Photoperiodism

Last updated

Photoperiod is the change of day length around the seasons. The rotation of the earth around its axis produces 24 hour changes in light (day) and dark (night) cycles on earth. The length of the light and dark in each phase varies across the seasons due to the tilt of the earth around its axis. The photoperiod defines the length of the light, for example a summer day the length of light could be 16 hours while the dark is 8 hours, whereas a winter day the length of day could be 8 hours, whereas the dark is 16 hours. Importantly, the seasons are different in the northern hemisphere than the southern hemisphere.

Contents

Photoperiodism is the physiological reaction of organisms to the length of light or a dark period. It occurs in plants and animals. Plant photoperiodism can also be defined as the developmental responses of plants to the relative lengths of light and dark periods. They are classified under three groups according to the photoperiods: short-day plants, long-day plants, and day-neutral plants.

In animals photoperiodism (sometimes called seasonality) is the suite of physiological changes that occur in response to changes in day length. This allows animals to respond to a temporally changing environment associated with changing seasons as the earth orbits the sun.

Plants

Pr converts to Pfr during the day time and Pfr slowly reverts to Pr during the night time. When nights are short, an excess amount of Pfr remains in the day time and during long nights, most of the Pfr is reverted to Pr. Photoperiodism in plants.jpg
Pr converts to Pfr during the day time and Pfr slowly reverts to Pr during the night time. When nights are short, an excess amount of Pfr remains in the day time and during long nights, most of the Pfr is reverted to Pr.

In 1920, W. W. Garner and H. A. Allard published their discoveries on photoperiodism and felt it was the length of daylight that was critical, [1] [2] but it was later discovered that the length of the night was the controlling factor. [3] [4] Photoperiodic flowering plants are classified as long-day plants or short-day plants even though night is the critical factor because of the initial misunderstanding about daylight being the controlling factor. Along with long-day plants and short-day plants, there are plants that fall into a "dual-day length category". These plants are either long-short-day plants (LSDP) or short-long-day plants (SLDP). LSDPs flower after a series of long days followed by short days whereas SLDPs flower after a series of short days followed by long days. [5] Each plant has a different length critical photoperiod, or critical night length. [1]

Many flowering plants (angiosperms) use a circadian rhythm together with photoreceptor protein, such as phytochrome or cryptochrome, [1] to sense seasonal changes in night length, or photoperiod, which they take as signals to flower. In a further subdivision, obligate photoperiodic plants absolutely require a long or short enough night before flowering, whereas facultative photoperiodic plants are more likely to flower under one condition.

Phytochrome comes in two forms: Pr and Pfr. Red light (which is present during the day) converts phytochrome to its active form (Pfr) which then stimulates various processes such as germination, flowering or branching. In comparison, plants receive more far-red in the shade, and this converts phytochrome from Pfr to its inactive form, Pr, inhibiting germination. This system of Pfr to Pr conversion allows the plant to sense when it is night and when it is day. [6] Pfr can also be converted back to Pr by a process known as dark reversion, where long periods of darkness trigger the conversion of Pfr. [7] This is important in regards to plant flowering. Experiments by Halliday et al. showed that manipulations of the red-to far-red ratio in Arabidopsis can alter flowering. They discovered that plants tend to flower later when exposed to more red light, proving that red light is inhibitory to flowering. [8] Other experiments have proven this by exposing plants to extra red-light in the middle of the night. A short-day plant will not flower if light is turned on for a few minutes in the middle of the night and a long-day plant can flower if exposed to more red-light in the middle of the night. [9]

Cryptochromes are another type of photoreceptor that is important in photoperiodism. Cryptochromes absorb blue light and UV-A. Cryptochromes entrain the circadian clock to light. [10] It has been found that both cryptochrome and phytochrome abundance relies on light and the amount of cryptochrome can change depending on day-length. This shows how important both of the photoreceptors are in regards to determining day-length. [11]

