From the Cover: An estimate of the number of tropical tree species

The high species richness of tropical forests has long been recognized, yet there remains substantial uncertainty regarding the actual number of tropical tree species. Using a pantropical tree inventory database from closed canopy forests, consisting of 657,630 trees belonging to 11,371 species, we use a fitted value of Fisher’s alpha and an approximate pantropical stem total to estimate the minimum number of tropical forest tree species to fall between ∼40,000 and ∼53,000, i.e., at the high end of previous estimates. Contrary to common assumption, the Indo-Pacific region was found to be as species-rich as the Neotropics, with both regions having a minimum of ∼19,000–25,000 tree species. Continental Africa is relatively depauperate with a minimum of ∼4,500–6,000 tree species. Very few species are shared among the African, American, and the Indo-Pacific regions. We provide a methodological framework for estimating species richness in trees that may help refine species richness estimates of tree-dependent taxa.Despite decades of biological inventories worldwide, we still do not know how many species exist and how they are distributed (1). Although global patterns of estimated vascular plant species richness and distribution have become more clear (2–5), no previous study has focused on trees as a distinct growth form. As a consequence, our estimation of the number of tree species in tropical forests still depends on untested expert opinions (6–8) rather than on an appropriate methodological framework and data set.Given the importance of trees as key structural components of forest ecosystems, sources of timber and nontimber products, and providers of vital ecosystem services (9, 10), the lack of reliable estimates of the total number of tropical tree species represents a critical knowledge gap that has direct consequences for estimating the diversity of other tree-dependent taxa (11). A classic example is Erwin’s (6) estimate of the existence of 30 million arthropod species, which was based on observed host specificities of arthropods with individual tropical tree species combined with an estimate of the total number of tropical tree species. Global arthropod richness has subsequently been revised downward (7, 11), but current estimates still suffer from the lack of information on the number of tropical tree species.In recent decades, the number of tree inventory plots across the tropics has grown to such an extent that species richness estimation at the continental and pantropical scale can now be addressed using standardized species lists with abundance data. Prior estimates of plant richness at such broad scales have mostly been based on analyses of incidence data obtained from herbarium collections and flora treatments (2–5). However, these methods are highly sensitive to collecting biases and ignore valuable information on species’ abundances (12). Abundance data enable extrapolation of richness from local to global scales using diversity estimators that fit the observed species rank abundance data (13–15).     

From the Cover: 1.36 million years of Mediterranean forest refugium dynamics in response to glacial–interglacial cycle strength

The sediment record from Lake Ohrid (Southwestern Balkans) represents the longest continuous lake archive in Europe, extending back to 1.36 Ma. We reconstruct the vegetation history based on pollen analysis of the DEEP core to reveal changes in vegetation cover and forest diversity during glacial–interglacial (G–IG) cycles and early basin development. The earliest lake phase saw a significantly different composition rich in relict tree taxa and few herbs. Subsequent establishment of a permanent steppic herb association around 1.2 Ma implies a threshold response to changes in moisture availability and temperature and gradual adjustment of the basin morphology. A change in the character of G–IG cycles during the Early–Middle Pleistocene Transition is reflected in the record by reorganization of the vegetation from obliquity- to eccentricity-paced cycles. Based on a quantitative analysis of tree taxa richness, the first large-scale decline in tree diversity occurred around 0.94 Ma. Subsequent variations in tree richness were largely driven by the amplitude and duration of G–IG cycles. Significant tree richness declines occurred in periods with abundant dry herb associations, pointing to aridity affecting tree population survival. Assessment of long-term legacy effects between global climate and regional vegetation change reveals a significant influence of cool interglacial conditions on subsequent glacial vegetation composition and diversity. This effect is contrary to observations at high latitudes, where glacial intensity is known to control subsequent interglacial vegetation, and the evidence demonstrates that the Lake Ohrid catchment functioned as a refugium for both thermophilous and temperate tree species.

Identification and protection of past forest refugia, supporting a relict population, has gained interest in light of projected forest responses to anthropogenic climate change (1–4). Understanding the past and present composition of Mediterranean forest refugia is central to the study of long-term survival of tree taxa and the systematic relation between forest dynamics and climate (5). The Quaternary vegetation history of Europe, studied for over a century, is characterized by successive loss of tree species (6–8). Species loss was originally explained by the repeated migration across east–west oriented mountain chains during glacial–interglacial (G–IG) cycles (9). Later views gave more importance to the survival of tree populations during warm and arid stages in southern refugia (10, 11). Tree survival likely depends on persistence of suitable climate and tolerable levels of climate variability, as well as niche differentiation and population size at the refugium (12), although the precise relation between regional extinctions, climate variability, and local edaphic factors is not well known (13). Mediterranean mountain regions are considered to serve as forest refugia over multiple glacial cycles and frequently coincide with present-day biodiversity hotspots (14). Across the Mediterranean, increases in aridity and fire occurrence have impacted past vegetation communities (15–18). Comprehensive review of available Quaternary Mediterranean records indicates that Early (2.58 to 0.77 Ma) and Middle Pleistocene (0.77 to 0.129 Ma) tree diversity was higher compared to the present (13, 19–21). Particularly drought intolerant, thermophilic taxa were more abundant and diverse (8) but with strong spatial and temporal variations in tree diversity across the region. Long-term relationships between refugia function and environmental change over multiple G–IG cycles are hard to quantify due to the rarity of long, uninterrupted records.The Early–Middle Pleistocene Transition (EMPT), between 1.4 and 0.4 Ma (22), is of particular importance for understanding the relation between past climate change, vegetation dynamics, and biodiversity in the Mediterranean region. The EMPT is characterized by a gradual transition of G–IG cycle duration from obliquity (41 thousand years; kyr) to eccentricity (100 kyr) scale with increasing amplitude of each G–IG cycle (e.g., refs. 23, 24). The EMPT was accompanied by long-term cooling of the deep and surface ocean and was likely caused by atmospheric CO₂ decline and ice-sheet feedbacks (25–30). In Europe, the EMPT is associated with pronounced vegetation changes and local extinction and isolation of small tree populations (31).Here, we document vegetation history of the last 1.36 Ma in the Lake Ohrid (LO) catchment, located at the Albanian/North Macedonian border at 693 m above sea level (m asl, Fig. 1), the longest continuous sedimentary lake record in Europe (32, 33). The chronology of the DEEP core (International Continental Scientific Drilling Program site 5045-1; 41°02’57’’ N, 20°42’54’’ E, Fig. 1) is based on tuning of biogeochemical proxy data to orbital parameters with independent tephrostratigraphic and paleomagnetic age control (32, 33). The Balkan Peninsula has long been considered an important glacial forest refugium for presently widespread taxa such as Abies, Picea, Carpinus, Corylus, Fagus Ostrya, Quercus, Tilia, and Ulmus (7, 34–36). More than 60% of the Balkans is currently located >1,000 m asl (36), providing steep latitudinal and elevational gradients to support refugia under both cold and warm conditions. Today, the LO catchment is dominated by (semi) deciduous oak (Quercus) and hornbeam (Carpinus/Ostrya) forests. Above 1,250 m elevation, mixed mesophyllous forest with montane elements occurs (Fagus and at higher elevations Abies), which above 1,800 m elevation develops into subalpine grassland with Juniperus shrubs (see ref. 37 for site details). Isolated populations of Pinus peuce and Pinus nigra currently grow in the area (37–40).Open in a separate windowFig. 1.(A) Location of LO and TP on the Balkan Peninsula. (B) Local setting around LO, bathymetry (81), and DEEP coring site (adapted from ref. 32).Previous analysis of pollen composition of the last 500 kyr at the DEEP site revealed that the LO has been an important refugium. Arboreal pollen (AP) is deposited continuously and changes in abundance on multimillennial timescales in association with G–IG cycles, whereas millennial-scale variability is tightly coupled to Mediterranean sea-surface temperature variations (37, 41–45). Subsequent studies confirm the refugial character of the site recording Early Pleistocene (1.365 to 1.165 Ma) high relict tree diversity and abundance—and significant hydrological changes, including an increase in lake size and depth (38). Here, we present a continuous palynological record from LO with millennial resolution (∼2 kyr) back to 1.36 Ma to assess the systematic relationships between tree pollen abundance, forest diversity, and G–IG climate variability.Our objective is as follows: 1) infer the impact of past climate variability on local vegetation across the EMPT, 2) estimate tree species diversity in the catchment, and 3) examine how the amplitude and duration of preceding G–IG intervals affected the vegetation development and plant species diversity in this refugial area.     

Forests synchronize their growth in contrasting Eurasian regions in response to climate warming

Forests play a key role in the carbon balance of terrestrial ecosystems. One of the main uncertainties in global change predictions lies in how the spatiotemporal dynamics of forest productivity will be affected by climate warming. Here we show an increasing influence of climate on the spatial variability of tree growth during the last 120 y, ultimately leading to unprecedented temporal coherence in ring-width records over wide geographical scales (spatial synchrony). Synchrony in growth patterns across cold-constrained (central Siberia) and drought-constrained (Spain) Eurasian conifer forests have peaked in the early 21st century at subcontinental scales (∼1,000 km). Such enhanced synchrony is similar to that observed in trees co-occurring within a stand. In boreal forests, the combined effects of recent warming and increasing intensity of climate extremes are enhancing synchrony through an earlier start of wood formation and a stronger impact of year-to-year fluctuations of growing-season temperatures on growth. In Mediterranean forests, the impact of warming on synchrony is related mainly to an advanced onset of growth and the strengthening of drought-induced growth limitations. Spatial patterns of enhanced synchrony represent early warning signals of climate change impacts on forest ecosystems at subcontinental scales.Understanding how climate change affects forests across multiple spatiotemporal scales is important for anticipating its impacts on terrestrial ecosystems. Increases in atmospheric CO₂ concentration and shifts in phenology (1–3) could favor tree growth by enhancing photosynthesis and extending the effective growing period, respectively (4). Conversely, recent warming could increase respiration rates and, together with increasing heat and drought stresses, exert negative impacts on forest productivity (5, 6). Given the uncertainty as to what extent enhanced carbon uptake could be offset by the detrimental effects of warming on tree performance, the actual consequences of climate change on forest carbon cycling remain under debate. Notably, climate change has a stronger impact on forests constrained by climatic stressors, such as suboptimal temperatures or water shortage (7). As high-resolution repositories of biological responses to the environment, dendrochronological archives can be used to monitor this impact (8).The concept of spatial synchrony in tree growth refers to the extent of coincident changes in ring-width patterns among geographically disjunct tree populations (9). Climatic restrictions tend to strengthen growth–climate relationships, resulting in enhanced common ring-width signals (i.e., more synchronous tree growth). Thus, regional bioclimatic patterns can be delineated by identifying groups of trees whose growth is synchronously driven by certain climatic constraints (10, 11). Previous synthesis studies have provided evidence for globally coherent multispecies responses to climate change in natural systems, including forests, with a focus on the role of increasingly warmer temperatures (12, 13). Indeed, climate has changed markedly over the last decades, prompting an array of physiological reactions in trees that could strengthen growth–climate relationships, thereby enhancing spatial synchrony. Such tree responses may be linked to global shifts in the timing of plant activity (2), drought stress in mid-latitudes (6, 14), or an uncoupling of air and soil thermal regimes in the early growing season (15) and direct heat stress (16) in high latitudes, among other factors. Changing tree growth patterns associated with enhanced synchrony in response to warming have been reported at small geographical scales (<150 km) (14–18, but see ref. 19); however, an extended examination of synchrony patterns is currently lacking for large (i.e., subcontinental) areas.To determine whether climate warming and increased variability (1) lead to more synchronous tree growth, we examined changes in spatial synchrony over the last 120 y across subcontinental areas by using a comprehensive network of 93 ring-width chronologies from six different conifer species across two climatically contrasting Eurasian biomes: boreal forests in central Siberia (n = 45 chronologies) and Mediterranean forests in Spain (n = 48 chronologies) (SI Appendix, Fig. S1 and Table S1). Central Siberia has a severe continental climate with a prolonged cold season, large intra-annual temperature variations, and moderate precipitation. Spain is dominated by a typical Mediterranean climate, with mild (coast) to cool (inland) wet winters and summer droughts. Thus, temperature exerts the main climatic control over productivity in boreal forests, whereas Mediterranean forests are primarily water-limited (SI Appendix, section 1A).Temporal changes in spatial synchrony (hereinafter, â_C) are quantified using a novel mixed model framework (20). This methodology has two fundamental advantages for dendroscience (21) over other alternative approaches useful for interpreting population dynamics in ecology (22) or patterns of environmental synchrony (23): (i) it is capable of dealing with partially overlapping chronologies, yielding valid inferences of spatial synchrony for large areas in which ring-width data are available but covering different time periods, and (ii) it is highly flexible to fit general statistical structures for subdivided groups of chronologies, opening new avenues for interpreting complex spatial patterns through geographic or taxonomic stratification of a target region.We hypothesized that climate warming (1) triggers more synchronous tree growth at subcontinental scales owing to an amplified climatic control of growth, e.g., through higher temperatures in Siberia and decreased water availability in Spain. Our objective was to interpret forest reactions to warming through an alternative approach to model-based assessment or field experimentation. Specifically, this study asked the following questions: (i) is spatial synchrony of tree growth increasing across terrestrial biomes and if so, at what pace?; (ii) how are synchrony patterns related to intraspecific and interspecific responses to climate warming?; and (iii) what are the main climate factors underlying more synchronous forest growth? In ecological theory, it is widely accepted that spatial synchrony influences metapopulation persistence and the likelihood of species extinction (24). As forests are becoming more prone to widespread mortality (25), interpreting long-term synchrony patterns of tree growth may be relevant to identifying broad-scale threshold responses to climate change.     

