environments, much less in the field using pre-existing plants. To make a practical, conceptually robust comparison between species, we interpret photosynthetic light responses in relative to the biomass invested in leaves and shoots. Annual production of leafy shoots by winter-deciduous species is essential to survival. Shoot production not only replaces the essential organs of photosynthesis and reproduction, but also provides the means to overtop and/or overspread competitors. We propose that species-level differences in the biomass costs and photosynthetic returns of shoots are very likely to affect the odds of persistence through time.
The background literature for the three study species varies in its depth. Photosynthesis/shade tolerance in Amur honeysuckle has been investigated by Luken et al. (1997), Fridley (2012), and Lieurance and Landsbergen (2016). Luken et al. (1997) examined the capacity to capitalize on increases in light intensity caused by canopy disturbance by transplanting small shade-grown shrubs to shade structures providing 1, 25, and 100% sunlight. Although the study relied on recently transplanted plants, it clearly showed preexisting leaves can acclimate to increased light. In addition, increased light stimulated production of new light-acclimated leaves and caused modification in tissue allocation patterns. Luken et al. (1997) conclude that honeysuckle is a habitat generalist with high phenotypic plasticity. Fridley (2012) compared estimates of carbon gain by native and exotic understory shrubs before the tree canopy expanded in spring and after the canopy opened in fall. Compared to most species, Amur honeysuckle obtained fairly little of its carbon during either period (total C < 15%), while many natives were more reliant on the light windows during early spring and late fall. Notably, shrubs of the genus Lonicera show wide variation in carbon gain patterns in spring and fall. The common tendency to generalize to Amur honeysuckle from the high rates measured by Harrington et al. (1989) in L. X bella Zabel is inappropriate (Fridley 2012). Lieurance and Landsbergen (2016) examined photosynthesis and allocation patterns across a light gradient (64–12% canopy openness) and concluded that high phenotypic and physiological plasticity allowed honeysuckle to “persist in all habitats”.
Pawpaw is an abundant clonal shrub/subcanopy tree distributed across the southeastern U.S. on deep, moist soils. Clones may largely shade the forest floor, and individual ramets can achieve heights of 3–12 m (Immel 2001), reaching stem diameters of 25 cm (K. Schulz, pers. obs.). Thus, it is functionally both a large shrub and a subcanopy tree capable of overtopping honeysuckle (maximum height 5.2 m) or spicebush (maximum height 3–5 m) (PLANTS Database 2022). In southwestern Illinois, the location of this study, pawpaw is restricted to the forest interior, where it produces a low canopy of large, horizontally oriented leaves 10–30 cm long (Immel 2001). Larger individuals flower and produce banana-like berries 7–16 cm long (Immel 2001) in early fall. A number of mammals consume pawpaw fruits and disperse the seeds, although most stands likely consist of large clones (Rogstad et al. 1991, Larimore et al. 2003). White-tailed deer (Odocoileus virginianus Zimmermann), common understory browsers, do not browse on pawpaw foliage (Slater and Anderson 2014). In commercial forests pawpaw is regarded a significant competitor with tree seedlings (Olson and Keeley 2018). Baumer and Runkle (2010) demonstrated strong competitive ability in pawpaw against very tolerant sugar maple and moderately tolerant black cherry (Prunus serotina Ehrh.). Tree seedlings under pawpaw were less abundant and smaller than in surrounding locations. Accounts of the photosynthetic behavior of pawpaw are seemingly absent in the literature.
Spicebush is a dioecious clonal species of moist forest interiors and has a range similar to pawpaw. It achieves height and spread comparable to forest-grown honeysuckle (1–3(5)) m tall, Nesom 2002). The leaves are moderately large, 6–14 cm long. It is an aggressive competitor in the understory, but evidence is mixed concerning its ability to capitalize on canopy gaps (see below). Female shrubs produce shiny red, oily drupes in early fall. These are favored by birds and disappear far earlier than honeysuckle fruits. Spicebush seeds are ca. 3 mm in diameter and germinate easily after stratification. Seeds persist in the litter layer for a number of years (Nesom 2002), but most shrubs arise from clonal reproduction (Nesom 2002). Deer and other mammalian herbivores appear not to browse on spicebush foliage (Schulz, pers. obs.).
Luken et al. (1997) compared light acclimation responses of spicebush to honeysuckle and observed marked differences. Unlike honeysuckle, spicebush transplanted to 25 and 100% sunlight weakly expressed plastic responses to high light (plants grown at 1% sunlight failed to thrive). Davidson (1966) examined growth responses of six shrub species maintained in growth chamber simulating open (14% full sun) and closed canopy (3% full sun) forest light levels. Spicebush was distinctive among species because it gained height faster and produced more leaves under closed canopy, suggesting it was a shade specialist. In contrast to Luken et al. (1997), Niesenbaum (1992) observed greater leaf area and annual branch growth in spicebush exposed to 20% vs. 1% full sun in natural habitats. Moreover, Veres and Pickett (1982) observed substantially greater leaf area, leaf biomass, branch biomass, and primary stem production in high light (4300 foot candles, estimated as ca. 43% full sun) vs. low light (300 foot candles, estimated as 3% full sun) habitats.