Modern biologists believe [12] that it is the coincidence of the active forms of phytochrome or cryptochrome, created by light during the daytime, with the rhythms of the circadian clock that allows plants to measure the length of the night. Other than flowering, photoperiodism in plants includes the growth of stems or roots during certain seasons and the loss of leaves. Artificial lighting can be used to induce extra-long days. [1]

Long-day plants

Long Day Plants.jpg

Long-day plants flower when the night length falls below their critical photoperiod. [13] These plants typically flower during late spring or early summer as days are getting longer. In the northern hemisphere, the longest day of the year (summer solstice) is on or about 21 June. [14] After that date, days grow shorter (i.e. nights grow longer) until 21 December (the winter solstice). This situation is reversed in the southern hemisphere (i.e., longest day is 21 December and shortest day is 21 June). [1] [2]

Some long-day obligate plants are:

Some long-day facultative plants are:

Short-day plants

Short Day Plants.jpg

Short-day (also called long-night) plants flower when the night lengths exceed their critical photoperiod. [15] They cannot flower under short nights or if a pulse of artificial light is shone on the plant for several minutes during the night; they require a continuous period of darkness before floral development can begin. Natural nighttime light, such as moonlight or lightning, is not of sufficient brightness or duration to interrupt flowering. [1] [2]

Short-day plants flower as days grow shorter (and nights grow longer) after September 21st in the northern hemisphere, which is during summer or fall. The length of the dark period required to induce flowering differs among species and varieties of a species.

Photoperiodism affects flowering by inducing the shoot to produce floral buds instead of leaves and lateral buds.

Some short-day facultative plants are: [16]

Day-neutral plants

Day-neutral plants, such as cucumbers, roses, tomatoes, and Ruderalis (autoflowering cannabis) do not initiate flowering based on photoperiodism. [18] Instead, they may initiate flowering after attaining a certain overall developmental stage or age, or in response to alternative environmental stimuli, such as vernalisation (a period of low temperature). [1] [2]

Animals

Daylength, and thus knowledge of the season of the year, is vital to many animals. A number of biological and behavioural changes are dependent on this knowledge. Together with temperature changes, photoperiod provokes changes in the color of fur and feathers, migration, entry into hibernation, sexual behaviour, and even the resizing of organs.

In insects, sensitivity to photoperiod has been proven to be initiated by photoreceptors located in the brain. [19] [20] Photoperiod can affect insects at different life stages, serving as an environmental cue for physiological processes such as diapause induction and termination, and seasonal morphs. [21] In the water strider Aquarius paludum, for instance, photoperiod conditions during nymphal development have been shown to trigger seasonal changes in wing frequency and also induce diapause, although the threshold critical day lengths for the determination of both traits diverged by about an hour. [22] In Gerris buenoi , another water strider species, photoperiod has also been shown to be the cause of wing polyphenism, [23] although the specific daylengths changed between species, suggesting that phenotypic plasticity in response to photoperiod has evolved even between relatively closely related species.

The singing frequency of birds such as the canary depends on the photoperiod. In the spring, when the photoperiod increases (more daylight), the male canary's testes grow. As the testes grow, more androgens are secreted and song frequency increases. During autumn, when the photoperiod decreases (less daylight), the male canary's testes regress and androgen levels drop dramatically, resulting in decreased singing frequency. Not only is singing frequency dependent on the photoperiod but the song repertoire is also. The long photoperiod of spring results in a greater song repertoire. Autumn's shorter photoperiod results in a reduction in song repertoire. These behavioral photoperiod changes in male canaries are caused by changes in the song center of the brain. As the photoperiod increases, the high vocal center (HVC) and the robust nucleus of the archistriatum (RA) increase in size. When the photoperiod decreases, these areas of the brain regress. [24]

Mammals

In mammals, daylength is registered in the suprachiasmatic nucleus (SCN), which is informed by retinal light-sensitive ganglion cells, which are not involved in vision. The information travels through the retinohypothalamic tract (RHT). In most species the hormone melatonin is produced by the pineal gland only during the hours of darkness, influenced by the light input through the RHT and by innate circadian rhythms. This hormonal signal, combined with outputs from the SCN inform the rest of the body about the time of day, and the length of time that melatonin is secreted is how the time of year is perceived.

