Phenology is the study of periodic plant and animal life cycle events and how these are influenced by seasonal and interannual variations in climate, as well as habitat factors (such as elevation). The word, coined by the Belgian botanist Charles Morren around 1849,[1] is derived from the Greek ????? (phain?), "to show, to bring to light, make to appear"[2] + ????? (logos), amongst others "study, discourse, reasoning"[3] and indicates that phenology has been principally concerned with the dates of first occurrence of biological events in their annual cycle. Examples include the date of emergence of leaves and flowers, the first flight of butterflies and the first appearance of migratory birds, the date of leaf colouring and fall in deciduous trees, the dates of egg-laying of birds and amphibia, or the timing of the developmental cycles of temperate-zone honey bee colonies. In the scientific literature on ecology, the term is used more generally to indicate the time frame for any seasonal biological phenomena, including the dates of last appearance (e.g., the seasonal phenology of a species may be from April through September).

Phenological development of Olive flowering, following BBCH standard scale. a-50, b-51, c-54, d-57, (<15% open flowers); f-65, (>15% open flowers); g-67, (<15% open flowers); h-68 (Oteros et al., 2013)[4]

Because many such phenomena are very sensitive to small variations in climate, especially to temperature, phenological records can be a useful proxy for temperature in historical climatology, especially in the study of climate change and global warming. For example, viticultural records of grape harvests in Europe have been used to reconstruct a record of summer growing season temperatures going back more than 500 years.[5][6] In addition to providing a longer historical baseline than instrumental measurements, phenological observations provide high temporal resolution of ongoing changes related to global warming.[7][8]

Past records

Observations of phenological events have provided indications of the progress of the natural calendar since ancient agricultural times. Many cultures have traditional phenological proverbs and sayings which indicate a time for action: "When the sloe tree is white as a sheet, sow your barley whether it be dry or wet" or attempt to forecast future climate: "If oak's before ash, you're in for a splash. If ash before oak, you're in for a soak". But the indications can be pretty unreliable, as an alternative version of the rhyme shows: "If the oak is out before the ash, 'Twill be a summer of wet and splash; If the ash is out before the oak,'Twill be a summer of fire and smoke." Theoretically, though, these are not mutually exclusive, as one forecasts immediate conditions and one forecasts future conditions.

The North American Bird Phenology Program at USGS Patuxent Wildlife Research Center (PWRC) is in possession of a collection of millions of bird arrival and departure date records for over 870 species across North America, dating between 1880 and 1970. This program, originally started by Wells W. Cooke, involved over 3,000 observers including many notable naturalists of the time. The program ran for 90 years and came to a close in 1970 when other programs starting up at PWRC took precedence. The program was again started in 2009 to digitize the collection of records and now with the help of citizens worldwide, each record is being transcribed into a database which will be publicly accessible for use.

The English naturalists Gilbert White and William Markwick reported the seasonal events of more than 400 plant and animal species, Gilbert White in Selborne, Hampshire and William Markwick in Battle, Sussex over a 25-year period between 1768 and 1793. The data, reported in White's Natural History and Antiquities of Selborne[9] are reported as the earliest and latest dates for each event over 25 years; so annual changes cannot therefore be determined.

In Japan and China the time of blossoming of cherry and peach trees is associated with ancient festivals and some of these dates can be traced back to the eighth century. Such historical records may, in principle, be capable of providing estimates of climate at dates before instrumental records became available. For example, records of the harvest dates of the pinot noir grape in Burgundy have been used in an attempt to reconstruct spring-summer temperatures from 1370 to 2003;[10][11] the reconstructed values during 1787-2000 have a correlation with Paris instrumental data of about 0.75.

