Biodiversity Among Haptophyte Algae

Home , Chrysochromulina, Coccolithus, Gephyrocapsa, Haptophyte, Isochrysidales, Pleurochrysis carterae

Biodiversity and Conservation 6, 131±152 (1997)

R. W. JORDAN* Department of Earth and Environmental Sciences, Faculty of Science, Yamagata University, Yamagata, 990 Japan

A. H. L. CHAMBERLAIN Microbial Physiology and Ecology Research Group, School of Biological Sciences, University of Surrey, Guildford, Surrey GU2 5XH, UK

Received 31 October 1995; revised and accepted 24 January 1996

The division Haptophyta is represented only by about 300 extant species showing wide diversity in morphology, biochemistry and ecology. They have a world-wide distribution and are numerically important in phytoplankton populations in nearly all marine environments. Evidence from the geological record shows that they have been the major constituent of calcareous deposits since the Late Triassic and, as they have evolved quickly through time, their coccoliths have always shown wide morphological diversity. In today's oceans they occasionally produce extensive blooms, visible by satellite imagery, which have ecological impact. As a consequence of these blooms the haptophyte algae are now receiving greater attention, as their role in the global sulphur and carbon cycles may in¯uence the world's climate, and their potential as nuisance bloom algae have implications for commercial ®shing and the marine ecosystem. As it is likely that these organisms have always produced such blooms, these eects may have been in operation for the last 200 million years. Keywords: haptophyte; ultrastructure; morphology; bloom products; distribution; evolution.

Introduction The freshwater representatives of the Haptophyta are few, but marine species constitute one of the most successful groups of living organisms with a well-documented fossil record (Tappan, 1980). Their ubiquitous distribution and ability to form large blooms has al- lowed them to be globally important, both as primary producers and, after death, as a component of sedimentary rock. The coccolithophorids are probably the most important of the haptophytes, as they produce calci®ed scales (coccoliths), which, on the cell's death, are liberated and transported to the sea ¯oor. These calcareous deposits are the major constituent of chalk and have their greatest period, both in abundance and species diversity, in the Late Cretaceous (65±95 Ma) (Bown et al., 1992; Young et al., 1994). Due to their rapid evolution, abundance, and the ease with which they can be observed, they have become one of the most widely used microfossil groups for stratigraphy. Thus, they are common tools for age determinations in oil exploration. Furthermore, as many species display biogeographic zonation and live in restricted environments, the distribution of their coccoliths in the sediments may also be useful in palaeoclimatic reconstructions. Hence, coccoliths are useful fossils in both stratigraphic and palaeoceanographic studies. In more recent times the extant coccolithophorids have gained attention mainly through their ability to form mesoscale blooms, whose re¯ectance via birefringent loose coccoliths can be observed with satellite imagery (Holligan et al., 1983; Balch et al., 1991).

*To whom correspondence should be addressed. 0960-3115 Ó 1997 Chapman & Hall 132 Jordan and Chamberlain The processes of photosynthesis, calci®cation and respiration occurring in such large blooms as these have important implications for the global carbon cycle. In addition, blooms of Phaeocystis and Emiliania are involved in dimethyl sulphide (DMS) production and so their role in the global sulphur cycle is also important (Malin et al., 1992, 1994). Thus, haptophytes make a large contribution to the world's climate (Westbroek et al., 1993). Other haptophytes can also produce large blooms, some of which are known to cause economic problems either through toxin, mucilage or foam production (Underdal et al., 1989; Davidson and Marchant, 1992; Moestrup, 1994). In terms of diversity, there are now about 300 known extant species of haptophyte algae (Jordan and Green, 1994; cf Andersen, 1992; cf Vickerman, 1992), although undoubtedly many remain undescribed. While this number is relatively small, compared with diatoms for instance, diversity in haptophyte scale morphology is astounding. However, much of what is currently known about these organisms comes from observations on cultured material. In this respect the unmineralized taxa have proved easier to maintain than the coccolithophorids, and freshwater and coastal species better than open ocean taxa±see lists provided by the Culture Centre of Algae and Protozoa (Thompson et al., 1988), the Provasoli-Guillard National Centre for Culture of Marine Phytoplankton (Andersen, 1991), and the University of Texas (Starr and Zeikus, 1993). At present there are probably less than 10 species of coccolithophorids successfully maintained in culture throughout the world. However, Emiliania huxleyi grows easily in a variety of media under an enormous range of culture conditions, re¯ecting its very wide geographic range and, for this reason, it has become one of the most useful experimental marine organisms used today. As a consequence of this, more is known about this alga than probably any other marine species (for recent reviews see Westbroek et al., 1993; Heimdal et al., 1994). In the following sections haptophyte diversity will be discussed in terms of taxonomic concepts, internal and external structures, ecology and distribution in both water and sediments. A glossary of haptophyte terms has been published recently by Jordan et al., (1995).

