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The effects of phenological mismatches on demography
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Climate change is altering the phenology of species across the world, but what are the consequences of these phenological changes for the demography and population dynamics of species? Time-sensitive relationships, such as migration, breeding and predation, may be disrupted or altered, which may in turn alter the rates of reproduction and survival, leading some populations to decline and others to increase in abundance. However, finding evidence for disrupted relationships, or lack thereof, and their demographic effects, is difficult because the necessary detailed observational data are rare. Moreover, we do not know how sensitive species will generally be to phenological mismatches when they occur. Existing long-term studies provide preliminary data for analysing the phenology and demography of species in several locations. In many instances, though, observational protocols may need to be optimized to characterize timing-based multi-trophic interactions. As a basis for future research, we outline some of the key questions and approaches to improving our understanding of the relationships among phenology, demography and climate in a multi-trophic context. There are many challenges associated with this line of research, not the least of which is the need for detailed, long-term data on many organisms in a single system. However, we identify key questions that can be addressed with data that already exist and propose approaches that could guide future research.
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... In the middle and high latitudes of the Northern Hemisphere, the nestling growth period of passerines must be synchronized with the peak abundance of insect larva prey to maximize nestling growth and survival [1][2][3][4][5]. Climate change-induced spring temperature increases can advance the timing of insect development [6,7], whereas the timing of breeding in birds is regulated more by photoperiod than temperature [8], resulting in a trophic mismatch between nestlings and insect larvae [7][8][9][10][11][12]. Nestlings hatching outside the peak period of insect larvae abundance may suffer malnutrition, posing a significant challenge to nestling survival [9,10]. ...
... Climate change-induced spring temperature increases can advance the timing of insect development [6,7], whereas the timing of breeding in birds is regulated more by photoperiod than temperature [8], resulting in a trophic mismatch between nestlings and insect larvae [7][8][9][10][11][12]. Nestlings hatching outside the peak period of insect larvae abundance may suffer malnutrition, posing a significant challenge to nestling survival [9,10]. Although adults increase their feeding efforts to satisfy nestling nutritional requirements [13], little is known about how nestlings cope with the stress caused by trophic mismatch. ...
Passerine nestlings frequently suffer from sub-optimal food conditions due to climate change-induced trophic mismatch between the nestlings and their optimal food resources. The ability of nestlings to buffer this challenge is less well understood. We hypothesized that poor food conditions might induce a higher immune response and lower growth rate of nestlings, and such physiological plasticity is conducive to nestling survival. To test this, we examined how food (grasshopper nymphs) abundance affects the expression of interferon-γ (IFN-γ), tumor necrosis factor-α (TNF-α), interleukin-1 β (IL-1β) genes, plasma IGF-1 levels, body mass, and fledging rates in wild Asian short-toed lark (Alaudala cheleensis) nestlings. Linear mixed models revealed that nymph biomass significantly influenced the expression of IFN-γ, TNF-α, and IL-1β genes, and the level of plasma IGF-1. The expressions of IFN-γ, TNF-α, and IL-1β genes were negatively correlated with nymph biomass and plasma IGF-1 level. Plasma IGF-1 level, nestling body mass growth rate, was positively correlated with nymph biomass. Despite a positive correlation between the nestling fledge rate and nymph biomass, more than 60% of nestlings fledged when nymph biomass was at the lowest level. These results suggest that immunity and growth plasticity of nestlings may be an adaptation for birds to buffer the negative effects of trophic mismatch.
... There are also indications that increased primary productivity increases predation on the nests of ground-breeding birds, in particular, in the upper bioclimatic sub-zones . There is also some evidence for negative impacts of phenological mismatch, which affects migration and access to food supply during nesting (Carey 2009, Crick 2004, Miller-Rushing et al. 2010. Species that are specifically adapted to the habitat structures or trophic conditions in intact alpine ecosystems are expected to decline due to habitat loss in a warming climate (Lehikoinen et al. 2014 and to changes in alpine grazing regimes that affect tree line dynamics (Bryn and Potthof 2018). ...
