Mechanisms driving interspecific variation in regional synchrony of trees reproduction

Seed production in many plants is characterized by large interannual variation, which is synchronized at subcontinental scales in some species but local in others. The reproductive synchrony affects animal migrations, trophic responses to resource pulses and the planning of management and conservation. Spatial synchrony of reproduction is typically attributed to the Moran effect, but this alone is unable to explain interspecific differences in synchrony. We show that interspecific differences in the conservation of seed production-weather relationships combine with the Moran effect to explain variation in reproductive synchrony. Conservative timing of weather cues that trigger masting allows populations to be synchronized at distances >1000 km. Conversely, if populations respond to variable weather signals, synchrony cannot be achieved. Our study shows that species vary in the extent to which their weather cueing is spatiotemporally conserved, with important consequences, including an interspecific variation of masting vulnerability to climate change.     

Capital and income breeding traits differentiate trophic match–mismatch dynamics in large herbivores

For some species, climate change has altered environmental conditions away from those in which life-history strategies evolved. In such cases, if adaptation does not keep pace with these changes, existing life-history strategies may become maladaptive and lead to population declines. We use life-history theory, with a specific emphasis on breeding strategies, in the context of the trophic match–mismatch framework to form generalizable hypotheses about population-level consumer responses to climate-driven perturbations in resource availability. We first characterize the income and breeding traits of sympatric caribou and muskoxen populations in western Greenland, and then test trait-based hypotheses about the expected reproductive performance of each population during a period of high resource variability at that site. The immediate reproductive performance of income breeding caribou decreased with trophic mismatch. In contrast, capital breeding muskoxen were relatively unaffected by current breeding season resource variability, but their reproductive performance was sensitive to resource conditions from previous years. These responses matched our expectations about how capital and income breeding strategies should influence population susceptibility to phenological mismatch. We argue for a taxon-independent assessment of trophic mismatch vulnerability based on a life-history strategy perspective in the context of prevailing environmental conditions.     

(A bit) Earlier or later is always better: Phenological shifts in consumer–resource interactions

Phenology is a crucial life history trait for species interactions and it can have great repercussions on the persistence of communities and ecosystems. Changes in phenology caused by climate change can disrupt species interactions causing decreases in consumer growth rates, as suggested by the match–mismatch hypothesis (MMH). However, it is still not clear what the long-term consequences of such phenological changes are. In this paper, we present models in which phenology and consumer–resource feedbacks determine long-term community dynamics. Our results show that consumer viability is constrained by limits in the amount of phenological mismatch with their resources, in accordance with the MMH, but the effects of phenological shifts are often nonmonotonic. Consumers generally have higher abundances when they recruit some time before or after their resources because this reduces the long-term effects of overexploitation that would otherwise occur under closer synchrony. Changes in the duration of recruitment phenologies also have important impacts on community stability, with shorter phenologies promoting oscillations and cycles. For small community modules, the effects of phenological shifts on populations can be explained, to a great extent, as superpositions of their effects on consumer–resource pairs. We highlight that consumer–resource feedbacks and overexploitation, which are not typically considered in phenological models, are important factors shaping the long-term responses to phenological changes caused by climate change.     

Variation in breeding phenology provides insights into drivers of long-term population change in harbour seals

Phenological trends provide important indicators of environmental change and population dynamics. However, the use of untested population-level measures can lead to incorrect conclusions about phenological trends, particularly when changes in population structure or density are ignored. We used individual-based estimates of birth date and lactation duration of harbour seals (Phoca vitulina) to investigate energetic consequences of changes in pupping phenology. Using generalized linear mixed models, we first demonstrate annual variation in pupping phenology. Second, we show a negative relationship between lactation duration and the timing of pupping, indicating that females who pup early nurse their pups longer, thereby highlighting lactation duration as a useful proxy of female condition and resource availability. Third, individual-based data were used to derive a population-level proxy that demonstrated an advance in pupping date over the last 25 years, co-incident with a reduction in population abundance that resulted from fisheries-related shootings. These findings demonstrate that phenological studies examining the impacts of climate change on mammal populations must carefully control for changes in population density and highlight how joint investigations of phenological and demographic change provide insights into the drivers of population declines.     

