Trait-mediated assembly processes predict successional changes in community diversity of tropical forests

Interspecific differences in relative fitness can cause local dominance by a single species. However, stabilizing interspecific niche differences can promote local diversity. Understanding these mechanisms requires that we simultaneously quantify their effects on demography and link these effects to community dynamics. Successional forests are ideal systems for testing assembly theory because they exhibit rapid community assembly. Here, we leverage functional trait and long-term demographic data to build spatially explicit models of successional community dynamics of lowland rainforests in Costa Rica. First, we ask what the effects and relative importance of four trait-mediated community assembly processes are on tree survival, a major component of fitness. We model trait correlations with relative fitness differences that are both density-independent and -dependent in addition to trait correlations with stabilizing niche differences. Second, we ask how the relative importance of these trait-mediated processes relates to successional changes in functional diversity. Tree dynamics were more strongly influenced by trait-related interspecific variation in average survival than trait-related responses to neighbors, with wood specific gravity (WSG) positively correlated with greater survival. Our findings also suggest that competition was mediated by stabilizing niche differences associated with specific leaf area (SLA) and leaf dry matter content (LDMC). These drivers of individual-level survival were reflected in successional shifts to higher SLA and LDMC diversity but lower WSG diversity. Our study makes significant advances to identifying the links between individual tree performance, species functional traits, and mechanisms of tropical forest succession.Quantifying the relative importance of mechanisms that drive community assembly remains a central challenge in ecology. Interspecific variation in ecological strategies is considered a major driver of community assembly and has been classified by Chesson (1) into relative fitness (i.e., per capita population growth rate) differences and stabilizing niche differences (2). These processes act concurrently, and their importance may vary over space and time (3). However, the simultaneous effects of different assembly mechanisms on community dynamics have not been well-characterized, particularly in diverse communities such as tropical forests. High dynamism of vegetation composition during tropical forest succession creates an ideal opportunity to investigate the drivers of community assembly.Interspecific niche and fitness differences can be characterized through the lens of interspecific functional trait variation, an approach that can shed light on drivers of community functional composition and dynamics (2, 4, 5). Traits may mediate niche and fitness differences in at least four ways (Fig. 1). First, interspecific trait variation can be correlated with fitness independent of neighbor density, such that species possessing traits associated with the highest fitness should exclude species with unfavorable traits (1, 2) (1 in Fig. 1). Second, traits may be associated with a species’ sensitivity to neighbor density (i.e., a trait × crowding interaction effect on fitness). As a result, certain trait values may have relatively low fitness under high crowding (6–9) (2 in Fig. 1). For example, species with low wood specific gravity (WSG) might have higher fitness at the initiation of succession but be disadvantaged later in succession because of sensitivity to crowding. Third, negative density effects of neighbors may be asymmetric between species and dependent on hierarchies (i.e., species with favorable traits experience weaker negative density effects of neighbors with unfavorable traits, generating relative fitness differences) (10) (3 in Fig. 1). For example, species with high WSG may have stronger negative density effects on neighbors with low WSG than vice versa (10). Fourth, trait variation may be related to local niche differences between neighbors, such that greater trait differences weaken negative density effects of neighbors and promote stable coexistence of functionally diverse neighbors (11, 12) (4 in Fig. 1). Overall, traits associated with fitness differences (1–3 in Fig. 1) are expected to decrease in diversity over time, whereas traits associated with stabilizing niche differences (4 in Fig. 1) are expected to increase in diversity, assuming no trait bias in immigration. Gaining a more nuanced, complete, and predictive understanding of community assembly requires that we quantify the effects of these assembly processes on species demography and the associated changes at the community level (13, 14).Open in a separate windowFig. 