Plankton by Yulia Stern

contents

Experimentations Overview

1 Plankton viruses 1.1 History 1.2

General properties

1.3

What kinds of viruses occur in plankton?

2 Bacterioplankton 2.1

Nutrition and physiology

3 Protozoa, Radiolarians 3.1

Cellular morphology

3.2 Biomineralization

4 Copepods 4.1 4.2 4.3

Taxonomy Morphology Behaviour

5 Gelatinous zooplankton 5.1 Medusae 5.2 Bioluminescence 5.3 Biochemistry

Index

Figure 1 Viruses are so small that they are at or below the resolution limit of light microscopy (c. 0.1 μm). Therefore electron microscopy is the only way to observe any detail of viruses. Because viruses are denser than seawater, this can be done by ultracentrifugation, typically at forces of at least 100 000 × g for a few hours.

Figure 2 The standing stock of bacteria is still most commonly assessed by epifluorescence microscopy, following staining of the cells with a fluorochrome dye. Bacterial size is approximately 0.4 – 1 μm in diameter.

Caroline Herschel

Figure 3 Morphology of polycystine radiolaria. Spumellarian with spherical central capsule and halo of radiating axopodia emerging from the fusules in the capsular wall and surrounded by concentric, latticed, siliceous shells.

Figure 4 A Cyclostephanos dubius; B Rhopalodia gibberula; c Rhaphoneis amphiceros; d Azpeitia nodulifera; e Schuettia annulata; f Diploneis fusca var. pelagi; g Diploneis crabro h Coscinodiscus perforatus var cellulosa I Triceratium dubium j and k Triceratium favus fo. quadratus l Triceratium campechianum m Cocconeis pseudomarginata.

Figure 5 Cytoplasmic organization of a spumellarian radiolarian showing the central capsule with nucleus N, capsular wall CW and peripheral extracapsulum containing digestive vacuoles DV and algal symbionts in perialgal vacuoles PV. The skeletal matter SK is enclosed within the cytokalymma, an extension of the cytoplasm, that acts as a living mold to dictate the shape of the siliceous skeleton deposited within it.

dv N

urosome

anal somite

furca or caudal ramus

Diagrammatic illustration of the external morphology and appendages of a female calanoid copepod. The metasome has four clearly defined segments.

endopods

Figure 6

rostrum

cephalosome

antennule

labrum

labium

prosome

metasome

segments

genital somite

Figure 7 The diversity of calanoid body form. a Pseudocyclopidae; b Acartiidae; c Stephidae; d Metridinidae; e Euchaetidae; f Calocalanidae; g Temoridae.

Figure 8 Anthomedusae. This order of hydromedusae includes small species ranging in size from less than 1mm to several centimeters. The umbrella is usually shaped like a tall bell, and gonads are almost always found on the sides of the central stomach. There are four radial canals connecting the stomach to a marginal ring canal. Tentacles occur in varying numbers around the umbrella margin and sometimes around the mouth. Anthomedusae alternate with polyp forms, but some also bud medusae directly.

figure 9 Medusae, sutch as Aequorea, Solmissus, Atolla, Periphylla, Pelagia, Halicreas can produce flashes, scintilating secretions, and multiple waves of light.

Overview

The category of marine life known as plankton represents the first step in the food web of the ocean (and of large bodies of fresh water), and components of the plankton are food for many of the fish harvested by humans and for the baleen whales. The plankton play a major role in cycling of chemical elements in the ocean, and thereby also affect the chemical composition of sea water and air (through exchange of gases between the sea and the overlying atmosphere). In the parts of the ocean where planktonic life is abundant, the mineral remains of members of the plankton are major contributors to deep-sea sediments, both affecting the chemistry of the sediments and providing a micropaleontological record of great value in reconstructing the earth’s history. "Plankton" refers to "drifting", and describes organisms living in the water column (rather than on the bottom – the benthos) and too small and / or weak to move long distances independently of the ocean’s currents. However, the distinction between plankton and nekton (powerfully swimming animals) can be difficult to make, and is often based more on the traditional method of sampling than on the organisms themselves. Although horizontal movement of plankton at kilometer scales is passive, the metazoan zooplankton nearly all perform vertical migrations on scales of 10s to 100s of meters. This depth range can take them from the near surface lighted waters where the phytoplankton grow, to deeper, darker and usually colder environments. These migrations are generally diurnal, going deeper during the day, or seasonal, moving to deeper waters during the winter months to return to the surface around the time that phytoplankton production starts. The former pattern can serve various purposes: escaping visual predators and scanning the watercolumn for food. (It should be noted that predators such as pelagic fish also migrate diurnally.) Seasonal descent to greater depths is a common feature for several copepod species and may conserve energy at a time when food is scarce in the upper layers. However, vertical migration has another role. Because of differences in current strength and direction between surface and deeper layers in the ocean, time spent in deeper water acts as a transport mechanism relative to the near surface layers. On a daily basis this process can take plankton into different food concentrations. Seasonally, this effective "migration" can complete a spatial life cycle. The plankton can be subdivided along functional lines and in terms of size. The size category, picoplankton (0.2 – 2.0 μm), is approximately equivalent to the functional category, bacterioplankton; most phytoplankton (single-

