Editing IPCC:AR6/WGII/Chapter-2 (section)

==== 2.4.2.4 Observed Phenological Responses to Climate Change ====

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Since AR5, the number of studies of changes in phenology (timing of biological events) has increased substantially, aided by advances in remote sensing ( [[#Piao--2019|Piao et al., 2019]] ). Phenological studies have documented particularly consistent conclusions on responses of plants and animals to warming, including the advancement of spring events and the lengthening of growing seasons in temperate regions (via a combination of advancement of spring events and, to a lesser extent, the retardation of autumn events) ( ''robust evidence'' , ''high agreement'' ) (Table 2.2, Table 2.3, Table SM2.1) ( [[#Menzel--2020|Menzel et al., 2020]] ). In the Tropics, by contrast, changes in precipitation have more strongly influenced animal phenology than have temperature changes ( [[#Cohen--2018|Cohen et al., 2018]] ). A meta-analysis compared observed phenological advances in birds with expectations due to warming local climates, and concluded that the observed advances fell short of what was expected and that a substantial phenological climate debt had been generated ( [[#Radchuk--2019|Radchuk et al., 2019]] ).

Taxonomic groups have differed in their responses ( [[#Parmesan--2007|Parmesan, 2007]] ; [[#Thackeray--2010|Thackeray et al., 2010]] ), and a few have completely diverged from general trends. For example, seabirds continue to breed with their pre-climate-change phenologies ( [[#Keogan--2018|Keogan et al., 2018]] ). Newer reviews and analyses reveal differences in responses across continents and time intervals ( [[#Piao--2019|Piao et al., 2019]] ). Mean advance in days per decade for plants was 5.5 in China and 3.0–4.2 in Europe, but only 0.9 in North America ( [[#Piao--2019|Piao et al., 2019]] ). Mean values for the retardation of autumn leaf fall, which can be more influenced by photoperiod and less by temperature than spring leaf-out, were 0.36 days per decade in Europe ( [[#Menzel--2020|Menzel et al., 2020]] ), 2.6 days per decade in China and around 3 days per decade in the USA ( ''medium evidence'' , ''high agreement'' ) ( [[#Piao--2019|Piao et al., 2019]] ).

The rapid rate of the advancement of spring events in the 1990s slowed down in the 2000s, and stalled or even reversed in some regions ( [[#Menzel--2020|Menzel et al., 2020]] ). [[#Wang--2019|Wang et al. (2019)]] noted, from remote sensing, that during the ‘global warming hiatus’ from 1998 to 2012, there were no global trends in either spring green-up or autumn colouring. Annual crops, the timing of which is determined by farmers, were an exception. When natural systems were advancing fast prior to 1998, farmers advanced more slowly, but during the natural ‘hiatus’, farmed crops advanced faster than wild plants and cultivated trees ( [[#Menzel--2020|Menzel et al., 2020]] ). In a long (67 years) European time series ( [[#Menzel--2020|Menzel et al., 2020]] ), autumn leaf colouring showed delays attributed to winter and spring warming in 57% of observations (mean delay of 0.36 days per decade); spring and summer phenologies advanced in 89% of wild plants, despite decreased winter chilling, with around 60% of trends significant and ‘strongly attributable’ to winter and spring warming; and the growing season lengthened in 84% of cases (mean lengthening 0.26 days yr -1 ) (Table 2.2).

