Steven C. Pennings

Salt Marsh Plant Zonation: The Relative Importance of Competition and Physical Factors

In Carpinteria Salt Marsh, Salicornia virginica (pickleweed) grows at lower marsh elevations than does Arthrocnemum subterminalis (Parishs glasswort). Standing biomass of both species was greatest immediately adjacent to their abrupt border, suggesting that conditions for plant growth were best here. We utilized field experiments, in which growth rates of naturally occurring and transplanted individuals of both species were measured in four marsh zones, to investigate the role of edaphic factors and competition in maintaining this zonation pattern. The frequency of flooding, and hence soil waterlogging, was greatest at lower marsh elevations, whereas salinity was highest at higher marsh elevations. Consequently, it was not clear, a priori, which part of the marsh had the most severe physical conditions. In our field experiments, both Salicornia and Arthrocnemum grew better in the two middle marsh zones (high Salicornia zone and Arthrocnemum zone) than in either the low marsh (low Salicornia zone), where flooding was frequent and soils were waterlogged, or the high marsh (transition zone), where soil salinity was extremely high during much of the year and plant water potentials very low. However, Salicornia appeared better able to tolerate flooding, and so persisted in the low Salicornia zone, whereas Arthrocnemum appeared better able to tolerate high salinities, and so persisted in the transition zone. Interspecific competition was most important in the relatively benign middle marsh zones, where each species excluded the other from a portion of this prime habitat. In this marsh, flooding, soil salinity, and competition all interacted to determine plant zonation patterns, but the relative importance of these factors varied at different elevations.

PHENOTYPIC PLASTICITY AND INTERACTIONS AMONG PLANTS

We know a great deal about the plastic responses of plant phenotypes to the abiotic and biotic environment, but very little about the consequences of phenotypic plas- ticity for plant communities. In other words, we know that plant traits can vary widely for a given genotype, but we know little about the importance of trait-mediated interactions (TMI) among plants. Here, we discuss three major factors that affect the expression of phenotypic plasticity: variation in the abiotic environment, variation in the presence or identity of neighbors, and variation in herbivory. We consider how plastic responses to these factors might affect interactions among plants. Plastic responses to the abiotic en- vironment have important consequences for conditionality in competitive effects, to the point of causing shifts from competitive to facilitative interactions. Because plants show a high degree of plasticity in response to neighbors, and even to the specific identify of neighbors, phenotypic plasticity may allow species to adjust to the composition of their communities, promoting coexistence and community diversity. Likewise, plastic responses to consumers may have various and counterintuitive consequences: induction of plant re- sistance, compensatory growth, and increased resource uptake may affect interactions among plants in ways that cannot be predicted simply by considering biomass lost to consumers. What little we know about TMI among plants suggests that they should not be ignored in plant community theory. Although work to date on the community consequences of phenotypic plasticity has been hampered by experimental constraints, new approaches such as manipulating phenotypes by using signals instead of actual environmental conditions and the use of transgenic plants should allow us to rapidly expand our understanding of the community consequences of plant plasticity.

LINKING BIOGEOGRAPHY AND COMMUNITY ECOLOGY: LATITUDINAL VARIATION IN PLANT–HERBIVORE INTERACTION STRENGTH

Ecological interactions may vary geographically as a function of diversity, density, or per capita interaction strengths, but we know little about the relative importance of these three mechanisms. We examined variation in species richness, abundance, and interactions among leaf-chewing herbivores and the dominant salt-marsh plant Spartina alterniflora along the Atlantic Coast of the United States. High-latitude S. alterniflora plants are more palatable to herbivores than are low-latitude plants. Within this range of latitude, diversity and density of the dominant leaf-chewing consumers, snails and grasshoppers, in Spartina-dominated portions of the marsh varied little. Low-latitude plants, however, experienced much greater levels of leaf damage from consumers than did high-latitude plants. Per capita feeding rates of low-latitude snails (Littoraria irrorata) and grasshoppers (Orchelimum fidicinum) in the laboratory were greater than feeding rates of high-latitude snails (Melampus bidentatus) and grasshoppers (Conocephalus spartinae). In field experiments, low-latitude snails strongly suppressed S. alterniflora growth, but high-latitude snails had no effect on primary production. Thus, latitudinal differences in the effect of herbivores on plants (i.e., interaction strength), driven by differences in per capita effects among species, rather than differences in diversity or density, may contribute to selection for latitudinal differences in plant palatability. Because geographical differences in interaction strength can occur in the absence of differences in diversity or density, linking biogeography with community ecology will require experimental studies that explicitly measure interaction strength at multiple geographic locations.