... Birds expected to be most affected are species that are specialised on nest sites such as cavity-nesters, or species that require habitats or food resources that are now scarce, such as the late successional stages of pristine forest (e.g., White-backed Woodpecker and Siberian Jay, Bradter et al. 2021). Climate change can cause phenological mismatches, which affect migration and access to food resources during nesting and has been identified as generic mechanism that affects many species (Carey 2009, Crick 2004, Miller-Rushing et al. 2010, but lagged or indirect effects of climate change may also be involved (Jenouvrier 2013). Due to the simultaneous action of forestry and climate change during the timeframe when monitoring data on bird communities are available, it may be difficult to distinguish the relative impact of these two drivers. ...
The panel-based assessment of ecosystem condition (PAEC) is an evidence-based ap-proach to assess the condition of Norwegian ecosystems. The assessment is carried out by an expert panel with broad expertise in the ecosystems to be assessed and is inspired by approaches used in international assessments such as IPCC and IPBES. The assessment follows an earlier developed protocol. In this report, PAEC is piloted for major terrestrial ecosystems in the county of Trøndelag; forest, alpine, open-lowlands, and wetlands.
For each ecosystem, a list of indicators of change in ecosystem condition in response to anthropogenic drivers is developed. The indicators fall within seven main ecosystem char-acteristics: primary production, biomass distribution among trophic levels, functional groups within trophic levels, functionally important species, biological diversity, landscape ecologi-cal patterns, and abiotic factors. The expected change in indicators in response to anthro-pogenic drivers are termed phenomena, and their selection is based on published literature, including reference to the confidence of a change being observed in response to anthropo-genic drivers and the mechanism leading to a deterioration in ecosystem state. Datasets to quantify each indicator are identified and collated and the quality of each dataset is assessed in terms of its spatial and temporal appropriateness.
In the first assessment step, the validity (VP) of each phenomenon is scored and used to infer confidence in the causal relationship between changes in the indicator and anthropo-genic drivers. The next step is an evaluation of the biological and statistical significance of the evidence for the occurrence of each phenomenon, termed evidence (EP) of the phe-nomenon. The third step is a consolidated assessment of the ecological state based on the associated indicators and phenomena, first for each ecosystem characteristic, and subse-quently for the ecosystem as a whole. The assessment is based on the validity, the quality of the evidence, and the data quality for each phenomenon. This provides a qualitative as-sessment of deviation from the reference condition of “no deviation”, “limited deviation” or “substantial deviation”. The assessments are each supported by narrative accounts. The pilot assessment involved analysis of 24 datasets documenting 41 indicators. Several indi-cators were included in multiple ecosystems. In total there were 27 indicators used for forest ecosystems, 24 for alpine ecosystems, and 16 in each of wetlands and open lowlands.
In the forest ecosystems, substantial deviation from the reference condition was identified for five of the ecosystem characteristics. The two exceptions were primary productivity where there was a limited deviation from the reference condition, and biological diversity where there was no deviation from the reference condition (but the latter was based on a single indicator and hence an entirely inadequate indicator coverage). The deviations were found primarily in climatic variables, cervids and their forage and predators, and dead wood. Overall, the forest ecosystem was assessed as having a substantial deviation from the ref-erence condition.
In the alpine ecosystems, substantial deviation from the reference condition was identified for the abiotic ecosystem characteristic, largely attributed to indicators associated with tem-perature, seasonality, and snow. Limited deviation from the reference condition was as-sessed for functionally important species and primary productivity (both based on a partially
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adequate indicator coverage) and for biological diversity, functional groups within trophic levels and landscape ecological patterns (but these were based on an inadequate indicator coverage). For the ecosystem characteristic biomass distribution among trophic levels, the quality of evidence was insufficient to conclude regarding the condition of the single indicator involved, and no overall assessment of this ecosystem characteristic could be undertaken. Overall, the alpine ecosystem was assessed as having limited deviation from the reference condition.
