Patterns of flower-visiting insects depend on flowering phenological shifts along an altitudinal gradient in subalpine moorland ecosystems

Abstract Alpine and subalpine moorland ecosystems contain unique plant communities, often with many endemic and threatened species, some of which depend on insect pollination. Although alpine and subalpine moorland ecosystems are vulnerable to climatic change, few studies have investigated flower-visiting insects in such ecosystems and examined the factors regulating plant-pollinator interactions along altitudinal gradients. Here, we explored how altitudinal patterns in flower visitors change according to altitudinal shifts in flowering phenology in subalpine moorland ecosystems in northern Japan. We surveyed flower-visiting insects and flowering plants at five sites differing in altitude in early July (soon after snowmelt) and mid-August (peak growing season). In July, we found a higher visiting frequency by more variable insect orders including Dipteran, Hymenopteran, Coleopteran, and Lepidopteran species at the higher altitude sites in association with the mass flowering of Geum pentapetalum and Nephrophyllidium crista-galli. In August, such altitudinal patterns were not observed, and Dipteran species dominated across the sites due to the flowering of Narthecium asiaticum and Drosera rotundifolia. Earlier snowmelt associated with recent climate change is expected to extend the growth period of moorland plants and modify flowering phenology in moorland ecosystems, leading to altered plant-pollinator interactions. Our study provides key baselines for the detection of endangered biotic interactions and extinction risks of moorland plants under ongoing climate change.

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Phenological shifts of native and invasive species under climate change: insights from the Boechera–Lythrum model

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2016.0032 ◽

2017 ◽

Vol 372 (1712) ◽

pp. 20160032 ◽

Cited By ~ 13

Author(s):

Robert I. Colautti ◽

Jon Ågren ◽

Jill T. Anderson

Keyword(s):

Climate Change ◽

Environmental Conditions ◽

Rocky Mountain ◽

Flowering Phenology ◽

Lythrum Salicaria ◽

Genetic Constraints ◽

Floral Phenology ◽

Phenological Shifts ◽

Delayed Flowering

Warmer and drier climates have shifted phenologies of many species. However, the magnitude and direction of phenological shifts vary widely among taxa, and it is often unclear when shifts are adaptive or how they affect long-term viability. Here, we model evolution of flowering phenology based on our long-term research of two species exhibiting opposite shifts in floral phenology: Lythrum salicaria , which is invasive in North America, and the sparse Rocky Mountain native Boechera stricta . Genetic constraints are similar in both species, but differences in the timing of environmental conditions that favour growth lead to opposite phenological shifts under climate change. As temperatures increase, selection is predicted to favour earlier flowering in native B. stricta while reducing population viability, even if populations adapt rapidly to changing environmental conditions. By contrast, warming is predicted to favour delayed flowering in both native and introduced L. salicaria populations while increasing long-term viability. Relaxed selection from natural enemies in invasive L. salicaria is predicted to have little effect on flowering time but a large effect on reproductive fitness. Our approach highlights the importance of understanding ecological and genetic constraints to predict the ecological consequences of evolutionary responses to climate change on contemporary timescales. This article is part of the themed issue ‘Human influences on evolution, and the ecological and societal consequences’.

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Community and ecosystem responses to recent climate change

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2010.0021 ◽

2010 ◽

Vol 365 (1549) ◽

pp. 2019-2024 ◽

Cited By ~ 669

Author(s):

Gian-Reto Walther

Keyword(s):

Climate Change ◽

Biotic Interactions ◽

Climate Impact ◽

Trophic Levels ◽

Future Climate Change ◽

Individual Species ◽

Ecosystem Responses ◽

Ample Evidence ◽

Recent Climate Change ◽

Recent Climate

There is ample evidence for ecological responses to recent climate change. Most studies to date have concentrated on the effects of climate change on individuals and species, with particular emphasis on the effects on phenology and physiology of organisms as well as changes in the distribution and range shifts of species. However, responses by individual species to climate change are not isolated; they are connected through interactions with others at the same or adjacent trophic levels. Also from this more complex perspective, recent case studies have emphasized evidence on the effects of climate change on biotic interactions and ecosystem services. This review highlights the ‘knowns’ but also ‘unknowns’ resulting from recent climate impact studies and reveals limitations of (linear) extrapolations from recent climate-induced responses of species to expected trends and magnitudes of future climate change. Hence, there is need not only to continue to focus on the impacts of climate change on the actors in ecological networks but also and more intensively to focus on the linkages between them, and to acknowledge that biotic interactions and feedback processes lead to highly complex, nonlinear and sometimes abrupt responses.