Taxonomic concepts In general, haptophytes may be identi®ed by a number of key characters (Table 1), and variation in some of these characters forms the basis for their separation at the ordinal level (Table 2). Another set of criteria can be used to separate them into three arti®cial groups relating to: (a) the extant unmineralized haptophytes, (b) the extant coccolithophorids, and (c) fossil coccoliths. In the extant unmineralized haptophytes the main em- phasis is on organic scale morphology, ¯agellar and haptonematal arrangement, and cell shape. For living coccolithophorids organic scale morphology is replaced by coccolith morphology, with importance placed on the combination of coccolith types and their arrangement on the cell (Jordan et al., 1995). The classi®cation of fossil haptophytes is restricted almost entirely to coccolithophorids and, moreover, to isolated coccoliths (coccospheres are generally rare in sediments). This means that most of the conventional methods of identi®cation employed for living haptophytes, as described above, cannot be used for the fossil forms, and their taxonomy is therefore constrained solely by information on the coccolith morphology (Tappan, 1980; Perch-Nielsen, 1985). This approach leads to an overestimation of the number of species present and to a more diverse classi®cation system at all levels. Haptophyte algae 133 Table 1. Main characteristics of the division Haptophyta

Chloroplasts with no girdle lamella Flagella, usually 2, equal or subequal, sometimes unequal; no tubular hairs (Pavlovophycidae have ®brous hairs and knobscales on longer ¯agellum±possibly modi®ed hairs rather than scales±see Cavalier-Smith, 1994) Eyespots found only in Pavlovophycidae, usually associated with invagination of plasmalemma; not associated with ¯agellar swelling (except in Diacronema vlkianum) Haptonema (or trace) present Unmineralized body scales basically a ®brillar 2-layered plate; many species with calci®ed scales (coccoliths). Silici®cation rare

Reproduced in part from Green and Jordan (1994)

Table 2. Main characteristics of the orders in the Haptophyta

Subclass: Prymnesiophycidae Subclass: Pavlovophycidae

Isochrysidales Prymnesiales Coccosphaerales Pavlovales or Coccolithophorales

Unicellular, motile Unicellular, usually Unicellular, motile Unicellular or forming or non-motile, motile, sometimes or non-motile palmelloid masses sometimes non-motile. Cells ®lamentous free, occasionally colonial Flagella 2, equal or Flagella 2, equal or Flagella 2, equal or Flagella unequal, shorter subequal. One subequal. One subequal may be reduced, longer ¯agellum sometimes ¯agellum sometimes with investment of auto¯uorescent auto¯uorescent ®brous hairs, and knob-scales. Always heterodynamic Haptonema reduced Haptonema usually Haptonema Haptonema short, or absent conspicuous, often conspicuous or non-coiling well-developed and coiling reduced Body-scales small Body-scales various, Calci®ed scales Body-scales absent unmineralized one or more layers, (coccoliths) present (occasionally absent) and often several at some stage types of scale per cell during life cycle; non-mineralized scales also present Flagellar root system based on 3±4 microtubular roots Flagellar root system unique to group, based on two microtubular roots Mitotic spindle axis straight; no ®brous root MTOC Mitotic spindle axis V-shaped; ®brous root MTOC

