skip to main content


Title: Biotic and anthropogenic forces rival climatic/abiotic factors in determining global plant population growth and fitness
Multiple, simultaneous environmental changes, in climatic/abiotic factors, interacting species, and direct human influences, are impacting natural populations and thus biodiversity, ecosystem services, and evolutionary trajectories. Determining whether the magnitudes of the population impacts of abiotic, biotic, and anthropogenic drivers differ, accounting for their direct effects and effects mediated through other drivers, would allow us to better predict population fates and design mitigation strategies. We compiled 644 paired values of the population growth rate ( λ ) from high and low levels of an identified driver from demographic studies of terrestrial plants. Among abiotic drivers, natural disturbance (not climate), and among biotic drivers, interactions with neighboring plants had the strongest effects on λ . However, when drivers were combined into the 3 main types, their average effects on λ did not differ. For the subset of studies that measured both the average and variability of the driver, λ was marginally more sensitive to 1 SD of change in abiotic drivers relative to biotic drivers, but sensitivity to biotic drivers was still substantial. Similar impact magnitudes for abiotic/biotic/anthropogenic drivers hold for plants of different growth forms, for different latitudinal zones, and for biomes characterized by harsher or milder abiotic conditions, suggesting that all 3 drivers have equivalent impacts across a variety of contexts. Thus, the best available information about the integrated effects of drivers on all demographic rates provides no justification for ignoring drivers of any of these 3 types when projecting ecological and evolutionary responses of populations and of biodiversity to environmental changes.  more » « less
Award ID(s):
1753980
NSF-PAR ID:
10138509
Author(s) / Creator(s):
; ; ; ;
Date Published:
Journal Name:
Proceedings of the National Academy of Sciences
Volume:
117
Issue:
2
ISSN:
0027-8424
Page Range / eLocation ID:
1107 to 1112
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Climate change can impact plant fitness and population persistence directly through changing abiotic conditions and indirectly through its effects on species interactions. Pollination and seed predation are important biotic interactions that can impact plant fitness, but their impact on population growth rates relative to the role of direct climatic effects is unknown.

    We combined 13 years of experiments on pollen limitation of seed set and pre‐dispersal seed predation inIpomopsis aggregata, a subalpine wildflower, with a long‐term demographic study that has documented declining population growth with earlier spring snowmelt date. We determined how pollen limitation and seed predation changed with snowmelt date over 21 years and incorporated those effects into an integral projection model to assess relative impacts of biotic factors on population growth.

    Both pollen limitation and the difference in stigma pollen load between pollen‐supplemented and control plants declined over years. Neither pollen limitation nor seed predation changed detectably with snowmelt date, suggesting an absence of indirect effects of that specific abiotic factor on these indices of biotic interactions. The projected biotic impacts of pollen limitation and seed predation on population growth rate were small compared to factors associated with snowmelt date. Providing full pollination would delay the projected date when earlier snowmelt will cause populations to fall below replacement by only 14 years.

    Synthesis. Full pollination and elimination of seed predation would not compensate for the strong detrimental effects of early snowmelt on population growth rate, which inI. aggregataappears driven largely by abiotic environmental factors. The reduction over two decades in pollen limitation also suggests that natural selection on floral traits may weaken with continued climate change. These results highlight the value of studying both abiotic factors and biotic interactions to understand how climate change will influence plant populations.

     
    more » « less
  2. Abstract

    Seasonal variation in the availability of essential resources is one of the most important drivers of natural selection on the phasing and duration of annually recurring life-cycle events. Shifts in seasonal timing are among the most commonly reported responses to climate change and the capacity of organisms to adjust their timing, either through phenotypic plasticity or evolution, is a critical component of resilience. Despite growing interest in documenting and forecasting the impacts of climate change on phenology, our ability to predict how individuals, populations, and species might alter their seasonal timing in response to their changing environments is constrained by limited knowledge regarding the cues animals use to adjust timing, the endogenous genetic and molecular mechanisms that transduce cues into neural and endocrine signals, and the inherent capacity of animals to alter their timing and phasing within annual cycles. Further, the fitness consequences of phenological responses are often due to biotic interactions within and across trophic levels, rather than being simple outcomes of responses to changes in the abiotic environment. Here, we review the current state of knowledge regarding the mechanisms that control seasonal timing in vertebrates, as well as the ecological and evolutionary consequences of individual, population, and species-level variation in phenological responsiveness. Understanding the causes and consequences of climate-driven phenological shifts requires combining ecological, evolutionary, and mechanistic approaches at individual, populational, and community scales. Thus, to make progress in forecasting phenological responses and demographic consequences, we need to further develop interdisciplinary networks focused on climate change science.

