Scott N. Martens

The ecological significance of nickel hyperaccumulation: a plant chemical defense

Nickel hyperaccumulating plants have more than 1000 mg Ni kg−1 dry weight when grown on nickel-bearing soils. We hypothesized that Ni hyperaccumulation could serve as a chemical defense against herbivores In feeding experiments with potential insect herbivores and Ni hyperaccumulating plants, only those inseets fed leaves from plants grown on non-nickel-bearing soil survived or showed a weight gain. Among chemical parameters measured, only Ni content of plants was sufficient to explain this result. When subjected to herbivory by lepidopteran larvae, plants grown on Ni-amended soil showed greater survival and yield than plants on unamended soil. Ni hyperaccumulation may be an effective plant chemical defense against herbivores because of its high lethality, apparent low cost, and broad spectrum of toxicity.

Spatial distributions of understory light along the grassland/forest continuum: effects of cover, height, and spatial pattern of tree canopies

Abstract The understory light environment is a key determinant of vegetation pattern and ecosystem processes, and varies spatially perhaps more than any resource used by plants. Understory light varies along gradients of vegetation structure that range from grassland with no woody canopy cover to forest with nearly complete woody canopy cover. Spatial variability in understory light is largely determined by several characteristics of overstory plants — spatial pattern, height, and cover — which vary concurrently along the grassland/forest continuum. Using a spatially-explicit ray-tracing model, we quantified trends in mean and variance of understory light along the continuum. We modeled understory light over a growing season for two types of plots: (1) generated plots in which cover, spatial pattern, and height of trees were varied systematically, and (2) three actual plots using stand data from pinon-juniper woodland sites for which cover, spatial pattern and height varied concurrently. Mean understory light decreased with increasing canopy cover and was sensitive to changes in height, as expected, but was not sensitive to spatial pattern. Variance in understory light was maximum at an intermediate value of cover that was dependent on both spatial pattern and cover — maximum variance occurred at lower values of cover as height increased and as spatial pattern progressed from regular to random to aggregated. These trends in the overall patterns of understory light were also examined with respect to changes in understory light in canopy and intercanopy locations. Variance in understory light for intercanopy locations was less than that for canopy locations at low canopy cover, but exceeded that for canopy locations as canopy cover increased. The value of canopy cover at which variance in intercanopy locations exceeded that in canopy locations was sensitive to variation in height but not in spatial pattern. The distributions of understory light for the actual plots were generally similar to those for corresponding generated plots, with dissimilarities attributable to differences in cover and height. The general trends highlighted by our simulations are broadly applicable to sites along the grassland/forest continuum.

Nickel hyperaccumulated by Thlaspi montanum var. montanum is acutely toxic to an insect herbivore

Some plants growing on serpentine soils sequester (hyperaccumulate) nickel from those soils in their tissues. Several ecological functions for metal hyperaccumulation have been suggested, including defense against herbivores. This study tests the herbivore defense hypothesis using the Ni hyperaccumulator Thlaspi montanum var. montanum. Leaves differing 167-fold in Ni content (3,000 vs 18 ppm) were obtained by growing plants on high- and low-Ni soils. Leaves were fed to larvae of Pieris rapae, a generalist folivore. Larvae fed high-Ni leaves did not grow and suffered 100 % mortality after 12 d, whereas those fed low-Ni leaves quadrupled in weight with a corresponding mortality of only 21 % (...)

The significance of metal hyperaccumulation for biotic interactions

Abstract. Metal hyperaccumulating plants contain very high metal contents. Because of the general toxicity of metals, chemically-mediated biotic interactions involving hyperaccumulating plants may differ greatly from those of non-hyperaccumulators. Recent research has demonstrated a defensive function for hyperaccumulated metals against herbivores and pathogens. We predict that some herbivore/pathogen species have evolved metal tolerance, and suggest that resulting high metal levels in herbivores/pathogens may defend them against their own predators. Little is known regarding interference and commensal interactions involving hyperaccumulating plants. Decreased competition may occur through an interference interaction similar to allelopathy, in which enrichment of metal in the soil under a hyperaccumulator plants canopy may inhibit another plant species, thus resulting in “elemental allelopathy”. Metal enrichment of soil under hyperaccumulators also may result in commensalism if another plant species (possibly another hyperaccumulator) derives a benefit from growing in the metal-enriched soil under the canopy of a hyperaccumulating overstory plant. It seems likely that high-metal plant litter will host a specialized microflora of decomposers and may affect nutrient cycling rates. Mutualist biotic interactions also may be affected by the elevated metal contents of hyperaccumulating species. Mycorrhizal fungi may form mutualisms with hyperaccumulators, but the phenomenon is poorly-explored. The few cases investigated to date have not detected mycorrhizae. Pollination and seed dispersal mechanisms may require biotic vectors that might be affected by plant metal content. Hyperaccumulating plants may have solved this dilemma in three ways. First, some may rely on abiotic vectors for pollen or seed dispersal. Second, biotic vectors used by these species may have varied diets and thus dilute metal intake to non-toxic levels. Finally, biotic vectors may have evolved tolerance of elevated dietary levels of metals, and perhaps have become specialists on hyperaccumulator species.