From Green and Jordan (1994). Jordan and Green (1994) assign taxa in the Prymnesiophycidae to only one order; the Prymnesiales. Some authors include the coccolithophorid genera, Emiliania, Gephyrocapsa and Reticulofenestra, in the Isochrysidales±thus in the above table, coccoliths may also be present in this order 134 Jordan and Chamberlain Over the last few decades a number of discoveries have changed our approach to the classi®cation scheme. One of the main advances has been the determination of a number of haptophyte life cycles by cultural studies (Billard, 1994). This has produced some interesting results which have radically changed taxonomic concepts. For instance, several species of coccolithophorid (e.g. Coccolithus pelagicus) exhibit an alternating heterococcolithophorid±holococcolithophorid life cycle (Parke and Adams, 1960), whose in- dividual phases were once classi®ed in separate families. In the case of C. pelagicus the heterococcolith-bearing phase was found to be diploid and the holococcolith-bearing phase haploid (Rayns, 1962). The dierent phases of these life cycles have been shown now to possess dierent organic scale morphology (Billard, 1994). Sexual cycles also exist in Phaeocystis spp. and E. huxleyi, where motile and non-motile phases are haploid and diploid respectively (Course et al., 1994; Vaulot et al., 1994; Green et al., 1996), and in Pleurochrysis pseudoroscoensis, in which both phases are motile (Gayral and Fresnel, 1983). Molecular biology has provided information on the evolutionary relationship of se- lected haptophytes to other protist groups (Fujiwara et al., 1993, 1994; Bhattacharya and Medlin, 1995), and also more speci®cally about variation within a single genus, for instance, Phaeocystis (Medlin et al., 1994a, b; Vaulot et al., 1994). However, in clones of Emiliania huxleyi, intraspeci®c variation could not be demonstrated with the sequences examined so far (Medlin et al., 1994a). As morphometric, physiological, biochemical and immunological evidence has demonstrated the separation of four distinct varieties or morphotypes in this species, other sequences must be looked at in the future. Thus, it may be some time before the genetic approach can be used (in conjunction with coccolith/scale morphology) as a taxonomic tool for identi®cation within the group. Other discoveries have been more con®ned taxonomically but have clari®ed some of our classi®cation theories. From studies of lipid biomarkers some taxonomic inferences can be made (Conte et al., 1994); for example, it has been shown that long-chain (C37±39) un- saturated alkenones, with 2, 3 or 4 double bonds, are produced by only four of the genera (Chrysotila, Emiliania, Gephyrocapsa and Isochrysis ) tested so far (Marlowe et al., 1984; Conte et al., 1995). In some classi®cation schemes all these genera have been placed in the same order, the Isochrysidales (e.g. Parke and Green, 1976; Tappan, 1980). The removal of Emiliania and Gephyrocapsa from the Coccosphaerales on morphological and biochemical grounds has been supported further by the recent demonstration that genetically these genera appear more similar to Chrysochromulina hirta than to other coccolithophorids (Fujiwara et al., 1994). However, the value of these compounds is not restriced to taxonomy. It is now known that they are also important in oceanography and paleoceanography as sea-surface temperature (SST) indicators. A ratio of the abundance of K each double bond type was used to create an index known as U37. In culture experiments K these abundances were found to vary with the temperature of the medium. The U37 index has now been calibrated to temperature and compared with that derived from measure- ments in the ®eld (Conte and Eglinton, 1993). As these compounds are numerous in marine sediments and are resistant to degradation, the index can be used as a pa- laeothermometer for climate reconstruction (e.g. Jordan et al., 1996). In this respect they have also been used to determine the evolution of the Isochrysidales (Marlowe et al., 1990). Haptophyte algae 135 Intracellular ultrastructure Haptophytes have always been classi®ed by their external structures (¯agellar type, haptonema, scales and coccoliths) and their pigmentation (chlorophylls a and c). However, as detailed studies of their ultrastructure have shown, the group contains a diverse array of internal organelles (Pienaar, 1994). For instance, eyespots are only found in the Pavlovales and are usually associated with an invagination of the plasmalemma but not with a ¯agellar swelling (except in Diacronema±Green, 1980). Naturally, only the coccolithophorids possess specialized golgi-derived vesicles which are involved in coccolith formation, although interspeci®c dierences in these vesicles and the presence or absence of associated vesicles (e.g. coccolithosomes) have been noted (e.g. Westbroek et al., 1986). Several workers have recognized crystalline bodies (called the X-body) within the motile phase of Emiliania huxleyi, and although they were once thought to be associated with the calci®cation process, they are now known to be guanine crystals, and are identical to those found in some dino¯agellates and thraustochytrids (Chamberlain and Moss, 1988). The internal portion of the ¯agellar apparatus and the haptonema has also been studied in a number of species, with all root systems consisting of microtubular and ®brous components. However, there is considerable variability in the arrangement of these roots and in the levels of complexity shown in their structure (Green and Hori, 1994). In fact, several haptophytes (e.g. Umbilicosphaera sibogae var. foliosa) which lack external ¯agella and/or a haptonema have been shown to possess residual root systems and a haptonematal trace. In this way the inclusion of such species into the Haptophyta has been corroborated despite the absence of some of the key external identi®cation characters. All haptophyte chloroplasts lack girdle lamellae and most contain chlorophylls a and c1/c2, b, b-carotene, diadinoxanthin and diatoxanthin. However, there are interspeci®c and intraspeci®c dierences in the fucoxanthin derivatives and in the presence/absence of chlorophyll c3. Recently, four main subgroups have been recognised: type 1 has fucoxanthin, type 2 has fucoxanthin and chlorophyll c3, type 3 has 19¢-hexanoyloxyfucoxanthin and chlorophyll c3, and type 4 has 19¢-butanoyloxyfucoxanthin, chlorophyll c3 and variable traces of fucoxanthin and 19¢-hexanoyloxyfucoxanthin (Jerey and Wright, 1994). The haptophyte nucleus has also provided an example of diversity within the group. For instance, most haptophytes during nuclear division have a straight spindle axis, lack any type of obvious pole structure, and form a new nuclear envelope on the poleward face of the mass of daughter chromatin. However, members of the Pavlovales have a V-shaped spindle axis, a well-de®ned ®brous pole structure, and the nuclear envelope persists through much of the nuclear division (Hori and Green, 1994). In some species of Prymnesium (P. parvum and P.patelliferum) siliceous cysts are occasionally produced. The cyst wall is composed of several layers of small plate-scales, each associated on their distal face with a ¯occulent electron-dense material rich in silicon (Pienaar, 1980; Green, 1986).

