Preforming floral primordia converge on a narrow range of stages at dormancy despite multiple effects of temperature on development.

Phenological studies often focus on relationships between flowering date and temperature or other environmental variables. Yet in species that preform flowers, anthesis is one stage of a lengthy developmental process, and effects of temperature on flower development in the year(s) before flowering are largely unknown. We investigated the effects of temperature during preformation on flower development in Vaccinium vitis-idaea. Using scanning electron microscopy, we established scores for developing primordia and examined effects of air temperature, depth of soil thaw, time of year and previous stage on development. Onset of flower initiation depends on soil thaw, and developmental change is greatest at early stages and during the warmest months. Regardless of temperature and time during the season, all basal floral primordia pause development at the same stage before whole-plant dormancy. Once primordia are initiated, development does not appear to be influenced by air temperature differences within the range of variation among our sites. There may be strong endogenous flower-level controls over development, particularly the stage at which morphogenesis ceases before dormancy. However, the strength of such internal controls in the face of continuing temperature extremes under a changing climate is unclear.

Patterns of pollen and resource limitation of fruit production in Vaccinium uliginosum and V. vitis-idaea in Interior Alaska.

Many recent studies assessing fruit productivity of plants in the boreal forest focus on interannual variability across a forested region, rather than on environmental variability within the forest. Frequency and severity of wildfires in the boreal forest affect soil moisture, canopy, and community structure at the landscape level, all of which may influence overall fruit production at a site directly or indirectly. We evaluated how fruit production in two boreal shrubs, Vaccinium uliginosum (blueberry) and V. vitis-idaea (lingonberry), was explained by factors associated with resource availability (such as canopy cover and soil conditions) and pollen limitation (such as floral resources for pollinators and pollen deposition) across boreal forest sites of Interior Alaska in 2017. We classified our study sites into upland and lowland sites, which differed in elevation, soil moisture, and active layer. We found that resource and pollen limitation differed between the two species and between uplands and lowlands. Lingonberry was more pollen limited than blueberry, and plants in lowland sites were more pollen limited relative to other sites while plants in upland sites were relatively more resource limited. Additionally, canopy cover had a significant negative effect in upland sites on a ramet's investment in reproductive tissues and leaves versus structural growth, but little effect in lowland sites. These results point to importance of including pollinator service as well as resource availability in predictions for changes in berry abundance.

Diverse Developmental Responses to Warming Temperatures Underlie Changes in Flowering Phenologies.

Climate change has resulted in increased temperature means across the globe. Many angiosperms flower earlier in response to rising temperature and the phenologies of these species are reasonably well predicted by models that account for spring (early growing season) and winter temperatures. Surprisingly, however, exceptions to the general pattern of precocious flowering are common. Many species either do not appear to respond or even delay flowering in, or following, warm growing seasons. Existing phenological models have not fully addressed such exceptions to the common association of advancing phenologies with warming temperatures. The phenological events that are typically recorded (e.g., onset of flowering) are but one phase in a complex developmental process that often begins one or more years previously, and flowering time may be strongly influenced by temperature over the entire multi-year course of flower development. We propose a series of models that explore effects of growing-season temperature increase on the multiple processes of flower development and how changes in development may impact the timing of anthesis. We focus on temperate forest trees, which are characterized by preformation, the initiation of flower primordia one or more years prior to anthesis. We then synthesize the literature on flower development to evaluate the models. Although fragmentary, the existing data suggest the potential for temperature to affect all aspects of flower development in woody perennials. But, even for relatively well studied taxa, the critical developmental responses that underlie phenological patterns are difficult to identify. Our proposed models explain the seemingly counter-intuitive observations that warmer growing-season temperatures delay flowering in many species. Future research might concentrate on taxa that do not appear to respond to temperature, or delay flowering in response to warm temperatures, to understand what processes contribute to this pattern.

Invasive rodents have multiple indirect effects on seabird island invertebrate food web structure.