foliar absorption of intercepted rainfall improves woody plant water status most during drought

A large proportion of rainfall in dryland ecosystems is intercepted by plant foliage and is generally assumed to evaporate to the atmosphere or drip onto the soil surface without being absorbed. We demonstrate foliar absorption of intercepted rainfall in a widely distributed, continental dryland, woody-plant genus: Juniperus. We observed substantial improvement in plant water status, exceeding 1.0 MPa water potential for drought-stressed plants, following precipitation on an experimental plot that excluded soil water infiltration. Experiments that wetted shoots with unlabeled and with isotopically labeled water confirmed that water potential responded substantially to foliar wetting, that these responses were not attributable to re-equilibration with other portions of the xylem, and that magnitude of response increased with water stress. Foliar absorption is not included in most ecological, hydrological, and atmospheric models; has implications for interpreting plant isotopic signatures; and not only supplements water acquisition associated with increases in soil moisture that follow large or repeated precipitation events, but also enables plants to bypass soil water uptake and benefit from the majority of precipitation events, which wet foliage but do not increase soil moisture substantially. Foliar absorption of intercepted water could be more important than previously appreciated, especially during drought when water stress is greatest.

Differential use of spatially heterogeneous soil moisture by two semiarid woody species: Pinus edulis and Juniperus monosperma

1 Soil moisture in semiarid woodlands varies both vertically with depth and horizontally between canopy patches beneath woody plants and the intercanopy patches that separate them, such that shallow soil layers in intercanopy locations are wettest, yet few studies have considered both dimensions of spatial variability in testing for acquisition of resources by plants. 2 Three hypotheses were tested relative to the use of shallow water in intercanopy locations by two coexisting semiarid-woodland tree species, Pinus edulis (a pinion) and Juniperus monosperma (a juniper): (i) both P. edulis and J. monosperma can use shallow water from intercanopy locations;. (ii) J. monosperma is able to obtain more shallow water from intercanopy locations than P. edulis, and (iii) the spatial arrangement of the trees influences the amount of water they obtain. Soil moisture and plant water potential (i.e. plant water stress) were measured before and after the addition of water to shallow depths (0-30 cm) of intercanopy locations for trees of both species in two spatial arrangements: isolated and paired with a contiguous tree of the other species. 3 Both species responded to the addition of shallow water in intercanopy locations, as measured by plant water potential. The response of J. monosperma was significantly greater than that of P. edulis, as measured by depletion of shallow soil moisture in intercanopy locations and by change in plant water potential per unit change in soil water potential (the difference was not detectable on the basis of plant water potential alone); in addition, the amount of depletion was correlated with basal area of J. monosperma but not of P. edulis. The responses were not influenced by spatial arrangement (isolated vs. paired with a contiguous tree of the other species). 4 The results of this study are consistent with differences in the relative abundances of the two species across locations, suggesting that species differences in ability to use shallow water in intercanopy locations is important in structuring semiarid woodlands. Further, the results suggest that current theoretical concepts for semiarid ecosystems, which ignore either vertical or horizontal variability in soil moisture, may be inadequate for predicting changes in the ratio of woody to herbaceous plant biomass, particularly for plant communities with co-dominant woody species that differ in ability to acquire spatially heterogeneous resources.

Estimation of tree canopy leaf area index by gap fraction analysis

Abstract We estimated leaf area index (LAI) in a needle-leaved forest and a broad-leaved orchard using four instruments which measure fractional light penetration through the canopy. Gap fraction data were analyzed by a one-dimensional inversion model or by using the Beer-Lambert Law. Instrument and analytical technique both had a strong influence on calculated LAI. There was no consistent pattern of LAI results among instruments so no simple cross-calibration can be offered. Three of the four instruments accurately estimated orchard LAI when used with one or the other analytical technique. In addition to performance, practical considerations including cost, sampling, and data analysis were also compared among the instruments. Because the instruments do not provide consistently accurate LAI estimates, LAI should be independently corroborated before use in any particular situation. These instruments may be most useful for relative LAI comparisons in a specific canopy type when a single combination of instrument and analytical technique is employed.