External structure Haptophytes are characterized by the possession of two smooth ¯agella and a specialized organelle, the haptonema. However, most taxa are separated taxonomically by the scales covering the cell surface. One exception to this is the order Pavlovales, whose members secrete only a mucilaginous cover outside the cell, although knob scales and ®brous hairs 136 Jordan and Chamberlain are present on the long (anterior) ¯agellum (for a review see Green, 1980). In other haptophytes, unmineralized organic scales composed mainly of cellulose are produced by the golgi body and transported via vesicles to the cell membrane (Brown et al., 1970). They are then exocytosed and rhythmically arranged around the cell (Pienaar, 1976). In P. carterae, several scales and coccoliths are produced at the same time in dierent vesicles, and as this process is relatively rapid, the entire cell surface can be covered in about 8 hours (van der Wal et al., 1987). In some haptophytes a second type of scale, a small elliptical scale, may be associated with the ¯agellar area or more speci®cally with a reduced haptonema. The possible functions of scales and coccoliths have been reviewed by Manton (1986) and Young (1994). Most coccolithophorids produce organic scales, however, overlying these may be some additional scales (base-plate scales) bearing organized calcite crystals. These mineralized scales, coccoliths, may form intricate structures involving several layers of crystals. Generally, coccoliths bearing structures of rhombohedric crystals are called holococcoliths (Fig. 3), while those whose crystals have undergone growth are called heterococcoliths (Fig. 4). These latter coccoliths are usually produced in golgi-derived vesicles, whereas it has been suggested that holococcoliths may be produced in a gap between the cell membrane and an external organic skin (Manton and Leedale, 1963; Klaveness, 1973; Rowson et al., 1986). Furthermore, in the case of the motile phase of Coccolithus pelagicus (ex Crystallolithus) there may be more than one scale±coccolith±skin complex around the cell (Green, 1986). In some species (e.g. Emiliania huxleyi) the cell can only produce one coccolith (i.e. only one coccolith vesicle) at a time, while in others (e.g. Pleurochrysis carterae) several coccolith vesicles, each in a dierent stage of maturation, may be seen simultaneously (Westbroek et al., 1986). This dierence in coccolith productivity may be related to the number of coccoliths within a single layer on the cell; for instance, E. huxleyi has about 15 and P. carterae about 200 (Fig. 1; Westbroek et al., 1986). Most coccolithophorids can produce only one layer as their coccoliths merely abut on the cell surface, and so, on production of further coccoliths, the old layer is discarded. However, in the case of E. huxleyi in culture as many as three to ®ve layers have been seen (Fig. 2; Braarud, 1963; Balch et al., 1993), the coccoliths in the older layers remaining attached to each other by interlocking shields. Presumably, only when the circumference is larger than their interlocking capability are the coccoliths ®nally released into the surrounding medium. One haptophyte, Chrysotila lamellosa, can produce massive extracellular calcite structures in addition to organic scales. These structures are thought to be formed by precipitation of CaCO3 from the surrounding seawater, onto the multi-layered mucilage sheath around the cell. This process, unlike coccolith formation, does not appear to involve the secretion of a pre-formed structure (Green and Course, 1983; Green, 1986).

Bloom products Haptophytes, like many organisms, can produce a number of extracellular products, many of which may be harmful to other species or have an eect on the environment (Moestrup, 1994). These compounds are largely associated with the ®nal stages of a bloom when the cells are stressed or dying. For instance, it is well known that, at the end of a Phaeocystis bloom, large quantities of dissolved organic carbon (DOC) are released into the surrounding waters leading directly to the spectacular formation of foam that accumulates on the beaches, smothering nearshore animals. Phaeocystis is also a colony producer, and so Haptophyte algae 137

Figures 1±4. Photomicrographs of some coccolithophorids. Figure 1. Pleurochrysis carterae in culture. Note the two ¯agella (in upper specimen only), two chloroplasts, and the mass of ring-like coccoliths. LM. Figure 2. E. huxleyi in culture with several layers of coccoliths around each cell. LM. Figure 3. Holococcoliths of Coccolithus pelagicus (Crystallolithus phase). Note the elliptical base plate scales and the associated rhombohedral microcrystals (in black). TEM. Figure 4. Hetero- coccoliths of Emiliania huxleyi with shields of T-shaped elements. TEM (reversed image). Scale bars: Figs 1 and 2 = 20 lm; Figs 3 and 4 = 1 lm. large blooms of this alga can interfere with commercial ®shing, by clogging the nets with mucilage. These blooms appear to deter ®sh and their cells are of little nutritional value to zooplankton herbivores (Davidson and Marchant, 1992). At the end of a Phaeocystis bloom when there is an increase in dying cells, the release of dimethylsulphoniopropionate (DMSP) is increased, either naturally or by cell lysis, into the surrounding water, where it hydrolyses into two compounds, dimethyl sulphide (DMS) and acrylic acid. It seems likely that the majority of DMS derives from the extracellular pool of DMSP, although some is known to be produced intracellularly. A proportion of 138 Jordan and Chamberlain this DMS is then subsequently released into the atmosphere, where it reacts to form a sulphate and methane sulphonate aerosol. It is postulated that these aerosol particles then act as cloud-condensation nuclei (Charlson et al., 1987; Malin et al., 1992). Hence, marine biogenic sulphur contributes directly to cloud formation and, by increasing the planet's albedo, partly controls the amount of solar radiation reaching the Earth's surface (Bates et al., 1987). In the atmosphere, DMS may also be oxidized to sulphur dioxide and then to sulphuric acid, forming acid rain on precipitation (Charlson and Rodhe, 1982). Thus, haptophytes may profoundly aect climate through their release of DMSP and its sub- sequent conversion to DMS (Fig. 5). Acrylic acid, formed in the cleavage of DMSP, is also released into the surrounding waters where it acts as an antibacterial agent (Davidson and Marchant, 1992) and may even suppress grazing by copepod herbivores (Huntley et al., 1983). The coccolithophorids, E. huxleyi and Pleurochrysis carterae, are also known to release DMS and acrylic acid (Vairavamurthy et al., 1985; Keller, 1989), and some authors have even suggested that they are the main producers of DMS in ocean waters (Turner et al., 1988; Aiken et al., 1992). Haptophyte blooms have also been associated with the mass mortality of ®sh and other marine organisms through the release of toxic compounds. These toxins, again, are produced mainly at the end of the bloom when cells may be subjected to nutrient (e.g., phosphorus) starvation. There are two principal genera involved in toxin production; Prymnesium and Chrysochromulina (Moestrup, 1994). The `toxin' produced by C. polylepis appears to be a group of compounds rather than a single entity and its eect on the surrounding marine life varies with time. In the initial stages it acts as a grazing repellent, forcing grazers to select other algae, while later it is so concentrated that it aects all organisms, in the end probably causing autotoxicity in C. polylepis (Underdal et al., 1989; Maestrini and GraneÂli, 1991). One species, Chrysochromulina breviturrita, blooms in Canadian lakes where it may become a nuisance alga by producing obnoxious odours. These odours, described as `rotten cabbage', `dead animal' or `garbage dump', may be the only report of odour production in the Haptophyta (Nicholls et al., 1982). However, release of these compounds would be more noticeable in a con®ned water body than in the open ocean.

