The roots of defense: plant resistance and tolerance to belowground herbivory.

BACKGROUND: There is conclusive evidence that there are fitness costs of plant defense and that herbivores can drive selection for defense. However, most work has focused on above-ground interactions, even though belowground herbivory may have greater impacts on individual plants than above-ground herbivory. Given the role of belowground plant structures in resource acquisition and storage, research on belowground herbivores has much to contribute to theories on the evolution of plant defense. Pocket gophers (Geomyidae) provide an excellent opportunity to study root herbivory. These subterranean rodents spend their entire lives belowground and specialize on consuming belowground plant parts. METHODOLOGY AND PRINCIPAL FINDINGS: We compared the root defenses of native forbs from mainland populations (with a history of gopher herbivory) to island populations (free from gophers for up to 500,000 years). Defense includes both resistance against herbivores and tolerance of herbivore damage. We used three approaches to compare these traits in island and mainland populations of two native California forbs: 1) Eschscholzia californica populations were assayed to compare alkaloid deterrents, 2) captive gophers were used to test the palatability of E. californica roots and 3) simulated root herbivory assessed tolerance to root damage in Deinandra fasciculata and E. californica. Mainland forms of E. californica contained 2.5 times greater concentration of alkaloids and were less palatable to gophers than island forms. Mainland forms of D. fasciculata and, to a lesser extent, E. californica were also more tolerant of root damage than island conspecifics. Interestingly, undamaged island individuals of D. fasciculata produced significantly more fruit than either damaged or undamaged mainland individuals. CONCLUSIONS AND SIGNIFICANCE: These results suggest that mainland plants are effective at deterring and tolerating pocket gopher herbivory. Results also suggest that both forms of defense are costly to fitness and thus reduced in the absence of the putative target herbivore.

Challenges and opportunities of open data in ecology.

Ecology is a synthetic discipline benefiting from open access to data from the earth, life, and social sciences. Technological challenges exist, however, due to the dispersed and heterogeneous nature of these data. Standardization of methods and development of robust metadata can increase data access but are not sufficient. Reproducibility of analyses is also important, and executable workflows are addressing this issue by capturing data provenance. Sociological challenges, including inadequate rewards for sharing data, must also be resolved. The establishment of well-curated, federated data repositories will provide a means to preserve data while promoting attribution and acknowledgement of its use.

Apparent competition with an exotic plant reduces native plant establishment.

Biological invasions can change ecosystem function, have tremendous economic costs, and impact human health; understanding the forces that cause and maintain biological invasions is thus of immediate importance. A mechanism by which exotic plants might displace native plants is by increasing the pressure of native consumers on native plants, a form of indirect interaction termed "apparent competition." Using experimental exclosures, seed addition, and monitoring of small mammals in a California grassland, we examined whether exotic Brassica nigra increases the pressure of native consumers on a native bunchgrass, Nassella pulchra. Experimental plots were weeded to focus entirely on indirect effects via consumers. We demonstrate that B. nigra alters the activity of native small-mammal consumers, creating a gradient of consumption that dramatically reduces N. pulchra establishment. Previous work has shown that N. pulchra is a strong competitor, but that it is heavily seed limited. By demonstrating that consumer pressure is sufficient to curtail establishment, our work provides a mechanism for this seed limitation and suggests that, despite being a good competitor, N. pulchra cannot reestablish close to B. nigra within its old habitats because exotic-mediated consumption preempts direct competitive exclusion. Moreover, we find that apparent competition has a spatial extent, suggesting that consumers may dictate the rate of invasion and the area available for restoration, and that nonspatial studies of apparent competition may miss important dynamics.

Costs and benefits of pocket gopher foraging: linking behavior and physiology.

Animals can attain fitness benefits by maintaining a positive net energy balance, including costs of movement during resource acquisition and the profits from foraging. Subterranean rodent burrowing provides an excellent system in which to examine the effects of movement costs on foraging behavior because it is energetically expensive to excavate burrows. We used an individual-based modeling approach to study pocket gopher foraging and its relationship to digging cost, food abundance, and food distribution. We used a unique combination of an individual-based foraging-behavior model and an energetic model to assess survival, body mass dynamics, and burrow configurations. Our model revealed that even the extreme cost of digging is not as costly as it appears when compared to metabolic costs. Concentrating digging in the area where food was found, or area-restricted search (ARS), was the most energetically efficient digging strategy compared to a random strategy. Field data show that natural burrow configurations were more closely approximated by the animals we modeled using ARS compared to random diggers. By using behavior and simple physiological principles in our model, we were able to observe realistic body mass dynamics and recreate natural movement patterns.

Invasion, competitive dominance, and resource use by exotic and native California grassland species.