'''Table 2.2 |''' Global fingerprints of climate change impacts across wild species. (Updated from ( [[#Parmesan--2015|Parmesan and Hanley, 2015]] ). For each study for which data were made available, a response for an individual species or functional group was classified as (1) no response (i.e., no significant change in the measured trait over time), (2) if a significant change was found, the response was classified as either consistent or not consistent with expectations according to local or regional climate trends. Percentages are approximate and estimated for the studies as a whole. Individual analyses within the studies may differ. The specific metrics of climate change analysed for associations with biological change vary somewhat across studies, but most use changes in local or regional temperatures (e.g., mean monthly T or mean annual T), with some using precipitation metrics (e.g., total annual rainfall). For example, a consistent response would be poleward range shifts in areas that are warming. Probability (P) of getting the observed ratio of consistent-to-not consistent responses by chance was &lt;10–13 for ( [[#Parmesan--2003|Parmesan and Yohe, 2003]] ; [[#Root--2003|Root et al., 2003]] ; [[#Root--2005|Root et al., 2005]] ; [[#Poloczanska--2013|Poloczanska et al., 2013]] ) and &lt;0.001 for [[#Rosenzweig--2008|Rosenzweig et al. (2008)]] . The last collumn distinguishes studies that were designed for attribution to climate change (e.g. by analysing only long-term data from relatively undisturbed habitats (see section 2.1.3 and 2.4.1)( [[#Parmesan--2013|Parmesan et al., 2013]] ; [[#Cramer--2014|Cramer et al., 2014]] ) from those that analysed all available data, including data from areas highly-impacted by non-climate drivers (e.g. LULCC).

{| class="wikitable"
|-
! '''Study'''

! '''N: total numbers of species, functional groups or studies'''

! '''Species in given system: Terrestrial (T) Marine (M) Freshwater (F)'''

! '''Types of change'''

! '''Changes documented'''

! '''Geographical region'''

! '''Study allows for attribution to climate change'''

|-
| colspan="7"| '''2.2a Observed phenological changes'''

|-
| ( [[#Parmesan--2003|Parmesan and Yohe, 2003]] )

| 677 species

| T: 461 plants, 168 birds, 35 insects; T/F: 9 amphibians; F: 2 fish

| Spring phenology

| Overall: 9% delay; 27% no trend; 62% advance

Mean change 2.3 days per decade advance

| Global

| Yes

|-
| ( [[#Menzel--2006|Menzel et al., 2006]] )

| Agricultural crops, fruit trees, wild plants

| 100% T

| Spring and autumn phenology

| From 1971 to 2000, 48% responding as expected; spring advance 2.5 days per decade, mean autumn delay 0.2 days per decade, fruit ripening 2.4 days per decade advance; farming activities 0.4 days per decade advance

| Europe

| Yes

|-
| ( [[#Parmesan--2007|Parmesan, 2007]] )

| 203 species

| T, F

| Spring phenology

| Overall advance 2.8 days per decade

20 changes (delays), 153 advances, 8 no change; significantly more advance at higher latitudes

| Global

| Yes

|-
| ( [[#Rosenzweig--2008|Rosenzweig et al., 2008]] )

| 55 studies (~100–200 species)

| T: 65%

M: 13%

F: 22%

| Various

| 90% of changes consistent with local/regional climate change

| Global

| Yes

|-
| ( [[#Thackeray--2010|Thackeray et al., 2010]] )

| 726 taxa

| T: birds, moths, aphids, terrestrial plants; M and F: phytoplankton

| Spring phenology

| 83.5% of ‘trends’ were advances; mean overall advance 3.9 days per decade; T plants 93% advancing, mean 5.8 days per decade; F plants 62% advancing, mean 2.3 days per decade; secondary consumers advanced less than primary consumers and producers

| UK

| No

|-
| ( [[#While--2014|While and Uller, 2014]] )

| 59 populations, 17 studies

| T/F, 100% Amphibians

| Phenology

| 35% statistically significant change; mean advance 6.1 ± 1.65 days per decade; range 17.5 days delay to 41.9 days advance; 65% ( ''n'' = 47 populations) found significant relationship between breeding phenology and temperature; higher latitudes advanced more

| Global

| No

|-
| ( [[#Gill--2015|Gill et al., 2015]] )

| 64 studies

| T: 100%

trees

| Delay of autumn senescence

| Delay averaged 0.33 days yr -1 and 1.20 days per degree Celsius warming; more delay at low latitudes across Northern Hemisphere; high-latitude species driven more by photoperiod than low-latitude species

| Global

| No

|-
| ( [[#Ficetola--2016|Ficetola and Maiorano, 2016]] )

| 66 studies of temperature effects;

