Extended Leaf Phenology Research Articles

Leaf phenology and freeze tolerance of the invasive tree Pyrus calleryana (Roseaceae) and potential native competitors1

Pyrus calleryana is one of the most problematic invasive species in the eastern United States. The mechanisms that enable Py. calleryana to establish and outcompete native plants are not fully understood but likely include a profile of advantageous traits. Extended leaf phenology is a characteristic noted in many woody invasive plants. Leaf phenology of Py. calleryana and two native woody species, Populus deltoides and Platanus occidentalis, was observed in natural areas near Dayton, OH from December 2019 to November 2020. A frost event in May also gave us the serendipitous opportunity to assess frost tolerance of these species. We found that Py. calleryana began leafing out almost a month before its native competitors in the spring and kept its leaves on significantly longer than both Po. deltoides and Pl. occidentalis throughout the fall. After the frost event, almost every leaf on Pl. occidentalis died and almost 70% of the leaves on Po. deltoides were damaged; however, Py. calleryana exhibited damage on only 6% of its leaves. Our study suggests that Py. calleryana has a nearly 1-mo advantage in leaf phenology in both spring and fall, and much greater frost tolerance, as compared with native species. These attributes likely contribute to its capacity to outcompete native trees in early successional habitats.

The Seasonal Influence of Invasive Shrubs on Light and Temperature in an Eastern Deciduous Forest Understory

Invasive shrubs are flourishing in temperate, deciduous forest understories of eastern North America where resources, especially light, are limited. However, understory light is more available before the overstory canopy leaves emerge in the spring and after fall senescence. Extended leaf phenology of invasive shrubs in the spring and fall compared to native shrubs and the overstory canopy is conspicuous, as well as higher foliage abundance of invasive compared to native shrubs. Extended leaf phenology of invasive shrubs provides photosynthetic benefits, but also seasonally novel shade. Light and temperature regulate life history characteristics across taxa and influence ecosystem processes. Here, a long-term invasive shrub removal experiment is used to quantify the effect on light and air temperature over 3–4 y. There was a pattern of reduced maximum air temperature in the presence of invasive shrubs during the growing season of most years. We find less light energy infiltration (lumens m–2) below invasive shrubs than native shrubs with mean differences largest in the spring (–1981 [–2604, –1380], a 26.8% reduction relative to below natives). Differences diminish through summer (–1038 [–1221, –845]), fall (–547 [–660, –429]), and winter (–257 [–372, –151]). Invasive shrubs also filter more photosynthetically active radiation than natives (58.4 [38.5, 78.7] µmol m–2 s–1, a 39.4% reduction), but seasonal differences were not detected indicating denser canopy structure for invasive shrubs throughout the year. When compared to the native understory community, the presence of invasive shrubs seasonally reduces temperature and light availability near the forest floor, which could affect resident plant and animal species.

Citizen scientists record novel leaf phenology of invasive shrubs in eastern U.S. forests

Invasive shrubs are an emergent concern in deciduous forests of eastern North America. Their extended leaf phenology (ELP)—earlier leaf emergence and later leaf off compared to native shrubs and the overstory canopy—can simultaneously provide photosynthetic benefits to invasive shrubs while negatively affecting native flora and fauna through producing novel understory shade when the overstory canopy is leafless. However, phenology varies geographically, and the degree to which ELP from local-scale studies applies across the range of forests experiencing shrub invasion is unknown. In partnership with the USA National Phenology Network, we developed a citizen science campaign to record broad patterns of species-specific ELP—an otherwise prohibitively large effort. Using 1500 observations of 14 species spanning 4 years, we found that the difference in leaf phenology between native and invasive shrubs can exceed 77 days within a growing season, a gap that decreases with increasing latitude by 2.9 [1.6, 4.2] days per degree latitude in the spring, and 2.2 [0.6, 1.9] in the fall. Geographic trends in ELP provide a context for interpreting local scale phenology research while bridging inconsistent findings between existing studies and can streamline management by targeting detection and removal of invasive shrubs with leaves while natives are dormant. Furthermore, even small changes to seasonal phenology can impact forest communities, especially if there is a differential response to climate cues by nativity. After exploring broad-scale environmental variables associated with leaf phenology, we find a similar correlation with pre-growing season warmth for native and invasive shrubs, but a different relationship with dormant chill days—a variable less frequently considered for modeling spring phenology for forest productivity.

