A test of balanced fitness limitations theory: Pollen limitation in plants.

When reproductive success is determined by the relative availabilities of a series of essential, non-substitutable resources, the theory of balanced fitness limitations predicts that the cost of harvesting a particular resource shapes the likelihood that a shortfall of that resource will constrain realized fitness. Plant reproduction through female function offers a special opportunity to test this theory; essential resources in this context include, first, the pollen received from pollinators or abiotic vectors that is used to fertilize ovules, and, second, the resources needed to provision the developing seeds and fruit. For many plants realized reproductive success through female function can be readily quantified in the field, and one key potential constraint on fitness, pollen limitation, can be assessed experimentally by manually supplementing pollen receipt. We assembled a comparative dataset of pollen limitation using only studies that supplement pollen to all flowers produced over the plant's reproductive lifespan. Pre- and post-pollination costs were estimated using the weight of flowers and fruits and estimates of fruit set. Consistent with expectations, we find self-incompatible plants make greater pre-pollination investments and experience greater pollen limitation. However, contrary to theoretical expectations, when variation due to self-compatibility is accounted for by including self-compatibility in the statistical model as a covariate, we find no support for the prediction that plants that invest more heavily in pre-pollination costs are subject to greater pollen limitation. Strong within-species, between-population variation in the expression of pollen limitation makes the quantification of mean pollen limitation difficult. We urge plant ecologists to conduct more studies of pollen limitation using whole-plant pollen supplementation to produce a richer comparative dataset that would support a more robust test of the balanced limitations hypothesis.

Bryophyte stable isotope composition, diversity and biomass define tropical montane cloud forest extent.

Liverworts and mosses are a major component of the epiphyte flora of tropical montane forest ecosystems. Canopy access was used to analyse the distribution and vertical stratification of bryophyte epiphytes within tree crowns at nine forest sites across a 3400 m elevational gradient in Peru, from the Amazonian basin to the high Andes. The stable isotope compositions of bryophyte organic material (13C/12C and 18O/16O) are associated with surface water diffusive limitations and, along with C/N content, provide a generic index for the extent of cloud immersion. From lowland to cloud forest δ13C increased from -33‰ to -27‰, while δ18O increased from 16.3‰ to 18.0‰. Epiphytic bryophyte and associated canopy soil biomass in the cloud immersion zone was estimated at up to 45 t dry mass ha-1, and overall water holding capacity was equivalent to a 20 mm precipitation event. The study emphasizes the importance of diverse bryophyte communities in sequestering carbon in threatened habitats, with stable isotope analysis allowing future elevational shifts in the cloud base associated with changes in climate to be tracked.

Multiple Browsers Structure Tree Recruitment in Logged Temperate Forests.

Historical extirpations have resulted in depauperate large herbivore assemblages in many northern forests. In eastern North America, most forests are inhabited by a single wild ungulate species, white-tailed deer (Odocoileus virginianus), and relationships between deer densities and impacts on forest regeneration are correspondingly well documented. Recent recolonizations by moose (Alces americanus) in northeastern regions complicate established deer density thresholds and predictions of browsing impacts on forest dynamics because size and foraging differences between the two animals suggest a lack of functional redundancy. We asked to what extent low densities of deer + moose would structure forest communities differently from that of low densities of deer in recently logged patch cuts of Massachusetts, USA. In each site, a randomized block with three treatment levels of large herbivores-no-ungulates (full exclosure), deer (partial exclosure), and deer + moose (control) was established. After 6-7 years, deer + moose reduced stem densities and basal area by 2-3-fold, Prunus pensylvanica and Quercus spp. recruitment by 3-6 fold, and species richness by 1.7 species (19%). In contrast, in the partial exclosures, deer had non-significant effects on stem density, basal area, and species composition, but significantly reduced species richness by 2.5 species on average (28%). Deer browsing in the partial exclosure was more selective than deer + moose browsing together, perhaps contributing to the decline in species richness in the former treatment and the lack of additional decline in the latter. Moose used the control plots at roughly the same frequency as deer (as determined by remote camera traps), suggesting that the much larger moose was the dominant browser species in terms of animal biomass in these cuts. A lack of functional redundancy with respect to foraging behavior between sympatric large herbivores may explain combined browsing effects that were both large and complex.

Ungulate browsers promote herbaceous layer diversity in logged temperate forests.