Many mammals, particularly those inhabiting temperate and polar regions, exhibit a remarkable degree of seasonality in response to changes in daylight hours(photoperiod). This seasonality manifests in a broad spectrum of behaviors and physiology, including hibernation, seasonal migrations, and coat color changes. A prime example of the adaptation to photoperiods is the seasonal coat color (SCC) species. [25] These animals undergo molting, transforming from dark summer fur to white coat in winter, that provides crucial camouflage in snowy environments.

Humans

The view has been expressed that humans' seasonality is largely believed to be evolutionary baggage. [26] [ relevant? ]. Human birth rate varies throughout the year, and the peak month of births appears to vary by latitude. [27] Seasonality in human birth rate appears to have largely decreased since the industrial revolution. [27] [28]

Other organisms

Photoperiodism has also been demonstrated in other organisms besides plants and animals. The fungus Neurospora crassa as well as the dinoflagellate Lingulodinium polyedra and the unicellular green alga Chlamydomonas reinhardtii have been shown to display photoperiodic responses. [29] [30] [31]

See also

Related Research Articles

<span class="mw-page-title-main">Circadian rhythm</span> Natural internal process that regulates the sleep-wake cycle

A circadian rhythm, or circadian cycle, is a natural oscillation that repeats roughly every 24 hours. Circadian rhythms can refer to any process that originates within an organism and responds to the environment. Circadian rhythms are regulated by a circadian clock whose primary function is to rhythmically co-ordinate biological processes so they occur at the correct time to maximize the fitness of an individual. Circadian rhythms have been widely observed in animals, plants, fungi and cyanobacteria and there is evidence that they evolved independently in each of these kingdoms of life.

<span class="mw-page-title-main">Plant physiology</span> Subdiscipline of botany

Plant physiology is a subdiscipline of botany concerned with the functioning, or physiology, of plants.

<span class="mw-page-title-main">Phytochrome</span> Protein used by plants, bacteria and fungi to detect light

Phytochromes are a class of photoreceptor proteins found in plants, bacteria and fungi. They respond to light in the red and far-red regions of the visible spectrum and can be classed as either Type I, which are activated by far-red light, or Type II that are activated by red light. Recent advances have suggested that phytochromes also act as temperature sensors, as warmer temperatures enhance their de-activation. All of these factors contribute to the plant's ability to germinate.

In developmental biology, photomorphogenesis is light-mediated development, where plant growth patterns respond to the light spectrum. This is a completely separate process from photosynthesis where light is used as a source of energy. Phytochromes, cryptochromes, and phototropins are photochromic sensory receptors that restrict the photomorphogenic effect of light to the UV-A, UV-B, blue, and red portions of the electromagnetic spectrum.

<span class="mw-page-title-main">Cryptochrome</span> Class of photoreceptors in plants and animals

Cryptochromes are a class of flavoproteins found in plants and animals that are sensitive to blue light. They are involved in the circadian rhythms and the sensing of magnetic fields in a number of species. The name cryptochrome was proposed as a portmanteau combining the chromatic nature of the photoreceptor, and the cryptogamic organisms on which many blue-light studies were carried out.

Far-red light is a range of light at the extreme red end of the visible spectrum, just before infrared light. Usually regarded as the region between 700 and 750 nm wavelength, it is dimly visible to human eyes. It is largely reflected or transmitted by plants because of the absorbance spectrum of chlorophyll, and it is perceived by the plant photoreceptor phytochrome. However, some organisms can use it as a source of energy in photosynthesis. Far-red light also is used for vision by certain organisms such as some species of deep-sea fishes and mantis shrimp.

