Echinoderms are an exclusively marine group and there is no fossil evidence of any exception to this, making them the largest animal phyla to lack any freshwater or terrestrial representatives. They occupy nearly all depths and habitats in the sea, mainly on or in the sea bed, where they often form a major proportion of the biomass. They are among the most distinctive of all animal phyla and their main features are a calcitic skeleton composed of many plates (ossicles), a water vascular system used in locomotion, respiration, feeding and some sensory functions and five-fold radially symmetrical (pentaradia) body organization at some stage in their life.
There are approximately 100 species in the European area and they are arranged into five well-defined groups. Their larvae can be very common in plankton samples, especially those of sea urchins, starfish and brittle stars.
|Back to top|
Echinoderms usually have separate sexes, with a few exceptions among the asteroids, holothurians and ophuroids. The breeding season is mainly spring and summer and reproduction is generally through release of gametes into the water column and indirect development through a variety of larval stages. In some species of each class the females produce yolky eggs from which non-feeding, lecithotrophic larvae develop. Additionally, a few species brood large yolky eggs until they hatch as a small version of the adult.
Reproductive strategy and subsequent larval development within the Echinodermata is very varied, often with a number of species in each class/subclass differing in their strategies from the others. This makes a concise summary of larval development difficult, not helped, as pointed out by McEdward & Miner (2001), by the inconsistent terminology used between classes by different authors, especially for the non-feeding larvae with simple morphology. The various types of echinoderm larvae have been given individual names and while some types are particular to one class/subclass (Table 1), others are found in more than one group, making even identification to a particular group problematical to the non-specialist.
Larvae do not resemble the parent and are generally bilaterally symmetrical, even though they metamorphose into radially symmetrical adults. Many are planktotrophic, feeding on unicellular algae and particulates, using bands of cilia that run over their bodies. Some have spots or bands of pigment, usually only visible in fresh specimens. They spend a few weeks in the plankton and then settle over a short period. For those with indirect development, metamorphosis is typically very radical and may start before or after settlement.
Many of the larvae are small and delicate so will not survive sampling and preservation well, while some others are brooded or benthic, so the majority of echinoderm larvae found in plankton samples will be of a restricted number of types. Because some larval types are found in more than one group, larval types are sequentially described, rather than giving developmental information individually for each class/subclass.
Echinoderm larval types
Bipinnaria and brachiolaria larvae only occur in Asteroidea (starfish). Asteroids with small, non-yolky eggs have a free-swimming, feeding, bipinnaria larva that has two unconnected ciliated bands, extending over numerous lobes that later develop into hollow arms (Figure 1A-C), unsupported by skeletal rods. One of the ciliary bands is much longer than the other and loops over most of the body, while the other is short and restricted to a small area of the body (Figure 1A, B). The bipinnaria superficially resemble the auricularia larva of holothurians (Figure 4A), but the ciliary band in the auricularia is continuous and not in two parts. Some species metamorphose directly to a juvenile from the bipinnaria stage, while other bipinnaria become a brachiolaria (Figure 1D, E), which is a further developmental stage rather than a separate larval type. Luidia ciliaris has the largest bipinnaria and brachiolaria larvae of European species (Figure 1C), probably because it spends many months in the plankton before metamorphosis.
Figure 1. Asteroid bipinnaria and brachiolaria larvae: A) Early bipinnaria larvae; B) Later bipinnaria; C) Bipinnaria of Luida ciliaris; D) Early brachiolaria larva; E) Lat brachiolaria. (A-B from Mortensen 1913; C,E fom Mortensen 1901; D from Treegouboff & Rose 1957).
The bipinnaria/brachiolaria transformation begins with the appearance of a single dorsal and two ventral stubby brachiolar arms (Figure 1D, E), the only feature that distinguishes the two larval types. These have papillae on their tips that are used by the larva to test the substrate, but also produce adhesive secretions used in temporary attachment to the substrate. There is also an adhesive disc situated between the arms for more substantial attachment. The brachiolar arms are less obvious among the other arms in later larvae. Some asteroids with large yolky eggs have a non-feeding, pelagic brachiolaria stage. These morphologically simpler larvae lack ciliary bands and arms, but have obvious brachiolar arms (Figure 2B) and fall into the general larval type of vitellaria.
