Introduction This is a supplement to the text showing tables. Light Need of light
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Temperature Blue- green algae formed akinetes in cultures at water temperatures of 10 to 37˚C depending upon the species (Table 5). Most of the green algae investigated reproduced in cultures optimally at 20- 25˚C, but Scenedesmus obliquus and Ulva fenestrata formed gametes at 15˚C and Urospora sp. at 4˚C (Table 5). Different diatoms showed sexuality and resting spore formation at 2- 30˚C. Temperatures most favorable for reproduction of red algae assessed were 10- 20˚C, but subarctic Clathromorphum formed conceptacles at 2- 3˚C. Reproduction in brown algae occurred at somewhat lower temperatures than in red algae assessed (Table 5). In a brown alga, different life cycle stages may occur in different seasons since they have different temperature optima. In kelp members (Halosiphon=Chorda, Macrocystis), gametogenesis occurred at somewhat lower temperatures than zoosporogenesis. Dinoflagellate Alexandrium tamarense (= Gonyaulax tamarensis) formed sexual stages at 10- 12˚C and Gymnodinium pseudopalustre formed gametes at 15˚C (Table 5). Chrysophyceae members formed statospores at temperatures less than 20˚C and a Raphidophyceae member Gonyostomum formed resting cysts at temperatures less than 10˚C (Table 5). Table 5 Optimum temperature (˚C) to induce reproduction in different algae Alga Structure/ Optimum Reference process induced temperature (˚C) Cyanophyceae Anabaena crassa, Akinete 10 and 15 Li et al. 1997 A. flos-aquae, A. mucosa, A. spiroides, A. ucrainica Anabaena doliolum Akinete 32 ± 2 Pandey and (also growth) Kashyap 1987 Anabaena torulosa Akinete 37 > 32 > 29 Fernandes and Thomas 1982 Cylindrospermopsis Akinete 15- 25 Moore et al. 2003, raciborskii 2005 Nodularia spumigena Akinete 32 Pandey and Talpasayi 1980; Pandey 1989
Kaushik 2002 Chlorophyceae Anadyomene stellata, Swarmer 23- 25 Jónsson 1962; A. wrightii Enomoto and Hirose 1970 Chlamydomonas Zoospore 21 Mergenhagen 1980 reinhardtii (wild type strain) Chlamydomonas Zygospore 26 Trainor 1958 chlamydogama Chlorella sp. Cell division 27- 33 Novak and Brune 1985
Cladophora glomerata Zoosporogenesis 15- 20 McNaught 1964; Mason 1965; Bellis and McLarty 1967; Jansson 1974; Hoffman and Graham 1984 Akinete 0- 27 Mason 1965 (Year round) Closterium acerosum Conjugation 18- 22 Vidyavati and Nizam 1973 Coleochaete scutata Zoospore 20- 25 Graham et al. 1984, 1986
Enteromorpha Reproduction < 30 Mairh et al. 1986 flexuosa Enteromorpha Swarmer 20- 25 Dan et al. 2002; prolifera release/ asexual Fu et al. 2008 reproduction Gayralia spp. Zoospore 22 Pellizzari induction, (at 20 psu et al. 2008 release salinity)
mother cell and Machlis 1962 Pithophora oedogonia Akinete 20- 25 Agrawal and Sarma 1983; Agrawal and Singh 2000
formation (maximum O’Kelley 1966 at 25˚C)
formation 1922; Maher 1946, 1947
liberation Scenedesmus Gametogenesis 15 Trainor and Burg obliquus (to tolerate 1965 b; Cain and > 28˚C as zygotes) Trainor 1976; Trainor 1980, 1996
1982 a
Ulothrix zonata Zoosporogenesis 20 Graham et al. 1985 Ulva fasciata Gametophytes 20 Mohsen et al. 1973 a Zoospore induction 25 Mantri et al. 2011 Zoospore release 26 Subbaramaiah 1970 Ulva fenestrata Sporo- and 15 Kalita and Tytlianov gametogenesis 2003 Ulva mutabilis Meiotic zoospore 21-22 Nordby 1977 Ulva pertusa Zoospore 15- 20 Hiraoka and Enomoto 1998; Han and Choi 2005
(at which it 1985 grew vegetatively)
(in small cells) Cocconeis scutellum Sexuality 10- 14 Mizuno and Okuda 1985
asteromphalus (an increase in light intensity also) Eunotia soleirolii Spore 24 von Stosch and Fecher 1979 Leptocylindrus danicus Resting spore 2- 15 French and (at which it Hargraves 1985 grew vegetatively) Sexuality 10 and 15 French and Hargraves 1985