From the Cover: INAUGURAL ARTICLE by a Recently Elected Academy Member:Is there tree senescence? The fecundity evidence

Despite its importance for forest regeneration, food webs, and human economies, changes in tree fecundity with tree size and age remain largely unknown. The allometric increase with tree diameter assumed in ecological models would substantially overestimate seed contributions from large trees if fecundity eventually declines with size. Current estimates are dominated by overrepresentation of small trees in regression models. We combined global fecundity data, including a substantial representation of large trees. We compared size–fecundity relationships against traditional allometric scaling with diameter and two models based on crown architecture. All allometric models fail to describe the declining rate of increase in fecundity with diameter found for 80% of 597 species in our analysis. The strong evidence of declining fecundity, beyond what can be explained by crown architectural change, is consistent with physiological decline. A downward revision of projected fecundity of large trees can improve the next generation of forest dynamic models.

“Belgium, Luxembourg, and The Netherlands are characterized by “young” apple orchards, where over 60% of the trees are under 10 y old. In comparison, Estonia and the Czech Republic have relatively “old” orchard[s] with almost 60% and 43% over 25 y old” (1).

“The useful lives for fruit and nut trees range from 16 years (peach trees) to 37 years (almond trees)…. The Depreciation Analysis Division believes that 61 years is the best estimate of the class life of fruit and nut trees based on the information available” (2).

When mandated by the 1986 Tax Reform Act to depreciate aging orchards, the Office of the US Treasury found so little information that they ultimately resorted to interviews with individual growers (2). One thing is clear from the age distributions of fruit and nut orchards throughout the world (1, 3, 4): Standard practice often replaces trees long before most ecologists would view them to be in physiological decline, despite the interruption of profits borne by growers as transplants establish and mature. Although seed establishment represents the dominant mode for forest regeneration globally, and the seeds, nuts, and fruits of woody plants make up to 3% of the human diet (5, 6), change in fecundity with tree size and age is still poorly understood. We examine here the relationship between tree fecundity and diameter, which is related to tree age in the sense that trees do not shrink in diameter (cambial layers typically add a new increment annually), but growth rates can range widely. Still, it is important not to ignore the evidence that declines with size may also be caused by aging. Although most analyses do not separate effects of size from age (because age is often unknown and confounded with size), both may contribute to size–fecundity relationships (7). Grafting experiments designed to isolate extrinsic influences (size and/or environment) from age-related gene expression suggest that size alone can sometimes explain declines in growth rate and physiological performance (8–10), consistent with pruning/coppicing practice to extend the reproductive life of commercial fruit trees. Hydraulic limitation can affect physiological function, including reduced photosynthetic gain that might contribute to loss of apical dominance, or “flattening” of the crown with increasing height (11–16). The slowing of height growth relative to diameter growth in large trees is observed in many species (12, 17). At least one study suggests that age by itself may not lead to decline in fecundity of open-grown, generally small-statured bristlecone pine (Pinus longaeva) (18). By contrast, some studies provide evidence of tree senescence, including age-related genetic changes in meristems of grafted scions that cause declines in physiological function (19–22). Koenig et al. (23) found that fecundity declined in the 5 y preceding death in eight Quercus species, although cause of death here, as in most cases, is hard to identify. Fielding (24) found that cone size of Pinus radiata declines with tree age and smaller cones produce fewer seeds (25). Some studies support age-related fecundity declines in herbaceous species (26–28). Thus, there is evidence to suggest the fecundity schedules might show declines with size, age, or both.The reproductive potential of trees as they grow and age is of special concern to ecologists because, despite being relatively rare, large trees can contribute disproportionately to forest biomass due to the allometric scaling that amplifies linear growth in diameter to a volume increase that is more closely related to biomass (29, 30). Understanding the role of large trees can also benefit management in recovering forests (31). If allometric scaling applies to fecundity, then these large individuals might determine the species and genetic composition of seeds that compete for dominance in future forests.Unfortunately, underrepresentation of big trees in forests frustrates efforts to infer how fecundity changes with size. Simple allometric relationships between seed production and tree diameter can offer useful predictions for the small- to intermediate-size trees that dominate observational data, so it is not surprising that modeling began with the assumption of allometric scaling (32–36). Extrapolation from these models would predict that seed production by the small trees from which most observations come may be overwhelmed by big trees. Despite the increase with tree size assumed by ecologists (37), evidence for declining reproduction in large trees has continued to accumulate from horticultural practice (3, 4, 38, 39) and at least some ecological (40–45) and forestry literature (46, 47). However, we are unaware of studies that evaluate changes in fecundity that include substantial numbers of large trees.Understanding the role of size and age is further complicated by the fact that tree fecundity ranges over orders of magnitude from tree to tree of the same species and within the same tree from year to year—a phenomenon known as “masting.” The variation in seed-production data requires large sample sizes not only to infer the effects of size, but also to account for local habitat and interannual climate variation. For example, a one-time destructive harvest to count seeds in felled trees (48, 49) misses the fact that the same trees would offer a different picture had they been harvested in a different year. An oak that produces 100 acorns this year may produce 10,000 next year. A pine that produces 500 cones this year can produce zero next year. Few datasets offer the sample sizes of trees and tree years needed to estimate effects of size and habitat conditions in the face of this high intertree and interyear variability (43).We begin this analysis by extending allometric scaling to better reflect the geometry of fecundity with tree size. We then reexamine the size–fecundity relationship using data from the Masting Inference and Forecasting (MASTIF) project (50), which includes substantial representation of large trees, and a modeling framework that allows for the possibility that fecundity plateaus or even declines in large trees. Unlike previous studies, we account for the nonallometric influences that come through competition and climate. We demonstrate that fecundity–diameter relationships depart substantially from allometric scaling in ways that are consistent with physiological senescence.Continuous increase with size has been assumed in most models of tree fecundity, supported in part by allometric regressions against diameter, typically of the formlogMf=β0+βD⁡log⁡D[1]for fecundity mass Mf=m×f (48, 51), where D is tree diameter, m is mass per seed, and fecundity f is seeds per tree per year. Of course, this model cannot be used to determine whether or how fecundity changes with tree diameter unless expanded to include additional quadratic or higher-order terms (52).The assumption of continual increase in fecundity was interpreted from early seed-trap studies, which initially assumed that βD=2, i.e., fecundity proportional to stem basal area (33−34, 51). Models subsequently became more flexible, first with βD values fitted, rather than fixed, yielding estimates in the range (0.3, 0.9) in one study (ref. 52, 18 species) and (0, 4.1) in another (ref. 56, 4 species). However, underrepresentation of large trees in typical datasets means that model fitting is dominated by the abundant small size classes.To understand why data and models could fail to accurately represent change in fecundity with size, consider that allometric scaling in Eq. 1 can be maintained dynamically only if change in both adheres to a strict proportionality1fdfdt∝1DdDdt[2](57). For allometric scaling, any variable that affects diameter growth has to simultaneously affect change in fecundity and in the same, proportionate way. In other words, allometric scaling cannot hold if there are selective forces on fecundity that do not operate through diameter growth and vice versa.On top of this awkward constraint that demands proportionate responses of growth and fecundity, consider further that standard arguments for allometric scaling are not directly relevant for tree fecundity. Allometry is invoked for traits that maintain relationships between body parts as an organism changes size (29). For example, a diameter increment translates to an increase in volume throughout the tree (58, 59). Because the cambial layer essentially blankets the tree, a volume increment cannot depart much from a simple allometric relationship with diameter. However, the same cannot be said for all plant parts, many of which clearly do not allometrically scale; for example, seed size does not scale with leaf size (60), presumably because structural constraints are not the dominant forces that relate them (61).To highlight why selective forces might not generate strict allometric scaling for reproduction, consider that a tree allocates a small fraction of potential buds to reproduction in a given year (62, 63). Still, if the number of buds on a tree bears some direct relationship to crown dimensions and, thus, diameter, there might be allometric scaling. However, the fraction of buds allocated to reproduction and their subsequent development to seed is affected by interannual weather and other selective forces (e.g., bud abortion, pollen limitation) in ways that diameter growth is not (64–66). In fact, weather might have opposing effects on growth and reproduction (67). Furthermore, resources can change the relationship between diameter and fecundity, including light levels (52, 68–70) and atmospheric CO2 (71).Some arguments based on carbon balance anticipate a decline in fecundity with tree size (72). Increased stomatal limitation (11) and reduced leaf turgor pressure (14, 73) from increasing hydraulic path length could reduce carbon gains in large trees. Assimilation rates on a leaf area basis can decline with tree size (74), while respiration rate per leaf area can increase [Sequoia sempervirens (75), Liquidambar styraciflua (76), and Pinus sylvestris (77)], consistent with the notion that whole-plant respiration rate may roughly scale with biomass (78). Maintenance respiration costs scale with diameter in some tropical species (79) but perhaps not in Pinus contorta and Picea engelmannii (80). Self-pruning of lower branches can reduce maintenance costs (81), but the ratio of carbon gain to respiration cost can still decline with size, especially where leaf area plateaus and per-area assimilation rates of leaves decline in large trees.The question of size–fecundity relationships is related indirectly to the large literature on interannual variation in growth–fecundity allocation (3, 4, 43, 67, 82–87). The frequency and timing of mast years and species differences in the volatility of seed production can be related to short-term changes in physiological state and pollen limitation that might not predict the long-term relationships between size and reproductive effort. The interannual covariance in diameter growth and reproductive effort can range from strong in some species to weak in others (70, 87, 88). Understanding the relationships between short-term allocation and size–fecundity differences will be an important focus of future research.Estimating effects of size on fecundity depends on the distribution of diameter data, [D], where the bracket notation indicates a distribution or density. For some early-successional species, the size distribution changes from dominance by small trees in young stands to absence of small trees in old stands. If our goal was to describe the population represented by a forest inventory plot, we would typically think about the joint distribution of fecundity and diameter values, [f,D]=[f|D][D], that is represented by the sample. The size–fecundity relationship estimated for a stand at different successional stages would diverge simply due to the distribution of diameters, i.e., differences in [D]. For example, application of Eq. 1 to harvested trees selected to balance size classes (uniform [D]) (48) overpredicts fecundity for large trees (49), but the relevance of such regressions for natural stands, where large trees are often rare, is unclear. Studies that expand Eq. 1 to allow for changing relationships with tree size now provide increasing evidence for a departure from allometric scaling in large trees (43, 70), despite dominance by small- to intermediate-size trees in these datasets. Here our goal is to understand the size–fecundity relationship [f|D] as an attribute of a species, i.e., not tied to a specific distribution of size classes observed in a particular stand.The well-known weak relationship between tree size and age that comes from variable growth histories makes it important to clarify the implications of any finding of fecundity that declines with tree size: Can it happen if there are not also fecundity declines with tree age? The only argument for continuing increase in fecundity with age in the face of observed decreases with size would have to assume that the biggest trees are also the youngest trees. Of course, a large individual can be younger than a small individual. However, at the species level, integrating over populations sampled widely, mean diameter increases with age; at the species level, declines with size also imply declines with age. Estimating accurate species-level size effects requires distributed data and large sample sizes. The analysis here fits species-level parameters, with 585,670 trees and 10,542,239 tree years across 597 species.Phylogenetic analysis might provide insight into the pervasiveness of fecundity declines with size. Inferring change in fecundity with size necessarily requires more information than is needed to fit a single slope parameter βD in the simple allometric model. The noisier the data, the more difficult it becomes to estimate the additional parameters that are needed to describe changes in the fecundity relationship with size. We thus expect that noise alone will preclude finding size-related change in some species, depending on sample size and non–size-related variation. If the vagaries of noisy data and the distribution of diameters preclude estimation of declines in some species, then we do not expect that phylogeny will explain which species do and do not show these declines. Rather than phylogeny, this explanation would instead be tied to sample size and the distribution of diameter data. Conversely, phylogenetic conservatism, i.e., a tendency for declines to be clustered in related species, could suggest that fecundity declines are real.To understand how seed production changes with tree size, our approach combines theory and data to evaluate allometric scaling and the alternative that fecundity may decline in large trees, consistent with physiological decline and senescence. We exploit two advances that are needed to determine how fecundity scales with tree size. First, datasets are needed with large trees, because studies in the literature often include few or none (85, 89, 90). Second, methods are introduced that are flexible to the possibility that fecundity continues to increase with size or not. We begin with a reformulation of allometric scaling, recognizing that change in fecundity could be regulated by size, without taking the form of Eq. 1 (Materials and Methods and SI Appendix, section S2). In other words, there could be allometric scaling with diameter, but it is not the relationship that has been used for structural quantities like biomass. We then analyze the relationships in data using a model that not only allows for potential changes in fecundity with size, but at the same time accounts for self-shading and shading by neighbors and for environmental variables that can affect fecundity and growth (Materials and Methods and SI Appendix, section S3). The fitted model is compared with our expanded allometric model to identify potential agreement. Finally, we examined phylogenetic trends in the species that do and do not show declines.     