Inter-specific synchrony of two contrasting ungulates: wild boar (Sus scrofa) and roe deer (Capreolus capreolus)

Very few studies on ungulates address issues of inter-specific synchrony in population responses to environmental variation such as climate. Depending on whether annual variation in performance of ungulate populations is driven by direct or indirect (trophic) interactions, very different predictions regarding the pattern of inter-specific synchrony can be derived. We compared annual autumn body mass variation in roe deer (Capreolus capreolus) and wild boar (Sus scrofa) from Poland over the period 1982–2002, and related this to variation in winter and summer climate and plant phenological development [the Normalized Difference Vegetation Index (NDVI), derived from satellites]. Roe deer fawns (∼1.3 kg increase from year 1982 to 2002) and yearlings both increased markedly in mass over years. There was also an increase for wild boar mass over years (∼4.2 kg increase for piglets from 1982 to 2002). Despite our failure to link annual body mass to spring or winter conditions or the NDVI, the body mass of roe deer and wild boar fluctuated in synchrony. As this was a field roe deer population, and since wild boar is an omnivore, we suggest this may be linked to annual variation and trends in crop structure (mainly rye). We urge future studies to take advantage of studying multiple species in order to gain further insight into processes of how climate affect ungulate populations. Electronic supplementary material Supplementary material is available in the online version of this article at and is accessible for authorized users.     

Advancing breeding phenology in response to environmental change in a wild red deer population

Most evidence for advances in phenology of in response to recent climate warming in wild vertebrate populations has come from long‐term studies of birds. Few studies have either documented phenological advances or tested their climatic causes and demographic consequences in wild mammal systems. Using a long‐term study of red deer on the Isle of Rum, Scotland, we present evidence of significant temporal trends in six phenological traits: oestrus date and parturition date in females, and antler cast date, antler clean date, rut start date and rut end date in males. These traits advanced by between 5 and 12 days across a 28‐year study period. Local climate measures associated with plant growth in spring and summer (growing degree days) increased significantly over time and explained a significant amount of variation in all six phenological traits, largely accounting for temporal advances observed in some of the traits. However, there was no evidence for temporal changes in key female reproductive performance traits (offspring birth weight and offspring survival) in this population, despite significant relationships between these traits and female phenology. In males, average antler weights increased over time presumably as a result of improved resource availability and physiological condition through spring and summer. There was no evidence for any temporal change in average male annual breeding success, as might be expected if the timing of male rutting behaviour was failing to track advances in the timing of oestrus in females. Our results provide rare evidence linking phenological advances to climate warming in a wild mammal and highlight the potential complexity of relationships between climate warming, phenology and demography in wild vertebrates.     

Metapopulation dynamics in a changing climate: Increasing spatial synchrony in weather conditions drives metapopulation synchrony of a butterfly inhabiting a fragmented landscape

Habitat fragmentation and climate change are both prominent manifestations of global change, but there is little knowledge on the specific mechanisms of how climate change may modify the effects of habitat fragmentation, for example, by altering dynamics of spatially structured populations. The long‐term viability of metapopulations is dependent on independent dynamics of local populations, because it mitigates fluctuations in the size of the metapopulation as a whole. Metapopulation viability will be compromised if climate change increases spatial synchrony in weather conditions associated with population growth rates. We studied a recently reported increase in metapopulation synchrony of the Glanville fritillary butterfly (Melitaea cinxia) in the Finnish archipelago, to see if it could be explained by an increase in synchrony of weather conditions. For this, we used 23 years of butterfly survey data together with monthly weather records for the same period. We first examined the associations between population growth rates within different regions of the metapopulation and weather conditions during different life‐history stages of the butterfly. We then examined the association between the trends in the synchrony of the weather conditions and the synchrony of the butterfly metapopulation dynamics. We found that precipitation from spring to late summer are associated with the M. cinxia per capita growth rate, with early summer conditions being most important. We further found that the increase in metapopulation synchrony is paralleled by an increase in the synchrony of weather conditions. Alternative explanations for spatial synchrony, such as increased dispersal or trophic interactions with a specialist parasitoid, did not show paralleled trends and are not supported. The climate driven increase in M. cinxia metapopulation synchrony suggests that climate change can increase extinction risk of spatially structured populations living in fragmented landscapes by altering their dynamics.     

