The objective of science is to understand the natural world; we argue that prediction is the only way to demonstrate scientific understanding, implying that prediction should be a fundamental aspect of all scientific disciplines. Reproducibility is an essential requirement of good science and arises from the ability to develop models that make accurate predictions on new data. Ecology, however, with a few exceptions, has abandoned prediction as a central focus and faces its own crisis of reproducibility. Models are where ecological understanding is stored and they are the source of all predictions -no prediction is possible without a model of the world. Models can be improved in three ways: model variables, functional relationships among dependent and independent variables, and in parameter estimates. Ecologists rarely test to assess whether new models have made advances by identifying new and important variables, elucidating functional relationships, or improving parameter estimates. Without these tests it is difficult to know if we understand more today than we did yesterday. A new commitment to prediction in ecology would lead to, among other things, more mature (i.e. quantitative) hypotheses, prioritization of modeling techniques that are more appropriate for prediction (e.g. using continuous independent variables rather than categorical) and, ultimately, advancement towards a more general understanding of the natural world. Synthesis
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Human-caused disruptions to seed-dispersal mutualisms increase the extinction risk for both plant and animal species. Large-seeded plants can be particularly vulnerable due to highly specialized dispersal systems and no compensatory regeneration mechanisms. Whitebark pine (Pinus albicaulis), a keystone subalpine species, obligately depends upon the Clark's Nutcracker (Nucifraga columbiana) for dispersal of its large, wingless seeds. Clark's Nutcracker, a facultative mutualist with whitebark pine, is sensitive to rates of energy gain, and emigrates from subalpine forests during periods of cone shortages. The invasive fungal pathogen Cronartium ribicola, which causes white pine blister rust, reduces whitebark pine cone production by killing cone-bearing branches and trees. Mortality from blister rust reaches 90% or higher in some whitebark pine forests in the Northern Rocky Mountains, USA, and the rust now occurs nearly rangewide in whitebark pine. Our objectives were to identify the minimum level of cone production necessary to elicit seed dispersal by nutcrackers and to determine how cone production is influenced by forest structure and health. We quantified forest conditions and ecological interactions between nutcrackers and whitebark pine in three Rocky Mountain ecosystems that differ in levels of rust infection and mortality. Both the frequency of nutcracker occurrence and probability of seed dispersal were strongly related to annual whitebark pine cone production, which had a positive linear association with live whitebark pine basal area, and negative linear association with whitebark pine tree mortality and rust infection. From our data, we estimated that a threshold level of approximately 1000 cones/ha is needed for a high likelihood of seed dispersal by nutcrackers (probability > or = 0.7), and that this level of cone production can be met by forests with live whitebark pine basal area > 5.0 m2/ha. The risk of mutualism disruption is greatest in northern most Montana (USA), where three-year mean cone production and live basal area fell below predicted threshold levels. There, nutcracker occurrence, seed dispersal, and whitebark pine regeneration were the lowest of the three ecosystems. Managers can use these threshold values to differentiate between restoration sites requiring planting of rust-resistant seedlings and sites where nutcracker seed dispersal can be expected.
BackgroundAccurately quantifying key interactions between species is important for developing effective recovery strategies for threatened and endangered species. Whitebark pine (Pinus albicaulis), a candidate species for listing under the Endangered Species Act, depends on Clark's nutcracker (Nucifraga columbiana) for seed dispersal. As whitebark pine succumbs to exotic disease and mountain pine beetles (Dendroctonus ponderosae), cone production declines, and nutcrackers visit stands less frequently, reducing the probability of seed dispersal.Methodology/Principal FindingsWe quantified whitebark pine forest structure, health metrics, and the frequency of nutcracker occurrence in national parks within the Northern and Central Rocky Mountains in 2008 and 2009. Forest health characteristics varied between the two regions, with the northern region in overall poorer health. Using these data, we show that a previously published model consistently under-predicts the proportion of survey hours resulting in nutcracker observations at all cone density levels. We present a new statistical model of the relationship between whitebark pine cone production and the probability of Clark's nutcracker occurrence based on combining data from this study and the previous study.Conclusions/SignificanceOur model clarified earlier findings and suggested a lower cone production threshold value for predicting likely visitation by nutcrackers: Although nutcrackers do visit whitebark pine stands with few cones, the probability of visitation increases with increased cone production. We use information theoretics to show that beta regression is a more appropriate statistical framework for modeling the relationship between cone density and proportion of survey time resulting in nutcracker observations. We illustrate how resource managers may apply this model in the process of prioritizing areas for whitebark pine restoration.
It is common to use multiple field sampling methods when implementing wildlife surveys to compare method efficacy or cost efficiency, integrate distinct pieces of information provided by separate methods, or evaluate method-specific biases and misclassification error. Existing models that combine information from multiple field methods or sampling devices permit rigorous comparison of method-specific detection parameters, enable estimation of additional parameters such as false-positive detection probability, and improve occurrence or abundance estimates, but with the assumption that the separate sampling methods produce detections independently of one another. This assumption is tenuous if methods are paired or deployed in close proximity simultaneously, a common practice that reduces the additional effort required to implement multiple methods and reduces the risk that differences between method-specific detection parameters are confounded by other environmental factors. We develop occupancy and spatial capture-recapture models that permit covariance between the detections produced by different methods, use simulation to compare estimator performance of the new models to models assuming independence, and provide an empirical application based on American marten (Martes americana) surveys using paired remote cameras, hair catches, and snow tracking. Simulation results indicate existing models that assume that methods independently detect organisms produce biased parameter estimates and substantially understate estimate uncertainty when this assumption is violated, while our reformulated models are robust to either methodological independence or covariance. Empirical results suggested that remote cameras and snow tracking had comparable probability of detecting present martens, but that snow tracking also produced false-positive marten detections that could potentially substantially bias distribution estimates if not corrected for. Remote cameras detected marten individuals more readily than passive hair catches. Inability to photographically distinguish individual sex did not appear to induce negative bias in camera density estimates; instead, hair catches appeared to produce detection competition between individuals that may have been a source of negative bias. Our model reformulations broaden the range of circumstances in which analyses incorporating multiple sources of information can be robustly used, and our empirical results demonstrate that using multiple field-methods can enhance inferences regarding ecological parameters of interest and improve understanding of how reliably survey methods sample these parameters.