(strong light, fresh culture)
auxospore Drebes 1964 Resting spore 3- 15 von Stosch and Drebes 1964 Rhodophyceae Acrosymphyton Tetrasporangia 12 Cortel-Breeman purpuriferum and Hoopen 1978 Bangiadulcis atropurpurea Monospore 20 Graham and (=Bangia atropurpurea) Graham 1987 Clathromorphum Conceptacle 2- 3 Adey 1973 circumscriptum Colaconema proskaueri Tetrasporangia 15 West 1971 (=Acrochaetium proskaueri) Eupogodon planus Gametangia 20 Orfanidis et al. 1999 Tetrasporangia 15- 20 Orfanidis et al. 1999 Rhodochorton Tetrasporangia 10 Dring and West purpureum 1983 Phaeophyceae Desmarestia viridis Sex organs 3- 5 Kornmann 1962 Dictyota kunthii Tetrasporangia 20 Hoffmann and (=Glossophora kunthii) Malbrán 1989 Halosiphon tomentosus Gametogenesis 1- 8 Maier 1984 (=Chorda tomentosa) Macrocystis spp. Zoospore release 15 Buschmann et al. 2004
2004
(=Gonyaulax excavata) and Wall 1978 Alexandrium tamarense Sexual stages minimum Anderson et al. 1983 (=Gonyaulax tamarensis) 10- 12 Hypnozygote 22 Anderson 1980 Cyst 21 Anderson et al. 1984 Gymnodinium Gametes 15 von Stosch 1973 pseudopalustre Gyrodinium uncatenum Cyst 23- 27 Anderson et al. 1985
Chrysophyceae Dinobryon cylindricum Statospore < 20 Sandgren 1986 (with 2 nuclei) Dinobryon divergens Statospore 12- 17 Ruttner 1930; Sheath et al. 1975 Synura petersenii Statospore < 20 Sandgren and Flanagin 1986 Raphidophyceae Gonyostomum semen Resting cyst < 10 Cronberg 2005 Nutrients Nutrient depletion Induction of reproduction in many algae by nutrient limitation appears to be the result of reduction in cell division and cessation of growth. Culture media free or depleted of nitrogen, phosphorus or both, or of silicon, iron, sulfate or calcium induced akinete formation, sexuality or encystment (to tolerate nutrient shortage) in some algae (Table 6). An increase in cell density led to nutrient depletion and which was the most likely cause for cyst formation in dinoflagellates. Chlamydomonas reinhardtii formed gametes (to form zygotes) in response to nitrogen depletion (Table 6) but gametes can dedifferentiate to vegetative state by any nitrogen compounds which cells can use for growth. Silicon depletion induced resting spore formation in Eunotia soleirolli (Table 6). Nitrogen- fixing blue- green algae required two orders of magnitude more iron (because iron is a component of nitrogenase enzyme complex) than non- diazotrophic organisms (Raven 1988) and iron limitation induced akinete formation in Anabaena cylindrica (Table 6). Table 6 Nutrients deficiency induced initiation of reproduction in some algae Alga or flora Structure/ Inducing factor Reference process induced
nitrate
Anabaena doliolum Akinete Starvation of Singh and nitrate, nitrite, Srivastava 1968; or ammonium Tyagi 1974; (an increase in Rao et al. 1987; C/ N ratio is linked Pandey and with synthesis of Kashyap 1989 additional wall layers)
Thomas 1982 Calothrix sp. strain Hormogonium Absence of Herdman and combined Rippka 1988; nitrogen Damerval et al. 1991
Cylindrospermum sp. Akinete Nitrogen, Glade 1914 Nutrient depletion Gloeotrichia echinulata Akinete Absence of Wyman and Fay combined 1986 nitrogen
Kumar 1983 Chlorophyceae Chlamydomonas Sexuality Nitrogen depletion Trainor 1958 chlamydogama Chlamydomonas Gametogenesis Nitrogen, nutrient Bernstein and eugametos deficiency; sodium Jahn 1955; Lorch starvation 1972; Lorch and Karlander 1973; Tomson et al. 1985
Nečas 1981, 1982 a, b; Nečas and Tetik 1985; Sulek 1997