Burrowing seabirds that nest on islands transfer nutrients from the sea, disturb the soil through burrowing, damage tree foliage when landing, and thereby modify the surface litter. However, seabirds are in decline worldwide, as are their community- and ecosystem-level impacts, primarily due to invasive predatory mammals. The direct and indirect effects of seabird decline on communities and ecosystems are inherently complex. Here we employed network analysis, as a means of simplifying ecological complexity, to better understand the effects seabird loss may have on island invertebrate communities. Using data on leaf litter communities, we constructed invertebrate food webs for each of 18 offshore oceanic islands in northeastern New Zealand, nine of which have high seabird densities and nine of were invaded by rats. Ten network topological metrics (including entropy, generality, and vulnerability) were compared between rat-invaded and uninvaded (seabird-dominant) islands. We found that, on rat-invaded islands, the invertebrate food webs were smaller and less complex than on their seabird-dominated counterparts, which may be due to the suppression of seabird-derived nutrients and consequent effects on trophic cascades. This decreased complexity of food webs due to the presence of rats is indicative of lower ecosystem resistance via lower trophic redundancy. Our results show that rat effects on island ecosystems are manifested throughout entire food webs, and demonstrate how network analysis may be useful to assess ecosystem recovery status as these invaded islands are restored.

Increased variance in temperature and lag effects alter phenological responses to rapid warming in a subarctic plant community.

Summer temperature on the Cape Churchill Peninsula (Manitoba, Canada) has increased rapidly over the past 75 years, and flowering phenology of the plant community is advanced in years with warmer temperatures (higher cumulative growing degree days). Despite this, there has been no overall shift in flowering phenology over this period. However, climate change has also resulted in increased interannual variation in temperature; if relationships between phenology and temperature are not linear, an increase in temperature variance may interact with an increase in the mean to alter how community phenology changes over time. In our system, the relationship between phenology and temperature was log-linear, resulting in a steeper slope at the cold end of the temperature spectrum than at the warm end. Because below-average temperatures had a greater impact on phenology than above-average temperatures, the long-term advance in phenology was reduced. In addition, flowering phenology in a given year was delayed if summer temperatures were high the previous year or 2 years earlier (lag effects), further reducing the expected advance over time. Phenology of early-flowering plants was negatively affected only by temperatures in the previous year, and that of late-flowering plants primarily by temperatures 2 years earlier. Subarctic plants develop leaf primordia one or more years prior to flowering (preformation); these results suggest that temperature affects the development of flower primordia during this preformation period. Together, increased variance in temperature and lag effects interacted with a changing mean to reduce the expected phenological advance by 94%, a magnitude large enough to account for our inability to detect a significant advance over time. We conclude that changes in temperature variability and lag effects can alter trends in plant responses to a warming climate and that predictions for changes in plant phenology under future warming scenarios should incorporate such effects.

Effects of non-native Melilotus albus on pollination and reproduction in two boreal shrubs.

The establishment of abundantly flowered, highly rewarding non-native plant species is expected to have strong consequences for native plants through altered pollination services, particularly in boreal forest where the flowering season is short and the pollinator pool is small. In 18 boreal forest sites, we added flowering Melilotus albus to some sites and left some sites as controls in 2 different years to test if the invasive plant influences the pollination and reproductive success of two co-flowering ericaceous species: Vaccinium vitis-idaea and Rhododendron groenlandicum. We found that M. albus increased the pollinator diversity and tended to increase visitation rates to the focal native plant species compared to control sites. Melilotus albus facilitated greater seed production per berry in V. vitis-idaea when we added 120 plants compared to when we added 40 plants or in control sites. In R. groenlandicum, increasing numbers of M. albus inflorescences lowered conspecific pollen loads and percentage of flowers pollinated; however, no differences in fruit set were detected. The number of M. albus inflorescences had greater importance in explaining R. groenlandicum pollination compared to other environmental variables such as weather and number of native flowers, and had greater importance in lower quality black spruce sites than in mixed deciduous and white spruce sites for explaining the percentage of V. vitis-idaea flowers pollinated. Our data suggest that the identity of new pollinators attracted to the invaded sites, degree of shared pollinators between invasive and native species, and variation in resource limitation among sites are likely determining factors in the reproductive responses of boreal native plants in the presence of an invasive.