15 of precipitation

| T/F 100% amphibians

| Phenology and abundances

| Population dynamics driven by precipitation while breeding phenology driven by temperature

| Global

| No

|-
| ( [[#Halupka--2017|Halupka and Halupka, 2017]] )

| 28 species multi-brooded, 27 species single-brooded, some species several populations

| T 100% (birds)

| Phenology: length of breeding season

| Shows differences in sign of response between single and multi-broods and migrants vs. residents; Season extended by 4 days per decade for multi-brooded, shortened by 2 days per decade for single-brooded;

Multi: 26 species; 15 of 34 populations significantly extended, none significantly reduced

| Northern Hemisphere

| Yes

|-
| ( [[#Kharouba--2018|Kharouba et al., 2018]] )

| 88 species in 54 pair-wise interactions

|
| T: changes in relative phenologies of consumers and their resources

| Asynchrony between consumers and resources has increased in some cases and decreased in others, with no significant trend; the prediction that asynchronies should be increasing in general is not supported.

| Global

| No

|-
| ( [[#Cohen--2018|Cohen et al., 2018]] )

| 127 studies

| T: 100% animals

| Phenological trends

| 81% of 127 studies of animals show phenological change in direction of earlier spring; some studies were multi-species.

Mean advance since 1950: 2.88 days per decade.

| Europe

North America

Australia

Japan

| No

|-
| ( [[#Keogan--2018|Keogan et al., 2018]] )

| 145 populations, 209 time series

| T: Seabirds breeding sites

| Phenological trends

| No change in breeding dates between 1952 and 2015

| Global

| Yes

|-
| ( [[#Radchuk--2019|Radchuk et al., 2019]] )

| 4835 studies, 1413 species

| T: animals; T/F amphibians

| Phenological trends

| Greatest phenological advancements in amphibians, followed by insects and birds, in this order.

| Global but most in Northern Hemisphere

| No

|-
| ( [[#Piao--2019|Piao et al., 2019]] )

| Review

| T: Plants

| Spring and autumn phenologies

| Rate of advance slowing down across Northern Hemisphere and reversed in parts of western North America in response to regional cooling since 1980s

| Global

| No

|-
| ( [[#Menzel--2020|Menzel et al., 2020]] )

| 53 species in Germany, 37 in Austria, 21 in Switzerland (includes overlaps)

| T: Plants

| Spring and autumn phenologies

| Long time series: 1951–2018. Autumn leaf colouring: mean delay 0.36 days per decade; spring phenology (leaf-unfolding) mean advance 0.24 days per decade; summer phenology (fruit ripening) mean advance 0.26 days per decade. Growing season length mean increase 0.26 days yr -1 but farming season length decreased by 0.02 days yr -1 .

| Europe

| Yes

|-
| colspan="7"| '''2.2b. Observed Changes In Distributions, Abundances And Local Population Extinctions'''

|-
| ( [[#Parmesan--2003|Parmesan and Yohe, 2003]] )

| 920 species

| T: 85.2%

M: 13.5%

F: 1.3%

| Distributions and abundances

| 50% of species (460/920) showed changes in distribution or abundances consistent with local or regional climate change

| Global

| Yes

|-
| ( [[#Root--2003|Root et al., 2003]] )

| 926 species

| T: 94%

M: 5.4%

F: 0.6%

| Distributions and abundances

| 52% of species (483/926) showed changes in distribution or abundances consistent with local or regional climate change

| Global

| Yes

|-
| ( [[#Rosenzweig--2008|Rosenzweig et al., 2008]] )

| 18 studies

| T: 65%

M: 13%

F: 22%

| Distributions and abundances

| 90% of studies showed changes in distribution or abundances consistent with local or regional climate change

| Global

| Yes

|-
| ( [[#Pöyry--2009|Pöyry et al., 2009]] )

| 48 species

| T: butterflies

| Range shifts

| From 1992 to 2004, 37 ranges shifted poleward, 9 shifted equatorially, 2 no change. Non-threatened species expanded poleward by 84.5 km, threatened species showed no significant change (&lt;2.1 km)