1.Illustration of the four mechanisms of trait-mediated assembly included in our models. Assembly may be driven by species differences in (1) survival independent of crowding by neighbors, (2) response to increased crowding, (3) competitive hierarchies, and (4) local niche. All four processes may be revealed through the lens of functional trait variation (the spectrum from yellow to green) and its effects on mortality (black Xs). Note that the color schemes are not meant to be mutually compatible. In 1, the green color is associated with greater fitness (e.g., because of higher survival) compared with yellow, independent of neighborhood crowding. (2) Green traits have lower sensitivity to crowding relative to yellow traits (irrespective of neighbors'' traits, which are shown in gray). (3) Species have trait hierarchies. Here, green is dominant (i.e., greener species always have greater negative effect on the performance of yellower neighbors than vice versa). (a) Because their traits are very different, the green species has a stronger competitive effect on the yellow species compared with (b) the competitive effect of the yellow-green species on the yellow species. (4) In contrast, when trait variation is associated with stabilizing niche differences between neighbors, negative density effects are experienced similarly by both species. (a) Neighbors with greater trait-associated niche difference (green vs. yellow) have a weaker competitive effect relative to (b) species with less difference in traits (green vs. yellow-green).Successional tropical forests exhibit rapid community assembly and thus, provide an ideal system for testing assembly theory (15). High species richness and elevated tree growth and mortality rates relative to old-growth forests contribute to rapid species turnover and increase the likelihood of detecting assembly processes across succession (16). As succession proceeds, increased crowding alters local resource availability, which may drive species turnover (17–19). Early successional forests are typically dominated by species with acquisitive traits, such as low WSG and high specific leaf area (SLA), which enable rapid growth, resource capture, and high fitness under conditions of high resource availability (17, 20, 21). In contrast, traits that tend to dominate older forests [e.g., dense wood and tough leaves (22, 23)] are thought to promote long-term survival and fitness under high crowding and low resource availability (17, 24). Trait diversity is also expected to change as succession proceeds, although the direction and mechanisms of diversity changes remain unclear (23). Despite considerable previous efforts, few researchers have tested these hypotheses using demographic data in diverse systems.We use a long-term dataset of tropical forest succession to disentangle how trait-mediated processes drive community dynamics. Spatially explicit longitudinal studies of individual performance offer a powerful approach to reveal drivers of community dynamics (9, 12, 14, 25–27). Empirical studies of functional community assembly have typically compared static community patterns across sites using aggregated trait metrics (28–30). These studies assume that community patterns are the result of prior assembly processes. However, static and aggregated patterns provide limited capability to distinguish between multiple, often opposing assembly processes (14, 31).Our novel approach simultaneously quantifies the relative importance of multiple assembly processes and links these processes to contrasting effects on functional diversity. We use trait data for over 200 tree species, and we develop spatially explicit statistical models of tree survival over 15 y across eight 1-ha forest plots at diverse stages of succession in lowland wet forests of Costa Rica (SI Appendix, Table S1). We ask three central questions about trait-mediated effects on tree survival rates, a major component of fitness, and successional community dynamics.