Climate change, phenology, and habitat degradation: drivers of gosling body condition and juvenile survival in lesser snow geese.

Nesting migratory geese are among the dominant herbivores in (sub) arctic environments, which have undergone unprecedented increases in temperatures and plant growing days over the last three decades. Within these regions, the Hudson Bay Lowlands are home to an overabundant breeding population of lesser snow geese that has dramatically damaged the ecosystem, with cascading effects at multiple trophic levels. In some areas the overabundance of geese has led to a drastic reduction in available forage. In addition, warming of this region has widened the gap between goose migration timing and plant green-up, and this 'mismatch' between goose and plant phenologies could in turn affect gosling development. The dual effects of climate change and habitat quality on gosling body condition and juvenile survival are not known, but are critical for predicting population growth and related degradation of (sub) arctic ecosystems. To address these issues, we used information on female goslings marked and measured between 1978 and 2005 (4125 individuals). Goslings that developed within and near the traditional center of the breeding colony experienced the effects of long-term habitat degradation: body condition and juvenile survival declined over time. In newly colonized areas, however, we observed the opposite pattern (increase in body condition and juvenile survival). In addition, warmer than average winters and summers resulted in lower gosling body condition and first-year survival. Too few plant 'growing days' in the spring relative to hatch led to similar results. Our assessment indicates that geese are recovering from habitat degradation by moving to newly colonized locales. However, a warmer climate could negatively affect snow goose populations in the long-run, but it will depend on which seasons warm the fastest. These antagonistic mechanisms will require further study to help predict snow goose population dynamics and manage the trophic cascade they induce.

Correlations between physical and chemical defences in plants: tradeoffs, syndromes, or just many different ways to skin a herbivorous cat?

Most plant species have a range of traits that deter herbivores. However, understanding of how different defences are related to one another is surprisingly weak. Many authors argue that defence traits trade off against one another, while others argue that they form coordinated defence syndromes. We collected a dataset of unprecedented taxonomic and geographic scope (261 species spanning 80 families, from 75 sites across the globe) to investigate relationships among four chemical and six physical defences. Five of the 45 pairwise correlations between defence traits were significant and three of these were tradeoffs. The relationship between species' overall chemical and physical defence levels was marginally nonsignificant (P = 0.08), and remained nonsignificant after accounting for phylogeny, growth form and abundance. Neither categorical principal component analysis (PCA) nor hierarchical cluster analysis supported the idea that species displayed defence syndromes. Our results do not support arguments for tradeoffs or for coordinated defence syndromes. Rather, plants display a range of combinations of defence traits. We suggest this lack of consistent defence syndromes may be adaptive, resulting from selective pressure to deploy a different combination of defences to coexisting species.

Putting plant resistance traits on the map: a test of the idea that plants are better defended at lower latitudes.

• It has long been believed that plant species from the tropics have higher levels of traits associated with resistance to herbivores than do species from higher latitudes. A meta-analysis recently showed that the published literature does not support this theory. However, the idea has never been tested using data gathered with consistent methods from a wide range of latitudes. • We quantified the relationship between latitude and a broad range of chemical and physical traits across 301 species from 75 sites world-wide. • Six putative resistance traits, including tannins, the concentration of lipids (an indicator of oils, waxes and resins), and leaf toughness were greater in high-latitude species. Six traits, including cyanide production and the presence of spines, were unrelated to latitude. Only ash content (an indicator of inorganic substances such as calcium oxalates and phytoliths) and the properties of species with delayed greening were higher in the tropics. • Our results do not support the hypothesis that tropical plants have higher levels of resistance traits than do plants from higher latitudes. If anything, plants have higher resistance toward the poles. The greater resistance traits of high-latitude species might be explained by the greater cost of losing a given amount of leaf tissue in low-productivity environments.