Ungulates are leading drivers of plant communities worldwide, with impacts linked to animal density, disturbance and vegetation structure, and site productivity. Many ecosystems have more than one ungulate species; however, few studies have specifically examined the combined effects of two or more species on plant communities. We examined the extent to which two ungulate browsers (moose [Alces americanus]) and white-tailed deer [Odocoileus virginianus]) have additive (compounding) or compensatory (opposing) effects on herbaceous layer composition and diversity, 5-6 years after timber harvest in Massachusetts, USA. We established three combinations of ungulates using two types of fenced exclosures - none (full exclosure), deer (partial exclosure), and deer + moose (control) in six replicated blocks. Species composition diverged among browser treatments, and changes were generally additive. Plant assemblages characteristic of closed canopy forests were less abundant and assemblages characteristic of open/disturbed habitats were more abundant in deer + moose plots compared with ungulate excluded areas. Browsing by deer + moose resulted in greater herbaceous species richness at the plot scale (169 m(2)) and greater woody species richness at the subplot scale (1 m(2)) than ungulate exclusion and deer alone. Browsing by deer + moose resulted in strong changes to the composition, structure, and diversity of forest herbaceous layers, relative to areas free of ungulates and areas browed by white-tailed deer alone. Our results provide evidence that moderate browsing in forest openings can promote both herbaceous and woody plant diversity. These results are consistent with the classic grazing-species richness curve, but have rarely been documented in forests.

Modest Pollen Limitation of Lifetime Seed Production Is in Good Agreement with Modest Uncertainty in Whole-Plant Pollen Receipt.

We recently introduced a model that predicts the degree to which a plant's lifetime seed production may be constrained by unpredictable shortfalls of pollen receipt ("pollen limitation"). Burd's comment in this issue criticized our analysis, first by arguing that the empirical literature documents much higher levels of pollen limitation than our model predicts and then suggesting that the apparent discrepancy stemmed from our (1) underestimating the costs of securing a fertilized ovule and (2) assuming too little unpredictability in whole-plant pollen receipt. We reply as follows. First, the empirical literature must be consulted carefully. Burd relies on pollen supplementation experiments performed on parts of plants or on whole plants but during only one reproductive season for polycarpic perennials; in both cases, resource reallocation often leads to gross overestimates of pollen limitation. We comprehensively review pollen limitation estimates that are free of these estimation problems and find strong agreement with our model predictions. Second, although cost estimates for different components of seed production are imprecise, errors are likely to be small relative to the >1,000-fold differences observed across plant species, the primary focus of our article. Finally, contrary to Burd's argument, pollen receipt by entire plants is much more predictable than that by individual flowers because the flower-to-flower variation "averages out" when summed across many flowers. Our model uses parameter values that are in broad agreement with the empirical record of modest plant-to-plant variation in pollen receipt and thus predicts the generally modest pollen limitation that is observed in nature.

Epiphyte response to drought and experimental warming in an Andean cloud forest.

The high diversity and abundance of vascular epiphytes in tropical montane cloud forest is associated with frequent cloud immersion, which is thought to protect plants from drought stress. Increasing temperature and rising cloud bases associated with climate change may increase epiphyte drought stress, leading to species and biomass loss. We tested the hypothesis that warmer and drier conditions associated with a lifting cloud base will lead to increased mortality and/or decreased recruitment of epiphyte ramets, altering species composition in epiphyte mats. By using a reciprocal transplant design, where epiphyte mats were transplanted across an altitudinal gradient of increasing cloud immersion, we differentiated between the effects of warmer and drier conditions from the more general prediction of niche theory that transplanting epiphytes in any direction away from their home elevation should result in reduced performance. Effects differed among species, but effects were generally stronger and more negative for epiphytes in mats transplanted down slope from the highest elevation, into warmer and drier conditions, than for epiphyte mats transplanted from other elevations. In contrast, epiphytes from lower elevations showed greater resistance to drought in all treatments. Epiphyte community composition changed with elevation, but over the timescale of the experiment there were no consistent changes in species composition. Our results suggest some epiphytes may show resistance to climate change depending on the environmental and evolutionary context. In particular, sites where high rainfall makes cloud immersion less important for epiphyte water-balance, or where occasional drought has previously selected for drought-resistant taxa, may be less adversely affected by predicted climate changes.

Resource depletion, pollen coupling, and the ecology of mast seeding.