For both open lowland and wetland ecosystems, several ecosystem characteristics were not assessed due to a lack of relevant indicator datasets. For this reason, no overall assess-ment of the ecosystems as a whole could be undertaken. However, for both ecosystems, there was a substantial deviation from the reference condition for abiotic factors (tempera-ture, seasonality, and snow). In open lowlands, there was a substantial deviation in func-tionally important species (ungulates) and limited deviation in primary productivity and bio-logical diversity. In wetlands, there was a limited deviation from the reference condition in primary productivity, biological diversity, and landscape ecological patterns.
Most challenges encountered during this pilot assessment related to the inadequacy of the datasets for assessing ecosystem condition. Reasons behind this include that ecosystem ex-tents are not adequately mapped, particularly those characterised by small and fragmented patches, and a taxonomic or geographical limitation of datasets and environmental monitoring. The report suggests further development of indicators for operational application. Finally, the report also suggests knowledge needs and prioritisation for further research to support the future implementation of ecosystem assessments in Norway.
... There is also evidence that increased primary productivity increases predation on the nests of ground-breeding birds, in particular, in the colder bioclimatic sub-zones of the Low Arctic tundra . The links to anthropogenic drivers are assessed as certain, especially the relationship with phenological mismatch, which affects migration and access to food supply during nesting (Carey 2009, Crick 2004, Miller-Rushing et al. 2010. Species that are specifically adapted to the habitat structures, competitive, or trophic conditions (nutrient supply and predation pressure) in intact tundra ecosystems are expected to decline in a warming Arctic (Lehikoinen et al. 2019, Lehikoinen et al. 2014 The most important anthropogenic driver of changes in this indicator is climate change. ...
... Altered species interactions during reproduction may be more impactful than abiotic effects (Ockendon et al., 2014). While it remains contested if trophic mismatches can have population-level consequences (Both et al., 2006;Franks et al., 2018;Johansson et al., 2015;Miller-Rushing et al., 2010;Reed et al., 2013;Saino et al., 2011), inadequate food resources can cause reduced growth rates and may lead to reduced survival or fitness (Gaston et al., 2009;Lameris et al., 2018Lameris et al., , 2022Ross et al., 2018;Sedinger et al., 1995). A greater mechanistic understanding is needed as well as identification of baselines for defining optimal food resource characteristics. ...
Abstract Climate change is leading to phenological shifts across a wide range of species globally. Polar oceans are hotspots of rapid climate change where sea ice dynamics structure ecosystems and organismal life cycles are attuned to ice seasonality. To anticipate climate change impacts on populations and ecosystem services, it is critical to understand ecosystem phenology to determine species activity patterns, optimal environmental windows for processes like reproduction, and the ramifications of ecological mismatches. Since 1991, the Palmer Antarctica Long‐Term Ecological Research (LTER) program has monitored seasonal dynamics near Palmer Station. Here, we review the species that occupy this region as year‐round residents, seasonal breeders, or periodic visitors. We show that sea ice retreat and increasing photoperiod in the spring trigger a sequence of events from mid‐November to mid‐February, including Adélie penguin clutch initiation, snow melt, calm conditions (low winds and warm air/sea temperature), phytoplankton blooms, shallow mixed layer depths, particulate organic carbon flux, peak humpback whale abundances, nutrient drawdown, and bacterial accumulation. Subsequently, from May to June, snow accumulates, zooplankton indicator species appear, and sea ice advances. The standard deviation in the timing of most events ranged from ~20 to 45 days, which was striking compared with Adélie penguin clutch initiation that varied 30 days) than mean dates and the variability in timing was low (
... Proposed originally in the context of fisheries, the match/mismatch hypothesis posits that in seasonal environments, the recruitment of a consumer is determined by the degree of temporal overlap between the consumer's reproductive season and its resources [2,4,7,[9][10][11]. Put in a broader ecological context, this hypothesis predicts that, when they occur, phenological mismatches have stronger effects on specialist than generalist species, as the former should be less plastic in resource use than the latter [7,[12][13][14]. ...