Physiological performance of an Alaskan shrub (Alnus fruticosa) in response to disease (Valsa melanodiscus) and water stress.

• Following the decades-long warming and drying trend in Alaska, there is mounting evidence that temperature-induced drought stress is associated with disease outbreaks in the boreal forest. Recent evidence of this trend is an outbreak of Cytospora canker disease (fungal pathogen Valsa melanodiscus (anamorph = Cytospora umbrina)) on Alnus species. • For Alnus fruticosa, we examined the effects of water stress on disease predisposition, and the effects of disease and water stress on host physiology. In two trials, we conducted a full-factorial experiment that crossed two levels of water stress with three types of inoculum (two isolates of V. melanodiscus, one control isolate). • Water stress was not required for disease predisposition. However, the effects of water stress and disease on host physiology were greatest near the peak phenological stage of the host and during hot, dry conditions. During this time, water stress and disease reduced light-saturated photosynthesis (-30%), light saturation point (-60%) and stomatal conductance (-40%). • Our results depended on the timing of water stress and disease in relation to host phenology and the environment. These factors should not be overlooked in attempts to generalize predictions about the role of temperature-induced drought stress in this pathosystem.

Effects of invasive rats and burrowing seabirds on seeds and seedlings on New Zealand islands.

Rats (Rattus rattus, Rattus norvegicus, Rattus exulans) are important invaders on islands. They alter vegetation indirectly by preying on burrowing seabirds. These seabirds affect vegetation through nutrient inputs from sea to land and physical disturbance through trampling and burrowing. Rats also directly affect vegetation though consumption of seeds and seedlings. Seedling communities on northern New Zealand islands differ in composition and densities among islands which have never been invaded by rats, are currently invaded by rats, or from which rats have been eradicated. We conducted experimental investigations to determine the mechanisms driving these patterns. When the physical disturbance of seabirds was removed, in soils collected from islands and inside exclosures, seedling densities increased with seabird burrow density. For example, seedling densities inside exclosures were 10 times greater than those outside. Thus the negative effects of seabirds on seedlings, by trampling and uprooting, overwhelm the potentially beneficial effects of high levels of seed germination, seedling emergence, and possibly seed production, which result from seed burial and nutrient additions. Potential seedling density was reduced on an island where rats were present, germination of seeds from soils of this island was approximately half that found on other islands, but on this island seedling density inside exclosures was 7 times the density outside. Although the total negative effects of seabirds and rats on seedling densities are similar (reduced seedling density), the differences in mechanisms and life stages affected result in very different filters on the plant community.

Species removal and experimental warming in a subarctic tundra plant community.

Neighbor interactions are likely to play an important role in subarctic plant communities. We conducted experiments in Interior Alaska in which we crossed species removal with greenhouse warming manipulations. We examined changes in community biomass, and in plant survival and growth of individual species in response to experimental warming and to: (1) removal of whole species versus an equivalent amount of biomass across many species, and (2) removal of subdominant (locally common) versus minor (locally uncommon) plants. Community biomass indicated compensation in growth after removal of minor species and after biomass removal without elimination of entire species, but under-compensation after removal of subdominants. Growth and survival of individual species showed facilitation between some species. Warming increased growth of dominant vascular plants, but at the same time reduced survival, and these impacts were greater for larger, more mesic species than for the smaller species associated with drier habitats. Growth of mosses was reduced by the warming. Removal effects did not differ between warming and ambient conditions. The results indicate that common species are able to reduce resources for others (competitive effect) and increase their growth after neighbor removal, whereas locally uncommon species are not able to respond rapidly to increased resources made available by neighbor removal. Therefore, the impact of the presence of common species on locally uncommon species was facilitative overall, but not vice versa. The balance between disturbances such as changes in temperature and species losses from the community will likely be crucial in determining shifts in subsequent community composition.

