Alejandro A. Royo

On the formation of dense understory layers in forests worldwide: consequences and implications for forest dynamics, biodiversity, and succession

The mechanistic basis underpinning forest succession is the gap-phase paradigm in which overstory distur- bance interacts with seedling and sapling shade tolerance to determine successional trajectories. The theory, and ensu- ing simulation models, typically assume that understory plants have little impact on the advance regeneration layers composition. We challenge that assumption by reviewing over 125 papers on 38 species worldwide that form dense and persistent understory canopies. Once established, this layer strongly diminishes tree regeneration, thus altering the rate and direction of forest succession. We term these dense strata recalcitrant understory layers. Over half of the cases re- viewed were linked to increases in canopy disturbance and either altered herbivory or fire regimes. Nearly 75% of the studies declared that competition and allelopathy were the likely interference mechanisms decreasing tree regeneration, yet only 25% of the studies used manipulative field experiments to test these putative mechanisms. We present a con- ceptual model that links the factors predisposing the formation of recalcitrant understory layers with their interference mechanisms and subsequent impacts on succession. We propose that their presence constricts floristic diversity and ar- gue for their explicit inclusion in forest dynamics theory and models. Finally, we offer management suggestions to limit their establishment and mitigate their impacts.

Pervasive interactions between ungulate browsers and disturbance regimes promote temperate forest herbaceous diversity.

Disruptions to historic disturbance and herbivory regimes have altered plant assemblages in forests worldwide. An emerging consensus suggests that these disruptions often result in impoverished forest biotas. This is particularly true for eastern U.S. deciduous forests where large gaps and understory fires were once relatively common and browsers were far less abundant. Although much research has focused on how disturbance and browsers affect tree diversity, far less attention has been devoted to forest understories where the vast majority (>75%) of the vascular species reside. Here we test the hypothesis that the reintroduction of disturbances resembling historic disturbance regimes and moderate levels of ungulate browsing enhance plant diversity. We explore whether once-common disturbances and their interaction with the top-down influence of browsers can create conditions favorable for the maintenance of a rich herbaceous layer in a region recognized as a temperate biodiversity hotspot in West Virginia, U.S.A. We tested this hypothesis via a factorial experiment whereby we manipulated canopy gaps (presence/absence) of a size typically found in old-growth stands, low-intensity understory fire (burned/unburned), and deer browsing (fenced/unfenced). We tracked the abundance and diversity of more than 140 herb species for six years. Interactions among our treatments were pervasive. The combination of canopy gaps and understory fire increased herbaceous layer richness, cover, and diversity well beyond either disturbance alone. Furthermore, we documented evidence that deer at moderate levels of abundance promote herbaceous richness and abundance by preferentially browsing fast-growing pioneer species that thrive following co-occurring disturbances (i.e., fire and gaps). This finding sharply contrasts with the negative impact browsers have when their populations reach levels well beyond those that occurred for centuries. Although speculative, our results suggest that interactions among fire, canopy gaps, and browsing provided a variable set of habitats and conditions across the landscape that was potentially capable of maintaining much of the plant diversity found in temperate forests.

Historic disturbance regimes promote tree diversity only under low browsing regimes in eastern deciduous forest