celled plants or colonies) and protozooplankton (single-celled animals) are nano- or microplankton (2.0 – 20 μm and 20 – 200 μm, respectively). The metazoan zooplankton (ani-mals, the "insects of the sea") includes large medusae and siphonophores several meters in length. Size is more important in oceanic than in terrestrial ecosystems because most of the plants are small (the floating seaweed, Sargassum, being the notable exception), predators generally ingest their prey whole (there is no hard surface on which to rest prey while dismembering it), and the early life stages of many types of zooplankton are approximately the same size as the larger types of phytoplankton. Therefore, while the dependence on light for photosynthesis is characteristic of thephytoplankton, the concepts of "herbivore" and "carnivore" can be ambiguous when applied to zooplankton, since potential plant and animal prey overlap in size and can be equivalent sources of food. Though rabbits do not eat baby foxes on land, analogous ontogenetic role-switching is very common in the plankton. Among the animals, holoplanktonic species are those that spend their entire life in the plankton, whereas many benthic invertebrates have meroplanktonic larvae that are temporarily part of the plankton. Larval fish are also a temporary part of the plankton, becoming part of the nekton as they grow. There are also terms or prefixes indicating special habitats, such as "neuston" to describe zooplanktonic species whose distribution is restricted to within a few centimeters of the sea’s surface, or "abyssoplankton" to describe animals living only in the deepest waters of the ocean. Groups of such species form communities. Since the phytoplankton depend on sunlight for photosynthesis, this category of plankton occurs almost entirely from the surface to 50 – 200 m of the ocean — the euphotic depth (where light intensity is 0.1 – 1% of full surface sunlight). Nutrients such as nitrate and phosphate are incorporated into protoplasm in company with photosynthesis, and returned to dissolved form by excretion or remineralization of dead organic matter (particulate detritus). Since much of the latter process occurs after sinking of the detritus, uptake of nutrients and their regeneration are partially separated vertically. Where and when photosynthesis is proceeding actively and vertical mixing is not excessive, a near-surface layer of low nutrient concentrations is separated from a layer of abundant nutrients, some distance below the euphotic depth, by a nutricline (a layer in which nutrient concentrations increase rapidly with depth). Therefore, the spatial and temporal relations between the euphotic depth (dependent on light intensity at the surface and the turbidity of the water), the nutricline, and the pycnocline (a layer in which density increases rapidly with depth) are important determinants of the abundance and productivity of phytoplankton. Zooplankton is typically more concentrated within the euphotic zone than in deeper waters, but because of sinking of detritus and diel vertical

migration of some species into and out of the euphotic zone, organic matter is supplied and various types of zooplankton (and bacterioplankton and nekton) can be found at all depths in the ocean. An exception is anoxic zones such as the deep waters of the Black Sea, although certainly types of bacterioplankton that use molecules other than oxygen for their metabolism are in fact concentrated there. Even though the distributions of planktonic species are dependent on currents, species are not uniformly distributed throughout the ocean. Groups of species, from small invertebrates to active tuna, seem to "recognize" the same boundaries in the oceans, in the sense that their patterns of distribution are similar. Such groups are called "assemblages" (when emphasizing their statistical reality, occurring together more than expected by chance) or "communities" (when emphasizing the functional relations between the members in food webs), though terms such as "biocoenoses" can be found in older literature. Thus, one can identify central water mass, subantarctic, equatorial, and boreal assemblages associated with water masses defined by temperature and salinity; neritic (i.e. nearshore) versus oceanic assemblages with respect to depth of water over which they occur, and neustonic (i.e. air – sea interface), epipelagic, mesopelagic, bathypelagic, and abyssopelagic for assemblages distinguished by the depth at which they occur. Within many of these there may be seasonally distinguishable assemblages of organisms, especially those with life spans of less than one year. Regions which are boundaries between assemblages are sometimes called ecotones or transition zones; they generally contain a mixture of species from both sides, and (as in the transition zone between subpolar and central water mass assemblages) may also have an assemblage of species that occur only in the transition region. It is likely that a few important species have physiological limits confining them to a zone, and the other members of the assemblage are somehow linked to those species functionally, rather than being themselves physiologically constrained. Limits can be imposed on certain life stage, such as the epipelagic larvae of meso- or bathypelagic species, creating patterns that reflect the environment of the sensitive life stage rather than the adult. M. M. Mullin, Scripps Institution of Oceanography, La Jolla, California, USA

1 Viruses tend to selectively attack the most abundant potential hosts, thus may "kill the winner" of competition and thereby foster diversity.

2 These bacteria were thought to be heterotrophs (organisms that consume preformed organic carbon), because they apparently lacked photosynthetic pigments like chlorophyll (later it was learned that this was only partly right, as many in warm waters are in fact chlorophyllcontaining prochlorophytes).

3 In the initial analysis, most scientists thought that grazing by protists was the only significant mechanism keeping the bacterial abundance in check. This was because heterotrophic protists that can eat bacteria are extremely common, and laboratory experiments suggested they are able to control bacteria at nearnatural abundance levels.

Plankton Viruses Although they are the tiniest biological entities in the sea, typically 20 – 200 nm in diameter, viruses are integral components of marine planktonic systems. Figure 1 They are extremely abundant in the water column, typically 1010 per liter in the euphotic zone, and they play several roles in system function: 1 they are important agents in the mortality of prokaryotes and eukaryotes; 2 they act as catalysts of nutrient regeneration and recycling, through this mortality of host organisms; 3 because of their host specificity and density dependence, they tend to selectively attack the most abundant potential hosts, thus may "kill the winner" 1 of competition and thereby foster diversity; and 4 they may also act as agents in the exchange of genetic material between organisms, a critical factor in evolution and also in relation to the spread of human-engineered genes. Although these processes are only now becoming understood in any detail, there is little doubt that viruses are significant players in aquatic and marine plankton.