• i)What are the simultaneous effects and relative importance of four trait-mediated assembly processes on tree survival? Specifically, we ask four subquestions about the processes.
  • i.i) How are functional traits related to interspecific variation in average survival?
  • i.ii) How do trait relationships with survival change with variation in neighborhood crowding?
  • i.iii) Do competitive interactions depend on trait hierarchy, indicating that crowding effects are based on dominance?
  • i.iv) Do competitive interactions with neighbors depend on absolute trait differences between neighbors, suggesting stabilizing niche differences?
• ii)Is the demographic evidence for trait-mediated fitness and niche differences (i) reflected in community-level changes in trait diversity across successional stages? We expect that traits associated with relative fitness (i.e., associated with greater average survival, decreased sensitivity to crowding, and hierarchical dominance) will decrease in diversity over time, whereas traits associated with stabilizing niche differences will increase in diversity during forest succession.
• iii)Is the demographic evidence for trait-mediated fitness differences reflected in functional differences between second-growth specialists and old-growth specialists? We expect that traits associated with greater relative fitness will be more strongly associated with old-growth specialists compared with second-growth specialists.

To answer these questions, we built hierarchical Bayes models of community-wide stem survival, which include parameters for each assembly process in questions i.i–i.iv (12, 27) (details in Methods). We fit models for each of three functional traits associated with resource use and life history: SLA (defined as leaf area per unit dry mass), leaf dry matter content (LDMC; defined as leaf dry mass over leaf fresh mass), and WSG (defined as the density of wood relative to the density of water). These traits represent leading axes of ecological variation among tropical tree species that have been previously implicated in interspecific variation in resource use efficiency, species interactions, and life history strategies (32–34). SLA represents a major axis of variation between rapid resource acquisition for species with high SLA vs. conservative strategies with low tissue turnover for species with low SLA (32, 35). Species with high LDMC have lower leaf protein and reduced ability to exploit resource-rich environments but better performance under low resources and drought (7, 34, 36, 37). WSG is associated with a tradeoff between rapid growth rates for species with low WSG and high structural support and resistance to natural enemies for species with high WSG (9, 33).     

Blood–spinal cord barrier disruption contributes to early motor-neuron degeneration in ALS-model mice

Humans with ALS and transgenic rodents expressing ALS-associated superoxide dismutase (SOD1) mutations develop spontaneous blood–spinal cord barrier (BSCB) breakdown, causing microvascular spinal-cord lesions. The role of BSCB breakdown in ALS disease pathogenesis in humans and mice remains, however, unclear, although chronic blood–brain barrier opening has been shown to facilitate accumulation of toxic blood-derived products in the central nervous system, resulting in secondary neurodegenerative changes. By repairing the BSCB and/or removing the BSCB-derived injurious stimuli, we now identify that accumulation of blood-derived neurotoxic hemoglobin and iron in the spinal cord leads to early motor-neuron degeneration in SOD1^G93A mice at least in part through iron-dependent oxidant stress. Using spontaneous or warfarin-accelerated microvascular lesions, motor-neuron dysfunction and injury were found to be proportional to the degree of BSCB disruption at early disease stages in SOD1^G93A mice. Early treatment with an activated protein C analog restored BSCB integrity that developed from spontaneous or warfarin-accelerated microvascular lesions in SOD1^G93A mice and eliminated neurotoxic hemoglobin and iron deposits. Restoration of BSCB integrity delayed onset of motor-neuron impairment and degeneration. Early chelation of blood-derived iron and antioxidant treatment mitigated early motor-neuronal injury. Our data suggest that BSCB breakdown contributes to early motor-neuron degeneration in ALS mice and that restoring BSCB integrity during an early disease phase retards the disease process.The blood–brain barrier (BBB) and blood–spinal cord barrier (BSCB) prevent entry of toxic circulating molecules and cells into the central nervous system (CNS) (1). Amyotrophic lateral sclerosis (ALS) is the most prominent adult motor-neuron disorder resulting in progressive motor-neuron loss in the spinal cord, brainstem, and motor cortex (2). Most ALS cases are sporadic (90%) whereas 10% are familial ALS. Over twenty independent studies in postmortem human tissue and cerebrospinal fluid (CSF) sampling from living ALS patients have established that the BBB and BSCB are damaged in familial and sporadic ALS, as reviewed elsewhere (1, 3). This BBB and BSCB disruption has been shown by spinal-cord and/or motor-cortex accumulation of different plasma proteins (e.g., IgG, fibrin, thrombin), erythrocytes, erythrocyte-derived hemoglobin and iron-containing hemosiderin, elevated CSF/serum albumin ratios, and diminished expression or degradation of the BSCB tight-junction proteins (1, 3–5). Deposition of hemoglobin-derived iron within the CNS has also been shown in ALS patients (3, 6, 7). Because human postmortem studies reflect, however, end-stage disease, it has remained unclear as to which stage of disease is enhanced by BSCB disruption. Longitudinal CSF or BSCB imaging studies have yet to be performed in living ALS patients (3) to clarify whether spinal-cord vascular dysfunction contributes to early- or late-stage disease.Transgenic rodents expressing human ALS-associated Cu/Zn superoxide dismutase (SOD1) mutations that represent 20% of all familial cases also develop a spontaneous BBB/BSCB disruption (8–12) similar to vascular pathology reported in humans (1, 3–7). Mice with a chronic BBB disruption due to aberrant signal transduction between the central nervous system endothelial cells and pericytes or astrocytes and pericytes develop a chronic BBB opening accompanied by accumulation of toxic blood-derived products in the central nervous system and secondary functional and structural neuronal changes (13–15).To determine whether BSCB disruption contributes to fatal paralytic disease caused by expression of an ALS-causing mutant, we now report how perturbing the BSCB, repairing the BSCB, and/or removing the BSCB-derived injurious stimuli influence development of disease in SOD1^G93A mice that develop a spontaneous BSCB breakdown (8, 9, 12).     