Selectivity and Growth of the Generalist Herbivore Dolabella Auricularia Feeding Upon Complementary Resources

An assumption of most optimal diet theory is that different resources are substitutable, that is, that they are identical in all relevant aspects and so can be ranked in value using a single currency, such as energy. However, this assumption is probably not valid in many cases. The sea hare Dolabella auricularia (Gastropoda: Opisthobranchia: Anaspidea) grew far better upon an ad libitum mixture of four species of algae than upon any of the algal species alone, suggesting that algae were complementary resources. When offered three pairs of algae in 4:1 and 1:9 ratios, Dolabella changed its foraging behavior so that the rarer alga was preferred. Consequently, the mixtures of algae consumed were more similar between treatments (ratios) than the mixtures of algae offered. Replicate Dolabella were maintained on six single algal diets for 6-7 d and then offered the main- tenance alga and another alga at equal abundances. Preference for a species of algae was always higher when it was not the maintenance diet compared to when it was. These results suggest that Dolabella actively maintains a mixed diet because it is nutritionally superior to any single diet. An alternative hypothesis (the nonadditive toxin hypothesis) suggests that herbivores might consume a mixed diet because a mixture of plant secondary metab- olites is less toxic than any one metabolite alone; consequently, herbivores can consume more total biomass of a mixed than of a single diet. However, sea hares fed single- and mixed-species diets did not consume more of mixed diets than of single-species diets, and animals fed a mixed diet grew better than those fed single diets even when the biomass of algae offered was held constant. If resources are complementary, as suggested here, several important implications follow: (1) consumers will not rank resources in any absolute way because the value of each will depend upon what else is consumed, (2) consumer special- ization will be opposed by the benefits of a mixed diet, and (3) consumer foraging will tend to destabilize the resource community, because rarer resources will be disproportionately consumed.

Impact of a parasitic plant on the structure and dynamics of salt marsh vegetation

We investigated the effect of a native parasitic plant, Cuscuta salina, on the structure and dynamics of the plant community in a California salt marsh. Cuscuta was common in the middle marsh zones. The abundance of Cuscuta was positively correlated with the abundance of Limonium californicum at two sampling scales (0.25- and -40-m2 quadrats). Sampling at the scale of individual plants indicated that the dominant plant in the marsh, Salicornia virginica, was preferred by Cuscuta as a host over Arthrocnemum subterminale, Limonium californicum, and Frankenia salina. This result was confirmed with host-choice experiments in the field. Based on spatial correlations and host-choice experiments, we hypothesized that Cuscuta indirectly facilitated Limonium and Frankenia, increasing plant diversity and initiating vegetation cycles. This hypothesis was supported by sampling patches with different his- tories of Cuscuta infection. Patches with recent heavy Cuscuta infection had reduced Sal- icornia biomass and increased Limonium and Frankenia biomass relative to controls. This effect was most pronounced at higher elevations and in larger, older patches. The hypothesis was also supported by sampling permanent quadrats repeatedly over time. The probability that Cuscuta would invade a quadrat increased with increasing cover of Salicornia. Quadrats containing Cuscuta increased in Limonium and Frankenia cover between censuses relative to quadrats lacking Cuscuta. Our results indicate that parasitic plants can have strong effects on the structure and dynamics of natural vegetation assemblages. However, these effects are mediated by phys- ical and biological gradients across the landscape.

GEOGRAPHIC VARIATION IN POSITIVE AND NEGATIVE INTERACTIONS AMONG SALT MARSH PLANTS

A pressing problem for ecologists is determining whether our understanding of communities, often developed from work at fine scales, can explain processes across broader scales. Here, we explore whether models of positive interactions developed in southern New England can be applied to geographic scales. Salt marsh plants may interact positively by ameliorating harsh physical conditions such as salinity stress. Because marsh porewater salinities are higher in low- vs. high-latitude marshes, we tested the hypothesis that positive interactions are increasingly important at low latitudes. Previous work sup- ported this hypothesis at the regional scale: within New England, positive interactions were rare in Maine but common in Rhode Island. We conducted parallel experiments in Georgia and Alabama to determine whether similar results would be obtained in a geographic comparison. Nine species of salt marsh plants were transplanted into control plots or plots with neighboring vegetation removed, in three marsh zones, at two sites each in Georgia and Alabama. Removing neighbors increased porewater salinities; nevertheless, plants usu- ally performed best in neighbor-removal treatments, indicating that most interactions were competitive rather than facilitative. Several mechanisms might explain these results. For widely distributed species, southern individuals may be more salt tolerant than northern conspecifics. We tested this hypothesis by comparing the salt tolerance of northern and southern conspecifics of three species in a common garden experiment. In two species, southern plants were more salt tolerant than northern conspecifics. Although this pattern may explain the rarity of facilitation in the south for some species, it cannot explain our overall results because few species were studied in both geographic regions. The most likely explanation for our results is that northern marsh floras are dominated by salt-sensitive species that are likely to be facilitated by neighbors, whereas southern marsh floras are dominated by salt-tolerant species that are unlikely to benefit substantially from neighbor amelioration of soil salinities. These results illustrate the difficulties inherent in extrapolating results from even well understood systems to different geographic locations or scales. Intraspecific adaptations and community composition are often likely to vary geographically, complicating our efforts to construct geographically robust generalities about community structure and processes.