In both bipinnaria and brachiolaria stages, metamorphosis starts in the plankton and an obvious juvenile starfish develops on the larva (Figure 1E). The arms of the juveniles tend to be more rounded and less projecting compared to juvenile ophiuroids. Some of the longer arms begin to shorten as they are reabsorbed. Most brachiolaria larvae need to settle and attach to the substrate before metamorphosis can continue. The benthic juvenile then detaches from the larval body.
Vitellaria - barrel-shaped larvae (Asteroidea, Crinoidea, Ophiuroidea, Echinoidea and Holothuroidea)
Barrel-shaped and ovoid larvae of various types occur in all the echinoderm groups, but the momenclature used for the types has not been consisten amoung authors. McEdward & Milner (2001) suggest that all simple, non-feeding larvae, regardless of body form, be called vitellaria and vitellaria that have one or more transverse ciliary band should be termed doliolaria (Figure 3). Most vitellaria have a simple barrel-shaped body form, mainly uniformly ciliated (Figure 2A). Some examples of vitellaria are yolky brachiolaria (Figure 2B) and uniformly ciliated barrel-shaped larvae of asteroids, reduced echinoplutei (Figure 2C) and the simple cilliated larva of echinoids, uniformly ciliated barrel-shaped larvae of crinoids and holothuroids and reduced ophioplutei and uniformly cilliated, barrel-shaped larvae of ophiuroids. Vitellaria can be brooded, bnthic or free-living, with direct or indirect development. Most are small and delicate, would not survive net sampling and preservation well, so will rarely be encountered during routine plankton sampling. Identification, probably event to group may require a specialist.
Figure 2. Examples of vitellaria: A) Holothurian uniformly ciliated larva; B) Yolky asteroid brachiolaria; C) Reduced echinopluteus. (A after Strathmann 1987; B after Hyman 1955; C) after Raff 1987).
Doliolaria (Crinoidea, Ophiuroidea and Holothuroidea)
Doliolaria are barrel-shaped, non-feeding larvae with one or more transverse ciliary bands (Figure 3A), so named because of their superficial resemblance to the pelagic tunicate Doliolum. These larvae occur in Crinoidea, Ophiuroidea and Holothuroidea, but it is unclear if the doliolaria of the three groups can be separated on morphological features. They are usually only in the plankton for 2-8 days and metamorphose on settlement.
Crinoidea (sea lilies and feather stars) are the only echinoderm class that does not have any larvae that feed in the plankton. In free-spawning species a barrel-shaped, uniformly ciliated vitellaria larva emerges from the egg. The epidermis then transforms into regions with and without cilia, resulting in a single, locomotory ciliary band, looping over and around the body, similar to that found in other echinoderm larvae, such as the auricularia (Figure 4A). Within a few days longitudinal parts of the band disappear, leaving a series of 4 or 5 circular bands and an apical tuft (Figure 3A). This doliolaria stage is typical of most crinoids and is probably the only crinoid larva that is likely to be caught in plankton nets. Later in larval life the first band may become broken in the ventral region, or displaced posteriorly, by the formation of the adhesive pit, part of the complex used in attachment to the substrate prior to metamorphosis. The second ciliary band is displaced posteriorly by formation of the vestibule, also on the ventral surface. The vestibule is an ectodermal invagination that is the future site of the mouth and emergence of the primary tube feet during the early stages of metamorphosis. Internally the skeleton can be well developed, consisting of a number of perforated calcareous plates. Some crinoid species brood eggs and embryos and release fully formed doliolaria larvae. The doliolaria attaches to the substrate by the attachment disc, which develops from the adhesive pit, and metamorphoses into the stalked cystidean stage.