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Individualistic sensitivities and exposure to climate change explain variation in species’ distribution and abundance changes

Science Advances ◽

10.1126/sciadv.1400220 ◽

2015 ◽

Vol 1 (9) ◽

pp. e1400220 ◽

Cited By ~ 12

Author(s):

Georgina Palmer ◽

Jane K. Hill ◽

Tom M. Brereton ◽

David R. Brooks ◽

Jason W. Chapman ◽

...

Keyword(s):

Climate Change ◽

Climate Changes ◽

Biotic Interactions ◽

National Scale ◽

The Past ◽

Recent Climate Change ◽

Recent Climate ◽

Species Specific ◽

Abundance And Distribution ◽

Different Levels

The responses of animals and plants to recent climate change vary greatly from species to species, but attempts to understand this variation have met with limited success. This has led to concerns that predictions of responses are inherently uncertain because of the complexity of interacting drivers and biotic interactions. However, we show for an exemplar group of 155 Lepidoptera species that about 60% of the variation among species in their abundance trends over the past four decades can be explained by species-specific exposure and sensitivity to climate change. Distribution changes were less well predicted, but nonetheless, up to 53% of the variation was explained. We found that species vary in their overall sensitivity to climate and respond to different components of the climate despite ostensibly experiencing the same climate changes. Hence, species have undergone different levels of population “forcing” (exposure), driving variation among species in their national-scale abundance and distribution trends. We conclude that variation in species’ responses to recent climate change may be more predictable than previously recognized.

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Elevational differences in developmental plasticity determine phenological responses of grasshoppers to recent climate warming

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2015.0441 ◽

2015 ◽

Vol 282 (1809) ◽

pp. 20150441 ◽

Cited By ~ 29

Author(s):

Lauren B. Buckley ◽

César R. Nufio ◽

Evan M. Kirk ◽

Joel G. Kingsolver

Keyword(s):

Climate Change ◽

Climate Warming ◽

Developmental Plasticity ◽

Adult Emergence ◽

High Elevation ◽

Full Life Cycle ◽

Recent Climate ◽

Adult Body ◽

Phenological Shifts ◽

Advanced Development

Annual species may increase reproduction by increasing adult body size through extended development, but risk being unable to complete development in seasonally limited environments. Synthetic reviews indicate that most, but not all, species have responded to recent climate warming by advancing the seasonal timing of adult emergence or reproduction. Here, we show that 50 years of climate change have delayed development in high-elevation, season-limited grasshopper populations, but advanced development in populations at lower elevations. Developmental delays are most pronounced for early-season species, which might benefit most from delaying development when released from seasonal time constraints. Rearing experiments confirm that population, elevation and temperature interact to determine development time. Population differences in developmental plasticity may account for variability in phenological shifts among adults. An integrated consideration of the full life cycle that considers local adaptation and plasticity may be essential for understanding and predicting responses to climate change.

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Disorder or a new order: how climate change affects phenological variability

10.1101/2021.10.08.463688 ◽

2021 ◽

Author(s):

Michael Stemkovski ◽

James R. Bell ◽

Elizabeth R. Ellwood ◽

Brian D. Inouye ◽

Hiromi Kobori ◽

...

Keyword(s):

Climate Change ◽

Biotic Interactions ◽

New Order ◽

Spring Phenology ◽

Interacting Species ◽

First Occurrence ◽

Phenological Shifts ◽

Flower Phenology ◽

Over Time

Advancing spring phenology is a well-documented consequence of anthropogenic climate change, but it is not well understood how climate change will affect the variability of phenology year-to-year. Species' phenological timings reflect adaptation to a broad suite of abiotic needs (e.g. thermal energy) and biotic interactions (e.g. predation and pollination), and changes in patterns of variability may disrupt those adaptations and interactions. Here, we present a geographically and taxonomically broad analysis of phenological shifts, temperature sensitivity, and changes in inter-annual variance encompassing nearly 10,000 long-term phenology time-series representing over 1,000 species across much of the northern hemisphere. We show that early-season species in colder and less seasonal regions were the most sensitive to temperature change and had the least variable phenologies. The timings of leaf-out, flowering, insect first-occurrence, and bird arrival have all shifted earlier and tend to be less variable in warmer years. This has led leaf-out and flower phenology to become moderately but significantly less variable over time. These simultaneous changes in phenological averages and the variation around them have the potential to influence mismatches among interacting species that are difficult to anticipate if shifts in average are studied in isolation.