Species respond idiosyncratically to environmental variation, which may generate phenological mismatches. We assess the consequences of such mismatches for solitary bees. During 9 years, we studied flowering phenology and nesting phenology and demography of five wood-nesting solitary bee species representing a broad gradient of specialization/generalization in the use of floral resources. We found that the reproductive performance and population growth rate of bees tended to be lower with increasing nesting–flowering mismatches, except for the most generalized bee species. Our findings help elucidate the role of phenological mismatches for the demography of wild pollinators, which perform key ecosystem functions and provide important services for humanity. Furthermore, if climate change increases phenological mismatches in this system, we expect negative consequences of climate change for specialist bees.
... Climate can strongly influence phenology (the timing of life-history events) by speeding up or delaying events such as emergence, peak activity and reproduction [1]. In turn, phenology can influence individual fitness [2,3], species interactions [4,5] and ecosystem function [6]. Shifts in climate may alter phenology and consequently organismal fitness by exposing organisms to unfavorable abiotic environments and through altering the strength of species interactions ( phenological mismatch). ...
The timing of life events (phenology) can be influenced by climate. Studies from around the world tell us that climate cues and species' responses can vary greatly. If variation in climate effects on phenology is strong within a single ecosystem, climate change could lead to ecological disruption, but detailed data from diverse taxa within a single ecosystem are rare. We collated first sighting and median activity within a high-elevation environment for plants, insects, birds, mammals and an amphibian across 45 years (1975–2020). We related 10 812 phenological events to climate data to determine the relative importance of climate effects on species’ phenologies. We demonstrate significant variation in climate-phenology linkage across taxa in a single ecosystem. Both current and prior climate predicted changes in phenology. Taxa responded to some cues similarly, such as snowmelt date and spring temperatures; other cues affected phenology differently. For example, prior summer precipitation had no effect on most plants, delayed first activity of some insects, but advanced activity of the amphibian, some mammals, and birds. Comparing phenological responses of taxa at a single location, we find that important cues often differ among taxa, suggesting that changes to climate may disrupt synchrony of timing among taxa.
Understanding attributes of phenology beyond the mean date of a life history event, such as variability among individuals within a population, is critical to predict how climate‐induced phenological shifts may alter population dynamics. Identifying how phenological variability impacts organisms is especially needed to better understand how phenological shifts affect trophic dynamics (e.g., shifts in variability of top predators affecting primary production). To better understand the effects of phenological variability on both populations and communities, we examined how variation in egg hatching synchrony of predatory marbled salamanders (Ambystoma opacum) impacted intraspecific interactions at the larval stage, ultimately affecting demographic traits and survival through metamorphosis. We also examined how hatching synchrony affected overall trophic dynamics (e.g., primary consumers and producers) in pond food webs. We experimentally manipulated the degree of hatching synchrony of embryonic A. opacum and subsequently reared larvae in outdoor mesocosms. We monitored demographic traits such as larval growth, size at and time to metamorphosis, and survival. To assess trophic dynamics, we monitored zooplankton abundance and phytoplankton biomass during the experiment. Larvae exhibited greater variability in body size in medium and low hatching synchrony treatments compared to high synchrony treatments. Larval body size variation diminished over time to ultimately result in no differences in most life history traits at metamorphosis or survival among hatching synchrony treatments. We also found no differences among treatments in zooplankton abundance or phytoplankton biomass, likely because of minimal variation in A. opacum survival among treatments that would induce top‐down changes. Overall, we found that phenological variation may be context dependent in its influence on demography and overall community structure. Because of concerns for how phenological shifts will affect species interactions, greater scrutiny into conditions that would promote changes in population and community dynamics is needed.
Recent insect abundance declines may have affected populations of insectivorous bird species, but evidence for this is limited. Here, we use spatially overlapping 29‐year time‐series of aerial insect biomass and Barn Swallow Hirundo rustica numbers and breeding success from southern England to model the association between changes in invertebrate prey abundance, Swallow productivity, and population trends. We found a positive statistical relationship between Swallow chick survival and the biomass of aerial insects available for chicks. In nests where at least one chick fledged, 96.7% of chicks were predicted to survive to fledging where there was high insect biomass (an average of 0.62 g day‐1), compared to 87.4% of chicks surviving to fledging where there was the lowest insect biomass (0.02 g day‐1; excluding the greatest and smallest 5% of insect biomass measurements). The amount of food available for chicks was largely a function of annual variation in insect abundance rather than the phenology of egg laying and insect emergence. However, we did not find a correlation between annual insect abundance and subsequent Swallow population growth. In the context of concerns about declining insect abundance, this study shows how changes in insect biomass may affect the productivity of an insectivorous bird at a regional scale, but with uncertain implications for population size at that same scale.