Eastern deciduous forests are changing in species composition and diversity outside of classical successional trajectories. Three disturbance mechanisms appear central to this phenomenon: fire frequency is reduced, canopy gaps are smaller, and browsers are more abundant. Which factor is most responsible is a matter of great debate and remains unclear, at least partly because few studies have simultaneously investigated more than one process. We conducted a large-scale experiment in mesophytic forests of West Virginia, USA, to test three key hypotheses: (1) the fire hypothesis (fire suppression limits diversity to few shade-tolerant, fire-intolerant species that replace and suppress many fire-tolerant species); (2) the gap hypothesis (small gaps typical of todays forests promote dominance of a few shade-tolerant species); and (3) the browsing hypothesis (overbrowsing by deer limits diversity to a few unpalatable species). We tested these hypotheses using a factorial experiment that manipulated surface fire, large canopy gap formation (gap size ;255 m 2 ), and browsing by deer, and we followed the fates of .28 000 seedlings and saplings for five years. Understory tree communities in control plots were dominated (up to 90% )b yFagus grandifolia, averaging little more than two species, whereas overstories were diverse, with 10-15 species. Fire, large canopy gaps, and browsing all dramatically affected understory composition. However, our findings challenge views that fire and large canopy gaps can maintain or promote diversity, because browsers reduced the benefits of gaps and created depauperate understories following fire. Consequently, two major disturbances that once promoted tree diversity no longer do so because of browsing. Our findings appear to reconcile equivocal views on the role of fire and gaps. If browsers are abundant, these two disturbances either depress diversity or are less effective. Alternatively, with browsers absent, these disturbances promote diversity (three- to fivefold). Our results apply to large portions of eastern North America where deer are overabundant, and we provide compelling experimental evidence that historical disturbance regimes in combination with low browsing regimes typical of pre-European settlement forests could maintain high tree species diversity. However, restoring disturbances without controlling browsing may be counterproductive.

Long-term biological legacies of herbivore density in a landscape-scale experiment: forest understoreys reflect past deer density treatments for at least 20 years

Summary 1. Ungulate browsers, when at high densities, are major drivers of vegetation change in forests world-wide. Their effects operate via a variety of generalizable mechanisms related to plant palatability and relative growth rate with respect to browsing pressure. 2. Though such impacts are obviously long-lasting when they determine composition of tree regeneration, we document in a unique long-term (30 year) experiment that biological legacies of initial deer density persist in the understorey herbaceous vegetation at least 20 years after deer densities were equalized. 3. We sampled understorey vegetation in former clear-cut areas where density of white-tailed deer (Odocoileus virginianus) was manipulated (3.9–31.2 deer km 2 ) for 10 years (1979–1990), and stands experienced ambient deer density (ca. 10–12 deer km 2 ) for the next 20 years (1990–2010) to determine whether initial deer density treatments still influenced understorey vegetation in 30-year-old, closed-canopy forests. 4. Stands initially (1979–1990) exposed to higher deer densities had ca. five times higher fern cover and three times the seedling and forb cover in 2010, as well as significantly lower angiosperm species density, compared to stands initially exposed to lower deer densities. 5. These results appear driven by deer avoidance of ferns, allowing them to expand at high deer density and sequester sites for decades. 6. Synthesis. Our long-term, experimental results show unequivocally that elevated deer densities cause significant, profound legacy effects on understorey vegetation persisting at least 20 years. Of relevance regionally and globally where high deer densities have created depauperate understoreys, we expect that deer density reduction alone does not guarantee understorey recovery; stands may need to be managed by removing recalcitrant understorey layers (e.g. ferns).

Chronic over browsing and biodiversity collapse in a forest understory in Pennsylvania: Results from a 60 year-old deer exclusion plot

Abstract We evaluated the impact of chronic deer over browsing on the diversity and abundance of understory forbs and shrubs within a forest stand in the Allegheny High Plateau Region of Pennsylvania by comparing vegetation inside a 60-year-old exclosure to vegetation within an adjacent reference site. This is the oldest known exclosure in the Eastern Deciduous Forest. Browsing caused the formation of an extremely low diversity herbaceous understory dominated by a single fern species, caused the local extirpation of shrubs, and drove forbs to extremely low abundance (< 0.2% cover m−2 vs. 43% inside the exclosure). Our results confirm previous findings that demonstrate that browsing has caused 60–80% declines in herb and shrub richness regionally. Because many of these species have low dispersal and reproductive rates, we predict long-term legacy effects if deer numbers are ever reduced. Our results combined with other studies provide information on shrub and herb abundance in the absence of browsing that may serve as a baseline to compare potential community recovery in the future.

