Walter P. Carson

TREEFALL GAPS AND THE MAINTENANCE OF SPECIES DIVERSITY IN A TROPICAL FOREST

The maintenance of species diversity by treefall gaps is a long-standing paradigm in forest ecology. Gaps are presumed to provide an environment in which tree species of differing competitive abilities partition heterogeneous resources. The empirical evidence to support this paradigm, however, remains scarce, and some recent studies even suggest that gaps do not maintain the diversity of shade-tolerant species. Although there is evidence that gaps maintain the diversity of pioneer trees, most of this evidence comes from studies that did not make comparisons between gaps and intact forest sites (controls). Further, nearly all studies on the maintenance of diversity by gaps have ignored lianas, an important component of both old-world and neotropical forests. We tested the hypothesis that treefall gaps maintain shade-tolerant tree, pioneer tree, and liana species diversity in an old-growth forest on Barro Colorado Island (BCI), Panama. We compared the density and species richness of these guilds between paired gap and non-gap sites on both a per- area and a per-individual (per capita) basis. We found no difference in shade-tolerant tree density and species richness between the gap and non-gap sites. Both pioneer tree and liana density and species richness, however, were significantly higher in the gap than in the non- gap sites on both a per-area and a per-individual basis. These results suggest that gaps maintain liana species diversity and that this effect is not merely a consequence of increased density. Furthermore, our data confirm the long-held belief that gaps maintain pioneer tree species diversity. Because lianas and pioneer trees combined account for ;43% of the woody plant species on BCI, and in other forests, our results are likely to be broadly applicable and suggest that gaps play a strong role in the maintenance of woody species diversity.

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.

Overcompensation by plants: Herbivore optimization or red herring?

SummaryThe increased growth rates, higher total biomass, and increased seed production occasionally found in grazed or clipped plants are more accurately interpreted as the results of growth at one end of a spectrum of normal plant regrowth patterns, rather than as overcompensation, herbivore-stimulated growth, plantherbivore mutualisms, or herbivore enhanced fitness. Plants experience injury from a wide variety of sources besides herbivory, including fire, wind, freezing, heat, and trampling; rapid regrowth may have been selected for by any one of the many types of physical disturbance or extreme conditions that damage plant tissues, or by a combination of all of them. Rapid plant regrowth is more likely to have evolved as a strategy to reduce the negative impacts of all types of damage than as a strategy to increase fitness following herbivory above ungrazed levels. There is no evolutionary justification and little evidence to support the idea that plant-herbivore mutualisms are likely to evolve. Neither life history theory nor recent theoretical models provide plausible explanations for the benefits of herbivory.Several assumptions underlie all discussions of the benefits of herbivory: that plant species are able to evolve a strategy of depending on herbivores to increase their productivity and fitness; that herbivores do not preferentially regraze the overcompensating plants; that resources will be sufficient for regrowth; and that being larger is always ‘better’ than being smaller. None of these assumptions is necessarily correct.

HERBIVORY AND PLANT SPECIES COEXISTENCE: COMMUNITY REGULATION BY AN OUTBREAKING PHYTOPHAGOUS INSECT

Most general theories proposed to explain the trophic structure of communities ignore the possibility that insect outbreaks can severely damage vegetation and reduce the abundance of dominant plant species over vast areas. Specialist chrysomelid beetles can irrupt and defoliate goldenrods (Solidago spp.), a group of widespread, long-lived, herbaceous perennials. We examined the long-term effects (10 yr) of suppressing insects, using insecticide in replicated plots on the structure and diversity of an old field dominated by the goldenrod, Solidago altissima. An outbreak of the chrysomelid beetle, Microrhopala vittata, that specializes on S. altissima, occurred during the experiment and persisted several years. Damage caused by this outbreak dramatically reduced the biomass, density, height, survivorship, and reproduction of S. altissima. Herbivore exclusion caused the formation of dense stands of goldenrods with a twofold increase in both standing crop biomass and litter. The understory in these dense stands had significantly lower plant abundance, species richness, flowering shoot production, and light levels; these conditions persisted for years following the outbreak. Thus, M. vittata functioned as a keystone species. Furthermore, insect herbivory indirectly increased the abundance of invading trees, thereby increasing the rate of succession, by speeding the transition of this old field to a tree-dominated stage. We conducted two follow-up experiments to test the hypothesis that insects altered community dynamics by their indirect effect on litter accumulation and light availability in the understory. In the first experiment, we tied back the canopy to increase light into the understory and removed litter in both the insecticide-treated and control plots. We found little effect of removing litter. By contrast, increasing understory light levels significantly increased understory forb abundance and species richness. In the second experiment, we placed rosettes of Hieracium pratense, the dominant understory forb, under nine levels of shade cloth, ranging from 95% shade to full sun. Flowering-shoot production was a linear function of light availability (r2 = 0.92; P < 0.0001). We concluded that insect herbivores indirectly promoted plant species richness and coexistence, primarily by augmenting light availability to suppressed understory species. Insect herbivory may often play a strong role in goldenrod stands, because outbreaks will likely occur at least once, if not more, during the period when goldenrods are dominant. Furthermore, our findings provide compelling evidence for two general mechanisms whereby insect herbivory promotes plant species diversity and coexistence. The first mechanism operates during outbreaks when insects act as keystone species. The second mechanism can operate at less than outbreak levels and occurs whenever insect damage augments light to a sufficient degree to enhance the fecundity of suppressed nonhost species. If this increase in fecundity increases recruitment of subordinate species, then insect herbivory will promote plant species coexistence and diversity. Our data suggest that there is a continuum in the influence of insect herbivory on plant communities from the more subtle, but important, effects of herbivory on the fecundity of nonhost species to the devastating influence of outbreaks. Also, our results demonstrate that long-term experiments are required to elucidate the role of insect herbivores. Finally, we propose that insect outbreaks are common enough in many community types, particularly forests, to warrant explicit consideration in theories of trophic regulation, particularly in terrestrial communities inhabited by long-lived plant species.