Masting in ponderosa pine: comparisons of pollen and seed over space and time

Many plant species exhibit variable and synchronized reproduction, or masting, but less is known of the spatial scale of synchrony, effects of climate, or differences between patterns of pollen and seed production. We monitored pollen and seed cone production for seven Pinus ponderosa populations (607 trees) separated by up to 28?km and 1,350?m in elevation in Boulder County, Colorado, USA for periods of 4?C31?years for a mean per site of 8.7?years for pollen and 12.1 for seed cone production. We also analyzed climate data and a published dataset on 21?years of seed production for an eighth population (Manitou) 100?km away. Individual trees showed high inter-annual variation in reproduction. Synchrony was high within populations, but quickly became asynchronous among populations with a combination of increasing distance and elevational difference. Inter-annual variation in temperature and precipitation had differing influences on seed production for Boulder County and Manitou. We speculate that geographically variable effects of climate on reproduction arise from environmental heterogeneity and population genetic differentiation, which in turn result in localized synchrony. Although individual pines produce pollen and seed, only one-third of the covariation within trees was shared. As compared to seed cones, pollen had lower inter-annual variation at the level of the individual tree and was more synchronous. However, pollen and seed production were similar with respect to inter-annual variation at the population level, spatial scales of synchrony and associations with climate. Our results show that strong masting can occur at a localized scale, and that reproductive patterns can differ between pollen and seed cone production in a hermaphroditic plant.     

A perspective on match/mismatch of phenology in community contexts

Climate change has significant impacts on phenology of various organisms in a species‐specific manner. Facing this problem, the match/mismatch hypothesis that phenological (a)synchrony with resource availability strongly influences recruitment success of a consumer population has recently received much attention. In this article, we discuss extending the conventional pairwise concept and demonstrate a community module‐based approach as an initial step for exploring community consequences of species‐specific phenological shifts caused by climate change. Our multispecies match/mismatch perspective leads to the prediction that phenological (a)synchrony among interacting species critically affects not only population recruitment of species but also key dynamical features of ecological communities such as trophic cascades, competitive hierarchies, and species coexistence. Explicit identification and consideration of species relationships is therefore desirable for a better understanding of seasonal community dynamics and thus community consequences of climate change‐induced phenological shifts.     

The Potential Connectivity of Waterhole Networks and the Effectiveness of a Protected Area under Various Drought Scenarios

Landscape connectivity is considered a priority for ecosystem conservation because it may mitigate the synergistic effects of climate change and habitat loss. Climate change predictions suggest changes in precipitation regimes, which will affect the availability of water resources, with potential consequences for landscape connectivity. The Greater Calakmul Region of the Yucatan Peninsula (Mexico) has experienced a 16% decrease in precipitation over the last 50 years, which we hypothesise has affected water resource connectivity. We used a network model of connectivity, for three large endangered species (Baird’s tapir, white-lipped peccary and jaguar), to assess the effect of drought on waterhole availability and connectivity in a forested landscape inside and adjacent to the Calakmul Biosphere Reserve. We used reported travel distances and home ranges for our species to establish movement distances in our model. Specifically, we compared the effects of 10 drought scenarios on the number of waterholes (nodes) and the subsequent changes in network structure and node importance. Our analysis revealed that drought dramatically influenced spatial structure and potential connectivity of the network. Our results show that waterhole connectivity and suitable habitat (area surrounding waterholes) is lost faster inside than outside the reserve for all three study species, an outcome that may drive them outside the reserve boundaries. These results emphasize the need to assess how the variability in the availability of seasonal water resource may affect the viability of animal populations under current climate change inside and outside protected areas.     