Extended leaf phenology has limited benefits for invasive species growing at northern latitudes

Many understory woody invasive plants in North America leaf out earlier or retain leaves later than their native associates. This extended leaf phenology is thought to grant invasive species an advantage over native species because spring and fall are crucial times for light access and carbon acquisition in understory habitats. However, it is unclear whether this advantage persists at northern latitudes where freezing temperatures constrain growing season length and low light levels reduce carbon gain. To investigate the costs and benefits of extended leaf phenology at northern latitudes, we observed leaf phenology, estimated total carbon gain, measured growth, and tested susceptibility to freezing temperatures for four native and four invasive woody shrubs in a disturbed forest in northern Minnesota, USA. We found that the invaders leafed out simultaneously with the natives in the spring but retained their leaves later in the autumn than native species. This extended fall phenology did not enable greater total carbon gain for the invaders because they assimilated less carbon earlier in the year than the natives. There was also no significant difference between native and invasive species in their susceptibility to freezing temperatures. Instead freezing tolerance related more to native range then leaf phenology. Our results suggest that freezing temperatures do not limit invasive species’ northern expansion and instead indicate that at the northern edge of their ranges, these species may lose any competitive advantage granted by extended leaf phenology over their native associates. This study demonstrates the importance of considering latitude and forest structure when investigating phenology and growth.

Assisted migration across fixed seed zones detects adaptation lags in two major North American tree species.

Boreal forests are experiencing dramatic climate change, having warmed 1.0°–1.9°C over the last century. Yet forest regeneration practices are often still dictated by a fixed seed zone framework, in which seeds are both harvested from and planted into predefined areas. Our goal was to determine whether seedlings sourced from southern seed zones in Minnesota USA are already better adapted to northerly seed zones because of climate change. Bur oak (Quercus macrocarpa) and northern red oak (Quercus rubra) seedlings from two seed zones (i.e., tree ecotypes) were planted into 16 sites in two northern seed zones and measured for 3 yr. Our hypotheses were threefold: (1) tree species with more southern geographic distributions would thrive in northern forests where climate has already warmed substantially, (2) southern ecotypes of these species would have higher survival and growth than the northern ecotype in northern environments, and (3) natural selection would favor seedlings that expressed phenotypic and phenological traits characteristic of trees sourced from the more southern seed zone. For both species, survival was high (>93%), and southern ecotypes expressed traits consistent with our climate adaptation hypotheses. Ecotypic differences were especially evident for red oak; the southern ecotype had had higher survival, lower specific leaf area (SLA), faster height and diameter growth, and extended leaf phenology relative to the northern ecotype. Bur oak results were weaker, but the southern ecotype also had earlier budburst and lower SLA than the northern ecotype. Models based on the fixed seed zones failed to explain seedling performance as well as those with continuous predictors (e.g., climate and geographical position), suggesting that plant adaptations within current seed zone delineations do align with changing climate conditions. Adding support for this conclusion, natural selection favored traits expressed by the more southern tree ecotypes. Collectively, these results suggest that state seed sourcing guidelines should be reexamined to permit plantings across seed zones, a form of assisted migration. More extensive experiments (i.e., provenance trails) are necessary to make species‐specific seed transfer guidelines that account for climate trends while also considering the precise geographic origin of seed sources.

Deer browsing overwhelms extended leaf phenology benefits: A test case with Rubus allegheniensis and a recalcitrant hay-scented fern layer

Plant species coexistence can be promoted by multiple tradeoffs including temporal niche separation via differences in phenology. Namely, if phenological differences afford longer leaf life-spans that confer species the opportunity to exploit light and fix carbon during periods relatively free of other competitors, then coexistence, or even competitive superiority, may arise. Phenological niche separation explanations, including the Extended Leaf Phenology (ELP) hypothesis, have garnered considerable support as a mechanistic explanation for both exotic invasive species success and maintenance of native plant species. The benefits conferred by a phenological advantage, however, can be nullified if tissue losses from browsing are coincident with this phenological window of opportunity. This study experimentally tests the role of phenological advantage and white-tailed deer (Odocoileus virginianus) browsing, alone and in concert, in structuring coexistence between the native forest shrub Rubus allegheniensis, which possesses an extended phenological window, and the native invasive fern Dennstaedtia punctilobula. Browsing treatments (ambient versus excluded) were factorially crossed with shading treatments (none versus shading timed to eliminate phenological advantage). The results demonstrate the phenological advantage is an essential growth mechanism for Rubus as seedlings deprived of the ELP advantage were, on average, 50% shorter than those not treated with shade. However, this benefit was largely dependent on herbivory pressure, as deer browsing largely nullified the growth benefits provided by the phenological advantage. This experiment is the first experimental study documenting how browsing impacts affect a plant species by curtailing a phenological coexistence advantage. The results suggest elucidating the interacting roles of the ELP and browsing is critical, particularly as the phenological niche advantage does not necessarily constitute a fitness advantage where browsing pressure is high. Results from this work also provide broader insight into how exotic plant species invasions that are assumed to be aided by a phenological (ELP) advantage, may be modulated through their browse susceptibility. Overall, these results suggest understanding the co-occurring roles of phenology and browsing may guide management decisions to maintain or promote understory plant diversity.