Modern records

Robert Marsham is the founding father of modern phenological recording. Marsham was a wealthy landowner who kept systematic records of "Indications of spring" on his estate at Stratton Strawless, Norfolk, from 1736. These were in the form of dates of the first occurrence of events such as flowering, bud burst, emergence or flight of an insect. Consistent records of the same events or "phenophases" were maintained by generations of the same family over unprecedentedly long periods of time, eventually ending with the death of Mary Marsham in 1958, so that trends can be observed and related to long-term climate records. The data show significant variation in dates which broadly correspond with warm and cold years. Between 1850 and 1950 a long-term trend of gradual climate warming is observable, and during this same period the Marsham record of oak leafing dates tended to become earlier.[12]

After 1960 the rate of warming accelerated, and this is mirrored by increasing earliness of oak leafing, recorded in the data collected by Jean Combes in Surrey. Over the past 250 years, the first leafing date of oak appears to have advanced by about 8 days, corresponding to overall warming on the order of 1.5 °C in the same period.

Towards the end of the 19th century the recording of the appearance and development of plants and animals became a national pastime, and between 1891 and 1948 a programme of phenological recording was organised across the British Isles by the Royal Meteorological Society (RMS). Up to 600 observers submitted returns in some years, with numbers averaging a few hundred. During this period 11 main plant phenophases were consistently recorded over the 58 years from 1891-1948, and a further 14 phenophases were recorded for the 20 years between 1929 and 1948. The returns were summarised each year in the Quarterly Journal of the RMS as The Phenological Reports. The 58-year data have been summarised by Jeffree (1960),[13] and show that flowering dates could be as many as 21 days early and as many as 34 days late, with extreme earliness greatest in summer flowering species, and extreme lateness in spring flowering species. In all 25 species, the timings of all phenological events are significantly related to temperature,[14][15] indicating that phenological events are likely to get earlier as climate warms.

The Phenological Reports ended suddenly in 1948 after 58 years, and Britain was without a national recording scheme for almost 50 years, just at a time when climate change was becoming evident. During this period, important contributions were made by individual dedicated observers. The naturalist and author Richard Fitter recorded the First Flowering Date (FFD) of 557 species of British flowering plants in Oxfordshire between about 1954 and 1990. Writing in Science in 2002, Richard Fitter and his son Alistair Fitter found that "the average FFD of 385 British plant species has advanced by 4.5 days during the past decade compared with the previous four decades."[16][17] They note that FFD is sensitive to temperature, as is generally agreed, that "150 to 200 species may be flowering on average 15 days earlier in Britain now than in the very recent past" and that these earlier FFDs will have "profound ecosystem and evolutionary consequences".

In the last decade, national recording in Britain has been resumed by the UK Phenology network [2], run by Woodland Trust and the Centre for Ecology and Hydrology and the BBC Springwatch survey.[18] There is a USA National Phenology Network [3] in which both professional scientists and lay recorders participate, a European Phenology Network that has monitoring, research and educational remits[19] and many other countries such as Canada (Alberta Plantwatch [4] and Saskatchewan PlantWatch[20]), China and Australia[21][22] have phenological programs.

In eastern North America, almanacs are traditionally used for information on action phenology (in agriculture), taking into account the astronomical positions at the time. William Felker has studied phenology in Ohio, US, since 1973 and now publishes "Poor Will's Almanack", a phenological almanac for farmers (not to be confused with a late 18th-century almanac by the same name).

Airborne sensors

Recent technological advances in studying the earth from space have resulted in a new field of phenological research that is concerned with observing the phenology of whole ecosystems and stands of vegetation on a global scale using proxy approaches. These methods complement the traditional phenological methods which recorded the first occurrences of individual species and phenophases.

The most successful of these approaches is based on tracking the temporal change of a Vegetation Index (like Normalized Difference Vegetation Index(NDVI)). NDVI makes use of the vegetation's typical low reflection in the red (red energy is mostly absorbed by growing plants for Photosynthesis) and strong reflection in the Near Infrared (Infrared energy is mostly reflected by plants due to their cellular structure). Due to its robustness and simplicity, NDVI has become one of the most popular remote sensing based products. Typically, a vegetation index is constructed in such a way that the attenuated reflected sunlight energy (1% to 30% of incident sunlight) is amplified by ratio-ing red and NIR following this equation:

