Root systems are important for global models of below-ground carbon and nutrient cycling. Notoriously difficult sampling methods and the fractal distribution of root diameters in the soil make data being used in these models especially susceptible to error resulting from under-sampling. We applied the concept of species accumulation curves to root data to quantify the extent of under-sampling inherent to minirhizotron and soil coring sampling for both root uptake and carbon content studies. Based on differences in sample size alone, minirhizotron sampling missed approximately one third of the root diameters observed by soil core sampling. Sample volumes needed to encounter 90% of root diameters averaged 2481 cm3 for uptake studies and 5878 cm3 for root carbon content studies. These results show that small sample volumes encounter a non-representative sample of the overall root pool, and provide future guidelines for determining optimal sample volumes in root studies.
The roots of most land plants are colonised by mycorrhizal fungi that provide mineral nutrients in exchange for carbon. Here, we show that mycorrhizal mycelia can also act as a conduit for signalling between plants, acting as an early warning system for herbivore attack. Insect herbivory causes systemic changes in the production of plant volatiles, particularly methyl salicylate, making bean plants, Vicia faba, repellent to aphids but attractive to aphid enemies such as parasitoids. We demonstrate that these effects can also occur in aphid-free plants but only when they are connected to aphid-infested plants via a common mycorrhizal mycelial network. This underground messaging system allows neighbouring plants to invoke herbivore defences before attack. Our findings demonstrate that common mycorrhizal mycelial networks can determine the outcome of multitrophic interactions by communicating information on herbivore attack between plants, thereby influencing the behaviour of both herbivores and their natural enemies.
Evolutionary dead-end strategies are characterized by short-term productivity benefits and long-term evolutionary costs. Here, I detail a real-time dead-end strategy associated with the behavioural traits of lineage progenitors in the social spider Anelosimus studiosus. Specifically, colony lineages founded by docile spiders were eight times more likely to suffer extinction, despite their superior reproductive output. However, when inquilines were experimentally removed from progenitor colonies, differences in extinction probability among lineages vanished. Similarly, among lineages founded by purely docile or aggressive individuals, the descendants of lineages with the highest reproductive output suffered the lowest survivorship, whereas lineages founded by a mixture of docile/aggressive lacked such a trade-off. Finally, lineages with shorter progenitor-descendant distances gained more inquilines and their descendants had lower survivorship, relative to more diffuse lineages. Overall, this study demonstrates how the traits of lineage progenitors and species interactions can unite to determine the fates of entire lineages.
Ecologically mediated selection has increasingly become recognised as an important driver of speciation. The correlation between neutral genetic differentiation and environmental or phenotypic divergence among populations, to which we collectively refer to as isolation-by-ecology (IBE), is an indicator of ecological speciation. In a meta-analysis framework, we determined the strength and commonality of IBE in nature. On the basis of 106 studies, we calculated a mean effect size of IBE with and without controlling for spatial autocorrelation among populations. Effect sizes were 0.34 (95% CI 0.24–0.42) and 0.26 (95% CI 0.13–0.37), respectively, indicating that an average of 5% of the neutral genetic differentiation among populations was explained purely by ecological contrast. Importantly, spatial autocorrelation reduced IBE correlations for environmental variables, but not for phenotypes. Through simulation, we showed how the influence of isolation-by-distance and spatial autocorrelation of ecological variables can result in false positives or underestimated correlations if not accounted for in the IBE model. Collectively, this meta-analysis showed that ecologically induced genetic divergence is pervasive across time-scales and taxa, and largely independent of the choice of molecular marker. We discuss the importance of these results in the context of adaptation and ecological speciation and suggest future research avenues.
Carbon use efficiency (CUE) is a fundamental parameter for ecological models based on the physiology of microorganisms. CUE determines energy and material flows to higher trophic levels, conversion of plant-produced carbon into microbial products and rates of ecosystem carbon storage. Thermodynamic calculations support a maximum CUE value of ~ 0.60 (CUE max). Kinetic and stoichiometric constraints on microbial growth suggest that CUE in multi-resource limited natural systems should approach ~ 0.3 (CUE max/2). However, the mean CUE values reported for aquatic and terrestrial ecosystems differ by twofold (~ 0.26 vs. ~ 0.55) because the methods used to estimate CUE in aquatic and terrestrial systems generally differ and soil estimates are less likely to capture the full maintenance costs of community metabolism given the difficulty of measurements in water-limited environments. Moreover, many simulation models lack adequate representation of energy spilling pathways and stoichiometric constraints on metabolism, which can also lead to overestimates of CUE. We recommend that broad-scale models use a CUE value of 0.30, unless there is evidence for lower values as a result of pervasive nutrient limitations. Ecosystem models operating at finer scales should consider resource composition, stoichiometric constraints and biomass composition, as well as environmental drivers, to predict the CUE of microbial communities.
