Carol C. Horvitz

LONGEVITY CAN BUFFER PLANT AND ANIMAL POPULATIONS AGAINST CHANGING CLIMATIC VARIABILITY

Both means and year-to-year variances of climate variables such as temperature and precipitation are predicted to change. However, the potential impact of changing climatic variability on the fate of populations has been largely unexamined. We analyzed multiyear demographic data for 36 plant and animal species with a broad range of life histories and types of environment to ask how sensitive their long-term stochastic population growth rates are likely to be to changes in the means and standard deviations of vital rates (survival, reproduction, growth) in response to changing climate. We quantified responsiveness using elasticities of the long-term population growth rate predicted by stochastic projection matrix models. Short-lived species (insects and annual plants and algae) are predicted to be more strongly (and negatively) affected by increasing vital rate variability relative to longer-lived species (perennial plants, birds, ungulates). Taxonomic affiliation has little power to explain sensitivity to increasing variability once longevity has been taken into account. Our results highlight the potential vulnerability of short-lived species to an increasingly variable climate, but also suggest that problems associated with short-lived undesirable species (agricultural pests, disease vectors, invasive weedy plants) may be exacerbated in regions where climate variability decreases.

PLANT-ANIMAL INTERACTIONS AND FRUIT PRODUCTION IN A NEOTROPICAL HERB: A PATH ANALYSIS'

We used path analysis to estimate the direct and indirect effects of antguards, an ant-tended herbivore, and pollinators, on flower and fruit production in Calathea ovan- densis, a neotropical herb. The natural variation in these plant-animal interactions was quantified for individual plants in Veracruz, Mexico in 1984 and 1985. We conclude that variation in plant-animal interactions has significant, and complex, effects on flower and fruit production in this species. Antguards had a positive direct effect on flower number in both years, and because of the positive effect of flower number on fruit number, had a positive indirect effect on mature fruit number. The herbivore had a negative direct effect on flower number and mature fruit number in both years. Thus, direct and indirect effects contribute to the large negative effect of herbivores on mature fruit number. The composition of the pollinator community was very different in the two years, with a marked increase in the number of visits by efficient pollinators in 1985. This change was reflected in between-year differences in the effects of pollinators on number of initiated fruits. In 1984, pollinators had no significant effect on initiated fruit number, while the two pollinators that increased in abundance in 1985 had significant effects on initiated fruit number in that year. These results are consistent with experimental data for 1985, which indicate that supplemental pollination causes a significant increase in the number of fruit initiated. While pollinators may limit the number of fruit initiated in some years, our observational and experimental data suggest that number of mature fruits is primarily limited by resources, not by pollination.

Spatiotemporal Variation in Insect Mutualists of a Neotropical Herb

We observed striking spatiotemporal variation in the antguard and pollinator mutualist assemblages of a neotropical herb. Fifteen different ant taxa (in five subfamilies) and five pollinator taxa (four euglossine bees and one anthophorid bee) were associated with the plants during censuses at four sites. Ants and pollinators were censused for 4 and 3 yr, respectively. The mean number of taxa per site per year was 6.8 for ants and 3.6 for pollinators. The ant assemblage varied more than the pollinator assemblage, particularly spatially. The ant assemblage varied more through space than through time (means of the proportional similarities for pairwise comparisons of assemblages were 0.37 and 0.51, respectively), while the pollinator assemblage varied equally through space and time (means of the proportional similarities were 0.53 and 0.50, respectively). For individual taxa of both assemblages, the coefficient of variation in relative abundance was large (>75%) for the majority of spatial and temporal comparisons. In each assemblage there was a single taxon (in the antguard, a rare taxon, but in the pollinators, an abundant taxon) that was the least variable, surprisingly in both time and space, in its relative abundance. These results, coupled with our previous findings of significant variation among mu- tualist taxa in the magnitude of their beneficial effects, indicate that plants may be subject to highly variable selection by their mutualist assemblages. The most beneficial antguard was consistently rare; the most beneficial pollinator was abundant in one site-year but rare or absent in most site-years. The taxon that was consistently abundant was not an efficient pollinator. Evolutionary specialization of plants on particular animals may be constrained by lack of constancy in the relative abundance of animals and the opportunity for spe- cialization may differ greatly between interactions (e.g., antguards and pollinators) due to divergent patterns of constancy, rarity, and quality.