NDVI temporal profile for a typical patch of coniferous forest over a period of six years. This temporal profile depicts the growing season every year as well as changes in this profile from year to year due to climatic and other constraints. Data and graph are based on the MODIS sensor standard public vegetation index product.[23] Data archived at the ORNL DAAC [1], courtesy of Dr. Robert Cook.[24]

The evolution of the vegetation index through time, depicted by the graph above, exhibits a strong correlation with the typical green vegetation growth stages (emergence, vigor/growth, maturity, and harvest/senescence). These temporal curves are analyzed to extract useful parameters about the vegetation growing season (start of season, end of season, length of growing season, etc.). Other growing season parameters could potentially be extracted, and global maps of any of these growing season parameters could then be constructed and used in all sorts of climatic change studies.

A noteworthy example of the use of remote sensing based phenology is the work of Ranga Myneni[25] from Boston University. This work[26][27] showed an apparent increase in vegetation productivity that most likely resulted from the increase in temperature and lengthening of the growing season in the boreal forest.[28] Another example based on the MODIS enhanced vegetation index (EVI) reported by Alfredo Huete[29] at the University of Arizona and colleagues showed that the Amazon Rainforest, as opposed to the long held view of a monotonous growing season or growth only during the wet rainy season, does in fact exhibit growth spurts during the dry season.[30][31]

However, these phenological parameters are only an approximation of the true biological growth stages. This is mainly due to the limitation of current space-based remote sensing, especially the spatial resolution, and the nature of vegetation index. A pixel in an image does not contain a pure target (like a tree, a shrub, etc.) but contains a mixture of whatever intersected the sensor's field of view.

