Not all temperate deciduous trees are leafless in winter: The curious case of marcescence

Abstract

Temperate deciduous forests by definition include a large proportion of woody species that shed their leaves each autumn and are completely leafless during winter months. Leaf senescence in deciduous trees is an active, complex process typically involving the physiological formation of an abscission layer causing the petiole to mechanically detach from the branch. However, several deciduous species retain all or some senesced leaves on branches through much of winter, a phenomenon called leaf marcescence. Marcescence has long fascinated botanists, including Pehr Kalm as early as 1749. Yet, surprisingly little research has been done to date. Here, we review and explore patterns and mechanisms of leaf marcescence in temperate forests, bringing together six nonmutually exclusive but separately proposed hypotheses: (1) Marcescence has no adaptive function but rather an evolutionary byproduct; (2) Marcescent leaves deter winter browsing herbivores; (3) Leaf retention through winter improves nutrient resorption during autumn senescence; (4) Prolonged leaf shedding into spring minimizes nutrient leaching and promotes decomposition; (5) Marcescent leaves protect overwintering buds from frost or desiccation; and (6) Marcescent canopies provide winter cover for animals (including insects, birds, bats), thereby affecting plant nutrient availability via excrement. No hypothesis has complete support and few tests of multiple hypotheses have been done. It is likely that any adaptive value of marcescence is species and context dependent. Despite increased interest in plant phenology and prevalence of this trait, much remains to be understood on the physiology, evolution, function, and ecological implications of leaf marcescence.

Temperate deciduous forests are marked by the absence of leaves in the winter, bringing out the dendritic patterns of tree branches in the pensive quiet of snowfall. These forests are so seasonally distinct that winter scenes are nearly unrecognizable from the lush vegetation of summer when the dense tree canopies above shade the herbaceous layer below. Yet, not all trees are leafless in winter. In mixed deciduous forests with evergreen trees, some winter greenness is expected. More intriguing, though, are those branches of deciduous species with dead leaves still attached—a phenomenon botanically known as marcescence. Once noticed, this observation becomes pervasive, far more common than appreciated. Marcescence is especially visually striking in American beech (Fagus grandifolia), a widespread species dominating many late-successional stands across the Eastern Deciduous Forest of North America. The seasonal observation can be striking, such as at Powdermill Nature Reserve in the Laurel Highlands of Pennsylvania, USA (Figure 1). Given the winter bareness of these forests following autumn leaf drop, eyes are immediately drawn to the dry, wrinkled leaves that remain. On initial observation, patterns are unclear, with marcescent leaves on some branches but not others. This observation leads to a common question during any winter hike, often posed by both scientists and nonscientists alike: Why do some senesced leaves remain on branches through winter?

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Marcescent leaves have long fascinated botanists, yet the phenomenon is surprisingly understudied. As early as 1749, the Swedish-Finnish naturalist Pehr Kalm, a disciple of Linnaeus, specifically noted the prevalence and peculiarity of oak and beech leaves that failed to drop from branches in the fall during his winter travels in North America (Kalm, 1776). Kalm was struck by his observations that marcescent leaves were most common in smaller trees and only in the lower branches of larger trees. Indeed, these qualitative observations centuries ago closely match our quantitative measurements. In mid-winter (January–February 2021), we surveyed American beech (F. grandifolia) trees across plant sizes, recording the presence and relative intensity of leaf marcescence across trees and branches (see Appendix S1: Methods; Heberling & Muzika, 2022). We found overall marcescence was far more common in smaller trees (<5 m height) and on lower branches. Of the relatively fewer large trees that exhibited any marcescence, their leaves were almost exclusively restricted to lower branches (Figure 2a). These patterns were similar when considering stem diameter (Appendix S1: Figure S1). Although trends with plant size seem apparent, the variation in the trait is remarkable. In some cases, plants only a few centimeters apart and the same size can exhibit obvious marcescence or none at all (Appendix S1: Figure S2). Based on our observations in this species, it is unlikely that the greater retention of leaves in lower canopy and shorter trees can be explained by possible differences in wind speeds alone, as vigorous shaking, even late into winter, did not cause leaves to fall (Video S1).

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Despite the recently expanded interest in plant phenology, the phenology of marcescent leaves has not been well studied and usually overlooked. Are marcescent leaves retained until a sudden drop in spring or are these leaves slowly shed throughout winter with bare branches during spring leaf out? To answer this question, we regularly counted the number of marcescent leaves in medium-sized (2–4 m tall) beech saplings across tagged branches through winter. To our surprise, most marcescent leaves persist on branches well into spring, with a pronounced, short period of leaf shedding. Marcescent leaves remain as other plants have fully flushed leaves (Appendix S1: Figure S3). In early April 2021, 50% of monitored leaves were shed within a two-week period (Figure 2b).

