PHYLUM RADIOLARIA – Diversity of Life

PHYLUM RADIOLARIA (Müller 1858 em. Cavalier-Smith 2002)

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RADIOLARIA LINKS

Radiolaria (ra-de-o-LAR-e-a) is derived from the Latin radius, which means the spoke of a wheel. Radiolus is the diminutive of radius; so, the name literally means little spokes. The reference clearly is to the radiate appearance of the of the mineralized spines and axopods .

INTRODUCTION TO THE RADIOLARIA

The radiolarians are among the most beautiful microbial eukaryotes. They are significant components of the marine plankton and are characterized by mineralized cytoskeletal components that appear as nested spheres and spines; so that they often look like as tiny free-floating star-bursts. Ernst Haekel defined the group in 1862 and, in 1887, expanded on the descriptions of radiolarians based on collections made by the H.M.S. Challenger expedition. Haeckel found the radiolaria to be so beautiful that he devoted a significant portion of his Kunstformen der Natur (Art Forms in Nature) to them in 1904. Surprisingly, modern systematics of radiolarians confirms the monophyly of Acantharia + Polycystinea (e.g. Ishitani et al. 2011), the two groups that Haeckel defined, though Polycystinea may be paraphyletic (e.g. Gilg et al. 2010).

The acantharians have skeletons and spines made of strontium sulfate. Generally, they are spherical with two nested lattice-work strontium sulfate spheres and 20 mineralized spines that join in the center and emerge such that they are equidistant from each other in a geometric pattern called Müller’s Law (see Figures 1 and 2). The large cell has an inner endoplasm that is bounded by the inner sphere and contains the nuclei (most are multinucleate) and most other organelles. The outer cytoplasm (the ectoplasm) is bounded by the outer sphere and the cell membrane, but it has channels of sea water and a very dynamic reticular cytoplasmic network that traps and envelops prey organisms (diatoms, ciliates, haptomonads, silicoflagellates, etc). Many taxa have zooxanthellae, endosymbiotic dinoflagellates that inhabit the endoplasm. Thus, much of their nutrition likely is photosynthetic.

The life history of these organisms is only partly known, but they do seem to have a sexual life history. The vegetative cell undergoes mitosis many times to produce thousands of nuclei, each of which develops into an isogamete and is shed. They form zygotes, but development, the fate of the zygote, and timing of meiosis in the life history are not known. Furthermore, because strontium sulfate dissolves readily, very little is known about the acantharians in the fossil record.

They do seem to be responsible for the export of strontium and other elements from the surface to the deep ocean (see Figure 3). Decelle et al. (2012 and 2013) explored the phylogeny, diversity, and ecology of acantharians in the open oceans. They defined two different groups that have very different influences on geochemistry of the oceans. Acantharians with photosynthetic symbiotes appear to be monophyletic and remain in the photic zone throughout their life history. Most of the acantharian diversity, however, does not have photosynthetic symbionts. In their life history, they do form cysts that are dense and sink out of the photic zone into the dark abyssal zone, where photosynthesis cannot occur. Swarmers excyst and develop into the trophpozoite, which moves to the photic zone. Decelle et al. (2013) argue that the movement of acantharians from the abyssal zone can be significant transporters of Sr and other nutrients that would tend to be sequestered on the ocean floor.

The polycystines have skeletons made of silica and thus have a very complete fossil record which extends back to the Cambrian. In general, they are similar to the acantharians in overall structure in that they have a central capsule that contains the nuclei and most of the organelles. However, although polycystines may have more than one nested sphere or shell, they do not have the outer lattice sphere that is characteristic of the acantharians. The outer ectoplasm appears frothy and contains many food vacuoles. Polycystines are almost universal in their tastes and consume anything small enough to be caught. Many species also have zooxanthellae; so, their nutrition is supplemented by the photosynthate of the endosymbiotic algae. There are two general types of of polycystines. The spumellarids (Figure 4) have an inner shell with a uniform pattern of pores from which the axopods emerge. The nassellarids have an inner capsule that not spherical (Figure 5) and has a pore field concentrated on one part of it. In this way they resemble the phaeodarians (Cercozoa). Life histories are unknown. Some taxa release biflagellate cells each of which contains a strontium sulfate crystal; thus, they are called crystal swarmers, but their position in the life history is unknown. This utilization of strontium sulfate by two different groups suggests that it may be a deep-branching character that has been lost by other polycystines (and, also Foraminifera, suggested by Krabberod et al. 2011).