Environmental extremes versus ecological extremes: impact of a massive iceberg on the population dynamics of a high-level Antarctic marine predator

Extreme events have been suggested to play a disproportionate role in shaping ecological processes, but our understanding of the types of environmental conditions that elicit extreme consequences in natural ecosystems is limited. Here, we investigated the impact of a massive iceberg on the dynamics of a population of Weddell seals. Reproductive rates of females were reduced, but survival appeared unaffected. We also found suggestive evidence for a prolonged shift towards higher variability in reproductive rates. The annual number of females attending colonies showed unusual swings during the iceberg period, a pattern that was apparently the consequence of changes in sea-ice conditions. In contrast to the dramatic effects that were recorded in nearby populations of emperor penguins, our results suggest that this unusual environmental event did not have an extreme impact on the population of seals in the short-term, as they managed to avoid survival costs and were able to rapidly re-achieve high levels of reproduction by the end of the perturbation. Nevertheless, population projections suggest that even this modest impact on reproductive rates could negatively affect the population in the long run if such events were to occur more frequently, as is predicted by models of climate change.     

Earlier Migration Timing,Decreasing Phenotypic Variation,and Biocomplexity in Multiple Salmonid Species

Climate-induced phenological shifts can influence population, evolutionary, and ecological dynamics, but our understanding of these phenomena is hampered by a lack of long-term demographic data. We use a multi-decade census of 5 salmonid species representing 14 life histories in a warming Alaskan stream to address the following key questions about climate change and phenology: How consistent are temporal patterns and drivers of phenology for similar species and alternative life histories? Are shifts in phenology associated with changes in phenotypic variation? How do phenological changes influence the availability of resource subsidies? For most salmonid species, life stages, and life histories, freshwater temperature influences migration timing – migration events are occurring earlier in time (mean = 1.7 days earlier per decade over the 3–5 decades), and the number of days over which migration events occur is decreasing (mean = 1.5 days per decade). Temporal trends in migration timing were not correlated with changes in intra-annual phenotypic variation, suggesting that these components of the phenotypic distribution have responded to environmental change independently. Despite commonalities across species and life histories, there was important biocomplexity in the form of disparate shifts in migration timing and variation in the environmental factors influencing migration timing for alternative life history strategies in the same population. Overall, adult populations have been stable during these phenotypic and environmental changes (λ ≈1.0), but the temporal availability of salmon as a resource in freshwater has decreased by nearly 30 days since 1971 due to changes in the median date of migration timing and decreases in intra-annual variation in migration timing. These novel observations advance our understanding of phenological change in response to climate warming, and indicate that climate change has influenced the ecology of salmon populations, which will have important consequences for the numerous species that depend on this resource.     

Dynamics of births and juvenile recruitment in Mara–Serengeti ungulates in relation to climatic and land use changes

Natality and recruitment govern animal population dynamics, but their responses to fluctuating resources, competition, predation, shifting habitat conditions, density feedback and diseases are poorly understood. To understand the influences of climatic and land use changes on population dynamics, we monitored monthly changes in births and juvenile recruitment in seven ungulate species for 15 years (1989–2003) in the Masai Mara Reserve of Kenya. Recruitment rates declined for all species but giraffe, likely due to habitat alteration and increasing vulnerability of animals associated with recurrent severe droughts, rising temperatures, unprecedentedly strong and prolonged El Niño-Southern Oscillation (ENSO) episodes, expansion of settlements, cultivation and human population growth in pastoral ranches adjoining the reserve. Birth rate showed strong and humped relationships with moving averages of monthly rainfall, whereas recruitment responded strongly to cumulative past rainfall. Increasing livestock incursions into the reserve depressed recruitment rate for quarter-grown topi. Expansion of pastoral settlements depressed birth rate in impala, zebra and giraffe. Frequent ENSO-related droughts caused progressive habitat desiccation and hence nutritional shortfalls for ungulates. The responses to climatic, land use and resource influences did not reflect body size, migratory or resident lifestyle, dietary guild, digestive physiology or degree of synchrony of breeding of the ungulate species.     