Leaf senescence is an active process, regulated by hormones and affected by shorter daylengths and cooler temperatures of fall. Foliar nutrients are resorbed as chlorophyll breaks down, unmasking yellow pigments and in some species also newly produced red pigments, which together mark the colors of autumn. As auxin decreases in leaves, an abscission layer is formed by the weakening of cells at the base of the petiole where the leaf is subsequently shed. However, this abscission layer is not formed in marcescent leaves, as shown through anatomical studies of decades ago (Berkley, 1931; Hoshaw & Guard, 1949) and stated in classic tree physiology textbooks (Kramer & Kozlowski, 1979).

While the physiological mechanisms of autumn leaf senescence may be known, the most basic ecological and evolutionary questions about marcescence remain largely unanswered. A null hypothesis for any trait, including marcescence, is that it is an evolutionary byproduct with no current adaptive function. There is a strong phylogenetic pattern at our site for leaf marcescence, with nearly all species exhibiting the trait belonging to the plant order Fagales (oaks, beech, and chestnut; Appendix S1: Figure S4), a conclusion that has been noted elsewhere (Karban & Pearse, 2021). In these plant families, it is possible that the marcescent leaf habit may be a byproduct of incomplete evolution of deciduousness from evergreen ancestors. A comparative analysis of leaf marcescence is needed, and we suggest botanical gardens and arboreta as ideal resources for these studies. Further, community science data (e.g., images from iNaturalist) could assist in understanding whether marcescence is uniform across species' ranges, effects of environment, and population-level differences that might arise from different selection pressures.

A commonly mentioned hypothesis on the adaptive value is that marcescence deters winter herbivore damage. Marcescent leaves with low nutritional quality may deter both large (e.g., deer) and small (e.g., insects) herbivores from eating overwinter buds and twigs. Support for an anti-herbivore hypothesis was found in an experimental study testing deer browse preference in a temperate forest in Denmark (Svendsen, 2001). Though speculative, the increased presence of marcescent leaves within the deer browse line (on smaller trees and lower branches; Figure 2a) supports the prediction that the trait deters large herbivores. Similarly, the experimental removal of dead leaves in a grass species in a grassland in Argentina showed increased consumption by grazers (Mingo & Oesterheld, 2009). In contrast, studies focusing on insects in an oak species in Mediterranean woodlands in California were less clear. Karban (2007) found higher densities of gall-forming wasps on trees with marcescent leaves versus trees with leaves experimentally removed. However, the study did not distinguish between brown marcescent leaves and leaves that remain green through winter. However, when considering green and brown overwintering leaves separately, Pan et al. (2021) found lower densities of gall-forming wasps on trees with brown marcescent leaves. More experimental studies across more biomes, forests, and species are needed.

Another hypothesis explaining marcescence is that the retention of senescing leaves prolongs leaf longevity to enable more efficient nutrient resorption, resource use, and/or late-season photosynthetic gains. Marcescence might be expected to increase nutrient resorption if the senescence period is prolonged. Alternatively, one might expect leaf nutrient resorption to be lower if leaves are functional until killed by late frost. For instance, we have noticed some species to be irregularly marcescent, likely due to uncommon early frost events before abscission layer is fully formed (e.g., introduced Acer platanoides in southwestern Pennsylvania, Appendix S1: Figure S5). Abadía et al. (1996) measured a Mediterranean oak species in Spain, finding leaves that received more light (i.e., upper canopy) senesced later and were marcescent, whereas lower canopy leaves senesced and dropped leaves earlier. However, they found no difference in nutrients between leaves. The authors conclude marcescence increases the capacity for photosynthesis later into the season. Similarly Escudero and del Arco (1987) measured leaf abscission times across evergreen, deciduous, and marcescent species in the Iberian Peninsula, concluding that the timing of leaf abscission to be adaptive for mitigating moisture stress but surprisingly, unrelated to leaf habit. However, these studies are limited to Mediterranean woodlands and may not be applicable to temperate forests. Botanical gardens and arboreta can provide opportunities to evaluate whether nutrient resorption is higher in marcescent leaves.

Another hypothesis suggests marcescence promotes litter decomposition and the timing of soil nutrient release. Otto and Nilsson (1981) proposed that marcescence evolved as a mechanism to ensure the “closing of the nutrient cycle,” that is, two periods of leaf drop in autumn and spring result in a more gradual (and optimal) recycling of nutrients to the plant. They further suggest that the higher proportion of marcescent leaves in lower branches is adaptive with a functional explanation, suggesting these leaves are more likely to fall directly beneath the tree (and therefore directly benefit the individual tree). However, marcescence may not always be associated with a shorter period of abscission (Escudero & del Arco, 1987). Even if gradual shedding is not always true for marcescent species, the dead leaves retained on branches may change their properties than those shed in autumn. One study finds marcescent leaves increase litter decomposition because prolonged retention increases exposure to insolation that enables a more rapid breakdown in the soil of recalcitrant litter in spring (Angst et al., 2017). A related study further showed that marcescent leaf litter was more bioavailable (e.g., lower C:N, lignin content) compared to shed immediately after senescence (Angst et al., 2022). These nutrient cycling hypotheses remain controversial, but biogeochemical studies could further examine the association of leaf marcescence with nutrient cycling and plant nutrient uptake.