Over-browsing in Pennsylvania creates a depauperate forest dominated by an understory tree: Results from a 60-year-old deer exclosure

Abstract We evaluated the impact of long-term over-browsing by white-tailed deer on the diversity and density of trees in a forest in the Allegheny High Plateau region of central Pennsylvania. We compared tree diversity and density inside a 60 year-old deer exclosure to an adjacent reference site. Browsing caused a 55–100% decline in density of four tree species (Prunus serotina, Acer saccharum, Betula lenta, Cornus alternifolia) and created a forest dominated (> 70% of all stems) by Acer pensylvanicum, an understory tree that is known to be highly browse-tolerant. The total density of trees that are capable of ascending into the canopy (i.e., non subcanopy tree species) declined by 85%. Browsing caused a significant decline in both mean species richness and Shannon diversity and created communities that contrasted significantly in tree species composition (ANOSIM, R  =  0.8105, P < 0.0001). Our results suggest that long-term over-browsing can create low density, depauperate communities where dominance is concentrated in only a few browse-resistant species (Acer pensylvanicum and Fagus grandifolia; 82% of all individuals vs. 37% inside the exclosure). We suggest that this may lead to novel forest dynamics in the event of a large canopy disturbance because these two species were never co-dominant in this region and the beech saplings (typically root sprouts) will likely succumb to future bouts of beech bark disease. Our results combined with those of many other studies call for the long-term reduction in the size of the deer herd throughout this region.

Deer Browsing Creates Rock Refugia Gardens on Large Boulders in the Allegheny National Forest, Pennsylvania

Abstract We surveyed the vegetation growing on the surface of tall boulders (>1.5 m), on the surface of short boulders (<0.5 m) and in areas adjacent to these boulders on the soil surface in the Allegheny National Forest, Pennsylvania. Our purpose was to test the hypothesis that tall boulders serve as refugia from deer browsing for both woody plant species as well as understory herbs. We conducted our surveys during spring when many of these herbs reproduce sexually and their inflorescences are vulnerable to browsing. Deer cannot gain access and browse on these tall boulders, whereas they can easily browse plant species on shorter boulders and on the forest floor. We predicted that the tall boulders would have the highest plant diversity, woody species density and the density of reproductive individuals of understory herbs. We found a total of more than 1300 reproductive individuals of flowering herbs of more than 10 species growing on tall boulders and only 6 reproductive individuals of only a few species growing on the soil surface. Overall, there was a much greater density and diversity of woody species and sexually reproducing herbs on tall boulders or Rock Refugia Gardens than either on short boulders or the soil surface. Because the diversity and abundance of vegetation on the short boulders was nearly identical to that on the forest floor, our findings are unlikely to be explained by tall boulders providing a superior edaphic or abiotic habitat relative to habitats on the forest floor. Species accumulation curves showed that plant species continued to accrue with area on tall boulders, but did not increase with area on the forest floor or on the short boulders. These Rock Refugia Gardens demonstrate the pervasive and deleterious impact that deer are having on plant species diversity and forest regeneration in the Allegheny National Forest and likely elsewhere in the eastern US where these vertebrates are abundant.

Evaluating the ecological impacts of salvage logging: can natural and anthropogenic disturbances promote coexistence?