     
    more » « less
  3. BACKGROUND The availability of nitrogen (N) to plants and microbes has a major influence on the structure and function of ecosystems. Because N is an essential component of plant proteins, low N availability constrains the growth of plants and herbivores. To increase N availability, humans apply large amounts of fertilizer to agricultural systems. Losses from these systems, combined with atmospheric deposition of fossil fuel combustion products, introduce copious quantities of reactive N into ecosystems. The negative consequences of these anthropogenic N inputs—such as ecosystem eutrophication and reductions in terrestrial and aquatic biodiversity—are well documented. Yet although N availability is increasing in many locations, reactive N inputs are not evenly distributed globally. Furthermore, experiments and theory also suggest that global change factors such as elevated atmospheric CO 2 , rising temperatures, and altered precipitation and disturbance regimes can reduce the availability of N to plants and microbes in many terrestrial ecosystems. This can occur through increases in biotic demand for N or reductions in its supply to organisms. Reductions in N availability can be observed via several metrics, including lowered nitrogen concentrations ([N]) and isotope ratios (δ 15 N) in plant tissue, reduced rates of N mineralization, and reduced terrestrial N export to aquatic systems. However, a comprehensive synthesis of N availability metrics, outside of experimental settings and capable of revealing large-scale trends, has not yet been carried out. ADVANCES A growing body of observations confirms that N availability is declining in many nonagricultural ecosystems worldwide. Studies have demonstrated declining wood δ 15 N in forests across the continental US, declining foliar [N] in European forests, declining foliar [N] and δ 15 N in North American grasslands, and declining [N] in pollen from the US and southern Canada. This evidence is consistent with observed global-scale declines in foliar δ 15 N and [N] since 1980. Long-term monitoring of soil-based N availability indicators in unmanipulated systems is rare. However, forest studies in the northeast US have demonstrated decades-long decreases in soil N cycling and N exports to air and water, even in the face of elevated atmospheric N deposition. Collectively, these studies suggest a sustained decline in N availability across a range of terrestrial ecosystems, dating at least as far back as the early 20th century. Elevated atmospheric CO 2 levels are likely a main driver of declines in N availability. Terrestrial plants are now uniformly exposed to ~50% more of this essential resource than they were just 150 years ago, and experimentally exposing plants to elevated CO 2 often reduces foliar [N] as well as plant-available soil N. In addition, globally-rising temperatures may raise soil N supply in some systems but may also increase N losses and lead to lower foliar [N]. Changes in other ecosystem drivers—such as local climate patterns, N deposition rates, and disturbance regimes—individually affect smaller areas but may have important cumulative effects on global N availability. OUTLOOK Given the importance of N to ecosystem functioning, a decline in available N is likely to have far-reaching consequences. Reduced N availability likely constrains the response of plants to elevated CO 2 and the ability of ecosystems to sequester carbon. Because herbivore growth and reproduction scale with protein intake, declining foliar [N] may be contributing to widely reported declines in insect populations and may be negatively affecting the growth of grazing livestock and herbivorous wild mammals. Spatial and temporal patterns in N availability are not yet fully understood, particularly outside of Europe and North America. Developments in remote sensing, accompanied by additional historical reconstructions of N availability from tree rings, herbarium specimens, and sediments, will show how N availability trajectories vary among ecosystems. Such assessment and monitoring efforts need to be complemented by further experimental and theoretical investigations into the causes of declining N availability, its implications for global carbon sequestration, and how its effects propagate through food webs. Responses will need to involve reducing N demand via lowering atmospheric CO 2 concentrations, and/or increasing N supply. Successfully mitigating and adapting to declining N availability will require a broader understanding that this phenomenon is occurring alongside the more widely recognized issue of anthropogenic eutrophication. Intercalibration of isotopic records from leaves, tree rings, and lake sediments suggests that N availability in many terrestrial ecosystems has steadily declined since the beginning of the industrial era. Reductions in N availability may affect many aspects of ecosystem functioning, including carbon sequestration and herbivore nutrition. Shaded areas indicate 80% prediction intervals; marker size is proportional to the number of measurements in each annual mean. Isotope data: (tree ring) K. K. McLauchlan et al. , Sci. Rep. 7 , 7856 (2017); (lake sediment) G. W. Holtgrieve et al. , Science 334 , 1545–1548 (2011); (foliar) J. M. Craine et al. , Nat. Ecol. Evol. 2 , 1735–1744 (2018) 
    more » « less
  4. Abstract