Variation in leaf flushing date influences autumnal senescence and next year’s flushing date in two temperate tree species

Recent temperature increases have elicited strong phenological shifts in temperate tree species, with subsequent effects on photosynthesis. Here, we assess the impact of advanced leaf flushing in a winter warming experiment on the current year’s senescence and next year’s leaf flushing dates in two common tree species: Quercus robur L. and Fagus sylvatica L. Results suggest that earlier leaf flushing translated into earlier senescence, thereby partially offsetting the lengthening of the growing season. Moreover, saplings that were warmed in winter–spring 2009–2010 still exhibited earlier leaf flushing in 2011, even though the saplings had been exposed to similar ambient conditions for almost 1 y. Interestingly, for both species similar trends were found in mature trees using a long-term series of phenological records gathered from various locations in Europe. We hypothesize that this long-term legacy effect is related to an advancement of the endormancy phase (chilling phase) in response to the earlier autumnal senescence. Given the importance of phenology in plant and ecosystem functioning, and the prediction of more frequent extremely warm winters, our observations and postulated underlying mechanisms should be tested in other species.Leaf phenology of temperate trees has recently received particular attention because of its sensitivity to the ongoing climate change (1–3), and because of its crucial role in the forest ecosystem, water and carbon balances, and species distribution (4–6).A wide variety of methods, such as long-term phenological records (7), indirect measurements of ecosystem greening by remote sensing using satellites or webcam digital images (8–10), and modeling approaches (11–13), have been applied to monitor and study phenological changes. These different approaches, conducted at different spatial scales (from individual plants to biomes), have documented a clear advancement of leaf flushing in temperate climate zones and, to a lesser extent, a delay in leaf senescence (14, 15). Furthermore, various temperature manipulation experiments have simulated the impact of future winter warming on leaf phenology and confirmed an advancement in the timing of leaf flushing in response to warming (16–18). However, the response of leaf flushing to climate warming is highly nonlinear (16, 19, 20), because trees also depend on cold temperatures to break bud dormancy (21–23). This chilling requirement may not (fully) be met in a warming climate, especially at the southern edges of species distribution ranges (5, 24, 25).Most previous phenological studies have focused on specific phenophases, but how a phenological change (e.g., advanced leaf flushing) affects subsequent phenological events is rarely investigated. Nonetheless, the annual growth cycle of boreal and temperate trees forms an integrated system, where one phenophase in the cycle can affect the subsequent phases (26, 27). Such carryover effects have already been detected in fruit and nut trees, where winter warming resulted in insufficient chilling (28, 29), which subsequently postponed the onset of flowering, with an associated negative impact on crop yields and crop quality (30, 31). Heide (32) also found that delayed senescence in warm autumns delayed spring leaf flushing in the following year in boreal trees. To our knowledge, however, no study has explored the lagged effect of winter warming-induced earlier leaf flushing on the current year’s senescence and on leaf flushing dates after one growing season.In this study, we exposed young trees to manipulated winter temperature to assess the legacy effect of warming-induced variation in leaf flushing (spring 2010) on the timing of leaf senescence (autumn 2010) and flushing in the following year (spring 2011) in two common deciduous and late-successional temperate tree species: pedunculate oak (Quercus robur L.) and European beech (Fagus sylvatica L.). Specifically, we tested the hypothesis that the physiological impact of winter warming lasts longer than the current growing season. To confirm our experimental results on young trees, we further explored the legacy effects on mature trees of these two study species using the long-term phenological observations of the European phenology network (www.pep725.eu).     

Half-century evidence from western Canada shows forest dynamics are primarily driven by competition followed by climate

Tree mortality, growth, and recruitment are essential components of forest dynamics and resiliency, for which there is great concern as climate change progresses at high latitudes. Tree mortality has been observed to increase over the past decades in many regions, but the causes of this increase are not well understood, and we know even less about long-term changes in growth and recruitment rates. Using a dataset of long-term (1958–2009) observations on 1,680 permanent sample plots from undisturbed natural forests in western Canada, we found that tree demographic rates have changed markedly over the last five decades. We observed a widespread, significant increase in tree mortality, a significant decrease in tree growth, and a similar but weaker trend of decreasing recruitment. However, these changes varied widely across tree size, forest age, ecozones, and species. We found that competition was the primary factor causing the long-term changes in tree mortality, growth, and recruitment. Regional climate had a weaker yet still significant effect on tree mortality, but little effect on tree growth and recruitment. This finding suggests that internal community-level processes—more so than external climatic factors—are driving forest dynamics.Forests provide fundamental ecosystem services for sustaining the global environment, such as storing carbon and maintaining biodiversity. These services, however, are at risk for decline as evidence has increasingly shown that forests in many parts of the world are undergoing rapid changes (1–4). Climate at the regional or global scale is often presumed to be responsible for these changes (5–14), with surprisingly little attention being paid to the possible effects of endogenous processes despite the fact that competition is often an important force driving stand dynamics and succession (15–18). How climate change and competition interplay to affect the long-term change of demographic rates and what are their relative contributions to the change are unanswered questions (19, 20).We addressed these questions by compiling data from 1,680 permanent sample plots (PSPs) that are located in undisturbed natural forests across western Canada (Fig. 1). The trees in these plots, which cover a wide geographic region spanning 32° of longitude and 10° of latitude primarily in the boreal zone, were censused over a period from 1958 to 2009 (Fig. 1). Within each plot, all standing trees with diameter at breast height (DBH) ≥ 9 cm were tagged, recorded, and remeasured at irregular time intervals (mean = 10 y) (SI Appendix, Fig. S1). Plot sizes ranged from 0.04 ha to 0.81 ha (mean = 0.14 ha). To reduce possible impact of plot sizes on our analyses, only the plots with at least 50 trees at their first census were selected. The plots have been censused three to eight times (mean of four times). In total, these plots contained 320,878 living trees over the study period (SI Appendix, Table S1).Open in a separate windowFig. 1.Locations of 1,680 permanent sample plots (PSPs) in western Canada. Each dot stands for one PSP. Four colors (dark blue, red, pink, and light blue) were used to show the distribution of PSPs in each of four provinces: British Columbia (777), Alberta (563), Saskatchewan (290), and Manitoba (50). The background colors represent Canada’s ecozones.We analyzed the changes of tree demographic rates (mortality, growth, and recruitment rates) over time at the species, stand, and regional levels and by stand age, tree size, and plot elevation (Methods). Two major possible drivers of the changes, competition and regional climate, were considered in our analyses. To test the effect of competition on the demographic rates, we used stand basal area (BA), basal area of larger trees (BAL), and stand density index (SDI), all commonly used in forestry (6, 12) as indexes of competition. To assess the effect of climate change, we selected mean warmest month temperature (MWMT), mean coldest month temperature (MCMT), and mean annual precipitation (MAP). We incorporated both competition and climatic variables simultaneously in the models, rather than separately as previous studies did (6, 11), and considered possible interactions between competition and climatic variables (21) in the models.     

The fossilized birth–death process for coherent calibration of divergence-time estimates