Indirect effects of invasive predators on litter decomposition and nutrient resorption on seabird-dominated islands.

Despite recent interest in the ecosystem impacts of invasive aboveground organisms, most work in this area has focused on effects of invasive plants, and the effects of invasive herbivores and predators remain poorly understood. We studied 18 forested, offshore islands in northern New Zealand. Nine of these host high densities of burrowing seabirds that serve as ecosystem drivers by transporting nutrients from the ocean to land. The other nine have been invaded over the past 50-150 years by rat species introduced from Europe which serve as predators of seabird eggs and chicks and severely reduce their densities. We collected fully expanded leaves and fresh leaf litter from invaded and uninvaded islands for each of 12 perennial plant species that represent a wide spectrum of life forms from ground dwelling to emergent canopy species. We found that, across these species, invasion by rats significantly reduced nitrogen (N) but not phosphorus (P) concentrations of foliage and litter, promoted N but not P resorption from leaves before litter fall, and reduced the release of N but not P from decomposing litter. Rat invasion also negatively affected litter decomposability but had no overall effects on litter quality variables other than N. Our results provide evidence that rat invasion causes more conservative cycling of N but not P through foliage and litter and limitation of ecological processes by N but not P. We found few instances in which the effects of rat invasion on response variables varied significantly across plant species, meaning that invasion had similar effects for species that varied greatly in growth form and foliar and litter quality. Further, correlation analyses across the 12 species showed that foliar and litter quality traits were poor predictors of how invasion effects on resorption and decomposition variables varied among species. Our results show that the effects of invasive predators on native prey can have substantial indirect effects on variables relevant for ecosystem functioning. These types of effects are probably widespread, especially given the role of seabirds in improving soil fertility in many coastal ecosystems worldwide and the wide global distribution of predators of seabirds.

Promotion of ecosystem carbon sequestration by invasive predators.

Despite recent interest in understanding the effects of human-induced global change on carbon (C) storage in terrestrial ecosystems, most studies have overlooked the influence of a major element of global change, namely biological invasions. We quantified ecosystem C storage, both above- and below-ground, on each of 18 islands off the coast of New Zealand. Some islands support high densities of nesting seabirds, while others have been invaded by predatory rats and host few seabirds. Our results show that, by preying upon seabirds, rats have indirectly enhanced C sequestration in live plant biomass by 104%, reduced C sequestration in non-living pools by 26% and increased total ecosystem C storage by 37%. Given the current worldwide distribution of rats and other invasive predatory mammals, and the consequent disappearance of seabird colonies, these predators may be important determinants of ecosystem C sequestration.

Above- and below-ground impacts of introduced predators in seabird-dominated island ecosystems.

Predators often exert multi-trophic cascading effects in terrestrial ecosystems. However, how such predation may indirectly impact interactions between above- and below-ground biota is poorly understood, despite the functional importance of these interactions. Comparison of rat-free and rat-invaded offshore islands in New Zealand revealed that predation of seabirds by introduced rats reduced forest soil fertility by disrupting sea-to-land nutrient transport by seabirds, and that fertility reduction in turn led to wide-ranging cascading effects on belowground organisms and the ecosystem processes they drive. Our data further suggest that some effects on the belowground food web were attributable to changes in aboveground plant nutrients and biomass, which were themselves related to reduced soil disturbance and fertility on invaded islands. These results demonstrate that, by disrupting across-ecosystem nutrient subsidies, predators can indirectly induce strong shifts in both above- and below-ground biota via multiple pathways, and in doing so, act as major ecosystem drivers.

Improved water retention links high species richness with increased productivity in arctic tundra moss communities.