| Finland

| Yes

|-
| ( [[#Tingley--2009|Tingley et al., 2009]] )

| 53 species

| T: birds

| Elevational range shifts

| Resurvey (2003–2008) of historical elevational transects (1911–1929). 90.6% of species tracked their climate niche (temperature and/or precipitation) with regional climate change; Lower-elevation species (mean range centroid = 916 m) tracked only precipitation; high-elevation species (mean range centroid = 1944 m) tracked only temperature; species that tracked both temperature and precipitation had mid-elevation range centroids (1374–1841 m)

| California, USA

| Yes

|-
| ( [[#Chen--2011|Chen et al., 2011]] )

| 24 taxonomic group × region combinations for latitude, 31 for elevation

| T &gt;264

M &gt;10

F &gt;34

| Range shifts: elevation and latitude

| Mean upward elevation shift 11.0 m per decade

Poleward shift 16.9 km per decade

| Pseudo-global

| No

|-
| ( [[#Grewe--2013|Grewe et al., 2013]] )

| 90 species

| T/F Dragonflies

| Shifts of northern range boundaries

| 48 poleward shifts; 26 equatorial; 16 no change from 1988 to 2006

Southern lentic (standing water) species expanded 116 km polewards; southern lotic (running water) and all northern species stayed stable.

| Europe

| No

|-
| ( [[#Mason--2015|Mason et al., 2015]] )

| 21 animal groups, 1573 species

| T: birds, Lepidoptera

T/F: Odonates

| Range shifts in 3 time periods

| Northward shifts 23 km per decade (1966–1975) and 18 km per decade (1986–1995), with significant differences among taxa in rates of change

| UK

| Yes

|-
| ( [[#Gibson-Reinemer--2015|Gibson-Reinemer and Rahel, 2015]] )

| 13 studies, 273 species:

Plants, birds, mammals, marine inverterbrates

| T and M

| Range shifts in 2 or 3 areas for each species;

shift measured as change of limit or centroid

| 50% shifts of cold limits inconsistent with each other within species despite similar warming; species showing inconsistent shifts (including stable vs. directional or different directions) = 47% plants, 54% birds, 46% marine invertebrates, 60% mammals. Large difference in magnitude of range shifts when in same direction (mean difference 8.8 times)

| Global

| No

|-
| ( [[#Ficetola--2016|Ficetola and Maiorano, 2016]] )

| 66 studies of temperature effects; 15 studies of precipitation effects

| T/F 100% (amphibians)

| Phenology and abundances

| Population dynamics driven by precipitation, breeding phenology driven by temperature

| Global

| No

|-
| ( [[#Scheffers--2016|Scheffers et al., 2016]] )

| 94 ecological processes

| T, F, M

| All possible types and levels of ecological change

| 82% of ecological processes affected by climate change

| Global

| No

|-
| ( [[#Wiens--2016|Wiens, 2016]] )

| 976 species

| T, F, M

| Population extinction rates near warm latitudinal and elevational range limits

| 47% of species suffered climate-related local extinctions: fish 59%, insects 56%, birds 44%, plants 39%, amphibians 37%, mammals 35%

| Global

| Yes

|-
| ( [[#Bowler--2017|Bowler et al., 2017]] )

| 1167 populations, 22 communities

| T: 48%

M: 61%

F: 35%

| Abundance;

population trends

| T species with warm-temperature preference performed better than cool preferers; F and M species: no effect of temperature preference on performance; 47% of species with significant abundance changes: 61% M, 48% T, 35% F

| Europe

| Yes

|-
| ( [[#Pacifici--2017|Pacifici et al., 2017]] )

| 873 mammals, 1272 birds

| T: 100% (birds and mammals)

| Multiple: range change, abundance, reproductive rate, survival, body mass

| Estimated negative impacts (range contraction, reduced reproductive rates or other measures of fitness estimates) for IUCN-threatened species based on actual observed change in more common, related species; 47% threatened mammals and 23% birds negatively impacted by climate change in part of their ranges

| Global for birds; mammals North America

| Unclear (complex methods)

|-
| ( [[#MacLean--2017|MacLean and Beissinger, 2017]] )

| 21 studies

26 assemblages of taxonomically related species

| T: Plants and animals

| Range shifts in latitude and altitude related to species’ traits: dispersal, body size, habitat, diet specialization and historic range limit

| High-latitude/altitude range boundaries shifted less than lower-latitude/altitude boundaries. Author explanation is that habitat limits were reached (e.g., mountain tops). Magnitudes of shifts positively related to dispersal traits and habitat breadth.