reproduction, cell division Winkle-Swift mating et al. 1998 competence Chlamydomonas Gametogenesis Depletion of nitrate, Sager and Granick reinhardtii ammonium, urea, 1954; Kates and and glutamine Jones 1964; Martin and Goodenough 1975; Wiese 1984; Treier et al. 1989; Weissig and Beck 1991, Matsuda et al. 1992; Goodenough et al. 2007
sp. 24 sexuality withdrawal of Kates and Jones nitrogen 1964 Chlorococcum Gametogenesis, Low levels of O’Kelley 1983, echinozygotum Zygospore nitrate, ammonia, 1984 glutamine or urea Closterium moniliferum Conjugation KNO3 < 1.3 mM Dubois-Tylski 1977 Closterium Pairing of Nitrogen Ichimura 1971; peracerosum- conjugants, deficiency Kato et al. 1981; Strigosum zygote Akatsuka et al. littorale formation 2003 Coelastrum sp., Gametogenesis Nitrogen Trainor and Burg C. microporum deficiency 1965 a; Trainor 1996
brebissonii conjugation omission Biebel and Chamberlain 1970 Dunaliella sp. Sexual Dilution with Lerche 1937 reproduction two parts of distilled water
depletion Haematococcus Cyst Nitrogen Kakizono et al. pluvialis deficiency 1992 Mesotaenium Gametogenesis, Nitrate Tiftickjian and kramstai pairing depletion Rayburn 1986 Micrasterias Zygote Nitrogen Imaizumi and thomasiana depletion Doida 1990 Mougeotia sp. Conjugation N- depletion, Stabenau and (high light Säftel 1989 intensity, aeration) Netrium digitus Conjugation Nitrogen Biebel 1964, omission 1973 Oedogonium Sexuality Nitrogen Hoffman 1960 borysienum limitation Oedogonium Sexuality Nitrogen Gussewa 1931 capillare limitation Oedogonium Sexual Low nitrate, Hill and Machlis cardiacum stages mineral- deficient 1970; Coss and medium Pickett- Heaps 1973; Hill 1980
Chu- 10 medium Pandorina morum Conjugation Lowering or Coleman 1958 omission of nitrogen
strains 101- 104 zygote deficiency Rayburn 1974; (sulfate Rayburn and deficiency) Starr 1974 Pithophora Akinete Nitrogen Ernst 1908; oedogonia deficiency John and in Bold’s Anderson 1976; basal medium O’Neal et al 1985
deficiency 1969 Rhizoclonium Biflagellate Nitrogen Nienhuis 1974 riparium spores deficiency Scenedesmus Gametogenesis Nitrogen Trainor 1963, 1980; obliquus deficiency Trainor and Burg (at 15˚C) 1965 a; Cain and Trainor 1976
zygote depletion Grote 1977; formation (high C/ N Yamashita and ratio) Sasaki 1979; Simons et al. 1984
species concentrations et al. 1995 Xanthophyceae Ophiocytium mains Zoospores Nitrate- free Pecora and medium Rhodes 1973 Bacillariophyceae Chaetoceros Resting spore Nitrogen French and diadema, formation deficiency Hargraves 1980, C. didymus, 1985; Hollibaugh C.sociale, et al. 1981; C. teres Itakura et al. 1993
confervacea formation limitation Eunotia soleirolii Resting spore Nitrogen von Stosch and formation deficiency Fecher 1979 (phosphorus, silicon, iron deficiency)
Hargraves 1980, 1985
(iron depletion) 2008 (at 10˚C)
(=Rhodochorton floridulum) Dinophyceae Alexandrium Sexuqlity, Nitrogen Turpin et al. 1978; tamarense encystment (or phosphorus) Anderson et al. (=Gonyaulax limitation, low 1984; Anderson tamarensis) nutrient and Lindquist concentration 1985 Ceratium furcoides Encystment Nitrogen Hickel 1988 (or phosphorus) starvation
cyst deficiency Glenodinium Sexual Nitrogen Diwald 1938 lubiensiforme reproduction deficiency Gonyaulax Sexuality Nitrogen- Walker and monilata deprived medium Steidinger 1979 Gymnodinium Sexuality Nitrogen von Stosch 1973 pseudopalustre omission Peridinium cinctum, Gametes Nitrogen Pfiester 1975, 1976, P. gatunense, formation, deficient 1977; Pfiester and P. volzii, hypnozygote medium Skvarla 1979; P. willei formation, Chapman and encystment Pfiester 1995; Grigorszky et al. 2006
Scrippsiella Encystment Nitrogen Watanabe et al. lachrymosa, (or phosphorus) 1982; Olli and S. trochoidea limitation Anderson 2002 Woloszynskia Gametogenesis, Nitrogen von Stosch 1973 apiculata sexuality, (or phosphorus) cyst limitation, lack of major nutrients