Dispersal is a key parameter of adaptation, invasion and persistence. Yet standard population genetics inference methods hardly distinguish it from drift and many species cannot be studied by direct mark-recapture methods. Here, we introduce a method using rates of change in cline shapes for neutral markers to estimate contemporary dispersal. We apply it to the devastating banana pest Mycosphaerella fijiensis, a wind-dispersed fungus for which a secondary contact zone had previously been detected using landscape genetics tools. By tracking the spatio-temporal frequency change of 15 microsatellite markers, we find that σ, the standard deviation of parent–offspring dispersal distances, is 1.2 km/generation1/2. The analysis is further shown robust to a large range of dispersal kernels. We conclude that combining landscape genetics approaches to detect breaks in allelic frequencies with analyses of changes in neutral genetic clines offers a powerful way to obtain ecologically relevant estimates of dispersal in many species.
Amid a worldwide increase in tree mortality, mountain pine beetles (Dendroctonus ponderosae Hopkins) have led to the death of billions of trees from Mexico to Alaska since 2000. This is predicted to have important carbon, water and energy balance feedbacks on the Earth system. Counter to current projections, we show that on a decadal scale, tree mortality causes no increase in ecosystem respiration from scales of several square metres up to an 84 km2 valley. Rather, we found comparable declines in both gross primary productivity and respiration suggesting little change in net flux, with a transitory recovery of respiration 6–7 years after mortality associated with increased incorporation of leaf litter C into soil organic matter, followed by further decline in years 8–10. The mechanism of the impact of tree mortality caused by these biotic disturbances is consistent with reduced input rather than increased output of carbon.
Intrinsic processes are assumed to underlie life history expression and trade-offs, but extrinsic inputs are theorised to shift trait expression and mask trade-offs within species. Here, we explore application of this theory across species. We do this based on parentally induced embryo temperature as an extrinsic input, and mass-specific embryo metabolism as an intrinsic process, underlying embryonic development rate. We found that embryonic metabolism followed intrinsic allometry rules among 49 songbird species from temperate and tropical sites. Extrinsic inputs via parentally induced temperatures explained the majority of variation in development rates and masked a relationship with metabolism; metabolism explained a minor proportion of the variation in development rates among species, and only after accounting for temperature effects. We discuss evidence that temperature further obscures the expected interspecific trade-off between development rate and offspring quality. These results demonstrate the importance of considering extrinsic inputs to trait expression and trade-offs across species.
Within the same population, individuals often differ in how they respond to changes in their environment. A recent series of models predicts that competition in a heterogeneous environment might promote between-individual variation in behavioural plasticity. We tested groups of sticklebacks in patchy foraging environments that differed in the level of competition. We also tested the same individuals across two different social groups and while alone to determine the social environment's influence on behavioural plasticity. In support of model predictions, individuals consistently differed in behavioural plasticity when the presence of conspecifics influenced the potential payoffs of a foraging opportunity. Whether individuals maintained their level of behavioural plasticity when placed in a new social group depended on the environmental heterogeneity. By explicitly testing predictions of recent theoretical models, we provide evidence for the types of ecological conditions under which we would expect, and not expect, variation in behavioural plasticity to be favoured.
Understanding the consequences of environmental change on ecological and evolutionary dynamics is inherently problematic because of the complex interplay between them. Using invertebrates in microcosms, we characterise phenotypic, population and evolutionary dynamics before, during and after exposure to a novel environment and harvesting over 20 generations. We demonstrate an evolved change in life-history traits (the age- and size-at-maturity, and survival to maturity) in response to selection caused by environmental change (wild to laboratory) and to harvesting (juvenile or adult). Life-history evolution, which drives changes in population growth rate and thus population dynamics, includes an increase in age-to-maturity of 76% (from 12.5 to 22 days) in the unharvested populations as they adapt to the new environment. Evolutionary responses to harvesting are outweighed by the response to environmental change (~ 1.4 vs. 4% change in age-at-maturity per generation). The adaptive response to environmental change converts a negative population growth trajectory into a positive one: an example of evolutionary rescue.
Stoichiometric homeostasis of heterotrophs is a common, but not always well-examined premise in ecological stoichiometry. We experimentally evaluated the relationship between substrate (plant litter) and consumer (microorganisms) stoichiometry for a tropical terrestrial decomposer system. Variation in microbial C : P and N : P ratios tracked that of the soluble litter fraction, but not that of bulk leaf litter material. Microbial N and P were not isometrically related, suggesting higher rates of P than N sequestration in microbial biomass. Shifts in microbial stoichiometry were related to changes in microbial community structure. Our results indicate that P in dissolved form is a major driver of terrestrial microbial stoichiometry, similar to aquatic environments. The demonstrated relative plasticity in microbial C : P and N : P and the critical role of P have important implications for theoretical modelling and contribute to a process-based understanding of stoichiometric relationships and the flow of elements across trophic levels in decomposer systems.
We estimated the latitudinal velocity (km/decade) of northern and southern boundaries of core distributions for 30 woody taxa over the last 16 000 years (biotic velocities) using networks of fossil pollen records, and compared these with climate velocities estimated from CCSM3 simulations. Biotic velocities were faster during periods of rapid temperature change (i.e. 16 to 7 ka) than times of relative stability (i.e. 7 to 1 ka), with a consistent northward movement of northern and southern boundaries. For most taxa, biotic velocities were faster for northern than for southern boundaries between 12 and 7 ka, resulting in expanding distributions. For individual time periods, biotic velocities were as fast or faster than climate velocities calculated using multivariate approaches. These results indicate that climate change paced the rate of distribution shifts in both northern and southern populations while suggesting that northern populations were more sensitive. A similar sensitivity and pacing is expected under 21st century climate change.