Scales of above-ground and below-ground competition in a semi-arid woodland detected from spatial pattern

Abstract. Semi-arid woodlands are two-phase mosaics of canopy and inter-canopy patches. We hypothesized that both aboveground competition (within canopy patches), and below-ground competition (between canopy patches), would be important structuring processes in these communities. We investigated the spatial pattern of trees in a Pinus edulis-Juniperus monosperma woodland in New Mexico using Ripleys K-function. We found strong aggregation of trees at scales of 2 to 4 m, which indicates the scale of canopy patches. Canopy patches were composed of individuals of both species. Crown centers of both species were always less aggregated than stem centers at scales less than canopy patch size, indicating morphological plasticity of competing crowns. In the smallest size classes of both species, aggregation was most intense, and occurred over a larger range of scales; aggregation decreased with increasing size as is consistent with density-dependent mortality from intraspecific competition. Within canopy patches, younger trees were associated with older trees of the other species. At scales larger than canopy patches, younger trees showed repulsion from older conspecifics, indicating below-ground competition. Hence, intraspecific competition was stronger than interspecific competition, probably because the species differ in rooting depth. Woodland dynamics depend on the scale and composition of canopy patches, aggregated seed deposition and facilitation, above- and below-ground competition, and temporal changes in the spatial scale of interactions. This woodland is intermediate in a grassland-forest continuum (a gradient of increasing woody canopy cover) and hence we expected, and were able to detect, the effects of both above- and below-ground competition.

Nickel hyperaccumulation by Thlaspi montanum var. montanum (Brassicaceae): a constitutive trait.

Adaptations to particular stresses may occur only in populations experiencing those stresses or may be widespread within a species. Nickel hyperaccumulation is viewed as an adaptation to high-Ni (serpentine) soils, but few studies have determined if hyperaccumulation ability is restricted to populations from high-Ni soils or if it is a constitutive trait found in populations on both high- and low-Ni soils. We compared mineral element concentrations of Thlaspi montanum var. montanum plants grown on normal and high-Ni greenhouse soils to address this question. Seed sources were from four populations (two serpentine, two non-serpentine) in Oregon and northern California, USA. Plants from all populations were able to hyperaccumulate Ni, showing Ni hyperaccumulation to be a constitutive trait in this species. Populations differed in their ability to extract some elements (e.g., Ca, Mg, P) from greenhouse soils. We noted a negative correlation between tissue concentrations of Ni and Zn. We suggest that the ability to hyperaccumulate Ni has adaptive value to populations growing on non- serpentine soil. This adaptive value may be a consequence of metal-based plant defense against herbivores/pathogens, metal- based interference against neighboring plant species, or an efficient nutrient scavenging system. We suggest that the Ni hyperaccumulation ability of T. montanum var. montanum may be an inadvertent consequence of an efficient nutrient (possibly Zn or Ca) uptake system.

The defensive role of Ni hyperaccumulation by plants: a field experiment

Hyperaccumulation of Ni by plants is hypothesized to function as an elemental defense against herbivores and pathogens. Laboratory experiments have documented toxic effects to herbivores consuming high-Ni plant tissues, but this paper reports the first experiment to examine the defensive effectiveness of Ni hyperaccumulation under field conditions. The experiment was conducted at an ultramafic soil site naturally inhabited by the Ni hyperaccumulator Streptanthus polygaloides (Brassicaceae). Experimental treatments examined the response of herbivores to hyperaccumulated Ni, using exclosure and insecticide treatments to divide herbivores into groups based primarily upon herbivore size. Three soils (Ni-amended greenhouse soil, unamended greenhouse soil, ultramafic soil), three exclosure treatments (exclosure, control exclosure, no exclosure), and a systemic insecticide treatment were combined in a fractional factorial experimental design. Streptanthus polygaloides plants were grown in a greenhouse for 2 mo, transplanted into the field by inserting potted plants into holes dug on the experimental site, and periodically examined for herbivore damage during a 41-d period. Initial surveys showed greater amounts of insect damage to plants with low tissue Ni levels, confirming the defensive effect of Ni against some insect herbivores, but large herbivores (probably vertebrates) later consumed entire plants regardless of plant Ni status. We concluded that Ni was not an effective defense against these large herbivores, probably because their diets mix high-Ni S. polygaloides foliage with that of associated non-hyperaccumulating species. We suggest that such dietary dilution is one mechanism whereby some herbivores can circumvent elemental plant defenses.