Extended leaf phenology presents an opportunity for herbicidal control of invasive forest shrubs

SummaryFor many of the shrub species invading temperate deciduous forests, extended leaf phenology contributes substantially to annual carbon gains, helping to make possible rapid growth and spread. We carried out a pair of proof‐of‐concept studies to evaluate the susceptibility of such shrubs to foliar herbicide treatment during the period of delayed senescence, i.e. well after it is typically attempted. We first evaluated leaf‐level physiology in four species that lose leaves late in autumn; photosynthetic rates were comparable (80–111%) to those reported for the same species in summer. While preliminary, this finding provides a strong indication that diverse shrub taxa remain susceptible to control into late autumn. In addition, we conducted a field trial involving one of these species (Lonicera maackii) to directly evaluate the effectiveness of foliar treatment in November; applications included glyphosate and two concentrations of aminocyclopyrachlor plus metsulfuron methyl. Treatments killed (72%) or severely injured (14%) target plants, inducing greater cambial damage in plants that retained greater fractions of their canopy or had smaller canopy widths; there were no statistically significant differences among application types. This study demonstrated that late autumn can be a viable period in which to treat weedy species that delay senescence strongly, such as the many invasive Lonicera species in North America. Given that climate change and urbanisation are further delaying senescence in invasive plant populations, our study serves as a call for further investigation into what promises to be an increasingly viable opportunity for weed control in deciduous forests.

White-tailed deer browse on an invasive shrub with extended leaf phenology meets assumptions of an apparent competition hypothesis.

It has been hypothesized that invasive plant species with extended leaf phenology (ELP) elevate generalist herbivore populations, increasing herbivory on native plants (apparent competition). This hypothesis assumes that consumption of the invasive is associated with periods of ELP, the invasive is a major component of the herbivore's diet, and that it is more nutritious than native plants during periods of ELP. We tested these assumptions by estimating the proportion of the white-tailed deer diet comprised of Lonicera maackii, an invasive shrub with ELP, quantifying the seasonal pattern of deer browse on this invasive shrub, and comparing its nutritional quality to leafless woody stems. In the Miami University Natural Areas in southwest Ohio we quantified the frequency of leafy twigs of woody species 0.3-2.1 m high in three habitats (deciduous forest, Juniperus virginiana forest, and forest-field edge). Monthly we quantified deer browse on marked L. maackii twigs, and estimated the mass of leaf and stem tissue consumed with allometric relationships using diameter and length of unbrowsed twig portions. We estimated the percent of the annual deer diet comprised of L. maackii by dividing the sum of these estimates by the product of deer abundance (estimated by pellet-based distance sampling) and consumption estimates from the literature. Crude protein of L. maackii stems and leaves was determined by C:N analyser. In each habitat the frequency of L. maackii was greater than all other woody species combined. We estimated L. maackii comprised 14-47 % of the annual deer diet. Deer browsed L. maackii each month, but consumption was high in early spring and late summer. Crude protein of leafy twigs of L. maackii in early spring was 12.9 %, much higher than leafless twigs of native species on-site. These findings support the assumptions of the hypothesis that invasive plants with ELP impact native plants via deer-mediated apparent competition.

Quantification of Changes in Light and Temperature Associated with Invasive Amur Honeysuckle (Lonicera maackii)

Biological invasion by nonnative species is considered one of the major threats to the global environment. Amur honeysuckle (Lonicera maackii) is a shrub introduced from Asia which has become invasive in Eastern deciduous forests of North America. An interesting aspect of the life-history of Amur honeysuckle is its extended leaf phenology. It leafs out earlier in the spring than most native shrubs and understory trees and loses its leaves later in the fall. Thus, Amur honeysuckle has the potential to alter the natural light environment and possibly impact native species, particularly spring ephemerals which are dependent on high light levels prior to canopy leaf-out. We tested the hypothesis that light levels are lower in sites with Amur honeysuckle relative to sites with native forest understory and quantified differences between sites. We found that light levels were significantly lower under Amur honeysuckle compared to natural understory, with the greatest reduction occurring during spring. Temperature at ground level was also lower under Amur honeysuckle than under the natural understory during spring. The extended leaf phenology of Amur honeysuckle alters both temperature and light intensity, which may increase both its success as an invader and its impact on native species.