See also


  1. ^
  2. ^ ?????, Henry George Liddell, Robert Scott, A Greek-English Lexicon, on Perseus
  3. ^ ?????, Henry George Liddell, Robert Scott, A Greek-English Lexicon, on Perseus
  4. ^ Oteros, J., García-Mozo, H., Vázquez, L., Mestre, A., Domínguez-Vilches, E., Galán, C. (2013). Modelling olive phenological response to weather and topography. Agriculture Ecosystems & Environment, 179: 62-68. Link
  5. ^ Meier, Nicole (2007). "Grape Harvest Records as a Proxy for Swiss April to August Temperature Reconstructions" (PDF). Diplomarbeit der Philosophisch-naturwissenschaftlichen Fakultät der Universität Bern (Thesis of Philosophy and science faculty of the University of Bern). University of Bern. Retrieved . Phenological grape harvest observations in Switzerland over the last 500 years have been used as a proxy indicator for reconstructing past temperature variability. 
  6. ^ Meier, N.; Rutishauser, T.; Luterbacher, J.; Pfister, C.; Wanner, H. (2007). "Grape Harvest Dates as a proxy for Swiss April to August Temperature Reconstructions back to AD 1480". Geophysical Research Letters. 34 (20): L20705. Bibcode:2007GeoRL..3420705M. doi:10.1029/2007GL031381. Phenological grape harvest observations in Switzerland over the last 500 years have been used as a proxy indicator for reconstructing past temperature variability. 
  7. ^ Menzel, A.; Sparks, T.H.; Estrella, N.; Koch, E.; Aasa, A.; Ahas, R.; Alm-kübler, K.; Bissolli, P.; Braslavská, O.; Briede, A.; et al. (2006). "European phenological response to climate change matches the warming pattern". Global Change Biology. 12 (10): 1969-1976. doi:10.1111/j.1365-2486.2006.01193.x. One of the preferred indicators is phenology, the science of natural recurring events, as their recorded dates provide a high-temporal resolution of ongoing changes. 
  8. ^ Schwartz, M. D.; Ahas, R.; Aasa, A. (2006). "Onset of spring starting earlier across the Northern Hemisphere". Global Change Biology. 12 (2): 343-351. doi:10.1111/j.1365-2486.2005.01097.x. SI first leaf dates, measuring change in the start of 'early spring' (roughly the time of shrub budburst and lawn first greening), are getting earlier in nearly all parts of the Northern Hemisphere. The average rate of change over the 1955-2002 period is approximately -1.2 days per decade. 
  9. ^ White, G (1789) The Natural History and Antiquities of Selborne
  10. ^ Chuine, I.; Yiou, P.; Viovy, N.; Seguin, B.; Daux, V.; Le Roy, Ladurie (2004). "Grape ripening as a past climate indicator" (PDF). Nature. 432 (7015): 289-290. Bibcode:2004Natur.432..289C. PMID 15549085. doi:10.1038/432289a. 
  11. ^ Keenan, D.J. (2007). "Grape harvest dates are poor indicators of summer warmth" (PDF). Theoretical and Applied Climatology. 87: 255-256. Bibcode:2007ThApC..87..255K. doi:10.1007/s00704-006-0197-9. 
  12. ^ Sparks, T.H.; Carey, P.D. (1995). "The responses of species to climate over two centuries: an analysis of the Marsham phenological record, 1736-1947". Journal of Ecology. 83 (2): 321-329. doi:10.2307/2261570. 
  13. ^ Jeffree, E.P. (1960). "Some long-term means from the Phenological reports (1891-1948) of the Royal Meteorological Society". Quarterly Journal of the Royal Meteorological Society. 86 (367): 95-103. Bibcode:1960QJRMS..86...95J. doi:10.1002/qj.49708636710. 
  14. ^ Sparks T, Jeffree E, Jeffree C (2000). "An examination of the relationship between flowering times and temperature at the national scale using long-term phenological records from the UK". International Journal of Biometeorology. 44 (2): 82-87. Bibcode:2000IJBm...44...82S. PMID 10993562. doi:10.1007/s004840000049. 
  15. ^ SpringerLink - Abstract
  16. ^ Fitter A, Fitter R (2002). "Rapid changes in flowering time in British plants". Science. 296 (5573): 1689-1691. Bibcode:2002Sci...296.1689F. PMID 12040195. doi:10.1126/science.1071617. 
  17. ^ "Rapid Changes in Flowering Time in British Plants" (PDF). 296. SCIENCE. 31 May 2002. Retrieved . 
  18. ^ BBC - Science & Nature - UK Wildlife - Springwatch survey
  19. ^ "European Phenology Network". Archived from the original on 2007-12-22. Retrieved . 
  20. ^ Nature Saskatchewan : PlantWatch
  21. ^ "ClimateWatch". EarthWatch Institute Australia. Retrieved 2013. 
  22. ^ BioWatch Home Archived July 22, 2012, at the Wayback Machine.
  23. ^ Tbrs, Modis Vi Cd-Rom
  24. ^ 49971CU_Txt
  25. ^ Welcome to the Climate and Vegetation Research Group, Boston University
  26. ^ Myneni, RB; Keeling, CD; Tucker, CJ; Asrar, G; Nemani, RR (1997). "Increased plant growth in the northern high latitudes from 1981 to 1991". Nature. 386 (6626): 698. Bibcode:1997Natur.386..698M. doi:10.1038/386698a0. 
  27. ^ Increased plant growth in the northern high latitudes from 1981 to 1991
  28. ^ ISI Web of Knowledge [v3.0]
  29. ^ Tbrs, Modis Vi Cd-Rom
  30. ^ Huete, Alfredo R.; Didan, Kamel; Shimabukuro, Yosio E.; Ratana, Piyachat; Saleska, Scott R.; Hutyra, Lucy R.; Yang, Wenze; Nemani, Ramakrishna R.; Myneni, Ranga (2006). "Amazon rainforests green-up with sunlight in dry season" (PDF). Geophysical Research Letters. 33 (6): L06405. Bibcode:2006GeoRL..33.6405H. doi:10.1029/2005GL025583. 
  31. ^ Lindsey, Rebecca; Robert Simmon (June 30, 2006). "Defying Dry: Amazon Greener in Dry Season than Wet". The Earth Observatory. EOS Project Science Office, NASA Goddard. Retrieved 2013. 

External links

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