| Global

| No

|-
| ( [[#Ralston--2017|Ralston et al., 2017]] )

| 46 species

| T: Birds

| Shifts in climate niche breadth, filling of climate space and overall abundance

| Species increasing in abundance were also increasing breeding climate niche breadth and niche filling. Declining species were opposite: niche breadths narrowing and greater climate debt.

| North America

| No

|-
| ( [[#Rumpf--2019|Rumpf et al., 2019]] )

| 1026 species

| T: plants, invertebrates, vertebrates

| Comparison of rates of range limit shift at leading and trailing elevational edges

| No difference in mean rate of shift of leading and trailing edges; elevational range sizes not changing systematically. Greater lags in regions with faster warming.

| Global

| No

|-
| ( [[#Freeman--2018|Freeman et al., 2018]] )

| 975 species, 32 elevational gradients

| T: plants, endotherms, ectotherms

| Comparison of rates of range limit shift at leading and trailing elevational edges

| Mean change at warm limit 92 ± 455 m per degree Celsius; cool limit 131 ± 465 m per degree Celsius; (± SD, not significantly different from each other). Available area and range sizes decreased for mountaintop species.

| Global

| No

|-
| ( [[#Anderegg--2019|Anderegg et al., 2019]] )

| Meta-analysis

50 studies, &gt;100 species

| T: 100% woody plants

| Mortality at dry range edges

| 100 individual species + a community of 828 species

mortality at range edges due to drought was 33% greater than for core populations

| Apparently global

| Yes;

drought not warming

|-
| ( [[#Román-Palacios--2020|Román-Palacios and Wiens, 2020]] )

| 10 studies, 538 species, 581 sites

| T: plants and animals

| Analysis for drivers of population extinctions at warm range edges

| 44% of species had suffered local population extinctions near warm-range limits. In temperate regions, sites with local extinction had greater increases in maximum temperature than those without (0.456°C vs. 0.153°C, P &lt; 0.001, ''n'' = 505 sites) and smaller increases in mean temperatures (0.412°C vs. 1.231°C, P &lt; 0.001). In tropical regions, range edges with local extinction also had greater increases in maximum temperatures (0.316°C vs. 0.061°C, P &lt; 0.001, ''n'' = 76), but changes in mean temperatures were similar between edges with and without extinctions (0.415°C vs. 0.406°C, P = 0.9)

| Global

| Yes

|}

Changes in freshwater systems are consistent with changes in terrestrial systems: earlier development of phytoplankton and zooplankton and earlier spawning by fish in spring as well as extension of the growing season are occurring ( ''robust evidence'' , ''high agreement'' ) ( [[#Adrian--2009|Adrian et al., 2009]] ; [[#De%20Senerpont%20Domis--2013|De Senerpont Domis et al., 2013]] ; [[#Adrian--2016|Adrian et al., 2016]] ; [[#Thackeray--2016|Thackeray et al., 2016]] ). Phenological changes in lakes have been related to rising water temperatures, reduced ice cover and prolonged thermal stratification (increasing evidence and agreement since AR5; ''very high confidence'' ). Crozier and Hutchings (2014) reviewed the phenological changes in fish and documented that changes in the timing of migration and reproduction, age at maturity, age at juvenile migration, growth, survival and fecundity were associated primarily with changes in temperature. The median return time of Atlantic salmon to rivers in Newfoundland and Labrador advanced by 12–21 days over the past decades, associated with overall warmer conditions ( [[#Dempson--2017|Dempson et al., 2017]] ).

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