Time-calibrated species phylogenies are critical for addressing a wide range of questions in evolutionary biology, such as those that elucidate historical biogeography or uncover patterns of coevolution and diversification. Because molecular sequence data are not informative on absolute time, external data—most commonly, fossil age estimates—are required to calibrate estimates of species divergence dates. For Bayesian divergence time methods, the common practice for calibration using fossil information involves placing arbitrarily chosen parametric distributions on internal nodes, often disregarding most of the information in the fossil record. We introduce the “fossilized birth–death” (FBD) process—a model for calibrating divergence time estimates in a Bayesian framework, explicitly acknowledging that extant species and fossils are part of the same macroevolutionary process. Under this model, absolute node age estimates are calibrated by a single diversification model and arbitrary calibration densities are not necessary. Moreover, the FBD model allows for inclusion of all available fossils. We performed analyses of simulated data and show that node age estimation under the FBD model results in robust and accurate estimates of species divergence times with realistic measures of statistical uncertainty, overcoming major limitations of standard divergence time estimation methods. We used this model to estimate the speciation times for a dataset composed of all living bears, indicating that the genus Ursus diversified in the Late Miocene to Middle Pliocene.A phylogenetic analysis of species has two goals: to infer the evolutionary relationships and the amount of divergence among species. Preferably, divergence is estimated in units proportional to time, thus revealing the times at which speciation events occurred. Once orthologous DNA sequences from the species have been aligned, both goals can be accomplished by assuming that nucleotide substitutions occur at the same rate in all lineages [the “molecular clock” assumption (1)] and that the time of at least one speciation event on the tree is known, i.e., one speciation event acts to “calibrate” the substitution rate.The goal of reconstructing rooted, time-calibrated phylogenies is complicated by substitution rates changing over the tree and by the difficulty of determining the date of any speciation event. Substitution rate variation among lineages is pervasive and has been accommodated in several ways. The most widely used method to account for rate heterogeneity is to assign an independent parameter to each branch of the tree. Branch lengths, then, are the product of substitution rate and time, and usually measured in units of expected number of substitutions per site. This solution allows estimation of the tree topology—which is informative about interspecies relationships—but does not attempt to estimate the rate and time separately. Thus, under this “unconstrained” parameterization, molecular sequence data allow inference of phylogenetic relationships and genetic distances among species, but the timing of speciation events is confounded in the branch-length parameter (2–4). Under a “relaxed-clock” model, substitution rates change over the tree in a constrained manner, thus separating the rate and time parameters associated with each branch and allowing inference of lineage divergence times. A considerable amount of effort has been directed at modeling lineage-specific substitution rate variation, with many different relaxed-clock models described in the literature (5–19). When such models are coupled with a model on the distribution of speciation events over time [e.g., the Yule model (20) or birth–death process (21)], molecular sequence data can inform the relative rates and node ages in a phylogenetic analysis.Estimates of branch lengths in units of absolute time (e.g., millions of years) are required for studies investigating comparative or biogeographical questions (e.g., refs. 22, 23). However, because commonly used diversification priors are imprecise on node ages, external information is required to infer the absolute timing of speciation events. Typically, a rooted time tree is calibrated by constraining the ages of a set of internal nodes. Age constraints may be derived from several sources, but the most common and reliable source of calibration information is the fossil record (24, 25). Despite the prevalence of these data in divergence time analyses, the problem of properly calibrating a phylogenetic tree has received less consideration than the problem of accommodating rate variation. Moreover, various factors may lead to substantial errors in parameter estimates (26–31). When estimating node ages, a calibration node must be identified for each fossil. For a given fossil, the calibration node is the node in the extant species tree that represents the most recent common ancestor (MRCA) of the fossil and a set of extant species. Based on the fossil, the calibration node’s age is estimated on an absolute timescale. Thus, fossil data typically can provide valid minimum-age constraints only on these nodes (24, 27), and erroneous conclusions may result if the calibration node is not specified properly (26).Bayesian inference methods are well adapted to accommodating uncertainty in calibration times by assuming that the age of the calibrated node is a random variable drawn from some parametric probability distribution (10, 14, 29, 31–35). Although this Bayesian approach properly propagates uncertainty in the calibration times through the analysis (reflected in the credible intervals on uncalibrated node ages), two problems remain unresolved.First, these approaches, as they commonly are applied, induce a probability distribution on the age of each calibrated node that comes from both the node-specific calibration prior and the tree-wide prior on node ages, leading to an incoherence in the model of branching times on the tree (35, 36). Typically, a birth–death process of cladogenesis is considered as the generating model for the tree and speciation times (20, 21, 37–40), serving as the tree-wide prior distribution on branch times in a Bayesian analysis. The speciation events acting as calibrations then are considered to be drawn from an additional, unrelated probability distribution intended to model uncertainty in the calibration time. This procedure results in overlaying two prior distributions for a calibration node: one from the tree prior and one from the calibration density (35, 41). Importantly, this incoherence is avoided by partitioning the nodes and applying a birth–death process to uncalibrated nodes conditioned on the calibrated nodes (32), although many divergence time methods do not use this approach. Nevertheless, a single model that acts as a prior on the speciation times for both calibrated and uncalibrated nodes is a better representation of the lineage diversification process and preferable as a prior on branching times when using fossil data.Second, the probability distributions used to model uncertainty in calibration times are poorly motivated. The standard practice in Bayesian divergence time methods is to model uncertainty in calibrated node ages by using simple probability distributions, such as the uniform, log-normal, gamma, or exponential distributions (29). When offset by a minimum age, these “calibration densities” (35) simply seek to characterize the age of the node with respect to its descendant fossil. However, the selection and parameterization of calibration priors rarely are informed by any biological process or knowledge of the fossil record (except see refs. 42–44). A probability model that acts as a fossil calibration prior should have parameters relevant to the preservation history of the group, such as the rate at which fossils occur in the rock record, a task that likely is difficult for most groups without an abundant fossil record (43, 45). Consequently, most biologists are faced with the challenge of choosing and parameterizing calibration densities without an explicit way to describe their prior knowledge about the calibration time. Thus, calibration priors often are specified based on arbitrary criteria or ad hoc validation methods (46), and ultimately, this may lead to arbitrary or ad hoc estimates of divergence times.We provide an alternative method for calibrating phylogenies with fossils. Because fossils and molecular sequences from extant species are different observations of the same diversification process, we use an explicit speciation–extinction–fossilization model to describe the distribution of speciation times and recovered fossils. This model—the fossilized birth–death (FBD) process—acts as a prior for divergence time dating. The parameters of the model—the speciation rate, extinction rate, fossil recovery rate, and proportion of sampled extant species—interact to inform the amount of uncertainty for every speciation event on the tree. These four parameters are the only quantities requiring prior assumptions, compared with assuming separate calibration densities for each fossil. Analyses of simulated data under the FBD model result in reliable estimates of absolute divergence times with realistic measures of statistical uncertainty. Moreover, node age estimates are robust to several biased sampling strategies of fossils and extant species—strategies that may be common practice or artifacts of fossil preservation but heavily violate assumptions of the model.     

From the Cover: Predicting overfishing and extinction threats in multispecies fisheries

Threats to species from commercial fishing are rarely identified until species have suffered large population declines, by which time remedial actions can have severe economic consequences, such as closure of fisheries. Many of the species most threatened by fishing are caught in multispecies fisheries, which can remain profitable even as populations of some species collapse. Here we show for multispecies fisheries that the biological and socioeconomic conditions that would eventually cause species to be severely depleted or even driven extinct can be identified decades before those species experience high harvest rates or marked population declines. Because fishing effort imposes a common source of mortality on all species in a fishery, the long-term impact of a fishery on a species is predicted by measuring its loss rate relative to that of species that influence the fishery’s maximal effort. We tested our approach on eight Pacific tuna and billfish populations, four of which have been identified recently as in decline and threatened with overfishing. The severe depletion of all four populations could have been predicted in the 1950s, using our approach. Our results demonstrate that species threatened by human harvesting can be identified much earlier, providing time for adjustments in harvesting practices before consequences become severe and fishery closures or other socioeconomically disruptive interventions are required to protect species.Marine fisheries are an important global source of food and livelihoods (1–4), but there are concerns that current fishing practices threaten some marine species with severe depletion or eventual extinction (2–5). Many of the largest commercial fishing methods, such as trawling, longlining, and seining, unavoidably catch multiple species simultaneously (6–9). Multispecies fisheries pose a particular threat of extinction or severe depletion because fishing can remain profitable as long as some valuable species remain abundant, even while others collapse (6–11). In contrast, in a single-species fishery profits tend to fall as the target population declines, thereby removing the incentive to fish before extinction occurs (10). Multispecies fisheries pose a threat to two types of species or stocks (populations): (i) commercially valued species, called “weak stocks”, which are more vulnerable to overharvesting than are other commercially valuable species (6), and (ii) by-catch species, which are caught accidentally and create little economic incentive to cease fishing as their populations collapse because they have little or no commercial value (7–9).Failure to prevent collapse of weak stocks and by-catch species can impose substantial long-term environmental and economic costs. Slow-growing populations are most likely to collapse, but can take several decades to recover (5). Recovery often requires long-term fishery closures or reductions in effort, having substantial economic and social consequences (3, 5). Moreover, population declines caused by one fishery can diminish yields and profits in other commercial or artisanal fisheries that depend on the same species (e.g., ref. 12).Despite these costs, species threatened by fishing have rarely been identified until after their populations have declined substantially (2–5, 7, 8). Assessments of fishery impacts on species mostly focus on estimating current exploitation rates or past population trends (13–15), which identifies already declining species rather than predicting future declines. Data limitations have made empirical prediction of future threats from fishing challenging, particularly for weak stocks and by-catch species. Oceans are difficult to sample extensively, and few economic incentives exist to gather data on species other than the most commercially valued species (7, 8). Some predictive models (e.g., ref. 16) have been developed to forecast the impacts of some fisheries, but these are often data intensive. Some of the characteristics that make a population susceptible to overfishing are well known—for example, low population growth rates (3–11, 17, 18), high value and/or low fishing costs (10, 11, 17–19), and schooling behavior (18). Recently, some correlative approaches based on these characteristics have been developed for assessing likely relative threats to data-poor species (4, 20–22). However, predicting the severity of future threats in absolute terms with this type of approach can be challenging.Here, we present a mechanistic approach that uses readily available data to predict the potential of current fishing practices, if maintained, to eventually cause a population to be driven extinct or “overfished”, here defined as depletion below its maximum sustainable yield (MSY) abundance (N_MSY) (3). Our approach identifies combinations of biological and socioeconomic conditions that are likely to eventually lead to high mortality rates and population declines. As we show, these conditions can be identified long before either occurs.We test the predictive power of our approach on eight tuna and billfish populations of the Western and Central Pacific Ocean fisheries. High-seas tuna and billfish have elicited recent conservation concern due to significant population declines and range contractions found in many species (17, 23, 24). Three of the populations in our study, bigeye tuna (Thunnus obesus) and both the northern and the southern striped marlin (Tetrapturus audax) populations, have been recently identified as experiencing overfishing—meaning their exploitation rates have exceeded the MSY exploitation rate (F_MSY) (24–27). A fourth, blue marlin (Makaira nigricans), whose overfishing status has been subject to considerable uncertainty (28), has undergone a significant population decline and range contraction (13, 23, 28). We determine whether our approach could have predicted threats to these four populations, using data from as early as the 1950s, and assess the threats predicted by the latest available data to all populations.     

From the Cover: The evolution of parasitism from mutualism in wasps pollinating the fig,Ficus microcarpa,in Yunnan Province,China

Theory identifies factors that can undermine the evolutionary stability of mutualisms. However, theory’s relevance to mutualism stability in nature is controversial. Detailed comparative studies of parasitic species that are embedded within otherwise mutualistic taxa (e.g., fig pollinator wasps) can identify factors that potentially promote or undermine mutualism stability. We describe results from behavioral, morphological, phylogenetic, and experimental studies of two functionally distinct, but closely related, Eupristina wasp species associated with the monoecious host fig, Ficus microcarpa, in Yunnan Province, China. One (Eupristina verticillata) is a competent pollinator exhibiting morphologies and behaviors consistent with observed seed production. The other (Eupristina sp.) lacks these traits, and dramatically reduces both female and male reproductive success of its host. Furthermore, observations and experiments indicate that individuals of this parasitic species exhibit greater relative fitness than the pollinators, in both indirect competition (individual wasps in separate fig inflorescences) and direct competition (wasps of both species within the same fig). Moreover, phylogenetic analyses suggest that these two Eupristina species are sister taxa. By the strictest definition, the nonpollinating species represents a “cheater” that has descended from a beneficial pollinating mutualist. In sharp contrast to all 15 existing studies of actively pollinated figs and their wasps, the local F. microcarpa exhibit no evidence for host sanctions that effectively reduce the relative fitness of wasps that do not pollinate. We suggest that the lack of sanctions in the local hosts promotes the loss of specialized morphologies and behaviors crucial for pollination and, thereby, the evolution of cheating.

