Acantharia
Introduction

Acantharia are delicate, free living, microphagic, exclusively marine microzooplanktonic protozoa. They are generally spherical, oblate or sometimes flattened, ranging in size from 0.05-5 mm in diameter. Acantharia share a feature with Radiolaria and the closely related group Heliozoa: the axopodia. These are long, radiating, unramified processes stiffened by patterned arrays of microtubules (Febvre-Chevalier and Febvre, 1993). For this reason, all these taxa are placed in the Superclass Actinopoda.

Distinguishing features are:

(1) the characteristic skeleton of strontium sulfate, based on a general plan of 10 diametral or 20 radial spicules arranged in a regular pattern called Müller's law (Müller, 1859);

polar view
side view

(2) division of the cell body into two parts, a centrally located endoplasm (central capsule), separated from the ectoplasm by the central capsule membrane; the ectoplasm in many species further subdivided by a distinctive outer layer termed the periplasmic or ectoplasmic cortex. ;
schematic cross section

(3) the myonemes, bundles of contractile filaments resembling umbrella ribs grouped around the spicules where they protrude from the peripheral cell body.
Amphibelone hydrotomica 2

Reproduction and the life cycle are incompletely known. There is no evidence for asexual reproduction, although it was previously reported in one genus (Schewiakoff, 1926). Sexual reproduction takes place in a gamont which maintains the aspect of the trophont (vegetative cells), or in a cyst (gamontocyst).

acantharian cysts 1
acantharian cysts 2
acantharian cysts 3
acantharian cysts 4
acantharian cysts 5
acantharian cysts 6

Encystment involves a complete reorganization of the mineral skeleton and a series of mitotic and meiotic fissions. Thousands of biflagellate isogametes are formed in the gamonts and gamontocysts, and shed within minutes. Further steps to the formation of the young acantharian remain unknown.

Acantharia consume a wide variety of prey. Reports from microscope observations of feeding vacuoles describe the remains of tintinnids and other types of ciliates, diatoms, dinoflagellates, copepod nauplii, copepodids and adults, pelagic molluscs, and other sarcodine taxa (Caron and Swanberg, 1990). Examination of cells under epifluorescent illumination (blue excitation, red and orange emission) reveals signs of microalgal prey including picoplankton sized (<2 µm) cyanobacteria (Michaels, pers. comm.). Small bacteria can also be observed within food vacuoles with the appropriate staining techniques; however, it is unclear if they are actively consumed or accidentally incorporated with larger food. There are no published quantitative estimates of grazing rates.

schematic cross section

Many species contain symbiotic algae generally known as zooxanthellae. According to Febvre et al. (in press), in most families they are located in the endoplasm, although Schewiakoff (1926) reports that they are usually in the ectoplasm. In natural assemblages of Acantharia, approximately half of the individuals have symbionts and the smallest and largest size classes have the lowest proportions of symbionts (Michaels 1988a, 1988b, 1991). Symbionts are found in all members of the order Arthracanthida (Febvre and Febvre-Chevalier, 1979; Febvre, 1990) at some part of the life cycle. Within a species, young trophonts and gamonts lack symbionts, and symbiont numbers appear to increase with size in the trophont stage. Symbionts seem to be shed or consumed immediately prior to gametogenesis. Acantharian symbionts are of diverse biologic origins, including dinoflagellates and haptophytes, and some species have more than one symbiont type within the same host.

Symbiont abundances vary within a host from a few large dinoflagellates in some species, to many thousands of smaller symbionts in others. Most Acantharia have symbionts at some stage in their life cycle, although in heterogeneous natural populations, generally about half of the individual Acantharia are aposymbiotic (Michaels, 1991). These aposymbiotic individuals are a mix of juveniles and near-reproductive adults (which lose the symbionts). Symbiont reproduction is likely under host control as the slow symbiont doubling times inferred by cell division (very few of the cells are seen in mitosis at any one time) are much lower than the rapid growth that could be inferred from the carbon-specific rates of symbiont production (9.4 ng C per ng symbiont C per day, Michaels, 1991). Most of the symbiont-fixed carbon is probably transferred to the host, suggesting that symbiotic algae are an important part of the nutrition of Acantharia. These symbionts have extremely high saturation irradiances and can continue to fix carbon even near the surface. This carbon can sometimes meet or exceed the inferred daily metabolic requirements of the host for carbon (Michaels, 1988a, 1988b, 1991; Caron et al., 1995).

Little is known about host-symbiont nitrogen dynamics. In the oligotrophic settings in which Acantharia are most common, it is likely that nitrogen and phosphorus are supplied to the association by the feeding activity of the acantharian as dissolved nutrients are present at very low concentrations. However, symbionts may play a role in retention of these nutrients either by recycling through the host or by meeting the host energy demands and thus allowing a more efficient use of particulate nutrient material.