The dynamics of invasive species may depend on their abilities to compete for resources and exploit disturbances relative to the abilities of native species. We test this hypothesis and explore its implications for the restoration of native ecosystems in one of the most dramatic ecological invasions worldwide, the replacement of native perennial grasses by exotic annual grasses and forbs in 9.2 million hectares of California grasslands. The long-term persistence of these exotic annuals has been thought to imply that the exotics are superior competitors. However, seed-addition experiments in a southern California grassland revealed that native perennial species, which had lower requirements for deep soil water, soil nitrate, and light, were strong competitors, and they markedly depressed the abundance and fecundity of exotic annuals after overcoming recruitment limitations. Native species reinvaded exotic grasslands across experimentally imposed nitrogen, water, and disturbance gradients. Thus, exotic annuals are not superior competitors but rather may dominate because of prior disturbance and the low dispersal abilities and extreme current rarity of native perennials. If our results prove to be general, it may be feasible to restore native California grassland flora to at least parts of its former range.

Physiology on a landscape scale: plant-animal interactions.

We explore in this paper how animals can be affected by variation in climate, topography, vegetation characteristics, and body size. We utilize new spatially explicit state-of-the-art models that incorporate principles from heat and mass transfer engineering, physiology, morphology, and behavior that have been modified to provide spatially explicit hypotheses using GIS. We demonstrate how temporal and spatial changes in microclimate resulting from differences in topography and vegetation cover alter animal energetics, and behavior. We explore the impacts of these energetic predictions on elk energetics in burned and unburned stands of conifer in winter in Yellowstone National Park, chuckwalla lizard distribution limits in North America, California Beechey Ground squirrel and Dusky Footed woodrat mass and energy requirements and activity patterns on the landscape, their predator prey interactions with a rattlesnake, Crotalus viridis, and shifts in that food web structure due to topographic and vegetative variation. We illustrate how different scales of data/observation provide different pieces of information that may collectively define the real distributions of a species. We then use sensitivity analyses of energetic models to evaluate hypotheses about the effects of changes in core temperature (fever) global climate (increased air temperature under a global warming scenario) and vegetation cover (deforestation) on winter survival of elk, the geographic distribution of chuckwallas and the activity overlap of predator and prey species within a subset of commonly observed species in a terrestrial food web. Variation in slope and aspect affect the spatial variance in solar radiation incident on the ground, hence ground surface temperature, at the same elevation, same hourly 2 m air temperatures, and wind speeds. We illustrate visually how spatial effects and landscape heterogeneity make statistical descriptions of animal responses problematic, since multiple distributions of their responses to climate, topography, and vegetation on the landscape can yield the same descriptive statistics, especially at high (30 m) resolution. This preliminary analysis suggests that the model has far-reaching implications for hypothesis testing in ecology at a variety of spatial and temporal scales.

Simulation models of the interactions between herbivore foraging strategies, social behavior, and plant community dynamics.

Herbivory often operates through a feedback in which herbivores affect the success and location of plants, which in turn affects the foraging behavior of animals. Factors other than food, such as social behavior, may influence the interactions between herbivores and the plants they consume. We used a simulation model to compare the effects of foraging and social behavior on plant distribution and foraging efficiency by gophers (Thomomys bottae) in a system characteristic of California grasslands. In this system, annual forbs are the preferred food items, and their abundance increases in areas disturbed by gopher burrowing. In addition, gopher social interactions generate buffer zones between adjacent burrows. During the first year of the simulations, before gophers affected the plant community, feeding efficiency declined with increased gopher density. However, after 40 yr, annual plant abundance increased with increasing gopher density, yielding higher maximum gopher density and per capita foraging efficiency. Conversely, increased width of the buffer zones lowered maximum gopher density and annual plant abundance resulting in lower feeding efficiency. In addition, the compact burrow structure of gophers employing an area-restricted search strategy allowed a higher density of gophers to coexist, resulting in higher annual plant abundance and higher per capita food-capture rates.

The effect of hillslope angle on pocket gopher (Thomomys bottae) burrow geometry.

One way for animals to decrease energy expenditures is to minimize the cost of movement. For animals dwelling on slopes, gravity can impart a large energetic cost to movement. For this reason, animals traveling aboveground alter their movement patterns in response to the steepness of terrain (specifically hillslope angle) so as to minimize their energetic costs. Subterranean animals should also benefit from choosing optimum movement paths in relation to hillslopes but concurrently must factor the cost of excavation into their movement decisions. In cases where the excavation costs are much higher than the costs of working against gravity, excavation costs may override the consideration of gravitational costs and movement of subterranean animals may be independent of hillslope angle. To determine the response of a subterranean animal to hillslope angle, we excavated tunnels in the burrow systems of 19 pocket gophers in southern California that occupied hillslopes ranging from 2 to 30°. At each excavation we measured several characteristics of burrow geometry and used these data in a model of pocket gopher energetics to calculate the cost of tunnel construction at the various hillslope angles. We found that the cost of tunnel construction was independent of hillslope angle, and that the costs of shearing soil and pushing soil horizontally through the tunnels were 3 orders of magnitude greater than the costs of lifting the soil against the force of gravity. Accordingly, pocket gopher foraging tunnels were oriented independently of the hillslope. The decoupling of the movement patterns of subterranean animals from the effects of gravity is a distinctive feature of the subterranean habit compared to the movement of aboveground animals. Because of the important effects of tunnel construction on soil processes, this unique biological feature of subterranean animals has implications for basic physical processes, such as soil erosion. We found that the rate of soil flux generated by pocket gopher activity was invariant to hillslope. This relationship is in contrast to the most common model of soil movement generated by purely physical processes.