The role of litter in an old-field community: impact of litter quantity in different seasons on plant species richness and abundance.

SummaryWe studied the effect of removing and adding plant litter in different seasons on biomass, density, and species richness in a Solidago dominated old-field community in New Jersey, USA. We removed all the naturally accumulated plant litter in November (658 g/m2) and in May (856 g/m2) and doubled the amount of litter in November and May in replicated plots (1 m2). An equal number of plots were left as controls. Litter removal and addition had little impact on total plant biomass or individual species biomass in the growing season following the manipulations. Litter removal, however, significantly increased plant densities but this varied depending upon the season of litter removal, species, and life history type. Specifically, the fall litter removal had a much greater impact than the spring litter removal suggesting that litter has its greatest impact after plant senescence in the fall and prior to major periods of early plant growth in spring. Annual species showed the greatest response, especially early in the growing season. Both spring and fall litter removal significantly increased species richness throughout the study. Litter additions in both spring and fall reduced both plant densities and species richness in June, but these differences disappeared near the end of the growing season in September. We concluded than in productive communities where litter accumulation may be substantial, litter may promote low species richness and plant density. This explanation does not invoke resource competition for the decline in species richness. Finally, we hypothesize that there may be broad thresholds of litter accumulation in different community types that may act to either increase or decrease plant yield and diversity.

Microsite variation and soil dynamics within newly created treefall pits and mounds.

We studied early soil dynamics, environmental conditions and plant colonization of microsites within 28 recently created treefall pits and mounds in a catastrophic windthrow. Pit and mound sizes were proportional to the size of the fallen trees, and deposition of eroded soil in the center of pits occurred at a decreasing rate over 2 yr. Instability of the substrate contributed to low plant abundance in the pits resulting in lower total plant cover than in the intact soil microsites adjacent to the pits. Larger pits revegetated more slowly than small ones. We recognized four microsites associated with the exhumed roots of each treefall: mound, pit, wall, and intact forest floor (no soil disturbed). Both growth forms and individual species differed in their colonization among microsites, resulting in lower species diversity and total cover on mounds relative to other microsites. Small-seeded, wind-dispersed species colonized the center of pits more readily than species that relied on vegetative spread. Species that are rare in intact forest were common on the disturbed soil of pits and mounds. During two successive years, we documented significant differences among microsites in light, soil moisture, and soil temperature. The species of fallen canopy trees had little influence on the plant community after disturbance, except in the intact soil microsite. We conclude that differential colonization of microsites within forest disturbances occurs at a finer scale than previously recognized and that this facilitates the maintenance of species diversity in the plant community.

Succession in Old-Field Plant Communities: Effects of Contrasting Types of Nutrient Enrichment

We investigated the effects of monthly nutrient applications on succession in two old-field plant communities. Succession was monitored for 3 yr in 1-yr (younger) and 4-yr (older) experimental plots. Three 0. 1-ha plots in each old field were treated with sludge, three with fertilizer, and two were left as untreated controls. In the younger community, herbaceous perennials and winter annuals replaced summer annuals by the 3rd yr of succession in control plots. Summer annuals, however, dominated enriched plots throughout the study. Species richness was significantly higher in enriched plots than in control plots during the 1st yr, but was significantly lower than control plots thereafter. Annual aboveground net primary productivity (ANPP) was significantly greater in enriched plots than in controls in the 1st yr, but the converse occurred in the 3rd yr. The type of nutrient enrichment affected ANPP; sludge plots had significantly lower ANPP than fertilizer plots in the 1st and 3rd yr. In the older community, two summer annuals and a biennial displaced dominant perennial grasses in enriched plots. In contrast to the younger community, ANPP was consistently greater in nutrient-enriched plots than in controls, and nutrient enrichment did not alter species richness. The type of nutrient enrichment affected the older community in an opposite manner from the younger community; sludge plots had significantly greater ANPP than fertilizer plots in the 3rd yr. We concluded that the age and physiognomy of the old-field community, the type of nutrients applied, and the duration of enrichment, each influenced the course of succession; responses observed in the 1st yr of enrichment were not indicative of later trends.