1.1 4 Regarding lytic infection, there are several studies with a variety of approaches that all generally conclude that viruses cause approximately 10 –50% of total microbial mortality, depending on location, season, etc. These estimates are convincing, having been determined in several independent ways. These include: (1) TEM observation of assembled viruses within host cells, representing the last step before lysis; (2) measurement of viral decay rates; (3) measurement of viral DNA synthesis; (4) measurement of the disappearance rate of bacterial DNA in the absence of protists; (5) use of fluorescent virus tracers to measure viral production and removal rates simultaneously; and (6) direct observation of viral appearance in incubations where the viral abundance has been decreased several fold, yet host abundances remain undiluted.

| History

It has only been in the past 25 years that microorganisms like bacteria and small protists have been considered "major players" in planktonic food webs. The initial critical discovery, during the mid-1970s, was of high bacterial abundance as learned by epifluorescence microscopy of stained cells, with counts typically 109 l–1 in the plankton.2 With such high abundance, it became important to learn how fast they were dividing, in order to quantify their function in the food web. Growth rates were estimated primarily by the development and application of methods measuring bacterial DNA synthesis. The results of these studies showed that bacterial doubling times in typical coastal waters are about 1 day. When this doubling time was applied to the high abundance, to calculate how much carbon the bacteria are taking up each day, it became apparent that bacteria are consuming a significant amount of dissolved organic matter, typically at a carbon uptake rate equivalent to about half the total primary production. However, the bacterial abundance remains relatively constant over the long term, and they are too small to sink out of the water column. Therefore, there must be mechanisms within the water to remove bacteria at rates similar to

the bacterial production rate.3 However, some results pointed to the possibility that protists are not the only things controlling bacteria. In the late 1980s, careful review of multiple studies showed that grazing by protists was often not enough to balance bacterial production, and this pointed to the existence of additional loss processes. About that same time, data began to accumulate that viruses may also be important as a mechanism of removing bacteria.

1.2

| General Properties

Viruses are small particles, usually about 20 – 200 nm long, and consist of genetic material (DNA or RNA, single or double stranded) surrounded by a protein coat (some have lipid as well). They have no metabolism of their own and function only via the cellular machinery of a host organism. As far as is known, all cellular organisms appear to be susceptible to infection by some kind of virus. Culture studies show that a given type of virus usually has a restricted host range, most often a single species or genus, although some viruses infect only certain subspecies and < 0.5% may infect more than one genus. Viruses have no motility of their own, and contact the host cell by diffusion. They attach to the host usually via some normally exposed cellular component, such as a transport protein or flagellum. There are three basic kinds of virus reproduction. In lytic infection, the virus attaches to a host cell and injects its nucleic acid. This nucleic acid (sometimes accompanied by proteins carried by the virus) causes the host to produce numerous progeny viruses, the cell then bursts, progeny are released, and the cycle begins again. In chronic infection, the progeny virus release is not lethal and the host cell releases the viruses by extrusion or budding over many generations. In lysogeny after injection, the viral genome becomes part of the genome of the host cell and reproduces as genetic material in the host cell line unless an "induction" event causes a switch to lytic infection. Induction is typically caused by DNA damage, such as from ultraviolet (UV) light or chemical mutagens such as mitomycin C. Viruses may also be involved in killing cells by mechanisms that do not result in virus reproduction.

| What Kinds of Viruses Occur in Plankton?

1.3

Microscopic observation shows the total, recognizable, virus community, but what kinds of viruses make up this community, and what organisms are they infecting? Most of the total virus community is thought to be made up of bacteriophages (viruses that infect bacteria). This is because viruses lack metabolism and have no means of actively moving from host to host (they depend on random diffusion), so the most common viruses would be expected to infect the most common organism, and bacteria are by far the most abundant organisms in the plankton.4 Field studies show a strong correlation between viral and bacterial numbers, whereas the correlations between viruses and chlorophyll are weaker. This suggests that most viruses are bacteriophages rather than those infecting phytoplankton or other eukaryotes. However, viruses infecting cyanobacteria (Synechococus) are also quite common and sometimes particularly abundant, exceeding 108 per liter in some cases. Even though most of the viruses probably infect prokaryotes, viruses for eukaryotic plankton are also readily found. For example, those infecting the common eukaryotic picoplankter, Micromonas pusilla, are sometimes quite abundant, occasionally near 108 per liter in coastal waters. Overall, the data suggest that most viruses from seawater infect nonphotosynthetic bacteria or archaea, but viruses infecting prokaryotic and eukaryotic phytoplankton also can make up a significant fraction of the total. These involve the analysis of variability of DNA sequence of a single gene product (e.g., a capsid head protein, or an enzyme that makes DNA), or through a technique known as viriomics, whereby all genomes in a sample are cut up into small pieces, then all the pieces sequenced and reassembled. These studies have revealed that: 1 there is a lot of diversity of closely related viruses infecting the same or similar strains of microorganisms, a phenomenon known as "microdiversity"; 2 RNA-containing viruses comprise a small percentage of the viral mix in oceanic waters, and are similar to viruses that infect insects and mollusks; and 3 that the diversity of viruses in a liter of seawater is astonishingly high, estimated at >104 different types for a sample from coastal California. J. Fuhrman, University of Southern California, Los Angeles, CA, USA I. Hewson, University of California Santa Cruz, Santa Cruz, CA, USA