Pandey and Kashyap 1987
(addition of Sarma et al. C and N) 2000, 2004
Reddy 1976; Lang 1980
(P is needed Meeks et al. 2002; for ATP Argueta and synthesis) Summers 2005 Nostoc sp. Akinete Phosphorus and Innok et al. 2009 VICCR1- 1 (iron) omission Chlorophyceae Stigeoclonium sp. Akinete Phosphorus Martin and strain limitation Whitton 1987 Bacillariophyceae Aulacoseira Sporulation Decline in Jewson et al. 2008 skvortzowii phosphate (< 15- 20 µg/L) Dinophyceae Alexandrium Encystment Phosphorus Figueroa et al. 2005 catenella deficiency Alexandrium Encystment Low P/ N ratio Figueroa et al. 2011 minutum Gloeodinium Gametogenesis Phosphorus Kelley and montanum limitation Pfiester 1990 Gymnodinium Gametogenesis Phosphorus Blackburn et al. catenatum limitation 1989 C. Depletion of both nitrogen and phosphorus initiated reproduction Xanthophyceae Vaucheria Sexuality N and P limitation Aberg and Fries dichotoma 1976 Dinophyceae Peridinium Encystment N and P limitation Sako et al. 1984 cunningtonii Gymnodinium Encystment N and P limitation Figueroa et al. 2006 catenatum Gyrodinium Encystment N and P limitation Anderson et al. 1985 uncatenum D. Depletion of nutrients other than N and P initiated reproduction Cyanophyceae Anabaena Akinete Depletion of Sinclair and cylindrica iron Whitton 1977 Aphanizomenon Akinete Depletion of Sukenik et al. ovalisporum potassium 2009 Westiellopsis Akinete Depletion of Agrawal and prolifica calcium, boron, Sharma 1994 micronutrients Chlorophyceae Halimeda sp. Sporulation Iron deficiency Tullock 1997 Bacillariophyceae Skeletonema Auxospore Silicon depletion Davis et al. 1973 costatum Thalassiosira Resting spore Iron depletion Sugie and Kuma nordenskioeldii (at 5˚C) 2008 Dinophyceae Alexandrium Gametes Iron limitation Doucette et al. tamarense 1989 Requirement of inorganic substances and nutrients Inorganic carbon compounds like carbon dioxide, bicarbonate or carbonate are usual source of carbon to algae and favored reproduction in many algae (Table 7). When carbon dioxide concentration is increased in the air over the culture media, a number of freshwater green algae becomes reproductive, e.g. Oedogonium spp. formed zoospores; Cosmarium, Closterium, Micrasterias and Staurestrum performed conjugation; Stigeoclonium turned reproductive; and Volvox formed gonidia (Table 7). This is believed to be a nutritive (and not pH) effect. Bicarbonate or carbonate has also been reported to induce akinete formation in Anabaena torulosa and Nodularia spumigena (Table 7). Of course, given the fundamental importance of the relative amounts of C, N, and P (i. e. the Redfield ratio), enrichment of carbon can potentially be perceived as a limitation of nitrogen and phosphorus. Presence of sufficient nitrate, phosphate or both induced reproduction in many algae (Table 7) and this may be because of sufficient algal growth requirement. Calcium, magnesium, sulfate and iron are needed for algal reproduction (Table 7) because of their specific role. Formation of akinetes in cultures of Anabaena cylindrica containing low concentrations of inorganic phosphate exhibited calcium2+ dependency (Wolk 1965). Sodium was needed for sexuality in diatoms Cyclotella, Coscinodiscus and Licmophora (Table 7). Although importance of boron and iodine in nature remains to be demonstrated, boron in limited levels was required for reproduction in Dictyota dichotoma and embryo development in Fucus edentatus. Iodine was implicated in growth and reproduction of Ectocarpus siliculosus and Petalonia fascia (Table 7).
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