Pollinator Limitation, Cost of Reproduction, and Fitness in Plants: A Transition-Matrix Demographic Approach

A model of population dynamics based on a transition-probability matrix was used to evaluate how pollinator limitation and demographic cost of reproduction interact to create a fitness surface for plants. The state variable was the size-fecundity class of an individual; in a given season, individuals were classified as having relatively high or low fecundity. Three parameters were investigated: cost of reproduction, c, was the probability that high-fecundity individuals regress one size class; population pollination level, p, was the probability that reproductive individuals have a high-fecundity year; fecundity difference, d, was the relative difference in fecundity between low- and high-fecundity individuals. Two kinds of life histories were modeled, in which fecundity was either size-dependent or size-independent. For each kind of life history, 100 matrices were constructed by assigning different values to the parameters, and their largest teal eigenvalue, which constitutes an estimate of the average overall fitness of individuals in the population, was obtained. The main results of the simulations were that (1) for any combination of c and d, there is a particular value of p that maximizes fitness, and this value can be very low or very high; (2) keeping the other parameters constant, higher cs reduce fitness and higher ds increase fitness; (3) the magnitude of the effects of c and d on fitness depends only on p and is lowest when p is lowest and highest when p is highest; and (4) increases in c and d move the optimal pollination level to the left and right, respectively. The empirical use of the model requires a detailed demographic study. It is pointed out that hand-pollination experiments that include only two extreme classes of fruit production may yield misleading results. Hand-pollinations should be designed to explicitly quantify the relationship between d and c. Future pollination-limitation studies should estimate p, a parameter that has been mostly ignored. Available evidence on pollinator limitation and c in orchids was reexamined in terms of this model. We concluded that most data available suggest that fruit set is pollinator-limited in orchids, even though reproduction may result in a cost.

DEMOGRAPHIC COST OF REPRODUCTION IN A NEOTROPICAL HERB: AN EXPERIMENTAL FIELD STUDY'

There are few empirical data for plants demonstrating unambiguously that an increase in current reproductive effort results in a demographic cost, i.e., a significant decrease in future growth, survival, or reproduction. In this study we experimentally created low- and high-reproductive-effort plants in a natural field population of a neotropical perennial herb and measured subsequent growth, survival, and reproduction. During the season subsequent to the experimental treatment, there were no significant differences in survival, growth, or reproduction between the two treatments. Thus, for long-lived peren- nial plants, an increase in reproduction may not result in a demographic cost. More ex- perimental studies are needed to determine the generality of this result.

Seed dispersal and environmental heterogeneity in a neotropical herb: a model of population and patch dynamics

We examined the effects of three kinds of seed dispersal on mean fitness in the ant-dispersed perennial herb Calathea ovandensis (Marantaceae): (1) local dispersal to safe sites, (2) longdistance dispersal, and (3) dispersal through time, i.e., dormancy. Because, persistence of this species depends upon periodic disturbance by treefalls, we propose a matrix model of population dynamics that combines the successional dynamics of the forest with the habitat-specific demographic dynamics of the plant. Using empirically determined values for the demographic parameters for Calathea ovandensis in a new gap, and three different models of how stage-specific growth and survival change as succession proceeds, we characterize the overall population dynamics of our study species. For the model best representing the demographic response of Calathea ovandensis to succession, the results of our computer simulations predict strong selection for local dispersal to safe sites, and selection against long-distance dispersal. These predictions are consistent with observed patterns of seed dispersal in Calathea ovandensis. In addition, the model predicts very weak selection for long-term seed dormancy, a life-history stage currently under investigation. Models combining patch dynamics with population dynamics provide a method of quantifying the demographic consequences of lifehistory variation for plants occupying variable environments.

Effects of Dispersers, Gaps, and Predators on Dormancy and Seedling Emergence in a Tropical Herb

The influence of biotic and abiotic factors on seed fates are exceptionally difficult to analyze in natural populations because it is not usually possible to identify an emerging seedling with its history as a seed. Large seed size and the unusual feature that the seed body remains attached to the new seedling in the ant—dispersed herb Calathea ovandensis provided an opportunity for field experiments that examine the influence of (1) seed dispersers, (2) treefall gaps, and (3) post—dispersal predators on seed survival, seed dormancy, seedling emergence, and seedling distributions. In a seed depot experiment, seed—dispersing ants significantly affected the seedling emergence patterns in three ways. Seeds with rewards for ants: (a) had improved seedling emergence, by 1.6—fold (17.4 vs. 10.6%); (b) gave rise to seedlings with a mean dispersal distance that was threefold farther (34 vs. 114 cm); and (c) generated a non—leptokurtic seedling shadow (kurtosis: —0.60, not significant vs. 10.84, P < 0.001) in contrast to seeds without ant rewards. There was significant spatial variation in the effect of ant rewards on seedling emergence and also temporal variation in seedling emergence, the greatest number of seedlings emerging in an el Nino year. In two germination box experiments: (1) treefall gaps enhanced seedling emergence 180—fold (72.4 vs 0.4%) compared to the deep shade, and ungerminated seeds in the deep shade were mostly dormant, not dead; (2) post—dispersal seed predation was very low (overall mean of 6.2%), with considerable microspatial variability, and pathogens and small invertebrates accounted for only one—fourth as much seed mortality as larger (vertebrate and large insect) post—dispersal predators. Seedling emergence in this ant—dispersed herb with a relatively long—lived seed bank depends upon a complex of factors, suggesting an interaction of the effects of biotic dispersal to local safe microsites with larger scale effects of spatial and temporal variation in the abiotic environment.