Florigens are proteins capable of inducing flowering time in angiosperms. The prototypical florigen is encoded by the FT gene and its orthologs in Arabidopsis and other plants. Florigens are produced in the leaves, and act in the shoot apical meristem of buds and growing tips.

Erwin Bünning was a German biologist. His most famous contributions were to the field of chronobiology, where he proposed a model for the endogenous circadian rhythms governing plant photoperiodism. From these contributions, Bünning is considered a co-founder of chronobiology along with Jürgen Aschoff and Colin Pittendrigh.

Photoreceptor proteins are light-sensitive proteins involved in the sensing and response to light in a variety of organisms. Some examples are rhodopsin in the photoreceptor cells of the vertebrate retina, phytochrome in plants, and bacteriorhodopsin and bacteriophytochromes in some bacteria. They mediate light responses as varied as visual perception, phototropism and phototaxis, as well as responses to light-dark cycles such as circadian rhythm and other photoperiodisms including control of flowering times in plants and mating seasons in animals.

<span class="mw-page-title-main">Nyctinasty</span> Movements of higher plants in response to the onset of darkness

In plant biology, nyctinasty is the circadian rhythm-based nastic movement of higher plants in response to the onset of darkness, or a plant "sleeping". Nyctinastic movements are associated with diurnal light and temperature changes and controlled by the circadian clock. It has been argued that for plants that display foliar nyctinasty, it is a crucial mechanism for survival; however, most plants do not exhibit any nyctinastic movements. Nyctinasty is found in a range of plant species and across xeric, mesic, and aquatic environments, suggesting that this singular behavior may serve a variety of evolutionary benefits. Examples are the closing of the petals of a flower at dusk and the sleep movements of the leaves of many legumes.

<i>Wyeomyia smithii</i> Species of mosquito

Wyeomyia smithii, the pitcher plant mosquito, is an inquiline mosquito that completes its pre-adult life cycle in the phytotelma of—that is, the water contained by—the purple pitcher plant, Sarracenia purpurea. In this microcommunity of bacteria, rotifers, protozoa, and midges, W. smithii is the top-level predator; its presence determines the bacterial species diversity within the pitcher.

<span class="mw-page-title-main">Phototropism</span> Growth of a plant in response to a light stimulus

In biology, phototropism is the growth of an organism in response to a light stimulus. Phototropism is most often observed in plants, but can also occur in other organisms such as fungi. The cells on the plant that are farthest from the light contain a hormone called auxin that reacts when phototropism occurs. This causes the plant to have elongated cells on the furthest side from the light. Phototropism is one of the many plant tropisms, or movements, which respond to external stimuli. Growth towards a light source is called positive phototropism, while growth away from light is called negative phototropism. Negative phototropism is not to be confused with skototropism, which is defined as the growth towards darkness, whereas negative phototropism can refer to either the growth away from a light source or towards the darkness. Most plant shoots exhibit positive phototropism, and rearrange their chloroplasts in the leaves to maximize photosynthetic energy and promote growth. Some vine shoot tips exhibit negative phototropism, which allows them to grow towards dark, solid objects and climb them. The combination of phototropism and gravitropism allow plants to grow in the correct direction.

Circadian Clock Associated 1 (CCA1) is a gene that is central to the circadian oscillator of angiosperms. It was first identified in Arabidopsis thaliana in 1993. CCA1 interacts with LHY and TOC1 to form the core of the oscillator system. CCA1 expression peaks at dawn. Loss of CCA1 function leads to a shortened period in the expression of many other genes.

Steve A. Kay is a British-born chronobiologist who mainly works in the United States. Dr. Kay has pioneered methods to monitor daily gene expression in real time and characterized circadian gene expression in plants, flies and mammals. In 2014, Steve Kay celebrated 25 years of successful chronobiology research at the Kaylab 25 Symposium, joined by over one hundred researchers with whom he had collaborated with or mentored. Dr. Kay, a member of the National Academy of Sciences, U.S.A., briefly served as president of The Scripps Research Institute. and is currently a professor at the University of Southern California. He also served on the Life Sciences jury for the Infosys Prize in 2011.