In ophiuroids, yolky eggs (lecithotrophic development) are the commonest means of reproduction, but many of the larvae produced are brooded or benthic, so will not be caught in plankton nets. However, some species produce free-swimming, non-feeding doliolaria with 4, sometimes 3 ciliary bands.
In some holothurians the auricularia larva (Figure 4A) transforms into a non-feeding doliolaria larva (Figure 3B, C), which is a transitional, metamorphic stage prior to the protrusion of the 5 primary tentacles from the vestibule and transformation into the pentactula settlement stage (Figure 4C). Skeletal plates or ossicles of various shapes may be seen in the body, such as wheel shapes (Figures 3B, 4B). In other species with lecithotrophic development the initial larva is a uniformly ciliated barrel-shaped vitellaria (Figure 2A), which in some species transforms into a doliolaria with 2-5 transverse rings. Parts of the larva may retain the uniform ciliation (Figure 3C). These also transform into a pentactula.
Figure 3. Doliolaria larvae: A) Crinoid doliolaria; B-C) Holothurian doliolaria. (A-B from Tregouboff & Rose 1957; C from Mortensen 1901).
Holothurians are generally the least common echinoderm group in the area. From small eggs may develop a planktotrophic, bilaterally symmetrical auricularia larva with an elaborate ciliated band extending around projecting lobes (Figure 4A). The lobes can become very numerous, but never develop into distinct larval arms as in the later bipinnaria larvae of asteroids or plutei of echinoids and ophiuroids. The auricularia superficially resembles the bipinnaria of asteroids, but the ciliary band is a continuous loop over the body, while in the bipinnaria of asteroids there are two unconnected loops, one smaller than the other (Figure 1A, B). Later auricularia stages may already have developed skeletal plates (ossicles) dotted all over the body. These small plates are variable in shape, in some groups resembling cart wheels (Figure 4B), but in others are irregular perforated plates or branching structures. These would not be found in larval asteroids. The auricularia transforms into a non-feeding doliolaria larva (Figure 3B, C), which then transforms into a pentactula larva with 5 primary tentacles (which develop into the ring of tentacles surrounding the mouth in adults) and 1 or 2 primary feet (Figure 4C, D). This is the settlement stage, but it may remain in the plankton for some time before metamorphosing into a juvenile.
Figure 4. Holothurian auricularia and pentactula larvae. A) Auricularia; B Wheel ossicle; C) Early pentactula, D) Late pentactula. (A-B from Mortensen 1901; C after Newell & Newell 1963; D from Thorsen 1946).
Sea urchins are typically broadcast spawners, producing small eggs that in the majority of species develop into a planktotrophic echinopluteus larva (Figure 5A). Echinoplutei are bilaterally symmetrical and have a series of paired arms that mainly project anteriorly, although some may project laterally or posteriorly. The arms are supported by a calcareous skeleton and are usually long and slender, but may be short and broad. There is a band of cilia forming a continuous loop over the body and arms, used in feeding and locomotion. In the older larvae of some species, lobes called epaulettes bearing longer cilia used in locomotion may develop toward the posterior body (Figure 5B). Echinoplutei initially usually have 1 pair of arms then 2 (Figure 5C) and when fully developed there may be up to 6 pairs of varying length (Figure 5D), but typically 5 or 4 pairs (Figures 5A, B). In the echinoplutei of two groups, the irregular urchins or heart urchins (Spatangoida) and in some members of the Diadematoida, there is a single, posterior projecting arm (Figure 5D). Echinoplutei of some orders have skeletal rods that are fenestrated (perforated along their length; Figure 5A). There are a few species with bizarre echinoplutei e.g. two pairs of arms, or with a long posteriolaterally directed pair of arms (Figure 5E).
Figure 5. Echinoplutei larvae. A) Echinopluteus; B) Late echinopluteus; C) Early echinopluteus; D) Spatangoida echinopluteus; E) Bizarre echinoplutei; F) Metamorphosing echinopluteus. (A, D from Mortensen 1901; B-C from Trégouboff & Rose 1957; F from McBride 1903).