Mutualisms are defined by the net benefits that are usually provided to individuals of each interacting species. These interactions often have influences far beyond the partner species directly interacting, and commonly provide many fundamental ecosystem services (1, 2). For example, in most cases, mycorrhizal fungi provide nutrients to forest trees, pollinators help flowering plants set fruit, intestinal bacteria promote nutrient uptake across diverse animal taxa, bacteria in lucinid clams help detoxify benthic sediments, and photosynthetic algae help maintain the coral reefs that structure nearshore marine environments around the world (3–6).However, while both partners in a mutualism usually receive net benefits from the interaction, mutualisms also usually impose costs on one or both partners interacting mutualistically. In the absence of fitness-aligning mechanisms between the partners (e.g., vertical transmission of symbionts, or repeated interactions with immediate fitness benefits), theory suggests that other mechanisms are needed to maintain a mutualism’s stability. Specifically, it has been proposed that a mutualism’s long-term stability often depends on mechanisms that limit the invasion of “cheater” individuals into the populations of either partner species (2, 3, 7–14). Broadly, cheaters can be defined as individuals (or species) that do not provide a beneficial service to their partners. By not providing a potentially costly service to their partners, cheaters are thought to benefit themselves relative to “cooperating” individuals or species in the short term (12–14). Invasion by such cheaters potentially erodes the net benefits resulting from the interaction, and therefore can lead to a breakdown of the mutualism itself.Consistent with this viewpoint, data suggest that in many cases the hosts (the larger of the two partners in the mutualism) can effectively promote cooperation by selectively allocating more resources to those symbionts that provide them with greater benefits. For example, some legumes have been shown to selectively allocate more resources to nodules containing rhizobia that are better at providing fixed nitrogen (14–16). In other studies, some host plants allocate more carbon to strains of mycorrhizal fungi that provide their hosts with more phosphorus (17–19).However, other authors question the biological relevance of much of this experimental evidence to natural species interactions, the direction of cause and effect, and the actual costs for providing benefits. A central question is the degree to which evidence for cheaters, defined as receiving fitness benefits by not providing services (relative to a mutualist that does provide benefits), exist at all (12, 13, 20). Key empirical issues concern whether or not individuals with a cheating phenotype do, in fact, cheat (impose a reproductive cost on their partner, relative to a cooperating mutualist). In addition, are cheating individuals that fail to benefit their host at least as fit as cooperating (mutualistic) individuals that do? Does the host allocate relatively more resources to more beneficial partners (effectively expressing sanctions against cheaters relative to cooperators)? Ultimately, this becomes a set of specific empirical questions: What is the relative fitness of cooperators and cheaters that interact with the same partner (host)? And, does the host effectively sanction cheaters relative to cooperators, and if so, to what degree (21, 22)? At a fundamental level, the relative fitness of cheaters and cooperators is only measurable and relevant within the context of a given host’s responses to them (3, 21, 22).To resolve these questions, it is useful to study those mutualistic host–symbiont interactions in which it is straightforward to measure and experimentally manipulate both benefits and costs to each partner under natural conditions (22–32). Ideally, we should be able to comparatively assess experimental results across a diversity of host–symbiont mutualisms that differ in what theory suggests should be key metrics (e.g., strength of host sanctions, existence and relative abundance of cheaters, and so forth).The over 750 species of host figs (Ficus: Moraceae) and their obligately pollinating wasps (Agaonidae: Hymenoptera) provide such a range of both experimental and comparative options that can be exploited to address these questions (22–32) (SI Appendix, Supplementary Text and Fig. S1). Ovipositing female fig wasps deposit a drop of fluid from their poison sac into the ovules of flowers into which they lay their eggs. This fluid initiates the formation of gall tissue upon which the developing larvae feed (33) (SI Appendix). At any given site, each fig species is typically pollinated by only one or two fig wasp species (24, 26). Morphological and molecular studies broadly support coevolution between genera of pollinating wasps and their respective sections of figs, while functional studies demonstrate coadaptation between them (33–51).For example, different groups of figs are characterized by either active or passive pollination (43–45) (SI Appendix). Passive pollination does not require specialized wasp morphologies or behaviors. In contrast, active pollination requires specialized female wasp morphologies and behaviors (44). The wasps collect pollen in their natal fig using coxal combs on their forelegs and store it in pollen pockets on their thoraxes (Fig. 1). After emerging from their natal figs, female wasps use volatile chemical scent cues produced by receptive figs to identify them (35–37). Dispersal flights from the natal fig are aided by prevailing winds and routinely cover scores of kilometers (38–41). Upon finding and entering a receptive fig of an appropriate host species, the foundress wasps repeatedly remove a few grains of pollen from their pockets and place them on the stigmatic surfaces of the individual flowers on which they attempt to lay eggs. Active pollination provides clear benefits for the host fig. Pollination is more efficient in actively pollinated fig species relative to passively pollinated species. This is reflected in the dramatically lower (∼1/10) amounts of pollen that active species typically produce (43–45). Conversely, active pollination appears to be costly for the wasps in terms of specialized body structures, energy, and time (22, 42, 45).Open in a separate windowFig. 1.Receptive F. microcarpa fig and pollinating structures of E. verticillata compared with Eupristina sp. (A) A cheater wasp (Eupristina sp.) laying eggs in a receptive fig of her host F. microcarpa. Pollinator wasps (E. verticillata) (B and C) have specialized morphological structures such as pollen pockets (black arrow) on the underside of their thorax and coxal combs on their forelegs (white arrows) that facilitate pollination. Pollen is stored in the pockets and coxal combs facilitate pollen transfer (43, 44). Cheater wasps (Eupristina sp.) (D and E) retain pollen pockets (black arrow) but lack coxal combs (white arrow).The most basic mutualistic services (e.g., the wasp’s ability to pollinate) can be experimentally manipulated. By allowing or restricting the female pollinator wasps’ access to, and ability to actively collect pollen, pollinators that either do (P+) or do not (P−) carry pollen can be produced and then introduced into receptive figs (22). Furthermore, the effects on pollinator wasp fitness (i.e., lifetime reproductive success) of pollinating the host fig (or not) can be quantified by counting their relative number of offspring in naturally occurring figs (22–32). Moreover, the many existing experimental studies using the same methodologies provide context for the findings of any given experiment (22–32). In previous experiments on actively pollinated fig species, wasps that do not pollinate (P−) have lower fitness than wasps that pollinate (P+) due to increased rates of fig abortion (killing all wasp larvae) and increased larval mortality reducing the number of P− offspring that emerge. These “host sanctions” are likely caused by selective resource allocation by the tree to better-pollinated figs (28). Although pollination typically leads to a higher number of wasp offspring, pollination is not an absolute requirement for wasp offspring to develop (28). Finally, there are at least two known cases of cheating wasp species, in which species of wasps that lack both morphologies and behaviors that permit efficient, active pollination of their host co-occur with a congeneric pollinator possessing these traits. Importantly, the species that lack these traits have clearly evolved within lineages of wasps that otherwise possess these apparently costly traits that permit them to actively pollinate their host (52, 53) (SI Appendix).Here, we exploit the opportunity provided by a third case (54, 55), in which a mutualistic active pollinator and a congeneric cheater species co-occur on the same monoecious host fig. Specifically, we conducted a combination of behavioral, morphological, phylogenetic, and experimental studies to compare these wasps and the outcomes of their interactions with their shared host fig, Ficus microcarpa (subgenus Urostigma: section Urostigma: subsection Conosycea), in and near the Xishuangbanna Tropical Botanical Garden (XTBG), China. Eupristina verticillata is the described active pollinator of F. microcarpa at this location, while an undescribed coexisting wasp species (Eupristina sp.) lacks the necessary adaptation for active pollination and appears to be a cheater (54, 55).In this study, we address and answer the following questions: 1) Does the undescribed Eupristina sp. wasp associated with F. microcarpa impose a reproductive cost on its host? We find that it does, and that the cost for host reproductive success is large. 2) Does the cheater exhibit significantly higher levels of reproductive success than the pollinator in their host? Yes, in both direct and indirect competition. Combined with the reproductive loss it imposes on the host, this species meets the strictest definition of cheater. 3) Is this cheater closely related (possibly a sister species) to the mutualist pollinator of their shared host? We find that within the context of other sympatric Eupristina species associated with seven fig hosts in this area, it is. Furthermore, it represents an independent loss of pollination structures from another case previously reported in this genus. 4) Does the host (F. microcarpa) locally exhibit detectable host sanctions against wasps that do not pollinate it? In sharp contrast with all 15 other cases of actively pollinated Ficus species that have been reported (22, 29–32), we find that it does not. 5) Given that cheaters exhibit equal or greater fitness than the pollinator, how do they coexist? Although deserving further study, we suggest that regular seasonal fluctuations in the relative abundances of the two wasp species facilitate their coexistence at this site (54, 55). Seasonal changes in the prevalence of westerly winds cause regional spatial heterogeneity in source pools of pollinators and cheaters that immigrate to the local host, F. microcarpa.     

From the Cover: A single macrolichen constitutes hundreds of unrecognized species

The number of Fungi is estimated at between 1.5 and 3 million. Lichenized species are thought to make up a comparatively small portion of this figure, with unrecognized species richness hidden among little-studied, tropical microlichens. Recent findings, however, suggest that some macrolichens contain a large number of unrecognized taxa, increasing known species richness by an order of magnitude or more. Here we report the existence of at least 126 species in what until recently was believed to be a single taxon: the basidiolichen fungus Dictyonema glabratum, also known as Cora pavonia. Notably, these species are not cryptic but morphologically distinct. A predictive model suggests an even larger number, with more than 400 species. These results call into question species concepts in presumably well-known macrolichens and demonstrate the need for accurately documenting such species richness, given the importance of these lichens in endangered ecosystems such as paramos and the alarming potential for species losses throughout the tropics.Fungi make up the second largest kingdom, with an estimated number of 1.5–3 million species (1–3). Lichenization plays an important role in fungal evolution, particularly in the Ascomycota, where lichens make up 30% of the currently recognized species (4–6). Transition toward a lichenized lifestyle appears to have taken place at least 10 times in the Ascomycota and 5 times in the Basidiomycota (7–9), but the distribution of lichen formers favors the Ascomycota, with the Basidiomycota accounting for less than 0.3% of all lichenized Fungi (7, 10). Altogether, ∼18,000 lichenized species are currently accepted, but estimates suggest that this represents only 50–65% of the true species richness (4, 6).Global species richness of lichenized Basidiomycota appears to be especially underestimated. The Dictyonema clade, which includes some of the best-known basidiolichens, until recently was considered to represent five species in a single genus, Dictyonema (11, 12). Subsequent taxonomic and molecular phylogenetic studies suggested that this concept did not reflect the true diversity in this clade (7, 12, 13). Currently, a total of 43 species are recognized in five genera (14, 15). Two genera, Cora and Corella, are foliose macrolichens, with a total of 16 species, corresponding to what was considered a single species, Dictyonema glabratum (11, 12, 16). This name is well known in the scientific community and even among nonspecialists and is included in the Listing of Interesting Plants of the World (17). The 16-fold increase in the number of species now recognized is a striking figure that even surpasses recent findings reported from the large macrolichens Lobariella and Sticta in the Ascomycota (18, 19). The dramatic change in the taxonomic concept of these basidiolichens has important implications for recognizing their role in ecosystem function and as model organisms. Species of Cora abound in tropical montane regions and, with their cyanobacterial photobionts capable of fixing atmospheric nitrogen, serve as biological fertilizers (20). Cora is also one of the best studied lichens in terms of ecomorphology, ecophysiology, and biochemistry (10, 21–28).     