LUX or Phytoclock1 (PCL1) is a gene that codes for LUX ARRHYTHMO, a protein necessary for circadian rhythms in Arabidopsis thaliana. LUX protein associates with Early Flowering 3 (ELF3) and Early Flowering 4 (ELF4) to form the Evening Complex (EC), a core component of the Arabidopsis repressilator model of the plant circadian clock. The LUX protein functions as a transcription factor that negatively regulates Pseudo-Response Regulator 9 (PRR9), a core gene of the Midday Complex, another component of the Arabidopsis repressilator model. LUX is also associated with circadian control of hypocotyl growth factor genes PHYTOCHROME INTERACTING FACTOR 4 (PIF4) and PHYTOCHROME INTERACTING FACTOR 5 (PIF5).

Pseudo-response regulator (PRR) refers to a group of genes that regulate the circadian oscillator in plants. There are four primary PRR proteins that perform the majority of interactions with other proteins within the circadian oscillator, and another (PRR3) that has limited function. These genes are all paralogs of each other, and all repress the transcription of Circadian Clock Associated 1 (CCA1) and Late Elongated Hypocotyl (LHY) at various times throughout the day. The expression of PRR9, PRR7, PRR5 and TOC1/PRR1 peak around morning, mid-day, afternoon and evening, respectively. As a group, these genes are one part of the three-part repressilator system that governs the biological clock in plants.

In chronobiology, the circannual cycle is characterized by biological processes and behaviors recurring on an approximate annual basis, spanning a period of about one year. This term is particularly relevant in the analysis of seasonal environmental changes and their influence on the physiology, behavior, and life cycles of organisms. Adaptations observed in response to these circannual rhythms include fur color transformation, molting, migration, breeding, fattening and hibernation, all of which are inherently driven and synchronized with external environmental changes.

Dmitri Nusinow is an American chronobiologist who studies plant circadian rhythms. He was born on November 7, 1976, in Inglewood, California. He currently resides in St. Louis, and his research focus includes a combination of molecular, biochemical, genetic, genomic, and proteomic tools to discover the molecular connections between signaling networks, circadian oscillators, and specific outputs. By combining these methods, he hopes to apply the knowledge elucidated from the Arabidopsis model to other plant species.

EARLY FLOWERING 3 (ELF3) is a plant-specific gene that encodes the hydroxyproline-rich glycoprotein and is required for the function of the circadian clock. ELF3 is one of the three components that make up the Evening Complex (EC) within the plant circadian clock, in which all three components reach peak gene expression and protein levels at dusk. ELF3 serves as a scaffold to bind EARLY FLOWERING 4 (ELF4) and LUX ARRHYTHMO (LUX), two other components of the EC, and functions to control photoperiod sensitivity in plants. ELF3 also plays an important role in temperature and light input within plants for circadian clock entrainment. Additionally, it plays roles in light and temperature signaling that are independent from its role in the EC.

Elaine Munsey Tobin is a professor of molecular, cell, and developmental biology at the University of California, Los Angeles (UCLA). Tobin is recognized as a Pioneer Member of the American Society of Plant Biologists (ASPB).