Effects of global climate change on population persistence are often mediated by life‐history traits of individuals, especially the timing of somatic growth, reproductive development, and reproduction itself. These traits can vary among age groups and between the sexes, a result of differential life‐history tactics and levels of lifetime reproductive investment. Unfortunately, the trait data necessary for revealing sex‐specific breeding behaviors and use of breeding cues over reasonably large geographic areas remain sparse for most taxa. In this study, we assembled and analyzed a new reproductive trait base for the North American deer mouse (Peromyscus maniculatus) from digitized natural history specimens and field censuses. We used the data to reconstruct sex‐specific breeding phenologies and their drivers within and among North American ecoregions. Male and female phenologies varied across the geographic range of this species, with discordance in timing and intensity being highest in regions of lower seasonality (and longer breeding seasons). Reliance on environmental variables as breeding cues also appeared to vary in a sex‐specific manner, being most similar for photoperiod and least similar for temperature (positive male response and negative female response); in addition, model validation indicated that phenological models generalized better for males than for females. Finally, our individual‐level trait data also show that male reproductive investment (quantified as relative testis size) varies across the vastly different abiotic and social (i.e., female breeding) contexts studied here. By harmonizing across a broad set of digital data resources, we demonstrate the potential to uncover drivers of phenological variation within species and inform global change predictions at multiple scales of biological organization.
Phenology refers to the seasonal timing patterns commonly exhibited by life on Earth, from blooming flowers to breeding birds to human agriculture. Climate change is altering abiotic seasonality (e.g., longer summers) and in turn, phenological patterns contained within. However, how phenology should evolve is still an unsolved problem. This problem lies at the crux of predicting future phenological changes that will likely have substantial ecosystem consequences, and more fundamentally, of understanding an undeniably global phenomenon. Most studies have associated proximate environmental variables with phenological responses in case-specific ways, making it difficult to contextualize observations within a general evolutionary framework. We outline the complex but universal ways in which seasonal timing maps onto evolutionary fitness. We borrow lessons from life history theory and evolutionary demography that have benefited from a first principles-based theoretical scaffold. Lastly, we identify key questions for theorists and empiricists to help advance our general understanding of phenology.
Inbreeding depression is commonly observed in natural populations. The deleterious effects of forced inbreeding are often thought to be less pronounced in populations with self-pollinating mating systems than in primarily outcrossing populations. We tested this hypothesis by comparing the performance of plants produced by artificial self- and cross-pollination from three populations whose outcrossing rate estimates were 0.03, 0.26, and 0.58. Outcrossing rates and inbreeding coefficients were estimated using isozyme polymorphisms as genetic markers. Analysis of F statistics suggests that biparental inbreeding as well as self-fertilization contribute to the level of homozygosity in the seed crop. Biparental inbreeding will reduce the heterozygosity of progeny produced by outcrossing, relative to random outcrossing expectations, and hence will reduce the effects of outcrossing versus self-fertilization. Heterotic selection may increase the average heterozygosity during the life history. Selfed and outcrossed seeds from all three populations were equally likely to germinate and survive to reproduce. However, inbreeding depression was observed in fecundity traits of plants surviving to reproduction in all three populations. Even in the population whose natural self-fertilization rate was 97%, plants grown from seed produced by self-pollination produced fewer fruits and less total seed weight than plants grown from outcrossed seed. There was no detectable inbreeding depression in estimated lifetime fitness. Inbreeding effects for all reproductive yield characters were most severe in the accession from the most outcrossing population and least severe in the accession from the most self-fertilizing population.