Region effects influence local tree species diversity

Global patterns of biodiversity reflect both regional and local processes, but the relative importance of local ecological limits to species coexistence, as influenced by the physical environment, in contrast to regional processes including species production, dispersal, and extinction, is poorly understood. Failure to distinguish regional influences from local effects has been due, in part, to sampling limitations at small scales, environmental heterogeneity within local or regional samples, and incomplete geographic sampling of species. Here, we use a global dataset comprising 47 forest plots to demonstrate significant region effects on diversity, beyond the influence of local climate, which together explain more than 92% of the global variation in local forest tree species richness. Significant region effects imply that large-scale processes shaping the regional diversity of forest trees exert influence down to the local scale, where they interact with local processes to determine the number of coexisting species.Ecologists generally agree that large-scale patterns of diversity reflect a balance between regional processes of species production, extinction, and dispersal, on one hand, and within-region sorting of species based on adaptations to physical conditions of the environment, as well as competition among species for limiting resources, on the other hand (1–4). Nonetheless, the spatial scale down to which region effects extend has not been well resolved (5–7), but has wide-ranging implications for understanding the origins of patterns in local species richness. If the species richness of a local assemblage were strictly limited by competition and other local interactions among populations, new species could not be added without others being forced out, and we would expect to find a common relationship between diversity and local environmental conditions across regions (6). However, if unique historical and biogeographic features of each region influenced within-region diversification and extinction (8–10), these region-specific effects might contribute to the global pattern in local species richness. Efforts to disentangle these effects have met with limited success and have led to a long-standing discussion of the relationship between local and regional diversity (6, 11–21).Analyses designed to distinguish local and regional influences on diversity have found strong region effects in some cases (8, 22) and weak or nonexistent region effects in others (15, 23–25). However, most studies that failed to find significant region effects either have addressed large, biologically heterogeneous samples, or they have used local samples (e.g., 0.1-ha “Gentry” plots) that are too small to characterize the diversity of local assemblages adequately (26, 27). Additionally, many large-scale samples have been compiled from maps generated from presence-only museum records or from coarse-scale atlases that document the extent of species occupancy, not actual local occurrence. Such data often undercount local species richness. Moreover, many tests of the diversity–environment relationship have analyzed data on local communities that extend over broad ranges of ecological conditions (e.g., tropical rainforests to arctic tundra and hot deserts; ref. 25) with a range of biomes and vegetation types unevenly represented among regions. These sampling issues have confounded the testing of region effects.In this study, we analyze a dataset of tree species richness from the Center for Tropical Forest Science—Forest Global Earth Observatories (CTFS—ForestGEO; www.forestgeo.si.edu/; ref. 28) to disentangle the influences of local climate and regional factors, i.e., differences between regions resulting from unique histories and geographic settings, on the global biodiversity pattern. The data represent 47 forest dynamics plots distributed worldwide (Fig. 1) with a median size of 25 ha, within which all individual trees equal to or greater than 1 cm diameter at breast height (DBH) were identified and counted (SI Appendix, Table S1). Plots of this size are large enough to include adequate samples of species richness, but small enough to avoid substantial heterogeneity in climate and vegetation structure within them. The CTFS data are complete censuses, and the species richness in each plot is accurate. Many previous studies have been based on data from herbarium records of coarse-scale species range maps, and species richness is generally underestimated, considerably so in some cases. Moreover, the forest plots represent a single vegetation type surveyed over a range of environmental conditions. We assembled for each plot a set of local plot characteristics and climate data, and used generalized linear models to characterize the relationship between number of tree species and local plot variables and to test the additional statistical effect of region on local species richness. Our analyses were repeated for species richness with tree DBH ≥ 1 cm and DBH ≥ 10 cm.Open in a separate windowFig. 1.Global distribution of the 47 CTFS plots. The number associated with each plot is its size in hectares. The base vegetation map is the 2012 MODIS global land cover map (www.landcover.org/data/lc/) with IGBP Land Cover Type Classification.     

From the Cover: Global patterns of raptor distribution and protected areas optimal selection to reduce the extinction crises

Globally, human-caused environmental impacts, such as habitat loss, have seriously impacted raptor species, with some 50% of species having decreasing populations. We analyzed global patterns of distribution of all 557 raptor species, focusing on richness, endemism, geographic range, conservation status, and population trends. Highest species diversity, endemism, species at risk, or restricted species were concentrated in different regions. Patterns of species distribution greatly differed between nocturnal and diurnal species. To test the efficiency of the global protected areas in conserving raptors, we simulated and compared global reserve systems created with strategies aiming at: 1) constraining the existing system into the final solution; and 2) minimizing the socioeconomic cost of reserve selection. We analyzed three targets of species distribution to be protected (10, 20, 30%). The first strategy was more efficient in meeting targets and less efficient in cost and compactness of reserves. Focusing on actions in the existing protected areas is fundamental to consolidate conservation, and politically and economically more viable than creating new reserves. However, creating new reserves is essential to protect more populations throughout the species’ geographic range. Our findings provide a fundamental understanding of reserves to maintain raptor diversity and reduce the global population and species extinction crisis.

Human activities are responsible for the catastrophic decline and extinction of thousands of animal and plant species throughout the world, and this loss is occurring at unprecedented rates (1–6). Raptors are some of the most threatened vertebrate taxa, and in the last three decades many species have experienced severe population declines or faced extinction (7, 8). This threat is primarily the result of habitat loss and fragmentation, pollution, human–wildlife conflicts, and global climate alterations (5–9). The relationship between raptors and humans is seemingly contradictory. Historically, raptors were important icons in different cultures and have been used for falconry in many places globally. In contrast, they have been persecuted due to conflicts with human interests, namely predation of game species and livestock (9). As top predators, raptors are flagship, umbrella, or keystone species and are used as surrogate species in biodiversity conservation efforts (9, 10). From an ecological perspective, raptors are top predators and scavengers, critical for maintaining ecosystem structure and function and ecosystem services (11–18). Their effect on trophic webs extends to the lower levels (e.g., herbivores), linking ecosystem processes and energy fluxes (12, 19). Raptors also indirectly increase seed production and control pest species by preying on a wide range of vertebrates and facilitate long-distance seed dispersal (19, 20).The population decline of some raptor species during the last few decades has been so dramatic that they face extinction unless effective conservation measures are implemented (Fig. 1) (7, 8). For example, the population of the Philippine eagle (Pithecophaga jefferyi), the largest eagle in the world, is decreasing very rapidly due to extensive deforestation (21). Some vulture species in Asia and Africa have undergone startling population decreases in recent years because of toxification and habitat loss (22–24). As scavengers, vultures contribute to regulating ecosystem services by recycling dead matter and preventing the spread of diseases (24). Despite such beneficial roles for humans, some vulture populations have declined by over 95% in many Asian countries, such as India, because of the widespread use of diclofenac, a nonsteroidal antiinflammatory drug (22, 23). In Africa, particularly West Africa, vulture populations have decreased by an average of 95% in rural areas over the last 30 y as the result of shooting, harassment, and poisoning through feeding on carcasses of livestock treated with diclofenac (23). The Annobon scops-owl (Otus feae), with an estimated population of fewer than 250 individuals and restricted to Annobon Island off West Africa, was recently classified as critically endangered because of rapid habitat loss and degradation (25).Open in a separate windowFig. 1.Examples of diurnal and nocturnal raptor species. Ridgway’s hawk (Buteo ridgwayi) is critically endangered and endemic to a very restricted region in the Dominican Republic (Top Left image credit: C.C.). The Harpy eagle (Harpia harpyja) is the largest eagle of the Neotropical region, with decreasing populations (Top right image credit; Carlos Navarro [photographer]). The Egyptian vulture (Neophron percnopterus), although widely distributed in southern Europe and northern Africa to India, is endangered (Bottom Left image credit: Subramaya Chandrashekar [photographer]). The brown fish owl (Ketupa zeylonensis) is a common species found in tropical regions of the Indian subcontinent (Bottom Right image credit: Subramaya Chandrashekar [photographer]).Recent assessments maintain that the world has entered the sixth mass extinction period, and habitat loss and degradation, primarily the result of rapid human population growth and its associated impacts, suggest that the future of wildlife in general, and of raptors in particular, is not encouraging (4, 6, 26). Estimates suggest that the overall vertebrate populations have decreased by 70% since 1970 (27). Evaluation of distribution patterns of taxonomic groups at different spatial scales is essential to understanding the full scope of the threats to biodiversity and developing conservation actions to mitigate them (e.g., refs. 5 and 28). Resource planners and managers can capitalize on the large amount of high-resolution global data on species distribution and conservation status to develop broad-scale strategies (1, 29–32). So, understanding the patterns of distribution of groups of species, especially those that are endangered with extinction, is fundamental to define large-scale conservation strategies (7, 8, 30–34). Two recent seminal studies have addressed the broad-scale patterns of raptor distribution, emphasizing the importance of hotspots of diversity concentrations and defining priority conservation actions, on the one hand, and the importance of supporting conservation strategies based on endemic and endangered species, on the other. Those studies have been fundamental to frame our current study (7, 8).Increasing accessibility to global-level data on land-use and socioeconomic features provides essential tools for the valuation of potential conflicts with human activities and cost estimations (actual or relative) of conservation priority areas for specific taxa (35–38). Integrating biological and socioeconomic objectives in global conservation planning has become essential in optimizing both the selection of protected areas and investment allocation (35), especially for those countries where socioeconomic instability corresponds to poor conservation outcomes (36, 39). In this study, we present a global analysis of the distribution patterns of 557 of all raptor species in order to evaluate conservation priorities based on four parameters: 1) global distribution patterns of total, diurnal, and nocturnal species, species at risk, endemic species, and species with restricted ranges; 2) species population trends (i.e., decreasing, stable, or increasing); 3) selection of areas that minimize conflict with human activities; and 4) effectiveness of the protected area network.     

From the Cover: A holistic picture of Austronesian migrations revealed by phylogeography of Pacific paper mulberry