Nutrition Most haptophytes possess chloroplasts and therefore can be assumed to use photosynthesis as the main means of acquiring carbon for cellular use. However, Balaniger balticus, and maybe other polar coccolithophorids, appear to lack a photosynthetic apparatus and so they may be operating as strict heterotrophs (Marchant and Thomsen, 1994). Furthermore, it has been demonstrated already that some species are capable of taking in either dissolved organic carbon or particulate organic material in addition to photosynthesizing, i.e., they are mixotrophic (Green, 1991; Jones et al., 1994). In the latter case, ingestion may involve either phagotrophy by a pseudopodium at the non-¯agellar pole of the cell (Green, 1991), or more spectacularly, by the food-capturing ability of the haptonema and spinose organic scales (Kawachi et al., 1991; Kawachi and Inouye, 1995). In Chrysochromulina hirta the haptonema collects food particles and transfers them to the posterior end of the cell, where they are ingested by phagocytosis into a vacuole (Kawachi et al., 1991). At present, at least 19 species of Chrysochromulina, 2 species of Prymnesium, Haptophyte algae 139

Figure 5. Overview of the major oceanic and atmospheric processes associated with Emiliania huxleyi blooms. Redrawn from Westbroek et al. (1993). 140 Jordan and Chamberlain and Coccolithus pelagicus are known to ingest particulate material by phagotrophy (Jones et al., 1994). However, in one species, Chrysochromulina spinifera, the long spinose organic scales act as capturing devices for passing food particles, which are then collected and transferred by the haptonema to a specialized protruding mouth-like structure, and from there to the food vacuole (Kawachi and Inouye, 1995). As many haptophytes are spinose, it will be interesting to know in the future if further species utilize a similar mode of food capture.

Oceanic distribution Knowledge of the biogeography of haptophytes in the world's oceans is by no means complete, due largely to our scant knowledge on the distribution of the unmineralized taxa (Thomsen et al., 1994). This paucity of information stems from the methods adopted by many scientists during collection, preservation and observation of the water samples. One of the commonest methods is to ®lter the water samples directly on board the research ship, air-dry and store the ®lters, and then later identify and count coccospheres using an SEM, or by LM with an oil-immersion lens. However, this method does not generally preserve the unmineralized taxa, which generally require retention in preservatives prior to their observation under LM or TEM (for further information see the techniques used in Leadbeater, 1972; Thomsen, 1977). Thus, the following subsections deal mainly with the distribution of coccolithophorids.

Latitudinal zonation Like many marine organisms the coccolithophorids can be separated into discrete biogeographic zones (McIntyre and BeÂ, 1967; Okada and Honjo, 1973; see Fig. 6). These zones correlate very strongly with ocean surface currents and thus with general wind patterns. Each current is characterized by a set of chemical and physical parameters, and so many of the species present in each zone are geographically restricted. However, the zonal scheme presented in Fig. 6 is an oversimpli®cation and does not allow for localized water conditions (e.g. coastal and equatorial upwelling, frontal systems, shallow benthic environments, topographic features and isolated warm or cold core rings). Furthermore, certain regions (e.g. the Mediterranean and Indian Ocean) are not as well known, and so zonal schemes are not yet available or corroborated. Nevertheless, generalized coccolithophorid assemblages can be used to de®ne each zone (Table 3), although some species have greater biogeographic ranges than others. At present, coastal assemblages are known only from a limited number of areas (mostly northern European coastlines) and so their distribution data are rather sparse. Only one freshwater coccolithophorid species is currently recognized, although numerous species (considered to be synonyms) have been described over the years.

Vertical distribution The depth range of coccolithophorids is dependent on the water characteristics: for example, the positions of the thermocline, nutricline, and penetration depth of surface ir- radiance. In the subarctic the thermocline is shallow (perhaps 30 m) and so the primary productivity (i.e. the chlorophyll maximum) is located mainly in the top 30 m or so. This depth range changes as one moves towards the lower latitudes, where the waters are warmer and the thermocline and nutricline are deeper. Consequently, the primary pro- atpyealgae Haptophyte

Figure 6. Biogeographic zonation of coccolithophorids. 1 = subarctic; 2 = temperate; 3 = subtropical; 4 = tropical (equatorial); 5 = subantarctic. Redrawn from Winter et al. (1994). 141 142 Jordan and Chamberlain