Extended leaf phenology may drive plant invasion through direct and apparent competition

Invasive plants can inflict great harm, yet drivers of successful invasion remain unclear. Many invaders of North American deciduous forests exhibit extended leaf phenology (ELP), or longer growing season relative to natives. ELP may grant invaders competitive advantages, but we argue that ELP more potently drives invasion in the presence of herbivores. ELP invaders can support herbivores by lessening starvation during winter; consequently, native plants may suffer when attacked later through apparent competition. As modeled here, even short ELP can promote competitive success of invaders, and apparent competition sharply enhances ELP invader dominance. In ‘partial enemy escape’ scenarios, a less palatable ELP invader nearly excludes a preferred native where an invader without ELP could not. Together, ELP and apparent competition enhance invasion even when biotic resistance should suppress it, i.e. when the invader competes weakly or provides preferred forage. Thus, ELP‐apparent competition interactions grant invaders considerable success while challenging core tenets of invasion ecology.

Extended leaf phenology, allelopathy, and inter-population variation influence invasion success of an understory forest herb

Extended leaf phenology (ELP) may commonly drive invasion in Eastern deciduous forests of North America. ELP may confer an advantage in competition, and may interact with other invasion factors. For example, ELP may interact with allelopathy (release of toxins) if exposure to seasonal light influences allelochemical production. Here, we examine ELP and its interaction with glucosinolate (allelochemical) production in invasive garlic mustard (Alliaria petiolata). To test ELP’s role in invasion, garlic mustard was grown in monoculture or polyculture with native species under natural and extended shade regimes. Consistent with an ELP invasion mechanism, garlic mustard survival was higher in natural shade than extended shade, although invader biomass and native responses did not differ between light treatments. While garlic mustard leaf glucosinolate concentration was higher in natural than extended shade during September of its first year, this pattern did not hold at three other time points. Stronger support for the role of ELP in driving garlic mustard invasion emerged from direct manipulation of germination phenology, with higher garlic mustard survival and biomass resulting when germination occurred earlier in the season. Analysis of allelochemical production across eight populations of garlic mustard revealed significant inter-population variation in glucosinolate responses to light availability. Overall, results of these three experiments indicate that ELP may facilitate garlic mustard’s survival in invaded communities. We did not find strong evidence for a synergistic relationship between ELP and allelopathic potential, possibly due to high levels of inter-population variation in the relationship between allelopathy and light.

Exotic invasive plants alter thermal regimes: implications for management using a case study of a native ectotherm

Summary Exotic invasive plants can alter ecosystem structure and function, yet there is a paucity of evidence regarding broadly applicable mechanisms. We hypothesized that denser growth patterns characteristic of exotic invasive plants lead to a common effect of reduction and homogenization of environmental temperatures and that these alterations compromise thermal quality of habitat for ectotherms. We quantified thermal regimes within native and exotic plant‐dominated habitats, including monocultures of 11 exotic species as well as stratified mixed‐exotic habitats in a temperate forest landscape in the eastern US. Exotic plant‐dominated habitats exhibited reduced and less variable temperature compared to their native counterparts, with stratified mixed‐exotic habitats exhibiting the lowest temperatures overall and exotic shrubs (six species) the lowest as a structural group. Thermal effects were extended beyond the growing season of native vegetation owing to extended leaf phenology of exotic woody species. To demonstrate that these effects can alter environmental cues and adversely impact native species, we used a 4‐year radiotelemetry study and laboratory thermal preference trials to relate habitat thermal quality to multiscale resource selection by a native snake, Agkistrodon contortrix. To further test the effect of vegetation structure and the efficacy of targeted management, we removed exotic foliar cover from eight 400 m2 plots. Radio‐tagged snakes avoided exotic vegetation at multiple spatial scales. In contrast to previous studies of A. contortrix, snakes exhibited preference for sites composed of higher native vegetation density and height. Response to exotic foliage removal was also rapid – including use of sites during gestation and parturition. Together with other recent studies, our results suggest a direct, non‐trophic effect that is common to a broad range of exotic invasive plant species in a variety of ecological contexts. We further offer a mitigation technique that may be implemented when large‐scale control or eradication is not cost‐effective or ecologically sound.