References

  1. 1 2 3 4 5 6 7 Mauseth JD (2003). Botany : An Introduction to Plant Biology (3rd ed.). Sudbury, MA: Jones and Bartlett Learning. pp. 422–27. ISBN   978-0-7637-2134-3.
  2. 1 2 3 4 Capon B (2005). Botany for Gardeners (2nd ed.). Portland, OR: Timber Publishing. pp. 148–51. ISBN   978-0-88192-655-2.
  3. ↑ Hamner KC, Bonner J (1938). "Photoperiodism in relation to hormones as factors in floral initiation and development" (PDF). Botanical Gazette. 100 (2): 388–431. doi:10.1086/334793. JSTOR   2471641. S2CID   84084837.
  4. ↑ Hamner KC (1940). "Interrelation of light and darkness in photoperiodic induction". Botanical Gazette. 101 (3): 658–87. doi:10.1086/334903. JSTOR   2472399. S2CID   83682483.
  5. ↑ Taiz L, Zeiger E, Møller I, Murphy A (2015). Plant Physiology and Development (Sixth ed.). Sunderland, MA: Sinauer Associates, Inc. ISBN   978-1-60535-353-1.
  6. ↑ Fankhauser C (April 2001). "The phytochromes, a family of red/far-red absorbing photoreceptors". The Journal of Biological Chemistry. 276 (15): 11453–11456. doi: 10.1074/jbc.R100006200 . PMID   11279228.
  7. ↑ Casal JJ, Candia AN, Sellaro R (June 2014). "Light perception and signalling by phytochrome A". Journal of Experimental Botany. 65 (11): 2835–2845. doi: 10.1093/jxb/ert379 . hdl: 11336/4338 . PMID   24220656.
  8. ↑ Lin C (May 2000). "Photoreceptors and regulation of flowering time". Plant Physiology. 123 (1): 39–50. doi:10.1104/pp.123.1.39. PMC   1539253 . PMID   10806223.
  9. ↑ Chamovitz D (2013). What A Plant Knows. Scientific American. pp. 17–18. ISBN   978-0-374-28873-0.
  10. ↑ Lin C, Todo T (2005). "The cryptochromes". Genome Biology. 6 (5): 220. doi: 10.1186/gb-2005-6-5-220 . PMC   1175950 . PMID   15892880.
  11. ↑ Mockler T, Yang H, Yu X, Parikh D, Cheng YC, Dolan S, Lin C (February 2003). "Regulation of photoperiodic flowering by Arabidopsis photoreceptors". Proceedings of the National Academy of Sciences of the United States of America. 100 (4): 2140–2145. Bibcode:2003PNAS..100.2140M. doi: 10.1073/pnas.0437826100 . PMC   149972 . PMID   12578985.
  12. ↑ Andrés F, Galbraith DW, Talón M, Domingo C (October 2009). "Analysis of PHOTOPERIOD SENSITIVITY5 sheds light on the role of phytochromes in photoperiodic flowering in rice". Plant Physiology. 151 (2): 681–690. doi:10.1104/pp.109.139097. PMC   2754645 . PMID   19675157.
  13. ↑ Starr C, Taggart R, Evers C, Starr L (2013). Plant Structure and Function. Vol. 4 (13th ed.). Brooks/Cole. p. 517. ISBN   978-1-111-58068-1.
  14. ↑ Gooley T (2010-03-30). The Natural Navigator. Random House. ISBN   978-0-7535-2311-7.
  15. ↑ BSCS Biology (9 ed.). BSCS. 2002. p. 519. ISBN   978-0-7872-9008-5.
  16. ↑ Jones HG (1992). Plants and Microclimate: A Quantitative Approach to Environmental Plant Physiology. Cambridge University Press. p.  225. ISBN   978-0-521-42524-7.
  17. ↑ Purcell LC, Salmeron M, Ashlock L (2014). "Chapter 2" (PDF). Arkansas Soybean Production Handbook - MP197. Little Rock, Arkansas: University of Arkansas Cooperative Extension Service. pp. 5–7. Retrieved 21 February 2016.
  18. ↑ Meneely P (2014). Genetic Analysis: Genes, Genomes, and Networks in Eukaryotes (2nd ed.). Oxford University Press. p. 373. ISBN   978-0-19-968126-6.
  19. ↑ Claret J (1966). "Recherche du centre photorecepteur lors de l'induction de la diapause chez Pieris brassicae L.". Comptes Rendus de l'Académie des Sciences. 262: 553–556.