Heme-protein vibrational couplings in cytochrome c provide a dynamic link that connects the heme-iron and the protein surface

The active site of cytochrome c (Cyt c) consists of a heme covalently linked to a pentapeptide segment (Cys-X-X-Cys-His), which provides a link between the heme and the protein surface, where the redox partners of Cyt c bind. To elucidate the vibrational properties of heme c, nuclear resonance vibrational spectroscopy (NRVS) measurements were performed on (57)Fe-labeled ferric Hydrogenobacter thermophilus cytochrome c(552), including (13)C(8)-heme-, (13)C(5)(15)N-Met-, and (13)C(15)N-polypeptide (pp)-labeled samples, revealing heme-based vibrational modes in the 200- to 450-cm(-1) spectral region. Simulations of the NRVS spectra of H. thermophilus cytochrome c(552) allowed for a complete assignment of the Fe vibrational spectrum of the protein-bound heme, as well as the quantitative determination of the amount of mixing between local heme vibrations and pp modes from the Cys-X-X-Cys-His motif. These results provide the basis to propose that heme-pp vibrational dynamic couplings play a role in electron transfer (ET) by coupling vibrations of the heme directly to vibrations of the pp at the protein-protein interface. This could allow for the direct transduction of the thermal (vibrational) energy from the protein surface to the heme that is released on protein/protein complex formation, or it could modulate the heme vibrations in the protein/protein complex to minimize reorganization energy. Both mechanisms lower energy barriers for ET. Notably, the conformation of the distal Met side chain is fine-tuned in the protein to localize heme-pp mixed vibrations within the 250- to 400-cm(-1) spectral region. These findings point to a particular orientation of the distal Met that maximizes ET.     

Timing of climate variability and grassland productivity

Future climates are forecast to include greater precipitation variability and more frequent heat waves, but the degree to which the timing of climate variability impacts ecosystems is uncertain. In a temperate, humid grassland, we examined the seasonal impacts of climate variability on 27 y of grass productivity. Drought and high-intensity precipitation reduced grass productivity only during a 110-d period, whereas high temperatures reduced productivity only during 25 d in July. The effects of drought and heat waves declined over the season and had no detectable impact on grass productivity in August. If these patterns are general across ecosystems, predictions of ecosystem response to climate change will have to account not only for the magnitude of climate variability but also for its timing.     

Detection of ultra-rare mutations by next-generation sequencing

Next-generation DNA sequencing promises to revolutionize clinical medicine and basic research. However, while this technology has the capacity to generate hundreds of billions of nucleotides of DNA sequence in a single experiment, the error rate of ～1% results in hundreds of millions of sequencing mistakes. These scattered errors can be tolerated in some applications but become extremely problematic when "deep sequencing" genetically heterogeneous mixtures, such as tumors or mixed microbial populations. To overcome limitations in sequencing accuracy, we have developed a method termed Duplex Sequencing. This approach greatly reduces errors by independently tagging and sequencing each of the two strands of a DNA duplex. As the two strands are complementary, true mutations are found at the same position in both strands. In contrast, PCR or sequencing errors result in mutations in only one strand and can thus be discounted as technical error. We determine that Duplex Sequencing has a theoretical background error rate of less than one artifactual mutation per billion nucleotides sequenced. In addition, we establish that detection of mutations present in only one of the two strands of duplex DNA can be used to identify sites of DNA damage. We apply the method to directly assess the frequency and pattern of random mutations in mitochondrial DNA from human cells.     

