Proximate causes and consequences of intergenerational influences of salient sensory experience

Salient sensory environments experienced by a parental generation can exert intergenerational influences on offspring. While these data provide an exciting new perspective on biological inheritance, questions remain about causes and consequences of intergenerational influences of salient sensory experience. We previously showed that exposing male mice to a salient olfactory experience, like olfactory fear conditioning, resulted in offspring demonstrating a sensitivity to the odor used to condition the paternal generation and possessing enhanced neuroanatomical representation for that odor. In this study, we first injected RNA extracted from sperm of male mice that underwent olfactory fear conditioning into naïve single‐cell zygotes and found that adults that developed from these embryos had increased sensitivity and enhanced neuroanatomical representation for the odor (Odor A) with which the paternal male had been conditioned. Next, we found that female, but not male offspring sired by males conditioned with Odor A show enhanced consolidation of a weak single‐trial Odor A + shock fear conditioning protocol. Our data provide evidence that RNA found in the paternal germline after exposure to salient sensory experiences can contribute to intergenerational influences of such experiences, and that such intergenerational influences confer an element of adaptation to the offspring. In so doing, our study of intergenerational influences of parental sensory experience adds to existing literature on intergenerational influences of parental exposures to stress and dietary manipulations and suggests that some causes (sperm RNA) and consequences (behavioral flexibility) of intergenerational influences of parental experiences may be conserved across a variety of parental experiences.     

Threshold responses of riverine fish communities to land use conversion across regions of the world

The growing human enterprise has sparked greater interest in identifying ecological thresholds in land use conversion beyond which populations or communities demonstrate abrupt nonlinear or substantive change in species composition. Such knowledge remains fundamental to understanding ecosystem resilience to environmental degradation and informing land use planning into the future. Confronting this challenge has been largely limited to inferring thresholds in univariate metrics of species richness and indices of biotic integrity and has largely ignored how land use legacies of the past may shape community responses of today. By leveraging data for 13,069 riverine sites from temperate, subtropical, and boreal climate zones on four continents, we characterize patterns of community change along diverse gradients of urbanization and agricultural land use, and identity threshold values beyond which significant alterations in species composition exists. Our results demonstrate the apparent universality by which freshwater fish communities are sensitive to even low levels of watershed urbanization (range of threshold values: 1%–12%), but consistently higher (and more variable) levels of agricultural development (2%–37%). We demonstrated that fish community compositional thresholds occurred, in general, at lower levels of watershed urbanization and agriculture when compared to threshold responses in species richness. This supports the notion that aggregated taxon‐specific responses may better reflect the complexity of assemblage responses to land use development. We further revealed that the ghost of land use past plays an important role in moderating how current‐day fish communities respond to land use intensification. Subbasins of the United States experiencing greater rates of past land use change demonstrated higher current‐day thresholds. Threshold responses of community composition, such as those identified in our study, illustrate the need for globally coordinated efforts to prioritize country‐specific management and policy initiatives that ensure that freshwater fish diversity is not inevitably lost in the future.     

Disturbance persistence in managed grasslands: shifts in aboveground community structure and the weed seed bank

The length of time and form in which disturbances persist in systems depends on the intensity and frequency of disturbance and on the abilities of resident species to recover from such events. In grazed grasslands, trampling by large mammalian herbivores can periodically facilitate weed establishment by exposing patches of bare ground but whether an intense soil disturbance event results in a temporary increase in weed abundance or a persistent weed problem remains unclear. In May 2002, cattle trampling following heavy rain caused severe damage to nine-month old, rotationally grazed, cool-season pastures (Midwest USA). In September 2002, we compared the aboveground composition of paddocks (i.e., fenced pasture sections) that were heavily disturbed to those that received no damage. Relative to undisturbed paddocks, forage species relative cover was 17% lower in disturbed paddocks, and weed species and bare ground relative cover was 61% and 100% higher, respectively. By September 2004, paddock types did not differ in all aboveground community components. However, the abundance and species richness of weed seeds in the soil seed bank averaged respectively 82% and 30% higher in disturbed paddocks between 2003 and 2004. These findings indicate that a spatially extensive, intense soil disturbance event may soon become undetectable in components of aboveground pasture structure but can persist as an augmented weed seed bank. Because of high weed seed bank longevity, disturbances to formerly disturbed pastures would likely result in higher weed recruitment, with more species represented, than in those which lack previous disturbance. Disturbance history may thus be a useful predictor of weed community composition following subsequent disturbance. Based on empirical data supporting this proposition, we recommend that grassland managers explicitly incorporate disturbance history into dynamic management planning and do not rely exclusively on aboveground characters to evaluate the invasion status or colonization potential of an area by undesirable plants. We emphasize that the ecological legacies of past soil disturbance events cannot only influence the contemporary patterns and processes of grasslands, but importantly, affect their compositional trajectories following subsequent perturbation.     