The peopling of Remote Oceanic islands by Austronesian speakers is a fascinating and yet contentious part of human prehistory. Linguistic, archaeological, and genetic studies have shown the complex nature of the process in which different components that helped to shape Lapita culture in Near Oceania each have their own unique history. Important evidence points to Taiwan as an Austronesian ancestral homeland with a more distant origin in South China, whereas alternative models favor South China to North Vietnam or a Southeast Asian origin. We test these propositions by studying phylogeography of paper mulberry, a common East Asian tree species introduced and clonally propagated since prehistoric times across the Pacific for making barkcloth, a practical and symbolic component of Austronesian cultures. Using the hypervariable chloroplast ndhF-rpl32 sequences of 604 samples collected from East Asia, Southeast Asia, and Oceanic islands (including 19 historical herbarium specimens from Near and Remote Oceania), 48 haplotypes are detected and haplotype cp-17 is predominant in both Near and Remote Oceania. Because cp-17 has an unambiguous Taiwanese origin and cp-17–carrying Oceanic paper mulberries are clonally propagated, our data concur with expectations of Taiwan as the Austronesian homeland, providing circumstantial support for the “out of Taiwan” hypothesis. Our data also provide insights into the dispersal of paper mulberry from South China “into North Taiwan,” the “out of South China–Indochina” expansion to New Guinea, and the geographic origins of post-European introductions of paper mulberry into Oceania.The peopling of Remote Oceania by Austronesian speakers (hereafter Austronesians) concludes the last stage of Neolithic human expansion (1–3). Understanding from where, when, and how ancestral Austronesians bridged the unprecedentedly broad water gaps of the Pacific is a fascinating and yet contentious subject in anthropology (1–8). Linguistic, archaeological, and genetic studies have demonstrated the complex nature of the process, where different components that helped to shape Lapita culture in Near Oceania each have their own unique history (1–3). Important evidence points to Taiwan as an Austronesian ancestral homeland with a more distant origin in South China (S China) (3, 4, 9–12), whereas alternative models suggest S China to North Vietnam (N Vietnam) (7) or a Southeast Asian (SE Asian) origin based mainly on human genetic data (5). The complexity of the subject is further manifested by models theorizing how different spheres of interaction with Near Oceanic indigenous populations during Austronesian migrations have contributed to the origin of Lapita culture (1–3), ranging from the “Express Train” model, assuming fast migrations from S China/Taiwan to Polynesia with limited interaction (4), to the models of “Slow Boat” (5) or “Voyaging Corridor Triple I,” in which “Intrusion” of slower Austronesian migrations plus the “Integration” with indigenous Near Oceanic cultures had resulted in the “Innovation” of the Lapita cultural complex (2, 13).Human migration entails complex skills of organization and cultural adaptations of migrants or colonizing groups (1, 3). Successful colonization to resource-poor islands in Remote Oceania involved conscious transport of a number of plant and animal species critical for both the physical survival of the settlers and their cultural transmission (14). In the process of Austronesian expansion into Oceania, a number of animals (e.g., chicken, pigs, rats, and dogs) and plant species (e.g., bananas, breadfruit, taro, yam, paper mulberry, etc.), either domesticated or managed, were introduced over time from different source regions (3, 8, 15). Although each of these species has been shown to have a different history (8), all these “commensal” species were totally dependent upon humans for dispersal across major water gaps (6, 8, 16). The continued presence of these species as living populations far outside their native ranges represents legacies of the highly skilled seafaring and navigational abilities of the Austronesian voyagers.Given their close association to and dependence on humans for their dispersal, phylogeographic analyses of these commensal species provide unique insights into the complexities of Austronesian expansion and migrations (6, 8, 17). This “commensal approach,” first used to investigate the transport of the Pacific rat Rattus exulans (6), has also been applied to other intentionally transported animals such as pigs, chickens, and the tree snail Partula hyalina, as well as to organisms transported accidentally, such as the moth skink Lipinia noctua and the bacterial pathogen Helicobacter pylori (see refs. 2, 8 for recent reviews).Ancestors of Polynesian settlers transported and introduced a suite of ∼70 useful plant species into the Pacific, but not all of these reached the most isolated islands (15). Most of the commensal plants, however, appear to have geographic origins on the Sahul Plate rather than being introduced from the Sunda Plate or East Asia (16). For example, Polynesian breadfruit (Artocarpus altilis) appears to have arisen over generations of vegetative propagation and selection from Artocarpus camansi that is found wild in New Guinea (18). Kava (Piper methysticum), cultivated for its sedative and anesthetic properties, is distributed entirely to Oceania, from New Guinea to Hawaii (16). On the other hand, ti (Cordyline fruticosa), also a multifunctional plant in Oceania, has no apparent “native” distribution of its own, although its high morphological diversity in New Guinea suggests its origin there (19). Other plants have a different history, such as sweet potato, which is of South American origin and was first introduced into Oceania in pre-Columbian times and secondarily transported across the Pacific by Portuguese and Spanish voyagers via historically documented routes from the Caribbean and Mexico (17).Of all commensal species introduced to Remote Oceania as part of the “transported landscapes” (1), paper mulberry (Broussonetia papyrifera; also called Wauke in Hawaii) is the only species that has a temperate to subtropical East Asian origin (15, 20, 21). As a wind-pollinated, dioecious tree species with globose syncarps of orange–red juicy drupes dispersed by birds and small mammals, paper mulberry is common in China, Taiwan, and Indochina, growing and often thriving in disturbed habitats (15, 20, 21). Because of its long fiber and ease of preparation, paper mulberry contributed to the invention of papermaking in China in A.D. 105 and continues as a prime source for high-quality paper (20, 21). In A.D. 610, this hardy tree species was introduced to Japan for papermaking (21). Subsequently it was also introduced to Europe and the United States (21). Paper mulberry was introduced to the Philippines for reforestation and fiber production in A.D. 1935 (22). In these introduced ranges, paper mulberry often becomes naturalized and invasive (20–22). In Oceania, linguistic evidence suggests strongly an ancient introduction of paper mulberry (15, 20); its propagation and importance across Remote Oceanic islands were well documented in Captain James Cook’s first voyage as the main material for making barkcloth (15, 20).Barkcloth, generally known as tapa (or kapa in Hawaii), is a nonwoven fabric used by prehistoric Austronesians (15, 21). Since the 19th century, daily uses of barkcloth have declined and were replaced by introduced woven textiles; however, tapa remains culturally important for ritual and ceremony in several Pacific islands such as Tonga, Fiji, Samoa, and the SE Asian island of Sulawesi (23). The symbolic status of barkcloth is also seen in recent revivals of traditional tapa making in several Austronesian cultures such as Taiwan (24) and Hawaii (25). To make tapa, the inner bark is peeled off and the bark pieces are expanded by pounding (20, 21, 23). Many pieces of the bark are assembled and felted together via additional poundings to create large textiles (23). The earliest stone beaters, a distinctive tool used for pounding bark fiber, were excavated in S China from a Late Paleolithic site at Guangxi dating back to ∼8,000 y B.P. (26) and from coastal Neolithic sites in the Pearl River Delta dating back to 7,000 y B.P. (27), providing the earliest known archaeological evidence for barkcloth making. Stone beaters dated to slightly later periods have also been excavated in Taiwan (24), Indochina, and SE Asia, suggesting the diffusion of barkcloth culture to these regions (24, 27). These archaeological findings suggest that barkcloth making was invented by Neolithic Austric-speaking peoples in S China long before Han-Chinese influences, which eventually replaced proto-Austronesian language as well as culture (27).In some regions (e.g., Philippines and Solomon Islands), tapa is made of other species of the mulberry family (Moraceae) such as breadfruit and/or wild fig (Ficus spp.); however, paper mulberry remains the primary source of raw material to produce the softest and finest cloth (20, 23). Before its eradication and extinction from many Pacific islands due to the decline of tapa culture, paper mulberry was widely grown across Pacific islands inhabited by Austronesians (15, 20). Both the literature (15, 20) and our own observations (28–30) indicate that extant paper mulberry populations in Oceania are only found in cultivation or as feral populations in abandoned gardens as on Rapa Nui (Easter Island), with naturalization only known from the Solomon Islands (20). For tapa making, its stems are cut and harvested before flowering, and as a majority of Polynesian-introduced crops (16), paper mulberry is propagated clonally by cuttings or root shoots (15, 20), reducing the possibility of fruiting and dispersal via seeds. The clonal nature of the Oceanic paper mulberry has been shown by the lack of genetic variability in nuclear internal transcribed spacer (ITS) DNA sequences (31). With a few exceptions (30), some authors suggest that only male trees of paper mulberry were introduced to Remote Oceania in prehistoric time (15, 20). Furthermore, because paper mulberry has no close relative in Near and Remote Oceania (20), the absence of sexual reproduction precludes the possibility of introgression and warrants paper mulberry as an ideal commensal species to track Austronesian migrations (6, 30).To increase our understanding of the prehistoric Austronesian expansion and migrations, we tracked geographic origins of Oceanic paper mulberry, the only Polynesian commensal plant likely originating in East Asia, using DNA sequence variation of the maternally inherited (32) and hypervariable (SI Text) chloroplast ndhF-rpl32 intergenic spacer (33). We sampled broadly in East Asia (Taiwan, S China, and Japan) and SE Asia (Indochina, the Philippines, and Sulawesi) as well as Oceanic islands where traditional tapa making is still practiced. Historical herbarium collections (A.D. 1899–1964) of Oceania were also sampled to strengthen inferences regarding geographic origins of Oceanic paper mulberry. The employment of ndhF-rpl32 sequences and expanded sampling greatly increased phylogeographic resolution not attainable in a recent study (31) using nuclear ITS sequences (also see SI Text and Fig. S1) and intersimple sequence repeat (ISSR) markers with much smaller sampling.Open in a separate windowFig. S1.ITS haplotype network (n = 17, A–Q) and haplotype distribution and frequency. The haplotype network was reconstructed using TCS (34), with alignment gaps treated as missing data. The sizes of the circles and pie charts are proportional to the frequency of the haplotype (shown in parentheses). Squares denote unique haplotypes (haplotype found only in one individual).     

Ancestral polymorphisms shape the adaptive radiation of Metrosideros across the Hawaiian Islands

Some of the most spectacular adaptive radiations begin with founder populations on remote islands. How genetically limited founder populations give rise to the striking phenotypic and ecological diversity characteristic of adaptive radiations is a paradox of evolutionary biology. We conducted an evolutionary genomics analysis of genus Metrosideros, a landscape-dominant, incipient adaptive radiation of woody plants that spans a striking range of phenotypes and environments across the Hawaiian Islands. Using nanopore-sequencing, we created a chromosome-level genome assembly for Metrosideros polymorpha var. incana and analyzed whole-genome sequences of 131 individuals from 11 taxa sampled across the islands. Demographic modeling and population genomics analyses suggested that Hawaiian Metrosideros originated from a single colonization event and subsequently spread across the archipelago following the formation of new islands. The evolutionary history of Hawaiian Metrosideros shows evidence of extensive reticulation associated with significant sharing of ancestral variation between taxa and secondarily with admixture. Taking advantage of the highly contiguous genome assembly, we investigated the genomic architecture underlying the adaptive radiation and discovered that divergent selection drove the formation of differentiation outliers in paired taxa representing early stages of speciation/divergence. Analysis of the evolutionary origins of the outlier single nucleotide polymorphisms (SNPs) showed enrichment for ancestral variations under divergent selection. Our findings suggest that Hawaiian Metrosideros possesses an unexpectedly rich pool of ancestral genetic variation, and the reassortment of these variations has fueled the island adaptive radiation.

Adaptive radiations exhibit extraordinary levels of morphological and ecological diversity (1). Although definitions of adaptive radiation vary (2–7), all center on ecological opportunity as a driver of adaptation and, ultimately, diversification (2, 8–10). Divergent selection, the primary mechanism underlying adaptive radiations, favors extreme phenotypes (11) and selects alleles that confer adaptation to unoccupied or under-utilized ecological niches. Differential adaptation results in divergence and, ultimately, reproductive isolation between populations (12). Adaptive radiations demonstrate the remarkable power of natural selection as a driver of biological diversity and provide excellent systems for studying evolutionary processes involved in diversification and speciation (13).Adaptive radiations on remote oceanic islands are especially interesting, as colonization of remote islands is expected to involve population bottlenecks that restrict genetic variation (14). Adaptive radiations in such settings are especially impressive and even paradoxical, given the generation of high species richness from an initially limited gene pool (15). Several classic examples of adaptive radiation occur on oceanic islands, such as Darwin’s finches from the Galapagos islands (16), anole lizards from the Caribbean islands (9), Hawaiian Drosophilids (17), and Hawaiian silverswords (18), to name a few.Recent advances in genome sequencing and analyses have greatly improved our ability to examine the genetics of speciation and adaptive radiation. By examining sequences of multiple individuals from their natural environment, it has become possible to “catch in the act” the speciation processes between incipient lineages (19). Genomic studies of early stage speciation show that differentiation accumulates in genomic regions that restrict the homogenizing effects of gene flow between incipient species (20). The number, size, and distribution of these genomic regions can shed light on evolutionary factors involved in speciation (19). Regions of high genomic differentiation can also form from evolutionary factors unrelated to speciation, such as linkage associated with recurrent background selection or selective sweeps on shared genomic features (21, 22).Genomic studies of lineages undergoing rapid ecological diversification have begun to reveal the evolutionary mechanisms underlying adaptive radiations. Importantly, these studies highlight the pivotal role of hybridization between populations and the consequent exchange of adaptive alleles that facilitates rapid speciation and the colonization of diverse niches (23–25). Most genomic studies of adaptive radiation involve animal systems, however, in particular, birds and fishes. In plants, genomic studies of adaptive radiation are sparse (26–28), and all examine continent-wide radiations. There are no genomics studies of plant adaptive radiations in geographically restricted systems such as remote islands. Because the eco-evolutionary scenarios associated with adaptive radiations are diverse (5, 29), whether commonalities identified in adaptive radiations in animals (23, 30) are applicable to plants is an open question. For example, the genetic architecture of animal adaptive radiations typically involves differentiation at a small number of genomic regions (31–33). In contrast, the limited insights available for plants suggest a more complex genetic architecture (26).We investigated the evolutionary genomics of adaptive radiation in Metrosideros Banks ex Gaertn. (Myrtaceae) across the Hawaiian Islands. Hawaiian Metrosideros is a landscape-dominant, hypervariable, and highly dispersible group of long-lived (possibly >650 y) (34) woody taxa that are nonrandomly distributed across Hawaii’s heterogeneous landscape, including cooled lava flows, wet forests and bogs, subalpine zones, and riparian zones (35, 36). About 25 taxa or morphotypes are distinguished by vegetative characters ranging from prostate plants that flower a few centimeters above ground to 30-m-tall trees, and leaves range dramatically in size, shape, pubescence, color, and rugosity (35, 37, 38); a majority of these forms are intraspecific varieties or races (provisional varieties) of the abundant species, Metrosideros polymorpha (35, 36, 38). Variation in leaf mass per area within the four Metrosideros taxa on Hawaii Island alone matches that observed for woody species globally (39). Common garden experiments (38, 40–44) and parent–offspring analysis (45) demonstrate heritability of taxon-diagnostic vegetative traits, indicating that taxa are distinct genetic groups and not the result of phenotypic plasticity. Metrosideros taxa display evidence of local adaptation to contrasting environments (46, 47), suggesting ecological divergent selection is responsible for diversification within the group (48). This diversification, which spans the past ∼3.1 to 3.9 million years (49, 50), has occurred despite the group’s high capacity for gene flow by way of showy bird-pollinated flowers and tiny wind-dispersed seeds (36, 51). Lastly, the presence of partial reproductive isolating barriers between taxa is consistent with the early stages of speciation (52). Here, we generated several genomic resources for Hawaiian Metrosideros and used these in population genomics analyses to gain deeper insights into the genomic architecture and evolutionary processes underlying this island adaptive radiation.     