    The center‐periphery hypothesis predicts a decline in population performance toward the periphery of a species' range, reflecting an alteration of environmental conditions at range periphery. However, the rare demographic tests of this hypothesis failed to disentangle the role of geography from that of ecological niche and are biased toward temperate regions. We hypothesized that, because species are expected to experience optimal abiotic conditions at their climatic niche center, (1) central populations will have better demographic growth, survival, and fertility than peripheral populations. As a result, (2) central populations are expected to have higher growth rates than peripheral populations. Peripheral populations are expected to decline, thus limiting species range expansion beyond these boundaries. Because peripheral populations are expected to be in harsh environmental conditions, (3) population growth rate will be more sensitive to perturbation of survival‐growth rather than fertility in peripheral populations. Finally, we hypothesized that (4) soils properties will drive the variations in population growth rates for narrowly distributed species for which small scale ecological factors could outweigh landscape level drivers. To test these hypotheses, we studied the demography ofThunbergia atacorensis(Acanthaceae), a range‐limited herb in West Africa. We collected three years of demographic data to parameterize an integral projection model (IPM) and estimated population level demographic statistics. Demographic vital rates and population growth rates did not change significantly with distance from geographic or climatic center, contrary to predictions. However, populations at the center of the geographic range were demographically more resilient to perturbation than those at the periphery. Soil nitrogen was the main driver of population growth rate variation. The relative influence of survival‐growth on population growth rates exceeded that of fertility at the geographic range center while we observed the opposite pattern for climatic niche. Our study highlights the importance of local scale processes in shaping the dynamics and distribution of range‐limited species. Our findings also suggest that the distinction between geographic distribution and climatic niche is important for a robust demographic test of the center‐periphery hypothesis.

     
    more » « less
  5. Abstract

    Plant succession is regulated by a combination of abiotic and biotic factors. However, previous studies of biotic drivers have focused overwhelmingly on direct pairwise species interactions, ignoring the likely prevalent higher-order interactions (HOIs) in natural systems. Climate also plays a significant role in determining successional dynamics with both direct effects and indirect effects via altered biotic interactions. Here we explored the relative effects of direct species interactions, HOIs, climate, and their interactions on population dynamics of herbaceous plants during 50 years of post-agricultural secondary succession and tested whether the inclusion of HOIs and climate data improved forecasts of population dynamics. Direct intraspecific interactions were competitive and prevalent across the 90 herbaceous plants examined, while direct interspecific interactions only affected populations of 29% species. HOIs, mainly arose from intraspecific HOIs of conspecifics, were mostly positive and thus largely mitigated the competitive effects of direct intraspecific interactions. Species with lower peak cover experienced stronger intraspecific competition and positive intraspecific HOIs of conspecifics. Direct interspecific interactions had neutral or facilitative effects on species with lower peak cover, and tended to have competitive effects on species with higher peak cover. Climate simultaneously influenced population dynamics both directly and indirectly via altered species interactions. Forecast performance was significantly improved with the inclusion of HOIs or climate for about half and one-third of species, respectively. Our study emphasizes the importance of HOIs, which largely mitigated direct competitive effects on population dynamics of herbaceous plants during succession. Teasing apart HOIs from direct species interactions substantially refined our understanding of successional dynamics of herbaceous plants and improved the accuracy of forecasting population dynamics during succession in a changing world.

     
    more » « less