Light, allelopathy, and post-mortem invasive impact on native forest understory species

Extended leaf phenology (early budbreak and/or delayed leaf drop) and allelopathy are potentially key invasion mechanisms in North American deciduous forests. Because extended phenology confers increased access to light energy and allelochemical production is energetically costly, these traits may interact synergistically to determine invader impact. Garlic mustard (Alliaria petiolata) exhibits both traits, and may also exploit high light in open habitats. We manipulated seasonal light availability to examine effects of light on garlic mustard’s growth, allelochemical production, and impact on native species. Invaded and not-invaded woodland microcosms were exposed to three light treatments: shading year-round (‘extended shade’), shading when the local tree canopy was closed (‘natural shade’), and ambient light year-round (‘no-shade’). Regardless of native presence, garlic mustard biomass was highest under natural shade and, due to apparent irradiation damage, lowest under no-shade. Similarly, growth and fruit production of garlic mustard monocultures were reduced in unshaded conditions. Consistent with these results, garlic mustard reduced the growth of native woodland forbs Blephilia hirsuta and Ageratina altissima most under natural shade, suggesting that extended leaf phenology mediates impact on these herbaceous species. However, garlic mustard growth did not predict reduction of whole-community biomass: invasion reduced native community growth most under no-shade, where invader biomass was lowest but allelochemical production was highest. This result may be driven by a ‘post-mortem’ pulse of allelochemicals from decaying garlic mustard tissue. We conclude that extended leaf phenology may mediate garlic mustard’s impact on some native species, and that light and allelopathy may interact to drive invasion.

Extended leaf phenology: a secret of successful invaders?

Smith (2013), in this issue, reviews the consequences of extended leaf phenology of invasive plant species in native deciduous forests. How important is early leaf emergence and/or late leaf senescence for the success of non-native species? What are the direct and indirect impacts on invaded communities and ecosystems? We are just at the very early stage in answering such questions.

Extended leaf phenology in deciduous forest invaders: mechanisms of impact on native communities

AbstractMany high‐impact invaders of temperate deciduous forests of Eastern North America exhibit extended leaf phenology compared to native species, with leaf emergence occurring earlier in the spring and abscission occurring later in the autumn. This observation indicates that extended phenology may be an important invasion mechanism for this system. However, most evidence that extended leaf phenology drives species invasion is anecdotal, and most studies that directly address the role of leaf phenology in invasion focus solely on increased invader growth. Beyond increasing invader growth, extended leaf phenology may drive invader impact on natives by (1) facilitating resource competition through nutrient pre‐emption and shading, (2) altering production of secondary chemicals by invasive plants, (3) altering apparent competition dynamics mediated by native herbivores, (4) allowing temporal enemy escape, and (5) altering behaviour of native pollinators. I review current evidence from the literature regarding each of these possible consequences of extended invader phenology and emphasize the need for experimental manipulations to measure the extent to which extended leaf phenology mediates impact on the native community. Understanding the importance of leaf phenology in species invasion will facilitate prevention of future invasions while elucidating the role of seasonality in shaping species interactions.

Extended leaf phenology as an invasion mechanism for Alliaria petiolata

Extended leaf phenology as an invasion mechanism for Alliaria petiolata

Extended leaf phenology and the autumn niche in deciduous forest invasions

The phenology of growth in temperate deciduous forests, including the timing of leaf emergence and senescence, has strong control over ecosystem properties such as productivity and nutrient cycling, and has an important role in the carbon economy of understory plants. Extended leaf phenology, whereby understory species assimilate carbon in early spring before canopy closure or in late autumn after canopy fall, has been identified as a key feature of many forest species invasions, but it remains unclear whether there are systematic differences in the growth phenology of native and invasive forest species or whether invaders are more responsive to warming trends that have lengthened the duration of spring or autumn growth. Here, in a 3-year monitoring study of 43 native and 30 non-native shrub and liana species common to deciduous forests in the eastern United States, I show that extended autumn leaf phenology is a common attribute of eastern US forest invasions, where non-native species are extending the autumn growing season by an average of 4 weeks compared with natives. In contrast, there was no consistent evidence that non-natives as a group show earlier spring growth phenology, and non-natives were not better able to track interannual variation in spring temperatures. Seasonal leaf production and photosynthetic data suggest that most non-native species capture a significant proportion of their annual carbon assimilate after canopy leaf fall, a behaviour that was virtually absent in natives and consistent across five phylogenetic groups. Pronounced differences in how native and non-native understory species use pre- and post-canopy environments suggest eastern US invaders are driving a seasonal redistribution of forest productivity that may rival climate change in its impact on forest processes.