Bacterioplankton Marine bacteria, unicellular prokaryotic plankton usuallyless than 0.5 – 1 μm in their longest dimension, are the smallest autonomous organisms in the sea — or perhaps in the biosphere. The nature of their roles in marine food webs and the difficulty of studying them both stem from their small size. Figure 2 A modern paradigm for bacterioplankton ecology was integrated into oceanography only following development of modern epifluorescence microscopy and the application of new radioisotopic tracer techniques in the late 1970s.1 Thus we are still in the process of constructing a realistic picture of marine bacterial ecology, consistent with knowledge of evolution, plankton dynamics, food web theory, and biogeochemistry. The lack of bacterioplankton compartments in most numerical models of plankton ecology testifies to out current level of ignorance. Nevertheless, much is now well known that was just beginning to be guessed in the 1980s. Bacterioplankton are important in marine food webs and biogeochemical cycles because they are the principal agents of dissolved organic matter (DOM) utilization and oxidation in the sea. All organisms liberate DOM through a variety of physiological processes, and additional DOM is released when zooplankton fecal pellets and other forms of organic detritus dissolve and decay. By recovering the released DOM, which would otherwise accumulate, bacterioplankton initiate the microbial loop, a complicated suite of organisms and processes based on the flow of detrital-based energy through the food web. The flows of energy and materials through the microbial loop can rival or surpass those flows passing through traditional phytoplankton-grazerbased food chains.

| Nutrition and Physiology 2.1

Knowledge of the nutrition and physiology of naturally occurring bacterioplankton as a functional group in the sea is based partly on laboratory study of individual species in pure culture, but mostly on sea water culture experiments. Traditional laboratory investigations show that bacteria can only utilize small-molecular-weight compounds less than ~500 Daltons. Larger polymeric substances and particles must first be hydrolyzed by extracellular enzymes.2 Such experiments, combined with size-fractionation using polycarbonate filters with precise and uniform

1 It was not until a decade later, with the use of modern genomic techniques, that their identity and taxonomy began to be understood at all.

2 In the sea water culture approach, samples with natural bacterioplankton assemblages are incubated for suitable periods (usually hours to a few days) while bacterial abundance is monitored, the utilization of various compounds with 14 C- or 3H-labelled radiotracers is estimated, and the net production or loss of metabolites like oxygen, CO2, and inorganic nutrients is measured.

1 Colonial species contain numerous radiolarian cells interconnected by a network of cytoplasmic strands and enclosed within a clear, gelatinous envelope secreted by the radiolarian. The colonies vary in size from several centimeters to nearly a meter in length.

2 Variations in the number and kind of radiolarian species (based on skeletal form) in relation to depth in the sediment provide information about climatic and environmental conditions in the overlying water mass at the time the radiolarian skeletons were deposited at that geographic location.

3 It may be thin or in some species very reduced, consisting of only a sparse de posit of organic matter contained within the surrounding cytoplasmic envelope. In others, the wall is quite thick and opalescent with a pearl-like appearance.

4 Thus far, symbionts have been observed within the central capsular cytoplasm in only a few species. Food particles, including small algae and protozoa or larger invertebrates such as copepods, larvacea, and crustacean larvae, are captured by the sticky rhizopodia of the extracapsulum.

pores of various diameter (0.2 – 10 μm), revealed that over 90% of added organic radiotracers are utilized by the smallest size fractions (<1 μm). Bacteria are overwhelmingly the sink for DOM in all habitats studied to date. Nutrient limitation of bacterial growth can be identified by adding various compounds (e.g., ammonium, phosphate, or iron salts; monosaccharides and amino acids) singly or in combination to experimental treatments and comparing growth responses to controls. Using this approach, it has been learned that bacteria are effective competitors with phytoplankton for inorganic nutrients, including iron, which bacteria can mobilize by producing ironbinding organic complexes called siderophores. In general, bacterial growth in the sea, from estuaries to the central gyres, tends to be limited by organic matter. Sea water cultures most often respond to additions of sugars and amino acids, with the response sometimes enhanced if inorganic nutrients (including iron) are also added. H. W. Ducklow, The College of Willian and Mary, Gloucester Point, VA, USA

Protozoa, radiolarians Radiolarians are exclusively open ocean, silicasecreting, zooplankton. They occur abundantly in major oceanic sites worldwide. However, some species are limited to certain regions and serve as indicators of water mass properties such as temperature, salinity, and total biological productivity. Abundances of total radiolarian species vary across geographic regions. For example, maximum densities reach 10 000 per m3 in some regions such as the subtropical Pacific. By contrast, densities range about 3 – 5 per m3 in the Sargasso Sea. Radiolarians are classified among the Protista, a large and eclectic group of eukaryotic microbiota including the algae and protozoa. Algae are photosynthetic, single-celled protists, while the protozoa obtain food by feeding on other organisms or absorbing dissolved organic matter from their environment. Radiolarians are single-celled or colonial protozoa Figure 3. The single-celled species vary in size from < 100 μm to very large species with diameters of 1 – 2 mm. The larger species are taxonomically less numerous and include mainly gelatinous species found commonly in surface waters. The smaller species typically secrete siliceous ske-