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Global shifts in the phenological synchrony of species interactions over recent decades

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1714511115 ◽

2018 ◽

Vol 115 (20) ◽

pp. 5211-5216 ◽

Cited By ~ 92

Author(s):

Heather M. Kharouba ◽

Johan Ehrlén ◽

Andrew Gelman ◽

Kjell Bolmgren ◽

Jenica M. Allen ◽

...

Keyword(s):

Climate Change ◽

Species Interactions ◽

Time Series Data ◽

Terrestrial Ecosystems ◽

Series Data ◽

Global Trends ◽

Predator Prey ◽

Interacting Species ◽

Recent Climate ◽

Phenological Shifts

Phenological responses to climate change (e.g., earlier leaf-out or egg hatch date) are now well documented and clearly linked to rising temperatures in recent decades. Such shifts in the phenologies of interacting species may lead to shifts in their synchrony, with cascading community and ecosystem consequences. To date, single-system studies have provided no clear picture, either finding synchrony shifts may be extremely prevalent [Mayor SJ, et al. (2017) Sci Rep 7:1902] or relatively uncommon [Iler AM, et al. (2013) Glob Chang Biol 19:2348–2359], suggesting that shifts toward asynchrony may be infrequent. A meta-analytic approach would provide insights into global trends and how they are linked to climate change. We compared phenological shifts among pairwise species interactions (e.g., predator–prey) using published long-term time-series data of phenological events from aquatic and terrestrial ecosystems across four continents since 1951 to determine whether recent climate change has led to overall shifts in synchrony. We show that the relative timing of key life cycle events of interacting species has changed significantly over the past 35 years. Further, by comparing the period before major climate change (pre-1980s) and after, we show that estimated changes in phenology and synchrony are greater in recent decades. However, there has been no consistent trend in the direction of these changes. Our findings show that there have been shifts in the timing of interacting species in recent decades; the next challenges are to improve our ability to predict the direction of change and understand the full consequences for communities and ecosystems.

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Does Phenological Plasticity Help or Hinder Range Shifts Under Climate Change?

Frontiers in Ecology and Evolution ◽

10.3389/fevo.2021.689192 ◽

2021 ◽

Vol 9 ◽

Author(s):

Meredith A. Zettlemoyer ◽

Megan L. Peterson

Keyword(s):

Climate Change ◽

Species Interactions ◽

Flowering Phenology ◽

Species Traits ◽

Species Range ◽

Range Shifts ◽

Suitable Habitat ◽

Species Ranges ◽

Population Spread ◽

Phenological Shifts

Climate warming is predicted to shift species’ ranges as previously uninhabitable environments just beyond the leading range edges become suitable habitat and trailing range edges become increasingly unsuitable. Understanding which aspects of the environment and species traits mediate these range shifts is critical for understanding species’ possible redistributions under global change, yet we have a limited understanding of the ecological and evolutionary responses underlying population spread or extinction at species’ range edges. Within plant populations, shifts in flowering phenology have been one of the strongest and most consistent responses to climate change, and are likely to play an important role in mediating population dynamics within and beyond species’ ranges. However, the role of phenological shifts, and particularly phenological plasticity, in species’ range shifts remains relatively unstudied. Here, we synthesize literature on phenology, plasticity, and adaptation to suggest ways in which phenological responses to climate may vary across species’ ranges and review the empirical evidence for and against these hypotheses. We then outline how phenological plasticity could facilitate or hinder persistence and potential consequences of phenological plasticity in range expansions, including phenological cues, shifts in correlated traits, altered species interactions, and effects on gene flow. Finally, we suggest future avenues for research, such as characterizing reaction norms for phenology across a species’ range and in beyond-the-range transplant experiments. Given the prevalence and magnitude of phenological shifts, future work should carefully dissect its costs and benefits for population persistence, and incorporate phenological plasticity into models predicting species’ persistence and geographic range shifts under climate change.

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