Salvage logging following windthrow is common throughout forests worldwide even though the practice is often considered inimical to forest recovery. Because salvaging removes trees, crushes seedlings, and compacts soils, many warn this practice may delay succession, suppress diversity, and alter composition. Here, over 8 yr following windthrow, we experimentally evaluate how salvaging affects tree succession across 11 gaps in Eastern deciduous forests of Pennsylvania, wherein each gap was divided into salvaged and control (unsalvaged) halves. Our gaps vary in size and windthrow severity, and we explicitly account for this variation as well as variation in soil disturbance (i.e., scarification) resulting from salvaging so that our results would be generalizable. Salvage logging had modest and ephemeral impacts on tree succession. Seedling richness and density declined similarly over time in both salvaged and unsalvaged areas as individuals grew into saplings. The primary impact of salvaging on succession occurred where salvaging scarified soils. Here, salvaging caused 41 to 82% declines in sapling abundance, richness, and diversity, but these differences largely disappeared within 5 yr. Additionally, we documented interactions between windthrow severity and scarification. Specifically, low-severity windthrow and scarification combined reinforced dominance by shade-tolerant and browse-tolerant species (Acer pensylvanicum, Fagus grandifolia). In contrast, high windthrow severity and scarification together reduced the density of a fast-growing pioneer tree (Prunus pensylvanica) and non-tree vegetation cover by 75% and 26%, respectively. This reduction enhanced the recruitment of two mid-successional tree species, Acer rubrum and Prunus serotina, by 2 and 3-fold, respectively. Thus, our findings demonstrate that salvaging creates novel microsites and mitigates competing vegetation, thereby enhancing establishment of important hardwoods and promoting tree species coexistence. Our results, coupled with an assessment of 27 published post-windthrow salvage studies, suggest short-term studies may overestimate the impact of salvaging on regeneration. We conclude that the ecological costs and benefits of salvaging depend upon the variation in canopy and soil disturbance severity as well as the timescale at which effects are evaluated. Thus, our findings are inconsistent with the view that salvaging inexorably undermines plant diversity; rather we suggest salvaging can promote tree species coexistence within various contexts.

The distribution of a non-native (Rosa multiflora) and native (Kalmia latifolia) shrub in mature closed-canopy forests across soil fertility gradients.

Background and aimsA soil fertility gradient, ranging from infertile to highly fertile soils, may define whether or not a plant will establish and spread at a site. We evaluated whether or not such a fertility gradient exists for Rosa multiflora Thunb., a nonnative invasive shrub, and Kalmia latifolia L., a native problem shrub, in closed-canopy forests of the eastern U.S.MethodsWe sampled soil and vegetation at the regional scale, along four randomly located 1-km transects in 70+ year-old undisturbed forests in each of three national forests in Ohio, Pennsylvania and West Virginia. We also sampled soil, vegetation and leaf tissue at the local scale, from ten individual shrubs of each species in each national forest.ResultsRegional analyses showed a significant fertility gradient with Ohio being the most fertile and West Virginia the least. Soil fertility was associated with pH (most acidic in West Virginia and least acidic in Ohio) and elevation (highest in West Virginia and lowest in Ohio). At the local level, R. multiflora was associated with soil Ca:Al ratios greater than 0.5, and K. latifolia was associated with Ca:Al ratios less than 0.3. Rosa multiflora foliage contained higher concentrations of Ca, Mg, and K than K. latifolia, while K. latifolia foliage contained higher concentrations of Mn and Zn.ConclusionsOur research documents the importance of soil fertility as a predictor of the establishment of invasive and expansive shrubs. This study further shows that R. multiflora can establish and spread across a broader range of soil conditions than K. latifolia.

The indirect impact of long-term overbrowsing on insects in the Allegheny National Forest region of Pennsylvania

Abstract Overbrowsing has created depauperate plant communities throughout the eastern deciduous forest. We hypothesized these low-diversity plant communities are associated with lower insect diversity. We compared insects inside and outside a 60-year-old fenced deer exclosure where plant species richness is 5x higher inside versus outside. We sampled aboveground and litter insects using sweep nets and pitfall traps and identified specimens to family. Aboveground insect abundance, richness, and diversity were up to 50% higher inside the fenced exclosure versus outside. Conversely, litter insect abundance and diversity were consistently higher outside the exclosure. Community composition of aboveground insects differed throughout the summer (P < 0.05), but litter insects differed only in late summer. Our results demonstrate that the indirect effects of long-term overbrowsing can reduce aboveground insect diversity and abundance, and change composition even when plant communities are in close proximity.