Lead poisoning and the deceptive recovery of the critically endangered California condor

Endangered species recovery programs seek to restore populations to self-sustaining levels. Nonetheless, many recovering species require continuing management to compensate for persistent threats in their environment. Judging true recovery in the face of this management is often difficult, impeding thorough analysis of the success of conservation programs. We illustrate these challenges with a multidisciplinary study of one of the world's rarest birds-the California condor (Gymnogyps californianus). California condors were brought to the brink of extinction, in part, because of lead poisoning, and lead poisoning remains a significant threat today. We evaluated individual lead-related health effects, the efficacy of current efforts to prevent lead-caused deaths, and the consequences of any reduction in currently intensive management actions. Our results show that condors in California remain chronically exposed to harmful levels of lead; 30% of the annual blood samples collected from condors indicate lead exposure (blood lead ≥ 200 ng/mL) that causes significant subclinical health effects, measured as >60% inhibition of the heme biosynthetic enzyme δ-aminolevulinic acid dehydratase. Furthermore, each year, ～20% of free-flying birds have blood lead levels (≥450 ng/mL) that indicate the need for clinical intervention to avert morbidity and mortality. Lead isotopic analysis shows that lead-based ammunition is the principle source of lead poisoning in condors. Finally, population models based on condor demographic data show that the condor's apparent recovery is solely because of intensive ongoing management, with the only hope of achieving true recovery dependent on the elimination or substantial reduction of lead poisoning rates.     

Recruitment and retention in academic medicine--what junior faculty and trainees want department chairs to know

Attracting and retaining bright and motivated physicians remains a high priority for academia. Historically, the recruitment of trainees into academia and the retention of junior faculty have been suboptimal. To learn more about the perceived obstacles that discourage the pursuit of academic careers, a Workshop on Academic Career Pathways was conducted during the 2011 Southern Regional Meetings held in New Orleans. The audience included mainly residents and fellows as well as junior and senior faculties. Speakers described career options in academic medicine focusing on the clinician-investigator and the clinician-educator tracks. Afterward, the audience was asked to identify perceived obstacles to recruitment and retention in academic medicine. The group identified 10 major obstacles in 3 categories: financial challenges, personal mentoring and academic skills acquisition. This article summarizes the workshop proceedings and ends with recommendations to chairs and department leaders for improving recruitment and retention in academic medicine based on the discussion.     

Outcomes in computer-assisted surgical simulation for orthognathic surgery

Orthognathic surgery is a powerful tool to address skeletal discrepancies of the jaws; however, the model surgery and splint fabrication necessary to successfully complete this surgery are laborious and time consuming. Previous studies have described the utility of computer-assisted surgical simulation (CASS) to eliminate the need for plaster cast model surgery. This article evaluates the implementation of a CASS system for treatment planning and splint fabrication in a series of 11 orthognathic surgery patients. All patients were treatment planned using a CASS system for computer-simulated osteotomies and splint fabrication. As a safety measure, traditional model surgery and splint fabrication were also performed on all cases. Each case was evaluated for accuracy of cephalometric analysis, splint accuracy, splint durability, and ease of treatment planning. All splints fit as well, or better, than those fabricated using traditional methods. In 2 cases, occlusal cants were detected by the CASS system that were undetected by traditional cephalometric analysis and physical examination. In 1 case, the skeletal midline identified on the computed tomographic scan was incongruent with the soft tissue clinical midline of the face, and this discrepancy was recognized and compensated for by correlation of the physical examination and preoperative clinical photos.In this series of 11 patients, the CASS system proved to be an effective mechanism to treatment plan cases and prepare surgical splints for patients undergoing orthognathic surgery.