Sticholonche is an odd taxon that has jointed or articulated axopods with which it rows through the water (Figure 6) at depths of about 100-300m. It has silicaceous spicules in the outer cytoplasm of its heart-shaped cell. Rowing is accomplished by the interactions of microfilaments that extend from the nuclear membrane to the “joint” into which the base of the axopod is inserted. The microfilaments contract and cause the axopod to move. The astonishing thing is how the movement is coordinated such that the recovery stroke does not counteract the power stroke. Molecular phylogenies have consistently associated Sticholonche with the acantharians in a group that Krabberod et al. (2011) call Spasmaria.

SYSTEMATICS OF THE RADIOLARIA

These taxa are among many that produce axopods, pseudopods that extend ray-like from the cell and are stiffened by internal microtubular supports. Margulis and Schwartz (1988 and 1998) lumped together all axopod-bearing taxa (acantharians, phaeodarians, polycystinids, and heliozoans) into a large heterogeneous phylum called the Actinopoda (designated Pr-16 and Pr-27, respectively). Earlier, Kudo (1966), Grell (1976), Cachon and Cachon (1985), Febvre-Chevalier (1985) and Sleigh et al (1984) all lumped this group with the amoebae, slime molds and forams. Then, Febvre (1990), Febvre-Chevalier (1990), and Cachon et al. (1990), separated the actinopod-bearing taxa and grouped them together into their own phylum. Their union was short-lived and the Actinopoda as a coherent group began to fragment such that Patterson (1999) defined at least 6 different sisterless actinopod-bearing groups. This was supported in part by studies like Zettler et al. (1997) in which the acantharians and polycystinids appeared to be polyphyletic in a ssu-rRNA study. Then, Mikrjukov and Patterson (2001) and Cavalier-Smith and Chao (2003) demonstrated the polyphyly of the heliozoans. Supertree analyses of rRNA and actin trees (Lopez-Garcia et al. 2002; and Nikolaev et al. 2004) demonstrated the polyphyletic nature of the axopod, but the monophyly of the Acantharia+Polycystinea clade. Interestingly, Nikolaev et al. (2004) also suggested an association with a very strange organism called Stilonoche, a group that rows its way through the water with articulated spines. Cavalier-Smith (2002) and Cavalier-Smith and Chao (2003) defined a clade that included the Radiolaria (as defined here) + the Formaminifera that they called the Retaria.

We have followed the suggestions of Nikolaev et al. (2004) and Lopez-Garcia et al. (2002) to rejoin the Acantharea and the Polycystinea together into the phylum Radiolaria. Our treatment of Acantharea is about the same as that of Febvre (1990) and Febvre et al. (2000). However, our taxonomic scheme which has 3 orders for the Polycystinea is quite different from that of Cachon et al. (1990) and Anderson et al. (2000) who lumped the taxa into 2 orders. In addition, we have included Sticholonche as a class in the Radiolaria, as our interpretation of the analysis of Nikolaev et al. (2004) in which Acantharea, Taxopodida, and Polycystina appear to be part of a single clade. Molecular phylogenies (summarized in Figure 7) have consistently associated Sticholonche with the acantharians in a group that Krabberod et al. (2011) call Spasmaria. The association of the Foraminifera with the Radiolaria in a monophyletic group was defined as Retaria by Cavalier-Smith (1999) and confirmed by most molecular analyses since (e.g. Polet et al. 2004, Moreira et al. 2007, Ishitani et al. 2011, Sierra et al. 2013). Problems do exist within the polycystines; however, in that the Spumellaria and Nassularia do not emerge as a monophyletc group that does not include the Acantharians in some analyses (e.g. Takahashi et al. 2004, Yuasa et al. 2006, Suzuki and Aita 2011).

LITERATURE CITED

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By Jack R. Holt. Last revised: 03/07/2013


FIGURE 1. Acantholithium has twenty large spines emerging from a central capsule. Image from Febvre et al. (2000)	FIGURE 2. A skeleton of Pleuraspis showing the lattice-like structure of the peripheral skeleton. The twenty spines emerge from a central capsule and are multifaceted. Image from Febvre et al. (2000)


FIGURE 4. Pongosphaera has a simple mineralized skeleton with radial spicules. Image from Anderson et al. (2000)	FIGURE 5. Theopilium is cone-shaped (characteristic of the nassellarids). Image from Grell (1973)	FIGURE 6. Sticholonche has articulated axopods, which it uses to “row” through the water. Image from Mikrjukov et al. (2000)

PHYLUM RADIOLARIA (Müller 1858 em. Cavalier-Smith 2002)

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