Masting, the highly variable and synchronous production of seeds across a population of perennial plants, is an ecologically important, but still poorly understood, phenomenon. While much is known about the fitness benefits of masting and its effects on seed consumers and trophic interactions, less is understood about the proximate mechanisms of masting. The resource budget model (RBM) posits that masting requires more resources than plants can gain in a single year. Individual plants store resources until a threshold is reached and then produce seeds, which depletes resources so that plants cannot reproduce again for 2 or more years. Individuals are synchronized by pollen coupling or environmental forcing. We review the assumptions of these models and assess the extent to which they are consistent with general patterns in plant populations. We discuss the implications of the RBM for how plants respond to changes in the external environment. Overall, the RBM is a likely cause of synchrony in many, but not all, masting species. This mechanistic hypothesis also leads to specific, but not always intuitive, expectations about how plant resources affect mast seeding.

Intra- and interspecific tree growth across a long altitudinal gradient in the Peruvian Andes.

Tree growth response across environmental gradients is fundamental to understanding species distributional ecology and forest ecosystem ecology and to predict future ecosystem services. Cross-sectional patterns of ecosystem properties with respect to climatic gradients are often used to predict ecosystem responses to global change. Across sites in the tropics, primary productivity increases with temperature, suggesting that forest ecosystems will become more productive as temperature rises. However, this trend is confounded with a shift in species composition and so may not reflect the response of in situ forests to warming. In this study, we simultaneously studied tree diameter growth across the altitudinal ranges of species within a single genus across a geographically compact temperature gradient, to separate the direct effect of temperature on tree growth from that of species compositional turnover. Using a Bayesian state space modeling framework we combined data from repeated diameter censuses and dendrometer measurements from across a 1700-m altitudinal gradient collected over six years on over 2400 trees in Weinmannia, a dominant and widespread genus of cloud forest trees in the Andes. Within species, growth showed no consistent trend with altitude, but higher-elevation species had lower growth rates than lower-elevation species, suggesting that species turnover is largely responsible for the positive correlation between productivity and temperature in tropical forests. Our results may indicate a significant difference in how low- and high-latitude forests will respond to climate change, since temperate and boreal tree species are consistently observed to have a positive relationship between growth and temperature. If our results hold for other tropical species, a positive response in ecosystem productivity to increasing temperatures in the Andes will depend on the altitudinal migration of tree species. The rapid pace of climate change, and slow observed rates of migration, suggest a slow, or even initially negative response of ecosystem productivity to warming. Finally, this study shows how the observed scale of biological organization can affect conclusions drawn from studies of ecological phenomena across environmental gradients, and calls into question the common practice in tropical ecology of lumping species at higher taxonomic levels.

Simulating forest productivity along a neotropical elevational transect: temperature variation and carbon use efficiency.

A better understanding of the mechanisms controlling the magnitude and sign of carbon components in tropical forest ecosystems is important for reliable estimation of this important regional component of the global carbon cycle. We used the JULES vegetation model to simulate all components of the carbon balance at six sites along an Andes-Amazon transect across Peru and Brazil and compared the results to published field measurements. In the upper montane zone the model predicted a lack of forest vegetation, indicating a need for better parameterization of the responses of cloud forest vegetation within the model. In the lower montane and lowland zones simulated ecosystem productivity and respiration were predicted with reasonable accuracy, although not always within the error bounds of the observations. Model-predicted carbon use efficiency in this transect surprisingly did not increase with elevation, but remained close to the 'temperate' value 0.5. Upper montane forests were predicted to allocate ~50% of carbon fixation to biomass maintenance and growth, despite available measurements showing that they only allocate ~33%. This may be explained by elevational changes in the balance between growth and maintenance respiration within the forest canopy, as controlled by both temperature- and pressure-mediated processes, which is not yet well represented in current vegetation models.

Microbes do not follow the elevational diversity patterns of plants and animals.

The elevational gradient in plant and animal diversity is one of the most widely documented patterns in ecology and, although no consensus explanation exists, many hypotheses have been proposed over the past century to explain these patterns. Historically, research on elevational diversity gradients has focused almost exclusively on plant and animal taxa. As a result, we do not know whether microbes exhibit elevational gradients in diversity that parallel those observed for macroscopic taxa. This represents a key knowledge gap in ecology, especially given the ubiquity, abundance, and functional importance of microbes. Here we show that, across a montane elevational gradient in eastern Peru, bacteria living in three distinct habitats (organic soil, mineral soil, and leaf surfaces) exhibit no significant elevational gradient in diversity (r2<0.17, P>0.1 in all cases), in direct contrast to the significant diversity changes observed for plant and animal taxa across the same montane gradient (r2>0.75, P<0.001 in all cases). This finding suggests that the biogeographical patterns exhibited by bacteria are fundamentally different from those of plants and animals, highlighting the need for the development of more inclusive concepts and theories in biogeography to explain these disparities.