LATITUDINAL DIFFERENCES IN PLANT PALATABILITY IN ATLANTIC COAST SALT MARSHES

A central hypothesis of biogeography is that consumer-prey interactions are more intense at lower latitudes, leading to increased defenses of prey. Because plants vary in many traits that might affect palatability to herbivores, however studies of latitudinal variation in single plant traits such as secondary chemistry provide only circumstantial evidence to test this hypothesis. We directly compared the palatability of 10 salt marsh plants from seven northern (Rhode Island and Maine) and eight southern (Georgia and Florida) coastal salt marshes by flying fresh plant material back and forth and allowing 13 species of herbivores direct choices between northern and southern nonspecific plants in laboratory assays. In 127 of 149 assays (85%), herbivores showed a significant or marginally significant preference for northern plants. In only one assay did herbivores prefer southern plants. These results occurred regardless of the geographic location of the assay, herbivore species, year, or season of plant collection, although there were hints that latitudinal dif- ferences became less pronounced for two plant species late in the growing season. Our results provide the most comprehensive evidence to date for a latitudinal gradient in plant palatability in any community. The proximate plant traits and the ultimate evolutionary factors responsible for this pattern remain to be determined.

EFFECT OF PLANT TOUGHNESS, CALCIFICATION, AND CHEMISTRY ON HERBIVORY BY DOLABELLA AURICULARIA

Most studies of feeding preferences of herbivores have focussed on the role of plant secondary metabolites; very few studies have experimentally tested the importance of plant toughness or calcification as feeding deterrents, although low preference has re- peatedly been shown to correlate with these factors. Feeding preferences of the unusual generalist herbivore Dolabella auricularia, an opisthobranch gastropod which, like many other herbivores of that group, sequesters secondary metabolites from some algae, were consistent with our expectation that they might not feed on algae and seagrasses that were tough, calcified, or chemically rich. We experimentally examined the importance of each of these three features in deterring feeding by Dolabella. Consumption of plants by Dolab/lla was negatively correlated with plant toughness, as determined by penetrometer measurements. Given a choice between two species of plants, Dolahella always preferred the softer of the pair. However, when both species were ground up and incorporated into soft carrageenan cakes, Dolabella were significantly less selective in 3 of 4 cases where the tougher plant had no other known line of defense, and in 1 of 3 cases where the tougher plant also had chemical or CaCO3 defenses. Frondose calcified algae on Guam are ?50% CaCO3 by dry mass. CaCO3 deterred Dolabella feeding at concentrations of 28 and 50% of dry mass, but not at 16%. CaCO3 occurs in algae in two crystal structures, calcite and aragonite; both deterred Dolabella feeding. CaCO, and chem- ical defenses of lali/tneda tnacroloba did not interact synergistically to enhance effective- ness. Dolabella feeding was not deterred by organic extracts from most plants, even when offered at very high concentrations. Extracts from many of these plants had previously been shown to deter feeding by fishes at lower concentrations. Of the 12 plants tested, Dolabella feeding was deterred only by extracts from Caulerpa racemosa, Hortmothaannion enteromorphoidcs, and lIalimeda inacroloha. We isolated and tested the two major me- tabolites of Caulerpa, caulerpenyne and caulerpin, and identified caulerpenyne as the de- terrent agent. These results indicate that Dolabella are relatively unaffected by chemical defenses and yet are deterred by other plant defenses such as calcification and toughness. The fact that IDolabella can sequester algal secondary metabolites may explain Dolabellas relative in- difference to chemically rich plant extracts.

FEEDING PREFERENCES OF A GENERALIST SALT-MARSH CRAB: RELATIVE IMPORTANCE OF MULTIPLE PLANT TRAITS

Few studies have evaluated the relative importance of multiple plant traits to herbivore diet choice, especially with an experimental approach. Moreover, although circumstantial evidence points to plant toughness and silica content as important determinents of diet choice, few studies have experimentally demonstrated that these factors actually deter feeding by herbivores. We examined feeding preferences of a generalist salt-marsh crab, Armases cinereum, for all the common angiosperms in its habitat. We took an experimental approach to evaluating the importance of toughness, secondary chemistry, silica, salt, and protein in determining feeding preferences. Consumption of plants by Armases in two experiments was correlated with decreasing toughness. Consumption was more equitable when plants were ground up and reconstituted in agar discs, with reduced differences in toughness. In four pairwise choice tests, Armases always preferred the softer plant of the pair, but in three of four cases exhibited no prefe...

Parasitic plants: parallels and contrasts with herbivores

Parasitic plants are common in natural communities, but are largely ignored in plant community theory. Interactions between parasitic plants and hosts often parallel those between herbivores and plants: both types of consumers display host preferences, reduce host biomass and alter host allocation patterns, modify plant community structure and dynamics, and mediate interactions between host plants and other organisms. In other cases, basic differences in mobility, hormonal and elemental composition and resource capture between plants and animals lead to different effects: parasitic plants have broad host ranges, affect and are affected by host plant physiology because of similar hormonal pathways between parasite and host, do not alter nutrient cycling as extensively as do herbivores, and may simultaneously parasitize and compete with hosts. Many fundamental aspects of the ecology of parasitic plants remain poorly studied, and research to date has been dominated by laboratory studies and studies of crop pests, rather than by studies of natural communities.