Kangaroo rat bone compared to white rat bone after short-term disuse and exercise.

Kangaroo rats (Dipodomys ordii) were used to study the effects of confinement on mechanical properties of bone with a long range objective of proposing an alternative to the white rat model for the study of disuse osteoporosis. Kangaroo rats exhibit bipedal locomotion, which subjects their limbs to substantial accelerative forces in addition to the normal stress of weight bearing. We subjected groups of kangaroo rats and white rats (Rattus norvegicus) to one of two confinement treatments or to an exercise regime; animals were exercised at a rate calculated to replicate their (respective) daily exercise patterns. White laboratory rats were used as the comparison because they are currently the accepted model used in the study of disuse osteoporosis. After 6 weeks of treatment, rats were killed and the long bones of their hind limbs were tested mechanically and examined for histomorphometric changes. We found that kangaroo rats held in confinement had less ash content in their hind limbs than exercised kangaroo rats. In general, treated kangaroo rats showed morphometric and mechanical bone deterioration compared to controls and exercised kangaroo rats appeared to have slightly "stronger" bones than confined animals. White rats exhibited no significant differences between treatments. These preliminary results suggest that kangaroo rats may be an effective model in the study of disuse osteoporosis.

Seismic signal transmission between burrows of the Cape mole-rat, Georychus capensis.

Both seismic and auditory signals were tested for their propagation characteristics in a field study of the Cape mole-rat (Georychus capensis), a subterranean rodent in the family Bathyergidae. This solitary animal is entirely fossorial and apparently communicates with its conspecifics by alternately drumming its hind legs on the burrow floor. Signal production in this species is sexually dimorphic, and mate attraction is likely mediated primarily by seismic signalling between individuals in neighboring burrows. Measurements within, and at various distances away from, natural burrows suggest that seismic signals propagate at least an order of magnitude better than auditory signals. Moreover, using a mechanical thumper which could be triggered from a tape recording of the mole-rat's seismic signals, we established that the vertically-polarized surface wave (Rayleigh wave) propagates with less attenuation than either of the two horizontally-polarized waves. Thus, we tentatively hypothesize that Rayleigh waves subserve intraspecific communication in this species.

Distribution of Seeds in Sonoran Desert Soils: Implications for Heteromyid Rodent Foraging.

We used a hierarchical sampling design to investigate temporal and spatial patterns of variation in the topsoil seedbank at a site on the Santa Rita Experimental Range, 50 km south of Tucson, Arizona. Replicate sets of contiguous 4 ° 4 cm samples to 2 cm depth ("transects") were collected three times per year, from 1980 to 1983, from four microhabitats that are differentiated by desert heteromyid rodents: large and small open spaces, under canopies of large shrubs, and under canopies of small trees. We also analyzed texture and organic content of soils from the four microhabitats. Seeds from 54 plant taxa were encountered, most of them rare. Average seed mass across species was 1.28 mg/seed, but because tiny seeds were most numerous, the abundance-weighted average was 0.16 mg/seed. Total seed abundance was highly variable, ranging from 0 to 256 seeds and from 0 to 146 mg per sample. The fourfold temporal variation in mean mass or number of seeds per sample was largely due to between-year rather than between-season effects. Seed standing crops were positively correlated with rainfall during the previous 6-mo rainy period, and were lowest in fall and winter of 1982 after 2 yr of poor winter rains. Mean seed number per sample, which reflects primarily abundance of tiny seeds, did not vary among microhabitats. Mean per-sample seed mass, which reflects abundance of the large seeds eaten by rodents, did vary among microhabitats, however, with values being higher under shrubs and trees than in open spaces. The low mean abundance in open spaces was due more to a high frequency of seedless samples than to low maximum per-sample abundance. Hence, profitable seed patches do occur in open spaces, but are rarer than under shrubs or trees. Within microhabitats there was significant variation among replicate transects and among samples within transects. On a local scale, seeds occurred in patches 12 cm in diameter in all microhabitats and sampling periods. Seed species composition varied seasonally and among microhabitats, and there was an overall correlation between seed and adult microhabitat distribution for spring ephemerals. Soil from open spaces was finer and had lower organic content than that under shrub or tree canopies. Our results suggest that the resource upon which desert granivores depend is highly variable in time and space. Microhabitat is one of the most conspicuous sources of variation, and heteromyid rodent species differ in use of those microhabitats (open spaces vs. areas under canopies of perennial plants) that differ most noticeably in seed abundances, species composition, and soil characteristics.