Acantharians also are thought to play an important role in the budgets of strontium and other metallic elements in the oceans. Prior to the 1950's, dissolved strontium (Sr) in seawater was considered a conservative element, i.e. varying with salinity (e.g., Chow and Thompson, 1955). Using a flame photometric internal standard technique, Mackenzie (1964) was the first to observe a significant increase in strontium to chlorinity ratios (Sr/Cl) at water depths of 500 to 800 meters, which he attributed to possible reaction with organic aggregates. More refined analytical methods (atomic absorption and neutron activation techniques) established a trend in Sr/Cl ratios in Pacific seawater samples, with significantly lower ratios in shallow waters from the eastern North Pacific than those from deeper waters (Brass and Turekian, 1974). Subsequently, a more sensitive technique using mass spectrometric isotope dilution, demonstrated differences between Atlantic and Pacific Sr/Cl ratios. In addition, Sr/Cl ratios in Pacific surface waters were shown to be approximately 2% lower than those in the deep Pacific. Brass and Turekian (1974) suggested acantharians as a possible mechanism for this depth trend.

Based on proton induced X-ray emission analyses, Brass (1980) noticed a variety of trace elements — Ca, Mn, Ni, Zn, Pb, Sr, As and Br — in 10 acantharian skeletons. And although Arrhenius (1963) reported high concentrations of barium (5400 ppm) in acantharian celestite (SrSO4), Brass (1980) found no barium in his study.

To date, low surface water Sr/Cl ratios have been correlated with uptake of Sr by surface-dwelling acantharians. Conversely, comparatively high ratios (about 2-7% higher) in intermediate waters may be the result of rapid dissolution of sinking acantharian celestite debris (Bernstein et al., 1987). To the extent that acantharians affect seawater Sr/Cl ratios, the trace metals reported in their skeletons and cysts suggests that cycling of other oceanic elements may also be influenced. Molar ratios of Ba to Sr in acantharians have been determined by Arrhenius (1963) and Rieder et al. (1982) as 4 x 10ö3. More recently, neutron activation analyses of Pacific acantharian specimens yielded a (Ba)T/(Sr)T molar ratio of (3.0±0.8) x 10ö3 (Bernstein et al., 1992). These molar ratios in acantharian celestite are approximately 10 times larger than the dissolved [Baö2+]T/[Srö2+]T molar ratios calculated for surface ocean waters (Bruland, 1983). Consequently, sinking dead-acantharian celestite may play a larger role in oceanic Ba cycling than is the case for cycling of Sr.

To further test this hypothesis, individual acantharian organisms (skeletons and cysts) were analyzed for Sr and Ba by inductively coupled plasma mass spectrometry (Bernstein et al., 1998). Specimens were obtained from four diverse areas of the world's oceans. Acantharian (Ba)T/(Sr)T molar ratios were compared to dissolved Ba and Sr concentration ratios from GEOSECS (Ostland et al., 1987) stations that corresponded most closely to the stations from which the acantharians had been collected. Results showed that for 61 of the 64 specimens analyzed, (Ba)T/(Sr)T molar ratios were significantly higher than those calculated from the corresponding seawater samples. Thus, acantharian particles exiting surface water remove a larger fraction of Ba than Sr.

It is beyond the scope of this chapter to elaborate on the thermodynamic principles supporting the data on enrichment of Ba in acantharian celestite relative to Ba/Sr ratios in seawater (Bernstein et al., 1998). Nevertheless, it is important to point out that thermodynamic principles and the reported inclusion of other trace metals in acantharian celestite (Michaels and Coale, unpublished data) suggest that acantharians may also be important in the oceanic cycling of metals other than Sr and Ba.

There is no direct evidence of the origin or geologic history of the Acantharia. Since their skeleton dissolves rapidly in sea water after death, they do not fossilize.

The Class Acantharia comprises around 50 genera and 150 species grouped into 18 families and 4 orders: Holacanthida, Symphyacanthida, Chaunacanthida and Arthracanthida. The primary reference for the systematics is the monograph by Schewiakoff (1926). This book contains a set of remarkable drawings and a clear and expansive description of acantharian taxonomy based on accurate in vivo observations of 80 species. Schewiakoff's system takes the character of the cell body into account, whereas his predecessors used skeletal morphology almost exclusively for taxonomic discrimination. More recently, general descriptions of morphology and systematics, in some cases largely compiled from Schewiakoff (1926), were produced by Trégouboff (1953), Reshetnjak (1981), Cachon and Cachon (1985), and Febvre et al. (in press). Reshetnjak's (1981) monograph is particularly relevant since it reviews all known acantharian species, including distributional data, identification keys, and diagnoses. Present knowledge of the fine structure of these protozoa, their life cycle, nuclear fission, endosymbiosis, and myoneme behavior are summarized in Febvre (1990). A few modern ecological data are available, including their abundance and distribution (Beers et al., 1975, 1982; Bishop et al., 1977, 1978, 1980; Massera Bottazzi et al., 1971; Massera Bottazzi and Andreoli, 1974, 1982a, 1982b; Michaels, 1988a, 1988b, 1991; Michaels et al., 1995), their role in cycling carbon through both photosynthesis by symbionts (Michaels, 1991; Caron et al., 1995), and their contributions to sinking particles (Caron and Swanberg, 1990; Michaels, 1991; Michaels et al., 1995).