Decomposing variation in population growth into contributions from environment and phenotypes in an age-structured population

Evaluating the relative importance of ecological drivers responsible for natural population fluctuations in size is challenging. Longitudinal studies where most individuals are monitored from birth to death and where environmental conditions are known provide a valuable resource to characterize complex ecological interactions. We used a recently developed approach to decompose the observed fluctuation in population growth of the red deer population on the Isle of Rum into contributions from climate, density and their interaction and to quantify their relative importance. We also quantified the contribution of individual covariates, including phenotypic and life-history traits, to population growth. Fluctuations in composition in age and sex classes ((st)age structure) of the population contributed substantially to the population dynamics. Density, climate, birth weight and reproductive status contributed less and approximately equally to the population growth. Our results support the contention that fluctuations in the population's (st)age structure have important consequences for population dynamics and underline the importance of including information on population composition to understand the effect of human-driven changes on population performance of long-lived species.     

Community‐wide changes in intertaxonomic temporal co‐occurrence resulting from phenological shifts

Global climate change is known to affect the assembly of ecological communities by altering species' spatial distribution patterns, but little is known about how climate change may affect community assembly by changing species' temporal co‐occurrence patterns, which is highly likely given the widely observed phenological shifts associated with climate change. Here, we analyzed a 29‐year phenological data set comprising community‐level information on the timing and span of temporal occurrence in 11 seasonally occurring animal taxon groups from 329 local meteorological observatories across China. We show that widespread shifts in phenology have resulted in community‐wide changes in the temporal overlap between taxa that are dominated by extensions, and that these changes are largely due to taxa's altered span of temporal occurrence rather than the degree of synchrony in phenological shifts. Importantly, our findings also suggest that climate change may have led to less phenological mismatch than generally presumed, and that the context under which to discuss the ecological consequences of phenological shifts should be expanded beyond asynchronous shifts.     

Movement can mediate temporal mismatches between resource availability and biological events in host–pathogen interactions

Global change is shifting the timing of biological events, leading to temporal mismatches between biological events and resource availability. These temporal mismatches can threaten species’ populations. Importantly, temporal mismatches not only exert strong pressures on the population dynamics of the focal species, but can also lead to substantial changes in pairwise species interactions such as host–pathogen systems. We adapted an established individual‐based model of host–pathogen dynamics. The model describes a viral agent in a social host, while accounting for the host''s explicit movement decisions. We aimed to investigate how temporal mismatches between seasonal resource availability and host life‐history events affect host–pathogen coexistence, that is, disease persistence. Seasonal resource fluctuations only increased coexistence probability when in synchrony with the hosts’ biological events. However, a temporal mismatch reduced host–pathogen coexistence, but only marginally. In tandem with an increasing temporal mismatch, our model showed a shift in the spatial distribution of infected hosts. It shifted from an even distribution under synchronous conditions toward the formation of disease hotspots, when host life history and resource availability mismatched completely. The spatial restriction of infected hosts to small hotspots in the landscape initially suggested a lower coexistence probability due to the critical loss of susceptible host individuals within those hotspots. However, the surrounding landscape facilitated demographic rescue through habitat‐dependent movement. Our work demonstrates that the negative effects of temporal mismatches between host resource availability and host life history on host–pathogen coexistence can be reduced through the formation of temporary disease hotspots and host movement decisions, with implications for disease management under disturbances and global change.     