Table 3. Biogeographic coccolithophorid assemblages

Subarctic Emiliania, Coccolithus, Papposphaeraceae, Algirosphaera robusta, Calciopappus caudatus, Syracosphaera borealis, Balaniger, Calciarcus, Quaternariella, Wigwamma Temperate Emiliania, Gephyrocapsa, Reticulofenestra, Calcidiscus, Coccolithus, Helicosphaera, Syracosphaera, Balaniger, Ericiolus Subtropical Emiliania, Ceratolithus, Cyclolithus, Hayaster, Neosphaera, Oolithotus, Umbilicosphaera, Helicosphaera, Pontosphaeraceae, Rhabdosphaeraceae, Syracosphaeraceae, Holococcolithophorids, Florisphaera, Gladiolithus, Polycrater, Turrilithus, Vexillarius Tropical Emiliania, Gephyrocapsa oceanica, Reticulofenestra sessilis, Calcidiscus, Umbellosphaera, Florisphaera, Gladiolithus, Polycrater Antarctic Papposphaeraceae, Calciarcus, Ericiolus, Quaternariella, Wigwamma

Coastal Braarudosphaera, Cruciplacolithus, Hymenomonas, Ochrosphaera, Pleurochrysis, Jomonlithus Freshwater Hymenomonas roseola

ductivity peak lies deeper (the so-called deep chlorophyll maximum, DCM). In addition, in the subtropical zone the environmental conditions are nearly permanent and so the water strati®cation parameters are stable. For example, the nutricline resides between 100 and 160 m, depending on the geographic location, and its stability allows specialized oligotrophic and eutrophic communities to occur. The location of these communities are referred to as the upper and lower photic zones respectively, with a narrow middle photic zone separating them (Okada and Honjo, 1973; see Fig. 7 and Table 4). However, few coccolithophorid workers have sampled thoroughly below 100 m, so lower photic communities are still poorly described, and there is no information on the depth at which the lower photic zone ends.

Seasonal variation A number of important contributions have been made on haptophyte seasonality and these data are brie¯y summarized below. It is now generally understood that coccolithophorid communities change during the seasons of the year, although these changes are more dramatic in particular seasons, depending on the geographic location. For instance, in the subarctic Atlantic, E. huxleyi dominates the rather sparse community from late summer through to early spring, but is replaced by the motile and non-motile phases of Coccolithus pelagicus during spring and early summer (Okada and McIntyre, 1979). In the temperate North-East Atlantic a similar situation may occur in which Gephyrocapsa muellerae dominates the spring and early summer, while E. huxleyi is more numerous in the other parts of the year (Jordan, unpublished data). In the temperate North-West and North-East Atlantic, near to the subtropical gyre, the decrease in E. huxleyi during the spring/summer months is coincident with an increase in Umbellosphaera tenuis within the top 100 m and Florisphaera profunda between 100 and 200 m (Okada and McIntyre, 1979; Jordan, unpublished data). In the North Atlantic subtropical gyre the summer community (May±July) is dominated by U. tenuis and holococcolithophorids in the top 100 m, and by F. profunda between 100 and 220 m. This community may persist throughout the year, as water and weather conditions are relatively stable and so seasonality is less distinctive. Haptophyte algae 143

Figure 7. Vertical zonation of coccolithophorids from the subtropical zone. Redrawn from Winter et al. (1994).

This assumption is corroborated by the evidence from the underlying subtropical/tropical sediments which shows that F. profunda is the most dominant species in the fossil as- semblage (Mol®no and McIntyre, 1990; Jordan et al., 1992). However, data from the North Paci®c subtropical gyre would tend to disagree with these assumptions. A seasonality similar to that seen in temperate/subtropical waters was reported whereby U. tenuis and F. profunda were numerous only during the spring/summer months when the E. huxleyi dominance had declined. Furthermore, the holococcolithophorids were present for 144 Jordan and Chamberlain Table 4. Depth-related coccolithophorid assemblages in subtropical waters

Upper photic zone Holococcolithophorids, Acanthoica, Anacanthoica, Cyrtosphaera, Discosphaera, Rhabdosphaera, Ceratolithus, Neosphaera, Alisphaera, Coronosphaera, Syracosphaera, Umbellosphaera, Polycrater Middle photic zone Anoplosolenia, Calciosolenia, Alisphaera, Coronosphaera, Michaelsarsia, Ophiaster, many Syracosphaera, Umbellosphaera Lower photic zone Cyclolithus anulus, Oolithotus fragilis, Reticulofenestra sessilis, Algirosphaera quadricornu, Canistrolithus, Syracosphaera anthos, Florisphaera, Gladiolithus, Hayaster, Turrilithus, Vexillarius No depth preference Emiliania, Gephyrocapsa, Helicosphaera