Individualistic responses of forest herb traits to environmental change

• Intraspecific trait variation (ITV; i.e. variability in mean and/or distribution of plant attribute values within species) can occur in response to multiple drivers. Environmental change and land‐use legacies could directly alter trait values within species but could also affect them indirectly through changes in vegetation cover. Increasing variability in environmental conditions could lead to more ITV, but responses might differ among species. Disentangling these drivers on ITV is necessary to accurately predict plant community responses to global change.
• We planted herb communities into forest soils with and without a recent history of agriculture. Soils were collected across temperate European regions, while the 15 selected herb species had different colonizing abilities and affinities to forest habitat. These mesocosms (384) were exposed to two‐level full‐factorial treatments of warming, nitrogen addition and illumination. We measured plant height and specific leaf area (SLA).
• For the majority of species, mean plant height increased as vegetation cover increased in response to light addition, warming and agricultural legacy. The coefficient of variation (CV) for height was larger in fast‐colonizing species. Mean SLA for vernal species increased with warming, while light addition generally decreased mean SLA for shade‐tolerant species. Interactions between treatments were not important predictors.
• Environmental change treatments influenced ITV, either via increasing vegetation cover or by affecting trait values directly. Species’ ITV was individualistic, i.e. species responded to different single resource and condition manipulations that benefited their growth in the short term. These individual responses could be important for altered community organization after a prolonged period.

     

Landscape host abundance and configuration regulate periodic outbreak behavior in spruce budworm Choristoneura fumiferana

Landscape‐level forest management has long been hypothesized to affect forest insect outbreak dynamics, but empirical evidence remains elusive. We hypothesized that the combination of increased hardwood relative to host tree species, prevalence of younger forests, and fragmentation of those forests due to forest harvesting legacies would reduce outbreak intensity, increase outbreak frequency, and decrease spatial synchrony in spruce budworm Choristoneura fumiferana outbreaks. We investigated these hypotheses using tree ring samples collected across 51 sites pooled into 16 subareas distributed across a large ecoregion spanning the international border between Ontario (Canada), and Minnesota (USA). This ecoregion contains contrasting land management zones with clear differences in forest landscape structure (i.e. forest composition and spatial configuration) while minimizing the confounding influence of climate. Cluster analyses of the 76‐yr time‐series generally grouped by subareas found within the same land management zone. Spatial nonparametric covariance analysis indicated that the highest and lowest degree of spatial synchrony of spruce budworm outbreaks were found within unmanaged wilderness and lands managed at fine spatial scales in Minnesota, respectively. Using multivariate analysis, we also found that forest composition, configuration, and climate together accounted for a total of 40% of the variance in outbreak chronologies, with a high level of shared variance between composition and configuration (13%) and between composition and climate (9%). At the scale of our study, climate on its own did not explain any of the spatial variation in outbreaks. Outbreaks were of higher frequency, lower intensity, and less spatially synchronized in more fragmented, younger forests with a lower proportion of host species, with opposing outbreak characteristics observed in regions characterised by older forests with more concentrated host species. Our study is the first quantitative evaluation of the long‐standing ‘silvicultural hypothesis’ of spruce budworm management specifically conducted at a spatio‐temporal scale for which it was intended.     

Large‐scale disturbance legacies and the climate sensitivity of primary Picea abies forests

Determining the drivers of shifting forest disturbance rates remains a pressing global change issue. Large‐scale forest dynamics are commonly assumed to be climate driven, but appropriately scaled disturbance histories are rarely available to assess how disturbance legacies alter subsequent disturbance rates and the climate sensitivity of disturbance. We compiled multiple tree ring‐based disturbance histories from primary Picea abies forest fragments distributed throughout five European landscapes spanning the Bohemian Forest and the Carpathian Mountains. The regional chronology includes 11,595 tree cores, with ring dates spanning the years 1750–2000, collected from 560 inventory plots in 37 stands distributed across a 1,000 km geographic gradient, amounting to the largest disturbance chronology yet constructed in Europe. Decadal disturbance rates varied significantly through time and declined after 1920, resulting in widespread increases in canopy tree age. Approximately 75% of current canopy area recruited prior to 1900. Long‐term disturbance patterns were compared to an historical drought reconstruction, and further linked to spatial variation in stand structure and contemporary disturbance patterns derived from LANDSAT imagery. Historically, decadal Palmer drought severity index minima corresponded to higher rates of canopy removal. The severity of contemporary disturbances increased with each stand's estimated time since last major disturbance, increased with mean diameter, and declined with increasing within‐stand structural variability. Reconstructed spatial patterns suggest that high small‐scale structural variability has historically acted to reduce large‐scale susceptibility and climate sensitivity of disturbance. Reduced disturbance rates since 1920, a potential legacy of high 19th century disturbance rates, have contributed to a recent region‐wide increase in disturbance susceptibility. Increasingly common high‐severity disturbances throughout primary Picea forests of Central Europe should be reinterpreted in light of both legacy effects (resulting in increased susceptibility) and climate change (resulting in increased exposure to extreme events).     