letons of remarkably complex design Figure 4. The skeletal morphology is species-specific and used in taxonomic identification. Larger, noncolonial species are either skeletonless, being enclosed only by a gelatinous coat, or produce scattered siliceous spicules within the peripheral cytoplasm and surrounding gelatinous layer.1 The shape of the colonies is highly variable among species. Some are spherical, others ellipsoidal, and some are elongate ribbonshaped or cylindrical forms. These larger species of radiolarians are arguably, the most diverse and largest of all known protozoa. Many of the surfacedwelling species contain algal symbionts in the peripheral cytoplasm that surrounds the central cell body. The algal symbionts provide some nutrition to the radiolarian host by secretion of photosynthetically produced organic products. The food resources are absorbed by the radiolarian and, combined with food gathered from the environment, are used to support metabolism and growth. Radiolarians that dwell at great depths in the water column where light is limited or absent typically lack algal symbionts. The siliceous skeletons of radiolarians settle into the ocean sediments where they form a stable and substantial fossil record. These microfossils are an important source of data in biostratigraphic and paleoclimatic studies.2 The radiolarians are second only to diatoms as a major source of biogenic opal (silicate) deposited in the ocean sediments.

| Cellular Morphology

3.1

The radiolarian cell body contains a dense mass of central cytoplasm known as the central capsule. Among the organelles included in the central capsule are the nucleus, or nuclei in species with more than one nucleus, most of the food reserves, major respiratory organelles, i.e., mitochondria, Golgi bodies for intracellular secretion, proteinsynthesizing organelles, and vacuoles. The central capsule is surrounded by a nonliving capsular wall secreted by the radiolarian cytoplasm. The thickness of the capsular wall varies among species.3 The extracapsular cytoplasm usually forms a network of cytoplasmic strands attached to stiffened strands of cytoplasm known as axopodia that extend outward from the fusules in the capsular wall. The central capsular wall and axopodia are major defining taxonomic attributes of radiolarians. A frothy or gelatinous coat typically surrounds the central capsule and supports the extracapsular cytoplasm. Algal symbionts, Figure 5 when present, are enclosed within perialgal vacuoles produced by the extracapsulum.

In most species, the algal symbionts are exclusively located in the extracapslum.4 The cytoplasm moves by cytoplasmic streaming to coat and enclose the captured prey. Eventually, the prey is engulfed by the extracapsular cytoplasm and digested in digestive vacuoles (lysosomes). These typically accumulate in the extracapsulum near the capsular wall. Large prey such as copepods are invaded by flowing strands of cytoplasm and the more nutritious soft parts such as muscle and organ tissues are broken apart, engulfed within the flowing cytoplasm and carried back into the extracapsulum where digestion takes place. The siliceous skeleton, when present, is deposited within cytoplasmic spaces formed by extensions of the rhizopodia. This elaborate framework of skeletaldepositing cytoplasm is known as the cytokalymma. Thus, the form of the skeleton is dictated by the dynamic streaming and molding action of the cytokalymma during the silica deposition process. Consequently, the very elaborate and species-specific form of the skeleton is determined by the dynamic activity of the radiolarian and is not simply a consequence of passive physical chemical processes taking place at interfaces among the frothy components of the cytoplasm as was previously proposed by some researchers.

3.2

| Biomineralization

Biomineralization is a biological process of secreting mineral matter as a skeleton or other hardened product. The skeleton of radiolaria is composed of hydrated opal, an oxidized compound of silicon (nominally SiO2· nH2O) highly polymerized to form a space-filling, glassy mass incorporating a variable number (n) of water molecules within the molecular structure of the solid. Electron microscopic evidence indicates that some organic matter is incorporated in the skeleton during early stages of deposition, but on the whole, the skeleton is composed mostly of pure silica. Electron microscopic, X-ray dispersive analysis shows that a small amount of divalent cations such as Ca2+ may be incorporated in the final veneer deposited on the surface to enhance the hardness of the skeleton.5 Small vesicles are observed streaming outward from the cell body into the cytoplasm of the cytokalymma and these may bring silica to be deposited within the skeletal spaces inside the cytokalymma. The cytoplasmic membrane surrounding the developing skeleton appears to act as a silicalemma or active membrane that deposits the molecular silica into the skeletal space. During deposition, the dynamic molding process is clearly evident as the living cytoplasm continuously undergoes transformations in form,

gradually approximating the ultimate geometry of the species-specific skeleton being deposited by the radiolarian cell. In general, species with multiple, concentric, lattice shells surrounding the central capsule appear to lay down the lattices successively, progressing outward from the innermost shell. O. R. Anderson, Columbia University, Palisades, NY, USA

Copepods Copepods are microscopic members of the phylum Crustacea, the taxonomic group that includes crabs, shrimps and lobsters and is the only large class of arthropods that is primarily aquatic. The name copepod comes from the Greek words kope (an oar) and podos (foot), the majority of members of the group having five pairs of flat paddle like swimming legs Figure 6. About 10 000 species are currently known, and their numerical dominance as members of the marine plankton means that they are probably the most numerous metazoan - multicellular - animals on earth. In addition to forming a major component of marine plankton communities, copepods are also found in sea-bottom sediments, as well as associated with many marine plants and animals. They play a pivotal role in marine ecosystems by controlling phytoplankton production through grazing, and by providing a major food source for larval and juvenile fish.