Revised from Winter et al. (1994)

most of the year, although they did increase dramatically during the summer (Reid, 1980). Data from a transect of the Mediterranean Sea during February/March and September/ October show a similar pattern to that above for warm temperate waters (Knapperts- busch, 1993). A study of the Gulf of Elat (North of the Red Sea) showed a water column dominated by E. huxleyi which declined in the summer to be replaced by U. tenuis and holococcolithophorids. However, F. profunda and other lower photic species were totally absent (Winter et al., 1979). Satellite imagery oers another way of studying the seasonal distribution of coccolithophorids, although it is useful only as a non-taxonomic tool and only when there is a sucient quantity of suspended birefringent coccoliths within the surface waters to enable detection (i.e. in bloom conditions). The detection limit of satellites is determined by the water characteristics; for instance, in clear non-productive waters they may `see' through 15±30 m, while in turbid or highly pigmented waters this may be signi®cantly less, and only as little as 1 m in coastal regions (Holligan et al., 1989). However, in recent years this technique has provided important data on the spatial and temporal distribution of coccolithophorid blooms, especially those in the North Atlantic (Holligan et al., 1983; Groom and Holligan, 1987; Ackleson et al., 1988; Balch et al., 1991). All these blooms seem to appear in early summer and persist for several weeks, often turning the surrounding water white or turquoise with discarded coccoliths (Berge, 1962; Ackleson et al., 1988). From one such bloom it was calculated, conservatively, that a single patch occupying 7200 km2 in the top 60 m of the water column was equivalent to 7.2 ´ 104 tonnes of calcite (Holligan et al., 1983). As E. huxleyi is known to live as deep as 220 m (Jordan, unpublished data) and a bloom may persist for several weeks, the total calcite production by a single bloom may be at least an order of magnitude higher than that given above. This is an astounding amount of biogenic calcite, and even if one considers, rather conservatively, that only 1% of this material reaches the sediment without being dissolved, these blooms must make a major contribution to sediment formation. The conditions responsible for the termination of these blooms, however, are still unknown but they are assumed to be nutrient-related, although recent evidence suggests that virus-like particles may be the cause of cell mortality and lysis (Bratbak et al., 1993). Since the devastating toxic bloom of Chrysochromulina polylepis in 1988 along the Norwegian coast of the North Sea, and the Norwegian and Swedish coasts in the Ska- gerrak and Kattegat, unmineralized haptophytes now have a higher pro®le in coastal Haptophyte algae 145 monitoring and, as a consequence, our knowledge of their life cycles, distribution and seasonality will improve. However, one genus, Phaeocystis, has already received a great deal of attention. In high latitudes this genus may dominate phytoplankton populations and reach bloom proportions, and because it produces large amounts of extracellular products (i.e. colonial mucilage, DMS and foam) it may be a nuisance to ®shermen and the environment. In warmer waters it is generally rare but in nutrient enriched conditions (i.e. sewage input) it may reach bloom concentrations. In the North Sea it has been routinely monitored, as part of the data from the Continuous Plankton Recorder (CPR), and in general, blooms for a short duration after the diatoms in spring and, to a lesser extent in autumn. However, winter blooms have also been recorded (Davidson and Marchant, 1992).

Annual variation Not much is known about the long-term changes occurring within living coccolithophorid populations. This is due largely to diculties in sampling opportunity (especially for open ocean locations) through the lack of sucient ship time and the current paucity of funding for extended projects. As a consequence, our knowledge is restricted to that gathered from coastal stations or open ocean sites extensively visited over short time periods (e.g. 24 months). For example, a 25-year study of three stations in the Western English Channel revealed that many species of phytoplankton were present for only short durations (e.g. Braarudosphaera bigelowii), while others were common throughout the study period (Boalch, 1987). The lack of cyclicity seen in this data set implies that annual phytoplankton succession is largely opportunistic and circumstantial and not aected by orbital forcing over short time periods. Long-term coastal monitoring has also been carried out by the Norwegians within various fjords and in the North Sea as part of the CPR programme. However, these observations rarely involve diverse haptophyte communities but tend to re¯ect the changes in abundance of bloom-forming taxa (e.g. E. huxleyi, Phaeocystis and Chrysochromulina spp.). Some sampling programmes (e.g. Okada and McIntyre, 1979), investigating seasonality at particular stations, covered more than 1 year, and, although they ran for only 2±3 years, their data were invaluable when faced with a lack of longer studies. However, there are few examples of studies of this duration, and most show either insigni®cant annual changes or totally random yearly successions. At present cyclicity within haptophyte populations is relatively unknown, although Owens et al. (1989) reported a 3-yearly cycle for Phaeocystis pouchetii in the North-East Atlantic.