Comparative ungulate dynamics: the devil is in the detail

Attempts to relate species differences in population dynamics to variation in life histories rely on the assumption that the causes of contrasts in demography are sufficiently simple to be derived from first principles. Here, we investigate the causes of contrasts in dynamics between two ungulate populations on Hebridean islands (red deer and Soay sheep) and show that differences in stability, as well as in the effects of variation in density and climate, are related to differences in timing of reproduction relative to seasonal variation in resource abundance. In both populations, attempts to predict changes in population size sufficiently accurately for the results to be useful for management purposes require a knowledge of the responses of different age and sex categories to changes in density and climate, as well as of population structure.     

Impact of land use intensity and temperature on the reproductive performance of <Emphasis Type="Italic">Dactylis glomerata</Emphasis> populations in the southeastern Alps

An understanding of the processes and environmental conditions governing spatial variation in reproductive performance of plants can provide important information about the factors characterizing plant community structure and influencing fitness in natural plant populations, especially in the context of climate and land use change. In this study, 60 mountain populations of Dactylis glomerata distributed along a fertilization regime in varying grassland hay meadows were evaluated. Variations in field management, climate, soil fertility, vegetation structure, population density and species richness on reproductive performance were examined. The results indicated that field management and soil nutrient availability are the main variables influencing population density and reproductive output of D. glomerata. Moreover, the results show the effect of temperature on seed mass and resource investment in reproduction. Climate and soil change suggest a morphological differentiation of reproductive traits: (i) individuals grown on sites with higher soil nutrient availability or nutrient supply have larger inflorescences with a greater number and heavier seeds; (ii) individuals grown on warmer sites have heavier seeds. We conclude that if the climate warms and increases land use intensification in hay meadows in the Alps, this will have a pronounced positive impact on the reproductive performance of D. glomerata. Moreover, it can be hypothesized that the migration potential of D. glomerata towards higher altitudes may be likely in the near future in response to accelerated climate change.     

Population and life-history consequences of within-cohort individual variation

The consequences of within-cohort (i.e., among-individual) variation for population dynamics are poorly understood, in particular for the case where life history is density dependent. We develop a physiologically structured population model that incorporates individual variation among and within cohorts and allows us to explore the intertwined relationship between individual life history and population dynamics. Our model is parameterized for the lizard Zootoca vivipara and reproduces well the species' dynamics and life history. We explore two common mechanisms that generate within-cohort variation: variability in food intake and variability in birth date. Predicted population dynamics are inherently very stable and do not qualitatively change when either of these sources of individual variation is introduced. However, increased within-cohort variation in food intake leads to changes in morphology, with longer but skinnier individuals, even though mean food intake does not change. Morphological changes result from a seemingly universal nonlinear relationship between growth and resource availability but may become apparent only in environments with strongly fluctuating resources. Overall, our results highlight the importance of using a mechanistic framework to gain insights into how different sources of intraspecific variability translate into life-history and population-dynamic changes.     

A cicada that ensures its fitness during climate warming by synchronizing its hatching time with the rainy season

A shift in phenology due to climate change is associated with some recent changes in populations, as it can disrupt the synchrony between organisms' requirements and resource availability. This conceptual framework has been developed mostly in systems of trophic interactions. Many coincidental changes, however, are involved in trophic interactions, preventing us from describing the direct impact of phenological shifts on fitness consequences. Here we address the phenological relationship in a simple non-trophic interaction to document a causal process of a warming-driven fitness change in a cicada, Cryptotympana facialis, whose numbers increased dramatically in Osaka, Japan in the late 20th century. We show that synchrony of the rainy season and hatching time may have a substantial influence on hatching success, by 1) shifting the time of completion of embryonic development, and 2) supplying water at various intervals. We estimate the change in hatching time over the last eleven decades (1901-2009) based on meteorological records and the temperature-dependent rate of C. facialis embryogenesis. Our estimate shows that hatching had initially occurred after the rainy season, and that warming had advanced it into the rainy season in the late 20th century. The probability of hatching success was markedly variable, and often very low before this synchronization occurred, but became stably high thereafter. Our findings suggest that the stabilizing effect of this synchrony on fitness was indispensable to the recent population increase of C. facialis.