Form,function, and evolution of living organisms

Despite the vast diversity of sizes and shapes of living organisms, life’s organization across scales exhibits remarkable commonalities, most notably through the approximate validity of Kleiber’s law, the power law scaling of metabolic rates with the mass of an organism. Here, we present a derivation of Kleiber’s law that is independent of the specificity of the myriads of organism species. Specifically, we account for the distinct geometries of trees and mammals as well as deviations from the pure power law behavior of Kleiber’s law, and predict the possibility of life forms with geometries intermediate between trees and mammals. We also make several predictions in excellent accord with empirical data. Our theory relates the separate evolutionary histories of plants and animals through the fundamental physics underlying their distinct overall forms and physiologies.Understanding the origin and evolution of the geometries of living forms is a formidable challenge (1, 2). The geometry of an object can be characterized by its surface−volume relationship—the surface area S of an object of volume V can scale at most as and at least as (3). These geometries have been used by nature in space-filling trees and animals, respectively. Here, our principal goal is to explore how it is that both geometries of life coexist on Earth, whether intermediate geometries are possible, and what all this implies for evolution of life on Earth.Living organisms span an impressive range of body mass, shapes, and scales. They are inherently complex, they have been shaped by history through evolution and natural section, and they continually extract, transform, and use energy from their environment. The most prevalent large multicellular organisms on Earth, namely plants and animals, exhibit distinct shapes, as determined by the distribution of mass over the volume. Animals are able to move and are approximately homogeneous in their mass distribution—yet they have beautiful fractal transportation networks. Plants are rooted organisms with a heterogeneous self-similar (fractal) geometry—the mass of the tree is more concentrated in the stem and branches than in the leaves.The approximate power law dependence of the metabolic rate, the rate at which an organism burns energy, on organism mass has been carefully studied for nearly two centuries and is known as allometric scaling (4–32). From the power law behavior, with an exponent around 3/4, one can deduce the scaling of characteristic quantities with mass and, through dimensional analysis, obtain wide-ranging predictions often in accord with empirical data. However, what underlies this ubiquitous quarter-power scaling, and with a dominant exponent of 3/4?In an influential series of papers, West and coworkers (11, 12, 14–16) suggested that fractality was at the heart of allometric scaling. Inspired by these papers, a contrasting view was presented (13), which argued that, although fractal circulatory networks may have advantages, quarter-power scaling came built in with the directed transport of nutrients. However, this latter paper was necessarily incomplete because it did not address the distinct geometries of animals and trees. More recently, members of both groups joined together to construct explicit models for animals, which showed (24) that “quarter-power scaling can arise even when there is no underlying fractality.” Here, we take a fresh look at the problem and derive quarter-power scaling quite generally for all living organisms. We then turn to a consideration of the sharp differences in the geometries of animals and trees and argue that the evolution of organismal forms follows from a rich interplay of geometry, evolutionary history, developmental symmetry, and efficient nutrient acquisition.Despite their independent evolution and different metabolisms, vascular plants and bilaterian animals share major design features, namely, an internal mass comprising organized cells capable of metabolic and bioenergetic activities, a transport mechanism for distributing molecules and energy within itself, and a surface capable of exchanging matter and energy with the environment. Regardless of the shape differences observed between these two groups, the physics associated with the transformation, transport, and exchange of matter and energy must unavoidably impose physical constraints on their designs. An organism is akin to an engine—part of the energy obtained from nourishment is used for organism function, growth, reproduction, while the rest is dissipated through its surface. We consider the hypothesis of the survival of the fittest in terms of energy metabolism and postulate that an organism with a higher energy intake would have a competitive advantage over another organism of similar mass performing energetically suboptimally, and explore its consequences.Consider an isotropic 3D organism of spatial extent h whose volume V scales as . Generalization to organisms with distinct scaling along the three different directions is straightforward. We make the simplifying assumption that the consumption and metabolic activity is distributed uniformly in space and in time or suitable averaging is used. We denote the basal metabolic rate of the organism by B and its mass by M. B is a measure of the energy being delivered to the organism per unit time and ought to be proportional to the energy dissipated through its surface. There is no evidence of size selection in empirical data, and this lends support to the assumption that the efficiency of the engine is independent of the organism’s size. We will derive Kleiber’s law based on energy intake considerations and study the role of geometry, as captured in the surface−volume relationship, on considering the expelled energy.Our goal is to understand the ideal dependence of B on M in the scaling regime. The characteristic time scale associated with the organism is known to scale as —it is a measure of how long it would take for energy proportional to M to be dissipated at a rate of B. Henceforth, proportionality constants, which serve to fix the correct units of various quantities related through scaling relations, will be omitted for the sake of simplicity.The number of metabolites, N, consumed in the organism per unit time is proportional to B. Let us define , so that a single metabolite is consumed per unit time in the local region surrounding each site of an grid. Each of these sites can be thought of as being within a service volume, in which one metabolite is consumed per unit time, of linear spatial extent . At the local level, the metabolites need to be transported this distance over unit time, and one immediately finds (24) that the transport velocity . Another measure of the transport velocity is obtained by noting that it is a characteristic length scale of the organism divided by the corresponding characteristic time scale and therefore scales as . Setting the two measures to be proportional to each other, one obtains Kleiber’s law .An alternative way of deriving the same result in a more rigorous manner is through the consideration of the properties of efficient transportation networks. The goal is to determine the minimum number of metabolites in transit, a measure of the organism mass, to ensure that metabolites are delivered in unit time within the organism volume. One can prove that the mass scales at least as with the optimality arising for efficient directed networks with no large-scale backtracking (13). This again leads to Kleiber’s law.Remarkably, the idealized metabolic rate−mass relationship is predicted to be algebraic with a exponent independent of the geometry of the organism. Such competitive equivalence explains the coexistence of animals with a homogeneous tissue density and fractal plants on Earth. The mass-specific metabolic rate, , scales as , whereas the transit time scales as . Indeed, characteristic biological rates (such as the heart beat and mutation rates) and characteristic biological times (such as circulation times or lifetimes) scale as and , respectively (6, 7, 9–12, 14–16).     

Evidence that dimethyl sulfide facilitates a tritrophic mutualism between marine primary producers and top predators

Tritrophic mutualistic interactions have been best studied in plant–insect systems. During these interactions, plants release volatiles in response to herbivore damage, which, in turn, facilitates predation on primary consumers or benefits the primary producer by providing nutrients. Here we explore a similar interaction in the Southern Ocean food web, where soluble iron limits primary productivity. Dimethyl sulfide has been studied in the context of global climate regulation and is an established foraging cue for marine top predators. We present evidence that procellariiform seabird species that use dimethyl sulfide as a foraging cue selectively forage on phytoplankton grazers. Their contribution of beneficial iron recycled to marine phytoplankton via excretion suggests a chemically mediated link between marine top predators and oceanic primary production.Many plant species interact with carnivores to gain protection from herbivory. Such mutualistic tritrophic interactions have been studied extensively in plant–insect systems, and are frequently mediated by plant volatiles released in response to insect feeding (1). One example that has received detailed study is the interaction between the phytophagous two-spotted spider mite Tetranychus urticae, the lima bean plant Phaseolus lunatus, and the predatory mite Phytoseiulus persimilis (2, 3). In this model system, grazing by the herbivorous spider mite has been demonstrated to elicit a cascade of biochemical reactions within the afflicted plants, stimulating the release of a suite of volatile terpenoids such as (E)-4,8-dimethyl-l,3,7-nonatriene, (E)-β-ocimene, and (E,E)-4,8,12-trimethyl-1,3,7,11-tridecatetraene (3). These volatiles attract olfactory-searching P. persimilis that prey upon herbivorous spider mites.The possibility of tritrophic mutualisms involving plant volatiles has received considerable attention in terrestrial communities (2–5); however, similar interactions have rarely been suggested for marine systems (6). Dimethyl sulfide (DMS) and its precursor dimethylsulfoniopropionate (DMSP) are well-established infochemicals in the marine environment, and as such are good candidate molecules for mediating tritrophic interactions between phytoplankton and carnivores (7–10). DMS arises as a catabolic breakdown product of DMSP, and has been studied extensively for its putative role as a global climate regulator (11). DMSP is produced by marine algae, where it has been proposed to function as an osmolyte (12) and a cryoprotectant (13). When algal cells lyse, due to biotic or abiotic stress, one of the fates of DMSP is catabolism by the enzyme DMSP lyase to DMS and acrylic acid (14–16). This process may also occur during autocatalytic cell death (17). It has been proposed that acrylic acid is the biologically salient product of this reaction due to its antimicrobial properties (18).DMS production has also been shown to increase during zooplankton grazing (14). It has been previously proposed that this phytoplankton-derived odorant is an important infochemical for marine apex predators including whale sharks (19), harbor seals (20), penguins (21–23), and procellariiform (tube-nosed) seabirds (24). Procellariiform seabirds have been the best-studied in this regard, and many species have been shown to detect and respond to biogenic concentrations of DMS in foraging contexts (24, 25). Members of this order share highly pelagic lifestyles and are central-place foragers associated with land only during incubation and chick rearing (26). Procellariiformes routinely range thousands of kilometers to forage (27) and have large olfactory bulbs compared with other avian clades (28), and some species have been shown to track their prey using their sense of smell (29). Some procellariiform species are attracted to DMS, whereas others are not (24, 30) (Fig. 1); however, the relationship between DMS behavioral sensitivity and the consumption of herbivorous crustacea has not previously been shown.Open in a separate windowFig. 1.Phylogenetic relationships between the species included in the meta-analysis, mapped with DMS responsiveness. DMS responsiveness is thought to be ancestral in this lineage (30). Certain species in the outgroup, sphenisciformes (penguins), have also been shown to be responsive to DMS (21–23).The Southern Ocean is the largest marine ecosystem in the world, with the polar front forming a distinct northern boundary to this ecoregion (31). Our rationale for using this system is twofold: (i) A majority of the world’s procellariiform species breed or forage in the Southern Ocean (32), and (ii) food web relationships are relatively simple by comparison with other marine systems. Phaeocystis antarctica and several siliceous diatom species are the dominant DMS-producing phytoplankton species in this ecosystem, and Antarctic krill (Euphasia superba) and other small crustaceans (copepods, decapods, amphipods, etc.) are their major consumers.Here we take advantage of a 50-y dietary database of Southern Ocean seabirds (33) to explore whether DMS mediates a mutualistic tritrophic interaction in the Southern Ocean pelagic ecosystem. If this is the case, then we predict that (i) carnivorous species, such as seabirds, that are attracted to this infochemical should specialize on primary consumers, such as crustaceans, and (ii) primary producers should gain some benefit from this interaction.