Invasive plants in wildland ecosystems: merging the study of invasion processes with management needs

Increasing numbers of non-native species threaten the values of wildland ecosystems. As a result, interest in and research on invasive plant species in wildland settings has accelerated. Nonetheless, the ecological and economic impacts of non-native species continue to grow, raising the question of how to best apply science to the regulation and management of invasive plants. A major constraint to controlling the flow of potentially undesirable plant species is the lack of a strong regulatory framework concurrent with increases in trade volume. To address this, ecologists have been developing models to predict which species will be harmful to wildland values and are working with the horticultural industry to apply this information to the sale of species. The management of established invasive plants is hampered by conflicting goals, a lack of information on management outcomes, and a lack of funding. Ecologists and weed scientists can provide a scientific basis for prioritizing species for control and for managing species composition through the application of control technology, which can take place simultaneously with the manipulation of the ecological processes that influence community susceptibility to invasion. A stronger scientific basis for land management decisions is needed and can be met through nationally funded partnerships between university and agency scientists and land managers.

A Test of the Pollinator Limitation Hypothesis for a Neotropical Herb

We hand—pollinated all flowers in inflorescences of the neotropical herb Calathea ovandensis (Marantaceae) and compared fruit and seed set of treatment plants to that of open—pollinated controls. Hand—pollination increased the number of initiated fruits by 24%, the number of mature fruits by 6.8%, and the number of seeds by 12.6%, but only the first of these differences was statistically significant. The proportion of flowers that matured fruits was very low compared with data reported for other species: 8.1% for the hand—pollinated treatment and 7.4% for open—pollinated controls. The proportion of flowers that initiated fruits was also quite low: 24.5% for hand—pollinated plants and 20.2% for open—pollinated plants. Mature fruit and seed production were significantly affected by nonpollinating animals that act at different developmental stages. Antguards attracted to extrafloral nectaries on the inflorescence appeared to stimulate flower production, while an ant—tended herbivore of reproductive tissues h...

In a long-term experimental demography study, excluding ungulates reversed invader's explosive population growth rate and restored natives

Significance In ecosystems worldwide, the presence of overabundant ungulates (e.g. deer, cows) and the invasion of exotic plants are disrupting native communities. A recent hypothesis causally links these problems implicating overabundant ungulates in enhancing invaders’ demographic success. We tested this hypothesis in a forest where white-tailed deer are overabundant and garlic mustard is aggressively invading. Using long-term, replicated deer exclusion/deer access plot pairs, we quantified population density, growth, and decline of this invader and native plants. We conclusively demonstrate that deer are required for garlic mustard success; its local extinction is projected where deer are absent. Our findings provide the first definitive support connecting overabundant ungulates to enhanced invader success, with broad implications for biodiversity and ecosystem function. A major goal in ecology is to understand mechanisms that increase invasion success of exotic species. A recent hypothesis implicates altered species interactions resulting from ungulate herbivore overabundance as a key cause of exotic plant domination. To test this hypothesis, we maintained an experimental demography deer exclusion study for 6 y in a forest where the native ungulate Odocoileus virginianus (white-tailed deer) is overabundant and Alliaria petiolata (garlic mustard) is aggressively invading. Because population growth is multiplicative across time, we introduce metrics that correctly integrate experimental effects across treatment years, the cumulative population growth rate, λc, and its geometric mean, λper-year, the time-averaged annual population growth rate. We determined λc and λper-year of the invader and of a common native, Trillium erectum. Our results conclusively demonstrate that deer are required for the success of Alliaria; its projected population trajectory shifted from explosive growth in the presence of deer (λper-year = 1.33) to decline toward extinction where deer are excluded (λper-year = 0.88). In contrast, Trillium’s λper-year was suppressed in the presence of deer relative to deer exclusion (λper-year = 1.04 vs. 1.20, respectively). Retrospective sensitivity analyses revealed that the largest negative effect of deer exclusion on Alliaria came from rosette transitions, whereas the largest positive effect on Trillium came from reproductive transitions. Deer exclusion lowered Alliaria density while increasing Trillium density. Our results provide definitive experimental support that interactions with overabundant ungulates enhance demographic success of invaders and depress natives’ success, with broad implications for biodiversity and ecosystem function worldwide.