4.1

| Taxonomy

There are 10 taxonomic orders of copepods, of which 9 have marine representatives. Of these the most important marine orders are the Calanoida, Cyclopoida, and Harpacticoida. Calanoid copepods are primarily pelagic, 75% of the known species are marine, and some are benthopelagic or commensal Figure 7. The group includes the species Calanus finmarchicus (Gunnerus), a dominant component of North Atlantic boreal ecosystems, first named nearly 250 years ago as Monoculus finmarchicus by Johan Ernst Gunnerus, Bishop of Trondheim in Norway. The Cyclopoida include pelagic commensal and parasitic species. Harpacticoid copepods are predominantly marine, with only 10% of species being freshwater. Most are benthic, with a few pelagic and commensal representatives, they represent the most abundant component of the meiofauna after nematode worms. The Platycopoida and Misophrioida are primarily benthopelagic groups, the latter having two pelagic species. The Poecilostomatoida and Siphonostomatoida

5 During deposition of the skeleton, the cytoplasm forms the living cytokalymma, i.e., the cytoplasmic silica-depositing mold, by extension of the surface of the rhizopodia. The cytokalymma enlarges as silica is deposited within it, gradually assuming a final form that dictates the morphology of the internally secreted skeleton.

are commensal or parasitic groups. Finally, the Monstrilloidaare exclusively marine, with parasitic juveniles, but a pelagic adult stage.

4.2 1 The body is divided into the prosome, which may be further subdivided into the cephalosome and metasome, and the urosome. The feeding appendages are on the cephalosome; in the calanoids these comprise, from anterior to posterior, the antennule, antenna, mandible, maxillulle, maxilla, and maxilliped.

2 This behavior, characteristic of most planktonicorganisms, involves the population remaining atdepth during the daytime. As night falls, the copepodsactively migrate upward to spend some hoursin the surface during the hours of darkness, before descending at dawn to the original daytime depth.

3 This results in very rapid jumps, which propel the copepod several body lengths from the source of stimulus. The benthic harpacticoids and some cyclopoids crawl over or burrow through sediment. The thoracic limbs are used in crawling, and this is accompanied in harpacticoids, by sideways undulations of the body.

4 The antennules, particularly of males, are covered with sensory structures, aesthetascs, which are important in detecting water movement, food, predators, and potential mates.

5 Many planktonic copepods are bioluminescent. The families Megacalanidae, Lucicutiidae, Heterohabdidae, Augaptilidae, and Metridinidae have luminescent glands that produce luminous glandular secretions. The number of light organs varies from 10 to 70, and they may be distributed widely over the body surface. The function of copepod bioluminescence is not certain. It may deter predators in the dark water column of the deep sea, and may act as a warning signal between individuals of the same species.

| Morphology

Most copepods are small, requiring study with a microscope. Small planktonic cyclopoids may be only 0.2 μm long and similarly harpacticoid copepods found in the interstitial space of sandy sediments are among the smallest Metazoa. In contrast, some large deep-sea calanoids, such as Valdiviella, may exceed 20 μm in length. Calanus finmarchicus is often said to be about the size of a grain of rice Figure 7. Parasitic forms are generally larger than the free living copepods. For example, species of the genus Penella, which is parasitic on fish and whales, may be over 30 cm in length. The body of a free-living copepod is normally cylindrical, and is distinctly segmented. The head, which is the site of the median naupliar eye, is either rounded or may bear a pointed rostrum. The presence of at least two pairs of swimming legs is characteristic of nearly all copepods at some stage in their life cycle. Similarly, antennules with up to 27 segments are general in the order, though segmentation may often be reduced.1 The swimming legs are attached to the metasome in adult calanoids, one pair for each of the five segments of the metasome. The urosome contains the genital and anal segments, and ends with the furca orcaudal rami, a series of spines or fine hairs. Most copepods are pale and transparent, though some species, particularly those living at the sea surface or in the deep sea, may be pigmented blue, red, orange, or black. The early developmental stages in the life history are the nauplii, with reduced numbers of appendages. In calanoids there are six naupliar stages, NI to NVI. Copepods, like all other Crustacea, molt by shedding their exoskeleton as they grow. Hence there is amolt between each naupliar stage. Molting from NVI involves a radical change inmorphology (metamorphosis) to the first copepodite stage. The copepodites, of which there are normally six stages (CI – CVI) are like small adults, and gradually develop adult characteristics during successive molts. The adult stage is CVI, and no further molts occur.

4.3

| Behavior

Perhaps the most striking aspect of the behavior ofplanktonic copepods is that of diel vertical migration.2 Although this is a general phenomenon, there are many variations, depending both on species, and the influence of environmental factors. Light is the dominant environmental factor controllingdiel vertical migration, with