PLANT DENSITY DETERMINES SPECIES RICHNESS ALONG AN EXPERIMENTAL FERTILITY GRADIENT

A number of authors have suggested that, within areas a few square meters to many square kilometers in size, species diversity appears to peak at moderate levels of productivity, and this pattern is currently unexplained. Among the best examples of this pattern have been descriptions of vegetation in which species richness declines as soil fertility increases. We tested two hypotheses that have been proposed to explain this pattern. The interspecific competitive exclusion hypothesis proposes that dominant species suppress the growth of competitively subordinate species and exclude subordinate species as fertility rises. In contrast, the assemblage-level thinning hypothesis proposes that individuals of all species tend to become larger as fertility rises, and individuals of all species tend to exclude subordinate individuals of each species. Because total density declines, samples of finite numbers of individuals will result in fewer species by chance alone. To test these hypotheses, we established an experimental productivity gradient in a first- year old field using four levels of slow-release NPK fertilizer (0, 8, 16, and 32 g N/M2). At the end of the growing season, we sampled aboveground biomass and numbers of stems for each species in 72 20 X 20 cm subplots (18 reps X 4 levels), with an average sample size of 260 individual stems per plot. We observed an 80% decline in stem density with increasing fertility, and a 50% decline in species richness along this fertility gradient. A simulation of random thinning along a fertility gradient showed a nearly identical decline in species richness, supporting the assemblage-level thinning hypothesis. We also found that responses of individual species to the soil fertility gradient showed virtually no support for interspecific competitive exclusion. The overwhelming influence of density found in this study suggests that plant species richness along many productivity gradients may be strongly influenced by total stem density, and that differences in competitive ability among species, although generally important, are not necessary to create dramatic changes in species richness along fertility gradients.

Role of resources and disturbance in the organization of an old-field plant community

The roles of disturbance and resource availability in influencing species richness and plant abundance were examined by conducting a factorial experiment for 2 yr in an old field in New Jersey, USA, dominated by goldenrods (Solidago spp.). Replicate plots were treated by (1) adding macronutrients, (2) adding water, (3) tying back tall herbs to increase light to ground layer species, and (4) creating gaps in the vegetation by disturbing the soil with a hand trowel early in the growing season. Nutrient additions increased the cover of the herbaceous canopy and enhanced the dominance of Solidago spp. Water additions also increased canopy cover during the second growing season, a year with low seasonal rainfall. Light enrichment as a consequence of canopy manipulations resulted in the competitive release of subcanopy species, primarily Fragaria virginiana. Other subcanopy dominants were limited by different resources; Hier- acium pretense responded most strongly to water and Rumex acetosella to nutrients. These differences in limiting resources may be responsible for the continued coexistence of these three subcanopy species. Additionally, we observed marked seasonal and yearly fluctuations in the severity of resource limitation which might serve to favor different species in this community at different times. Species richness was decreased by light enrichment alone, whereas light with irrigation interacted to increase species richness. Nutrient additions had little direct effect on species richness. A single small disturbance at the beginning of the growing season had little impact on species richness or abundance. Relative to the influence of resources, small-scale dis- turbance plays only a minor role in this community. Our results suggest that nonequilibrium organization of old-field communities can occur via a shifting resource base in the absence of natural disturbances.

Top-down effects of insect herbivores during early succession: influence on biomass and plant dominance

Abstract We tested the hypothesis that phytophagous insects would have a strong top-down effect on early successional plant communities and would thus alter the course of succession. To test this hypothesis, we suppressed above-ground insects at regular intervals with a broad-spectrum insecticide through the first 3 years of old-field succession at three widely scattered locations in central New York State. Insect herbivory substantially reduced total plant biomass to a similar degree at all three sites by reducing the abundance of meadow goldenrod, Solidago altissima. As a result, Euthamia graminifolia dominated control plots whereas S. altissima dominated insecticide-treated plots by the third year of succession. S. altissima is the dominant old-field herbaceous species in this region but typically requires at least 5 years to become dominant. Past explanations for this delay have implicated colonization limitation whereas our data demonstrate that insect herbivory is a likely alternative explanation. A widespread, highly polyphagous insect, the xylem-tapping spittlebug, Philaenus spumarius, appeared to be the herbivore responsible for the reduction in standing crop biomass at all three sites. Insect herbivory typically caused little direct leaf tissue loss for the ten plant species we examined, including S. altissima. Consequently, the amount of leaf area removed was not a reliable indicator of the influence of insect herbivory on standing crop biomass or on early succession. Overall, we found a strong top-down effect of insect herbivores on biomass at several sites, so our results may be broadly applicable. These findings run counter to generalizations that top-down effects of herbivores, particularly insects, are weak in terrestrial systems. These generalizations may not apply to insects, such as spittlebugs, that can potentially mount an effective defense (i.e., spittle) against predators and subsequently reach relatively high abundance on common plant species. Our results suggest that insect herbivory may play an important but often overlooked role during early old-field succession.