A less cited but experimentally unexamined hypothesis in deciduous trees is that marcescent leaves protect overwintering buds from frost damage or desiccation. In support, Nilsson (1983) speculated that marcescence is most common in lower branches of trees because they are exposed to lower minimum temperatures. Marcescent leaves common in rosette-forming herbaceous species adapted to alpine environments have been shown to significantly buffer the microclimate (Smith, 1979). Microclimatic buffering from frost has also been shown in the New Zealand endemic Cordyline australis, with marcescent leaves protecting the trunk of juvenile plants (Harris et al., 2004). Nilsson (1983) further predicts that a thicker leaf litter layer of later dropping marcescent leaves inhibits ground layer vegetation in the spring and minimizes interspecific competition. To our knowledge, this hypothesis remains untested. At our site, we observed no difference in phenology or failure to leaf out between buds with marcescent leaves and those with marcescent leaves we experimentally removed mid-winter (data not shown). However, it is unknown whether marcescence differs from year to year. Late spring frosts have been shown to delay autumn senescence in some species (Zohner et al., 2019). By extension, delayed autumn senescence might increase marcescence, or early autumn frosts might lead to failure to form a proper abscission layer. A recent study of California oaks demonstrated that marcescent species are at higher risk to branch loss during winter storms than other species (Karban & Pearse, 2021). Longer term observational data are needed, alongside marcescent leaf removal experiments.

Another proposed hypothesis posits that marcescent leaves provide animal habitat in winter. In fact, this was the only explanation given by Kalm, writing in reference to marcescence that “… it seems Providence has … aimed to protect several sorts of birds …” (Kalm, 1776). For marcescence to be adaptive, the tree must benefit. Natural selection might favor trees exhibiting marcescence if roosting animals (e.g., birds, bats) increase soil nutrients via excrement. To test this idea, we propose that more plant–animal winter observations and soil nutrient data across marcescent and nonmarcescent trees are needed. Beyond roosting animals, limited evidence also exists for effects of marcescence on invertebrates, including positive effects on spiders (Pearse et al., 2020) but negative effects on gall-forming wasps (Pan et al., 2021).

A last hypothesis is that marcescence increases flammability. The retention of dead leaves (or other plant parts, such as reproductive structures) might increase the incidence and severity of fires, which could be adaptive for species that depend upon fire for regeneration (e.g., He et al., 2011). This hypothesis is unlikely to be relevant for species not adapted to fire (such as F. grandifolia surveyed in the present study) or for temperate mesic deciduous forests. However, it has not been well tested in this system.

Our observations of leaf marcescence were not the first, yet many questions remain. Here, we provided an overview of some explanations for marcescence in temperate forests, which we categorized into six nonmutually exclusive hypotheses: (1) no adaptive function, (2) deters herbivory, (3) increases time for nutrient resorption and/or photosynthesis, (4) promotes litter decomposition and nutrient release timing, (5) protects overwintering buds, and (6) supports mutualisms through winter habitat. A seventh hypothesis invokes marcescence as a trait related to flammability, but this hypothesis is likely less relevant to mesic temperate deciduous forests. Mostly left to speculation, none of these hypotheses have complete support. Several hypotheses might be accurate, but it is likely dependent upon species, ecosystem, and ecological context.

Further studies are clearly needed on the functional, phylogenetic, geographic, and evolutionary patterns and explanations for marcescence. Limited studies have occurred in Mediterranean regions (Spain, California) or Northern Europe. Few studies examine multiple hypotheses together. Most studies focus on woody trees, but many herbaceous species with overwintering rosettes also have marcescent leaves. Plant structures other than leaves, such as inflorescences, may also exhibit marcescence, but are largely unstudied. Irrespective of adaptive significance, the ecosystem and ecological implications of marcescence may be profound, such as affecting nutrient cycling and species interactions. Despite its easy measurement, marcescence is not included in the more than 2000 traits on the TRY trait database (Kattge et al., 2020). We suggest botanical gardens and arboreta are well-suited for large-scale comparative phylogenetic studies on marcescence. Repeated multiyear observations can provide insight into the effects of environmental variation across years. Community science initiatives can contribute data on the geographic distribution within and across species ranges, which can be followed up with common garden experiments. The curious phenomenon of marcescence is ripe for exploration.

ACKNOWLEDGMENTS

We thank Andrew Hipp, Howard Neufeld, and Nicole Hughes for discussion and Michael Polechko for field assistance. We are grateful to Shan Kothari and an anonymous reviewer for thoughtful comments that substantially improved our paper. This work was partly supported by the US National Science Foundation (DEB 1936971 to J. Mason Heberling).

CONFLICT OF INTEREST STATEMENT

The authors declare no conflict of interest.

DATA AVAILABILITY STATEMENT

Data presented are available from Zenodo (Heberling & Muzika, 2022): . Herbarium vouchers (collector numbers: Heberling 1290 and 1493) were deposited at Carnegie Museum of Natural History herbarium (CM) and observations on GBIF (2022a) at . iNaturalist observations corresponding to the herbarium vouchers are also available on GBIF (2022b) at .

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