populationsfollowing diel changes in light intensity, isolumes (layers of constant light intensity). Predator avoid ancerelated to light is thought to be one of the major adaptive advantages of diel vertical migration. Bymigrating to deeper darker layers by day, copepodsminimize mortality from visual predators, in particularfish. Predator avoidance has to be balanced against the need to feed and, as the phytoplankton is concentrated in the surface layers, migration to the surface by night is generally associated with active feeding, diel cycles of digestive enzyme activity, and diel feeding rhythms. Where invertebrate predators detecting prey nonvisually are dominant, the phasing of migration may be reversed. Vertical migratory behavior involves active swimming. Most copepods swim by rapid beating of the appendages, the antennae, mandibular palps, the maxillules, and the maxillae. In some species of planktonic calanoids, such as the genera Metridia, Centropages, and Temora, these movements result in a smooth continuous swimming behavior. In others, periods of active swimming are interspersed with inactivity when the animal sinks. This hopand-sink behavior is characteristic of Calanus finmarchicus. Rapid jumping, often as apredator-avoidance behavior, involves strong strokes of the antennules and the swimming legs.3 Nauplii use three pairs of appendages in swimming: the antenules, the antennae, and the mandibles. Three swimming behaviors have been recognized; a slow gliding motion propelled by the antennae and mandibles; a rapid darting behavior driven by all three pairs of appendages beating together; a cruise and pause behavior. Swimming and feeding behaviors are interdependent in herbivores, omnivores, and carnivores. Swimming speeds of planktonic calanoids generally range from 1 to 20 mm s–1 which is equivalent to 1 – 5 body lengths per second. Estimates based on field studies of oceanic diel vertical migrators, such as Pleuromamma, range from 10 to 50 mm s –1, representing the ability of such copepods to migrate at rates in excess of 100 m h –1. The predominant sensory mechanisms are mechanoreception and chemoreception, and receptor structures are found on the antennules.4 Detection of mechanical stimuli appears only to operate over short distances, often less than one body length. Chemoreception probably operates over longer distances and is involved in mate detection and response to food concentrations and to predators. 5 R. Harris, Plymouth Marine Laboratory, Plymouth, UK

gelatinous zooplankton Gelatinous zooplankton comprise a diverse group of organisms with jellylike tissues that contain a high percentage of water. They have representatives from practically all the major, and many of the minor phyla, ranging from protists to chordates. The fact that so many unrelated groups of animals have independently evolved similarbody plans suggests that gelatinous organisms reflect the nature of the open ocean environment better than any other group. Whether as predators or grazing herbivores, they seem particularly well adapted to life in the oligotrophic regions of the world oceans, where their diversity and abundance relative to crustacean zooplankton is often greatest. The gelatinous body plan has evolved in a world where physical parameters are relatively constant but food resources are sparse or unpredictable. Gelatinous zooplankton exhibit many common adaptations to this habitat. ▲ Transparent tissues provide concealment in the upper layers of the ocean, an environment without physical cover. Transparency is less common below the photic zone. ▲ The high water content of gelatinous tissues gives the organisms a density very close to that of sea water. The resulting neutral buoyancy decreases the energy required to maintain depth, but may actually require more energy overall, because of drag. ▲ The environment lacks physical barriers, strong turbulence, and current shears, so that gelatinous bodies do not need great structural strength. However, fragility makes many species difficult to sample or handle, and excludes most from more energetic coastal environments. ▲ High water content and noncellular jelly permit rapid growth and large body sizes, which can act as, or produce, large surfaces for the collection of food. ▲ Relatively large size makes gelatinous animals too big to be attacked by some predators, while their high water content reduces the food value of their tissues, which may also deter predation. Large size also permits commensal crustaceans to live on or in the body. Thus, as we look at the diversity of gelatinous zooplankton, we should keep in mind the forces that have led to their remarkable convergence.

5.1

| Medusae

The phylum Cnidaria has many gelatinous representatives, comprising various groups of medusae and the strictly oceanic siphonophores Figure 8. What are commonly called jellyfish are medusae belonging to three Classes of the Cnidaria — the Hydrozoa, the Scyphzoa, and the Cubozoa.1 All are carnivorous, capturing prey with specialized stinging cells, called nematocysts. A wide variety of prey is eaten by different medusae, ranging from larval forms and small crustaceans to other gelatinous animals and large fish.2 However, many oceanic species have lost the polyp stage and evolved instead a variety of sexual and asexual reproductive mechanisms that do not require a benthic habitat.

1 Since the morphology and life history of all three groups is broadly similar, it is practical to treat them together here. There are perhaps 1000 species of hydro- and scyphomedusae, probably with more to be discovered, especially in deep or polar waters.

| Ecology of Gelatinous Zooplankton

5.2

Gelatinous zooplankton are found in all of the oceans of the world, from the tropics to polar regions. They also occur at all depths, and many of the largest and most delicate species have been collected in recent years from the mesopelagic and bathypelagic parts of the ocean. The absence of turbulence in the deep sea probably allows these species to attain such large sizes, but there are also robust species that thrive in surface and coastal environments.3 In general, gelatinous organisms have been rather neglected by zooplankton ecologists, primarily because their delicacy makes them difficult to sample and study. Most are damaged or destroyed in conventional plankton nets, and many deep-water siphonophores and ctenophores are too delicate to be captured intact even with the most gentle of techniques. Much recent progress in understanding their biology has been based on in situ methods of study using SCUBA diving, submersibles, or remote vehicles.4 Gelatinous animals occupy every trophic niche, ranging from primary producers (symbiotic colonial radiolaria) to grazers (pteropods and pelagic tunicates) and predators (medusae, siphonophores, and ctenophores).5 This energetic flexibility is probably important to the success of gelatinous species in the oligotrophic open ocean and deep sea. Many species of medusae and siphonophores, for example, appear able to survive at low population densities spread over very large areas. In other cases the efficiency of their feeding, growth, and reproduction allows gelatinous species to outcompete other types of zooplankton and form dense populations over large areas, which can have considerable impact on ecosystems. A dramatic recent example was the accidental in-

2 Many epipelagic medusae also harbor zooxanthellae, and presumably they share their resources in the same way as the polycystine radiolarians. Many of these medusae are part of a life history that alternates between a sessile, benthic, asexually reproducing polyp and a sexually reproducing and dispersing planktonic medusa.