In recent decades, global temperature has increased at an unprecedented rate. This has been causing rapid environmental shifts that have altered the selective regimes determining the annual organization of birds. In order to assess the potential for adaptive evolution in the timing of autumn migration, we estimated heritabilities of the onset of migratory activity in a southern German blackcap (Sylvia atricapilla) population, Heritabilities (h(2) =0.34-0.45) and coefficients of additive genetic variation (CVA=4.7-5.7) were significant and consistent when estimated by different methods, irrespective of whether they were derived from birds hatched in the wild or bred in captivity In an artificial selection experiment, we selected for later onset of migratory activity, simulating expected natural selection on this trait. We obtained a significant delay in the mean onset of migratory activity by more than one week after two generations of selection. Realized heritability (h(2) = 0.55) was in agreement with expected heritability in the cohort that the selection lille was derived from. Our results suggest that evolutionary changes in the timing of autumn migration may take place over a very short time period and will most probably be unconstrained by the lack of additive genetic variation.
Nutrition spans a wide range of mechanisms from acquisition of food to digestion, absorption and retention of energy substrates, water and other nutrients. Nutritional principles have been applied to improving individual health, athletic performance and longevity of humans and of their companion animals, and to maximizing agricultural efficiency by manipulating reproduction or growth of tissues such as muscle, hair or milk in livestock. Comparative nutrition borrows from these tra- tional approaches by applying similar techniques to studies of ecology and physiology of wildlife. Comparative approaches to nutrition integrate several levels of organization because the acquisition and flow of energy and nutrients connect individuals to populations, populations to communities, and communities to ecosystems. Integrative Wildlife Nutrition connects behavioral, morphological and biochemical traits of animals to the life history of species and thus the dynamics of populations. An integrated approach to nutrition provides a practical framework for understanding the interactions between food resources and wildlife popu- tions and for managing the harvest of abundant species and the conservation of threatened populations. This book is for students and professionals in animal physiology and ecology, conservation biology and wildlife management. It is based on our lectures, dem- strations and practical classes taught in the USA, Canada and Australia over the last three decades. Instructors can use Integrative Wildlife Nutrition as a text in wildlife and conservation biology programs, and as a reference source for related courses in wildlife ecology.
1. We exammed the effects of daily inflorescence size (three-, six-, nine- and 12-flowered) and the position of flowers within an inflorescence (bottom, middle and top) on the frequency of self-fertilization using genetic markers and experimental manipulation of garden populations of Eichhornia paniculata, a self-compatible bee-pollinated plant. 2. Based on the observed tendency for bees to forage upwards on inflorescences and a model of the relation between pollen carry-over and the number of flowers visited per inflorescence, we predicted that the frequency of self-fertilization should increase from bottom to top flowers and with increasing inflorescence sizes. 3. Electrophoretic analysis of open-pollinated progeny arrays supported both of these predictions. The fraction of self-fertilized seeds increased progressively from bottom to top flowers within an inflorescence and there was a significant increase in the frequency of self-fertilization with daily inflorescence size. Inflorescences of all sizes exhibited equivalent increases in the frequency of self-fertilization of flowers from bottom to top positions. 4. The general agreement between our experimental results and model expectations emphasizes the strong influence of pollinator behaviour on mating patterns in self-compatible plants. Such effects have the potential to act as strong selective forces maintaining both anti-selfing mechanisms in mass-flowering species and protandry in species with vertical inflorescences visited by negatively geotactic pollinators.
In the semiarid Intermountain West (Utah), Acer negundo var. interior, a deciduous, dioecious tree, exhibits significant habitat-specific sex ratio biases. The overall sex ratio (male/female) does not deviate significantly from one, but the sex ratio is significantly male-biased (1.62) in drought-prone habitats, while it is significantly female-biased (0.65) in moist, streamside habitats. Results suggest that: 1) gender-specific physiological traits can help explain the maintenance of habitat-specific sex ratio biases along a soil moisture gradient, and 2) that the combination of the gender-specific physiology, growth, and allocation differences contribute to differences in the size (=age) structure of male and female plants within the population. -from Authors