Distribution in the sediments In general, the scales of unmineralized haptophytes are not recognisable in the sediments, and as scales are the main taxonomic criterion for identi®cation within this group, the fossil record of these haptophytes is largely unknown. However, it is possible that their chemical signature may remain unaltered and hence recognisable within the sediments (e.g. as part of the alkenone fossil record), although this would not be taxon-speci®c. Therefore, our knowledge of haptophyte evolution derives almost entirely from the mineralized taxa: the coccolithophorids and possibly Chrysotila. It has been noted that the mineralized bodies of Chrysotila lamellosa resemble nannofossils included in the genera 146 Jordan and Chamberlain Tetralithus and Marthasterites (Parke, 1971; Green and Course, 1983). This connection, if proven, could provide another important piece of information in the study of haptophyte evolution. The evolution and diversity of coccoliths in the sediments has already been summarized in Bown et al. (1992) and will not be repeated here. However, it is important to note that coccoliths have a known marine fossil record dating back to the Late Triassic and have shown great diversity from that period through to the present day. This diversity reached peaks at three dierent times, the Late Cretaceous, the Eocene and the middle Miocene. The present trend is described by the above authors as an overall decline in diversity, a trend which is mirrored by other marine organisms. These changes in diversity through geological time are of course subjective, although they do provide a general picture. In modern oceans there are approximately 300 haptophytes, of which about 200 are coccolithophorids (Jordan and Green, 1994; Jordan and Kleijne, 1994). However, according to Bown et al., (1992, their Fig. 4) less than 30 of these species are recorded in the underlying sediments. This number is extremely conservative and probably refers to common species or does not include the surface sediments. Even in a later paper (Young et al., 1994) this number was revised to about only 40, although the authors acknowledged that this was due in part to size-selective observation. However, it is well known that many species still extant today have records dating back at least to the Late Miocene (Perch-Nielsen, 1985; von Salis, 1994; information within Deep Sea Drilling Project (DSDP) and Ocean Drilling Program (ODP) volumes). If all the species found in Quaternary sediments were counted then this time period would certainly rate as high in richness as the Eocene and possibly even the Late Cretaceous. There are also many species which are not incorporated into the sediments as recognisable coccoliths or fragments. These species possess delicate heterococcoliths or those made of numerous microcrystals (holococcoliths). In recent check-lists these species account for about half (approximately 100) of the known extant species. However, it is known that holococcoliths can be preserved in the sediments and have been in existence for as long as their more robust counterparts. This is not surprising, of course, as studies of extant taxa in culture have revealed holococcolithophorid-heterococcolithophorid life cycles. Since geological diversity does not account for missing ¯ora, the proportion of this holococcolith/delicate heterococcolith component may have varied through geological time, resulting in a radically dierent understanding of our current interpretation of pa- laeodiversity.

Future research In recent years haptophyte research has received more attention than ever before, and a lot of new information has been published. However, despite these achievements there are still a number of areas which need to be improved. At present, most of the detailed observations on haptophytes derive from cultured material, in particular those of unmineralized taxa. So, in the future, more species, especially coccolithophorids need to be isolated and maintained in culture. To our knowledge at least three laboratories, Miami (USA), Plymouth (UK) and Tsukuba (Japan), continue to be actively involved in isolating calcifying haptophytes. As our knowledge of haptophyte life cycles is still very poor, further cultures will enable us to identify phases of single species. This is of great importance in coccolithophorid research, because identifying the phases will help us to re- Haptophyte algae 147 duce the complexity of the existing taxonomy, and will improve our knowledge of coccolithophorid ecology (e.g. community structure, seasonality). Furthermore, availability of these cultures will allow investigation of their biochemical and ultrastructural components. Recent research programmes have been hugely successful, but they purposely concentrated on one or two species. With the availability of new cultures comparative studies can be performed and the data can be inputted into the Emiliania huxleyi model currently being generated. These cultures should also provide the molecular biologists with extremely useful data on haptophyte classi®cation and evolution. Presently, most coccolithophorid species have been described only from ®xed or ®ltered material and so, for instance, observations on the cell contents, the true position of the scales, the actions of the ¯agella and the haptonema, and life cycles are missing. As cultures of these organisms are unavailable, several scientists have started using video cameras onboard the ship in order to ®lm these organisms immediately after their capture by water bottle. In this way va- luable information is being gathered. Routine methods of water sampling and processing do not allow for the good recovery of unmineralized haptophytes. As a consequence, the distribution of these algae is poorly documented, despite recent eorts to determine the movements of Chrysochromulina populations in the North Sea and surrounding areas. In the future, distribution data on these organisms must be collected throughout the world. In a similar way, regular sampling of open ocean sites has also been neglected. Data on the seasonal distribution of haptophytes, including coccolithophorids, is still extremely fragmentary and there is a need to obtain more samples from water depths between 100 and 300 m (the lower photic zone). Improved biological data will naturally lead to better interpretation of past ocean history, especially in the last 10 million years, during which many of the present-day coccolithophorid species have lived. Constant re®ning of our sediment tools (e.g. biomarkers and coccoliths) must be achieved in order to understand the past with greater accuracy.

Concluding remarks In addition to displaying a wide range of morphological and ultrastructural details, the haptophyte algae are now known to be numerically important in marine and occasionally freshwater ecosystems, where they may produce large populations of bloom proportions. These blooms are often large enough to be seen by satellite imagery and persist for several weeks. The mere presence of these blooms can sometimes interfere with the local environment and its associated wildlife, and even with human activities, such as the eec- tiveness of commercial marine ®shing. Furthermore, the `chemical warfare' (toxins, foam and antibacterial agents) exhibited by some of these organisms can have devastating eects on the survival of marine life in the vicinity of these blooms. It is now recognised that DMS production by these blooms plays an important role in global climate and is an integral part of the sulphur cycle, while the formation and release of large quantities of calcite by coccolithophorid blooms is equally important in carbon cycling by providing a necessary sink for excess carbon in the form of chalk deposits. From the fossil record we now know that these organisms have been operating in the same way and on a similar scale for over 200 million years and so their role in the Earth's climate history, and hence their indirect eect on faunal and ¯oral evolution, may have been drastically under- estimated. 148 Jordan and Chamberlain Acknowledgements The authors would like to thank Dr Patricia Wells and Dr John Green for comments made on an earlier draft of the manuscript. Figures 1±4 were kindly printed by Mrs S. Lu. Cultured material was supplied by Dr John Green (MBA, Plymouth) to AHLC and RWJ, when they were working at Portsmouth Polytechnic and University of Surrey respectively. The manuscript has bene®tted from comments made by the editor and the reviewers.

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