The Effects of Spatial Legacies following Shifting Management Practices and Fire on Boreal Forest Age Structure

Forest age structure and its spatial arrangement are important elements of sustainable forestry because of their effects on biodiversity and timber availability. Forest management objectives that include specific forest age structure may not be easily attained due to constraints imposed by the legacies of historical management and natural disturbance. We used a spatially explicit stochastic model to explore the synergetic effects of forest management and fire on boreal forest age structure. Specifically, we examined (1) the duration of spatial legacies of different management practices in the boreal forest, (2) how multiple shifts in management practices affect legacy duration and the spatial trajectories of forest age structure, and (3) how fire influences legacy duration and pattern development in combination with harvesting. Results based on 30 replicates of 500 years for each scenario indicate that (1) spatial legacies persist over 200 years and the rate at which legacies are overcome depends on whether new management targets are in synchrony with existing spatial pattern; (2) age specific goals were met faster after multiple management shifts due to the similar spatial scale of the preceding management types; (3) because large fires can erase the spatial pattern created by smaller disturbances, scenarios with fire had shorter lags than scenarios without fire. These results suggest that forest management goals can be accelerated by applying management at a similar spatial scale as existing spatial patterns. Also, management planning should include careful consideration of historical management as well as current and likely future disturbances.     

Legacies of La Niña: North American monsoon can rescue trees from winter drought

While we often assume tree growth–climate relationships are time‐invariant, impacts of climate phenomena such as the El Niño Southern Oscillation (ENSO) and the North American Monsoon (NAM) may challenge this assumption. To test this assumption, we grouped ring widths (1900‐present) in three southwestern US conifers into La Niña periods (LNP) and other years (OY). The 4 years following each La Niña year are included in LNP, and despite 1–2 year growth declines, compensatory adjustments in tree growth responses result in essentially equal mean growth in LNP and OY, as average growth exceeds OY means 2–4 years after La Niña events. We found this arises because growth responses in the two periods are not interchangeable: Due to differences in growth–climate sensitivities and climatic memory, parameters representing LNP growth fail to predict OY growth and vice versa (decreases in R² up to 0.63; lowest R² = 0.06). Temporal relationships between growth and antecedent climate (memory) show warmer springs and longer growing seasons negatively impact growth following dry La Niña winters, but that NAM moisture can rescue trees after these events. Increased importance of monsoonal precipitation during LNP is key, as the largest La Niña‐related precipitation deficits and monsoonal precipitation contributions both occur in the southern part of the region. Decreases in first order autocorrelation during LNP were largest in the heart of the monsoon region, reflecting both the greatest initial growth declines and the largest recovery. Understanding the unique climatic controls on growth in Southwest conifers requires consideration of both the influences and interactions of drought, ENSO, and NAM, each of which is likely to change with continued warming. While plasticity of growth sensitivity and memory has allowed relatively quick recovery in the tree‐ring record, recent widespread mortality events suggest conditions may soon exceed the capacity for adjustment in current populations.     

Fire legacies in eastern ponderosa pine forests

Disturbance legacies structure communities and ecological memory, but due to increasing changes in disturbance regimes, it is becoming more difficult to characterize disturbance legacies or determine how long they persist. We sought to quantify the characteristics and persistence of material legacies (e.g., biotic residuals of disturbance) that arise from variation in fire severity in an eastern ponderosa pine forest in North America. We compared forest stand structure and understory woody plant and bird community composition and species richness across unburned, low‐, moderate‐, and high‐severity burn patches in a 27‐year‐old mixed‐severity wildfire that had received minimal post‐fire management. We identified distinct tree densities (high: 14.3 ± 7.4 trees per ha, moderate: 22.3 ± 12.6, low: 135.3 ± 57.1, unburned: 907.9 ± 246.2) and coarse woody debris cover (high: 8.5 ± 1.6% cover per 30 m transect, moderate: 4.3 ± 0.7, low: 2.3 ± 0.6, unburned: 1.0 ± 0.4) among burn severities. Understory woody plant communities differed between high‐severity patches, moderate‐ and low‐severity patches, and unburned patches (all p < 0.05). Bird communities differed between high‐ and moderate‐severity patches, low‐severity patches, and unburned patches (all p < 0.05). Bird species richness varied across burn severities: low‐severity patches had the highest (5.29 ± 1.44) and high‐severity patches had the lowest (2.87 ± 0.72). Understory woody plant richness was highest in unburned (5.93 ± 1.10) and high‐severity (5.07 ± 1.17) patches, and it was lower in moderate‐ (3.43 ± 1.17) and low‐severity (3.43 ± 1.06) patches. We show material fire legacies persisted decades after the mixed‐severity wildfire in eastern ponderosa forest, fostering distinct structures, communities, and species in burned versus unburned patches and across fire severities. At a patch scale, eastern and western ponderosa system responses to mixed‐severity fires were consistent.