A positive relationship between plant species richness and ecosystem functioning has been found in a number of experimental studies. Positive species interactions at high species numbers have been suggested as a cause, but mechanisms driving positive interactions have not often been tested. In this experiment we asked three questions: (1) What is the relationship between species richness and productivity in experimentally constructed moss communities? (2) Is this relationship affected by plant density? and (3) Can changes in moisture absorption and retention explain observed relationships? To answer these questions we exposed arctic tundra moss communities of different species richness levels (1-11 species) and two different densities in the greenhouse to two levels of drought (short and long). Biomass (by the community and individual species), height and community moisture absorption and retention were measured as response variables. High species diversity increased productivity (more so in low-density plots than in high-density plots), but only when plots were watered regularly. Plot moisture retention was improved at high species richness as well, and plant height and variation in height was increased compared to plants in monoculture. Under high-density and short-drought conditions 10 out of 12 species grew better in mixture than in monoculture, but under the long drought treatment only six species did. A positive feedback loop between biomass and improved humidity under high diversity was supported by path analysis. We conclude that in this community the relationship between species richness and productivity depends on moisture availability and density, with improved water absorption and retention likely to be the mechanism for increased plant growth when drought periods are short. Furthermore, since this is the opposite of what has been found for temperate moss communities, conclusions from one system cannot automatically be extrapolated to other systems.

Comparative analysis of late floral development and mating-system evolution in tribe Collinsieae (Scrophulariaceae s.l.).

Species of Collinsia and Tonella, the two sister genera of self-compatible annuals that constitute tribe Collinsieae, show extensive variation in floral size and morphology and in patterns of stamen and style elongation during the life of the flower (anthesis). We used a nuclear ribosomal ITS phylogeny, independent contrasts, and phylogenetically corrected path analysis to explore the patterns of covariance of the developmental and morphological traits potentially influencing mating system. Large-flowered taxa maintain herkogamy (spatial separation of anthers and stigmas) early in anthesis by differential elongation of staminal filaments, which positions each of the four anthers at the tip of the "keel" upon dehiscence. Small-flowered taxa do not show this pattern of filament elongation. The styles of large-flowered taxa elongate late in the 2-5 d of anthesis, resulting in late anther-stigma contact and delayed self-pollination. Anther-stigma contact and self-pollination occur early in anthesis in small-flowered species/populations. Thus, we found complex covariation of morphological and developmental traits that can be interpreted as the result of multitrait adaptation for early selfing and high levels of autogamy, delayed selfing and higher levels of outcrossing, or intermediate levels of outcrossing. Continuous variation in these traits suggests the operation of continuous variation in selective optima or the combined effects of divergent selection and phylogenetic inertia.

Numerical responses of different trophic groups of invertebrates to manipulations of plant diversity in grasslands.

We studied the effects of plant diversity on abundance of invertebrate herbivores, parasitoids and predators in two grassland communities (one in Switzerland and one in Sweden) in which plant species richness and functional diversity have been experimentally manipulated. Among herbivores, the abundance of only the most sessile and specialised groups (leafhoppers and wingless aphids) was affected by plant diversity. At both sites, numbers of leafhoppers in sweep net samples showed a linear, negative relationship with plant species number whereas numbers of wingless aphids in suction samples increased with the number of plant functional groups (grasses, legumes, and non-legume forbs) present in the plot. Activity of carabid beetles and spiders (as revealed by pitfall catches) and the total number of predators in pitfalls at the Swiss site decreased linearly with increases in the number of plant species and plant functional groups. Abundance of more specialised enemies, hymenopteran parasitoids, was not affected by the manipulations of plant diversity. Path analysis and analysis of covariance indicated that plant diversity effects on invertebrate abundance were mostly indirect and mediated by changes in plant biomass and cover. At both sites, plant species composition (i.e. the identity of plant species in a mixture) affected numbers of most of the examined groups of invertebrates and was, therefore, a more important determinant of invertebrate abundance in grasslands than plant species richness per se or the number of plant functional groups. The presence of legumes in a mixture was especially important and led to higher numbers of most invertebrate groups. The similarity of invertebrate responses to plant diversity at the two study sites indicates that general patterns in abundance of different trophic groups can be detected across plant diversity gradients under different environmental conditions.