3 Examples include the Portuguese man-of-war (Physalia physalis), which lives at the air – water interface and can ride out hurricanes, and the ctenophore Mnemiopsis leidyi, which lives in estuaries with strong tidal currents and turbulence.

4 These methods permit observation of undisturbed behavior and collection of intact living specimens. Advances in culture techniques and laboratory measurements have improved our understanding of energetics, reproduction, and life history of some species, but most remain only partially understood.

5 In all these niches, the gelatinous body plan confers advantages of size and low metabolic costs. In addition to attaining large sizes with relatively little food input, gelatinous organisms such as medusa and ctenophores are able to “de-grow” when deprived of food. Metabolic rates remain unchanged, and the animal simply shrinks until higher food levels allow it to resume growth.

6 The combination of rapid growth and advection can cause the sudden appearance of swarms of medusae, ctenophores, or salps in coastal waters. Although these blooms may sometimes have serious or even catastrophic effects on other organisms, including fisheries or human activities, they are a natural part of the life histories of the species, and not events for which action is needed, or even possible.

troduction of the ctenophore Mnemiopsis leidyi into the Black Sea from the eastern seaboard of the Americas. In the late 1980s, this ctenophore reproduced in prodigious quantities, and the resulting predation on zooplankton and larval fishes led to the collapse of pelagic fisheries in the Black Sea. Many other gelatinous species form dramatic seasonal blooms, such as the medusa Chrysaora quinquecirrha in the Chesapeake Bay, the salp Thalia democratica off Florida, Georgia, and Australia, and the medusa Pelagia noctiluca in the Mediterranean. In the Southern Ocean, immense populations of the salp Salpa thompsoni alternate with those of the Antarctic krill Euphausia superba. The formation of large aggregations through rapid reproduction appears to be a common strategy for taking advantage of favorable conditions. Dense populations are sometimes further concentrated by wind or current action, or are transported close to the coast from their normal habitats farther offshore.6 Gelatinous zooplankton are normal components of virtually all plank tonic ecosystems. They are among the most common and typical animals in the oceans, whose biology and ecological roles are now becoming better understood.

5.3 7 Some terrestrial species (e.g., fireflies) have the same ability, but this adaptation has been most extensively developed in the oceans. Bioluminescent species occur in only five terrestrial phyla, and only in one of these (Arthropoda, which includes the insects) are there many examples.

| BIOLUMINESCENCE

Bioluminescence is the capacity of living organisms to emit visible light. In doing so they utilize a variety of chemiluminescent reaction systems. It has historically been confused with phosphorescence and the latter term is still frequently (and erroneously) used to describe marine bioluminescence.7 In contrast, bioluminescence occurs in 14 marine phyla, many of which include numerous luminescent species. All oceanic habitats, shalow and deep, pelagic and benthic, include bioluminescent species, but the phenomenon is commonest in the upper 1000 m of the pelagic environment Figure 9.

5.4

| Biochemistry

Bioluminescence involves the oxidation of a substrate (luciferin) in the presence of an enzyme (luciferase). The distinctive feature of the reaction is that most of the energy generated is emitted as light rather than as heat. There are many different, and unrelated, kinds of luciferin, and biochemical and taxonomic criteria indicate that biolumine-scencehas been independently evolved many times. Marine animals are unusual, however, in that many species in at least seven phyla use the same luciferin. This compound is known as coelenterazine because it was first identified in jellyfish (coelenterates) and its molecular struc-

ture is derived from a ring of three amino acids (two tyrosines, and a phenylalanine). Nevertheless, many other marine organisms use different luciferins. In some animals (e.g., jellyfish) the luciferin / luciferase system can be extracted in the form of a stable "photoprotein" that will emit light when treated with calcium.

5.5

|Microorganisms

Bioluminescent organisms are found in all of the oceans of the world and at all depths. The prevalence of the phenomenon has long been known to seafarers, as the light seen at night in the wake or bow wave of their vessels. Three kinds of single - celled marine organisms include species that produce light, namely bacteria, dinoflagellates, and radiolarians, all with different luciferins. Individual luminous bacteria do not luminesce unless there are a lot of them together - colonies therefore become bright. This is because luciferase production is switched on only by the accumulation in the environment of a critical concentration of a chemical released by the bacteria (an autoinducer). Luminous bacteria are to be found free in the ocean but are more commonly encountered as glowing colonies on either marine snow or fecal pellets, or, as luminous symbionts, in the light organs of some fish and squid (see below). There are many species of luminous dinoflagellates and they are the usual cause of sea surface luminescence, visible in the bow wave or wake of a boat or the turbulence caused by a swimmer, whether man, fish, or dolphin. They can accumulate in dense "blooms," some dense enough to be recognized as red tides, and individual dinoflagellates flash when subject to sufficient shear force (e.g., in turbulence). Because they live close to the surface, their light would be invisible by day. In fact most species have a circadian rhythm that conserves the luminescence by turning it off during the day. These organisms, and probably the radiolarians too, defend themselves against planktonic predators by their flashing, which has the added "burglar alarm" benefit of alerting larger predators to the presence of the original grazer. P. J. Herring, Southampton Oceanography Centre, Southampton, UK E. A. Widder, Harbor Branch Oceanographic Institution, Fort Pierce, FL, USA

Plankton/ 8.Semester / Yulia Zvezdonkina/Gina Mรถnch & John Russo/2012

Plankton Viruses Bacteriaplankton Protozoa,Radiolarians Copepods Gelatinous Zooplankton