The rate of biological invasions has strongly increased during the last decades, mostly due to the accelerated spread of species by increasing global trade and transport. Here, we combine the network of global cargo ship movements with port environmental conditions and biogeography to quantify the probability of new primary invasions through the release of ballast water. We find that invasion risks vary widely between coastal ecosystems and classify marine ecoregions according to their total invasion risk and the diversity of their invasion sources. Thereby, we identify high-risk invasion routes, hot spots of bioinvasion and major source regions from which bioinvasion is likely to occur. Our predictions agree with observations in the field and reveal that the invasion probability is highest for intermediate geographic distances between donor and recipient ports. Our findings suggest that network-based invasion models may serve as a basis for the development of effective, targeted bioinvasion management strategies.
Plant–herbivore interactions vary across the landscape and have been hypothesised to promote local adaption in plants to the prevailing herbivore regime. Herbivores that feed on European aspen (Populus tremula) change across regional scales and selection on host defence genes may thus change at comparable scales. We have previously observed strong population differentiation in a set of inducible defence genes in Swedish P. tremula. Here, we study the geographic patterns of abundance and diversity of herbivorous insects, the untargeted metabolome of the foliage and genetic variation in a set of wound-induced genes and show that the geographic structure co-occurs in all three data sets. In response to this structure, we observe local maladaptation of herbivores, with fewer herbivores on local trees than on trees originated from more distant localities. Finally, we also identify 28 significant associations between single nucleotide polymorphisms SNPs from defence genes and a number of the herbivore traits and metabolic profiles.
Experimental studies assessing climatic effects on ecological communities have typically applied static warming treatments. Although these studies have been informative, they have usually failed to incorporate either current or predicted future, patterns of variability. Future climates are likely to include extreme events which have greater impacts on ecological systems than changes in means alone. Here, we review the studies which have used experiments to assess impacts of temperature on marine, freshwater and terrestrial communities, and classify them into a set of ‘generations’ based on how they incorporate variability. The majority of studies have failed to incorporate extreme events. In terrestrial ecosystems in particular, experimental treatments have reduced temperature variability, when most climate models predict increased variability. Marine studies have tended to not concentrate on changes in variability, likely in part because the thermal mass of oceans will moderate variation. In freshwaters, climate change experiments have a much shorter history than in the other ecosystems, and have tended to take a relatively simple approach. We propose a new ‘generation’ of climate change experiments using down-scaled climate models which incorporate predicted changes in climatic variability, and describe a process for generating data which can be applied as experimental climate change treatments.
Probiotic therapy through bioaugmentation is a feasible disease mitigation strategy based on growing evidence that microbes contribute to host defences of plants and animals. Amphibians are currently threatened by the rapid global spread of the pathogen, Batrachochytrium dendrobatidis (Bd), which causes the disease chytridiomycosis. Bioaugmentation of locally occurring protective bacteria on amphibians has mitigated this disease effectively in laboratory trials and one recent field trial. Areas still naïve to Bd provide an opportunity for conservationists to proactively implement probiotic strategies to prevent further amphibian declines. In areas where Bd is endemic, bioaugmentation can facilitate repatriation of susceptible amphibians currently maintained in assurance colonies. Here, we synthesise the current research in amphibian microbial ecology and bioaugmentation to identify characteristics of effective probiotics in relation to their interactions with Bd, their host, other resident microbes and the environment. To target at-risk species and amphibian communities, we develop sampling strategies and filtering protocols that result in probiotics that inhibit Bd under ecologically relevant conditions and persist on susceptible amphibians. This filtering tool can be used proactively to guide amphibian disease mitigation and can be extended to other taxa threatened by emerging infectious diseases.
Biological invasions depend in part on the resistance of native communities. Meta-analyses of terrestrial experiments demonstrate that native primary producers and herbivores generally resist invasions of primary producers, and that resistance through competition strengthens with native producer diversity. To test the generality of these findings, we conducted a meta-analysis of marine experiments. We found that native marine producers generally failed to resist producer invasions through competition unless the native community was diverse, and this diversity effect was weaker in marine than in terrestrial systems. In contrast, native consumers equally resisted invasive producers in both ecosystems. Most marine experiments, however, tested invasive consumers and these invasions were resisted more strongly than were producer invasions. Given these differences between ecosystems and between marine trophic levels, we used a model-selection approach to assess if factors other than the resistance mechanism (i.e. competition vs. consumption) are more important for predicting marine biotic resistance. These results suggest that understanding marine biotic resistance depends on latitude, habitat and invader taxon, in addition to distinguishing between competition with and consumption by native species. By examining biotic resistance within and across ecosystems, our work provides a more complete understanding of the factors that underlie biological invasions.