  20. ↑ Bowen MF, Saunders DS, Bollenbacher WE, Gilbert LI (September 1984). "In vitro reprogramming of the photoperiodic clock in an insect brain-retrocerebral complex". Proceedings of the National Academy of Sciences of the United States of America. 81 (18): 5881–4. Bibcode:1984PNAS...81.5881B. doi: 10.1073/pnas.81.18.5881 . PMC   391816 . PMID   6592591.
  21. ↑ Saunders DS (2012). "Insect photoperiodism: seeing the light". Physiological Entomology. 37 (3): 207–218. doi: 10.1111/j.1365-3032.2012.00837.x . S2CID   85249708.
  22. ↑ Harada T, Numata H (1993). "Two Critical Day Lengths for the Determination of Wing Forms and the Induction of Adult Diapause in the Water Strider, Aquarius paludum". Naturwissenschaften. 80 (9): 430–432. Bibcode:1993NW.....80..430H. doi:10.1007/BF01168342. S2CID   39616943.
  23. ↑ Gudmunds E, Narayanan S, Lachivier E, Duchemin M, Khila A, Husby A (April 2022). "Photoperiod controls wing polyphenism in a water strider independently of insulin receptor signalling". Proceedings. Biological Sciences. 289 (1973): 20212764. doi:10.1098/rspb.2021.2764. PMC   9043737 . PMID   35473377.
  24. ↑ Nelson RJ (2005). An Introduction to Behavioral Endocrinology. Sunderland, MA: Sinauer Associates. p. 189.
  25. ↑ Zimova, Marketa; Hackländer, Klaus; Good, Jeffrey M.; Melo-Ferreira, José; Alves, Paulo Célio; Mills, L. Scott (August 2018). "Function and underlying mechanisms of seasonal colour moulting in mammals and birds: what keeps them changing in a warming world?". Biological Reviews. 93 (3): 1478–1498. doi:10.1111/brv.12405. hdl: 10216/118423 . ISSN   1464-7931. PMID   29504224.
  26. ↑ Foster R, Williams R (5 December 2009). "Extra-retinal photo receptors" (Interview). Science Show. ABC Radio National. Retrieved 2010-05-28. ...we have the evolutionary baggage of showing seasonality but we're not entirely sure what the mechanism is.
  27. 1 2 Martinez-Bakker, Micaela; Bakker, Kevin M.; King, Aaron A.; Rohani, Pejman (2014-05-22). "Human birth seasonality: latitudinal gradient and interplay with childhood disease dynamics". Proceedings of the Royal Society B: Biological Sciences. 281 (1783): 20132438. doi:10.1098/rspb.2013.2438. ISSN   0962-8452. PMC   3996592 . PMID   24695423.
  28. ↑ Wehr, Thomas A. (August 2001). "Photoperiodism in Humans and Other Primates: Evidence and Implications" . Journal of Biological Rhythms. 16 (4): 348–364. doi:10.1177/074873001129002060. ISSN   0748-7304. PMID   11506380. S2CID   25886221.
  29. ↑ Tan Y, Merrow M, Roenneberg T. Photoperiodism in Neurospora crassa. J Biol Rhythms. 2004 Apr;19(2):135-43. https://doi.org/10.1177/0748730404263015. PMID 15038853.
  30. ↑ Suzuki, L., Johnson, C. Photoperiodic control of germination in the unicell Chlamydomonas. Naturwissenschaften 89, 214–220 (2002). https://doi.org/10.1007/s00114-002-0302-6
  31. ↑ Ivonne Balzer, Rüdiger Hardeland ,Photoperiodism and Effects of Indoleamines in a Unicellular Alga, Gonyaulax polyedra.Science253,795-797(1991).https://doi.org/10.1126/science.1876838

Further reading

This page is based on this Wikipedia article
Text is available under the CC BY-SA 4.0 license; additional terms may apply.
Images, videos and audio are available under their respective licenses.