We tested the hypotheses that white pine blister rust ( Cronartium ribicola J.C. Fisch.) damage in whitebark pine ( Pinus albicaulis Engelm.) stands leads to reduced (1) seed cone density, (2) predispersal seed survival, and (3) likelihood of Clark’s Nutcracker ( Nucifraga columbiana (Wilson, 1811)) seed dispersal. We gathered data from two sets of paired forest sites in the Bitterroot Mountains of eastern Idaho and western Montana that were similar in topography, canopy structure, tree species composition, and successional stage, but differed in rust infection level, crown kill, and tree mortality. We counted initial (mid-July) and final (late August) seed cones, observed vertebrate seed predator activity, and documented nutcracker seed dispersal in study sites in 2001 and 2002. High-rust sites had higher rates of seed predation relative to cone abundance, lower predispersal seed survival, and fewer observations of nutcracker seed dispersal than paired low-rust sites. These findings suggest that as blister-rust-induced damage increases within stands in the Bitterroot Mountains, the likelihood of nutcracker seed dispersal decreases. We propose that whitebark pine in heavily rust-damaged forests may not self-regenerate and would therefore require planting of seeds or seedlings from genetically rust-resistant trees.
Differential responses by species to modern perturbations in forest ecosystems may have undesirable impacts on plant-animal interactions. If such disruptions cause declines in a plant species without corresponding declines in a primary seed predator, the effects on the plant could be exacerbated. We examined one such interaction between Pinus albicaulis (whitebark pine), a bird-dispersed, subalpine forest species experiencing severe population declines in the northern part of its range, and Tamiasciurus hudsonicus (red squirrel), an efficient conifer seed predator, at 20 sites in two distinct ecosystems. Hypotheses about squirrel habitat preferences were tested to determine how changes in forest conditions influence habitat use and subsequent levels of predispersal cone predation. We performed habitat selection modeling and variable ranking based on Akaike's information criterion; compared the level and variance of habitat use between two forest types (P. albicaulis dominant and mixed conifer); and modeled the relationship between P. albicaulis relative abundance and predispersal cone predation. T. hudsonicus did not demonstrate strong habitat preference for P. albicaulis, and thus, declines in the pine were not met with proportional declines in squirrel habitat use. P. albicaulis habitat variables were the least important in squirrel habitat selection. Squirrel habitat use was lower and varied more in P. albicaulis-dominant forests, and predispersal cone predation decreased linearly with increasing P. albicaulis relative abundance. In Northern Rocky Mountain sites, where P. albicaulis mortality was higher and abundance lower, squirrel predation was greater than in Central Rocky Mountain sites. In ecosystems with reduced P. albicaulis abundance, altered interactions between the squirrel and pine may lead to a lower proportion of P. albicaulis contributing to population recruitment because of reduced seed availability. Reducing the abundance of competing conifers will create suboptimal squirrel habitat, thus lowering cone predation in P. albicaulis and ensuring more seeds are available for avian dispersal.
The Inventory & Monitoring Division of the U.S. National Park Service conducts long-term monitoring to provide park managers information on the status and trends in biological and environmental attributes including white pines. White pines are foundational species in many subalpine ecosystems and are currently experiencing population declines. Here we present results on the status of whitebark and foxtail pine in the southern Sierra Nevada of California, an area understudied relative to other parts of their ranges. We selected random plot locations in Yosemite, Sequoia, and Kings Canyon national parks using an equal probability spatially-balanced approach. Tree- and plot-level data were collected on forest structure, composition, demography, cone production, crown mortality, and incidence of white pine blister rust and mountain pine beetle. We measured 7899 whitebark pine, 1112 foxtail pine, and 6085 other trees from 2012–2017. All factors for both species were spatially highly variable. Whitebark pine occurred in nearly-pure krummholz stands at or near treeline and as a minor component of mixed species forests. Ovulate cones were observed on 25% of whitebark pine and 69% of foxtail pine. Whitebark pine seedlings were recorded in 58% of plots, and foxtail pine seedlings in only 21% of plots. Crown mortality (8% in whitebark, 6% in foxtail) was low and significantly higher in 2017 compared to previous years. Less than 1% of whitebark and zero foxtail pine were infected with white pine blister rust and <1% of whitebark and foxtail pine displayed symptoms of mountain pine beetle attack. High elevation white pines in the southern Sierra Nevada are healthy compared to other portions of their range where population declines are significant and well documented. However, increasing white pine blister rust and mountain pine beetle occurrence, coupled with climate change projections, portend future declines for these species, underscoring the need for broad-scale collaborative monitoring.
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