Echinoplutei larvae superficially resemble the ophioplutei larvae of ophiuroids (Figure 6A) and similar nomenclature is used for their arms, because the arrangement appears similar. However, the arms are not strictly equivalent in the two groups. Both groups generally have 4 pairs of arms, but most echinoplutei do not have arms corresponding to the pair of longer posterolateral arms of ophioplutei that extend laterally from the larval anterior/posterior axis. When these are present in echinoplutei they are either short processes (Figure 5A), or longer, but still shorter than most of the other arms (Figure 5D). The longest arms in advanced echinoplutei are the pairs of post-orals and posteriodorsals that extend dorsally and ventrally from the larval anterior/posterior axis (Figure 5A). The skeleton in echinoplutei is usually more complex than in ophioplutei. Additionally, the bodies of echinoplutei are generally laterally flattened, while ophioplutei bodies are more dorso-ventrally flattened.
Echinoplutei may spend from weeks to months in the plankton before metamorphosis. In late larvae, tube feet may be seen forming round the skeleton (Figure 5F). Juvenile urchins may also be taken in plankton samples, when the spherical shell, spines and tube feet are obvious.
Some species produce yolky, non-feeding echinoplutei larvae with simpler morphology than other echinoplutei and spend a shorter time in the plankton. These reduced plutei have 1-2 pairs of larval arms (Figure 2C), lack ciliated bands and are classified as vitellaria larvae.
Brittle stars are generally the most numerous echinoderm in the European area. Those releasing non-yolky eggs have a planktotrophic, bilaterally symmetrical, ophiopluteus larva. Ophioplutei generally have 4 pairs (occasionally 5 or 6) of arms, supported by delicate, calcareous skeletal rods (Figure 6A). A continuous band of cilia follows the contours of the arms, used in locomotion and feeding. The larvae typically swim with the arms pointed forwards. Some have very long thin arms and compact bodies (Figure 6A) while others have fleshy squat arms (Figure 6B). Red pigment cells are often present, scattered over the body.
The initial larval body is triangular and the skeletal rods can be seen internally. The two posterolateral arms develop first and are longer (Figure 6C) to much longer (Figure 6A) than the other arms and extend laterally. Each half of the larval skeleton comprises rods supporting the arms and an anchoring body rod positioned at the posterior end of the body (Figure 6A), generally with end and transverse rods connecting it to the corresponding parts on the other side of the skeleton. At least one ophiuroid species (Ophiura ophiura) has fenestrated skeletal rods (Figure 6C), but they are solid in most species. In some advanced larvae, ciliated lobes used in locomotion called epaulettes are located at the junction between the posterolateral and post-oral arms.
Ophioplutei larvae superficially resemble the echinoplutei larvae of echinoids (Figure 5A) and similar nomenclature is used for their arms, because the arrangement appears similar. However, the arms are not strictly equivalent in the two groups. Both generally have 4 pairs of arms, but there appears to be less variation in body form and number of larval arms in ophioplutei and the skeleton is generally less complex. The pair of longer posterolateral arms that extend laterally from the larval anterior/posterior axis (Figure 6A) are not found in most echinoplutei and when present are short (Figure 5A, D). Additionally, the bodies of ophioplutei are generally dorso-ventrally flattened, while echinoplutei are often more laterally flattened.
Figure 6. Ophioplutei larvae. A) Slender ophiopluteus; B) Stubby ophiopluteus; C) Ophiopluteus with fenestrated rods, Ophiura ophiura; D) Metamorphosing ophiopluteus; E) Metamorphosing Ophiothrix fragilis. (A-C, E from Mortensen 1901; D from Trégouboff & Rose 1957).
Metamorphosis starts while still in the plankton. The minor larval arms are reabsorbed into the juvenile rudiment in the centre of the pluteus body (Figure 6D) and eventually only the two posterolateral ones remain, very obviously in some species (Figure 6E). Metamorphosis is rapid and the juvenile brittle star with well developed arms, skeletal plates and several sets of tube feet, casts off the remaining pluteal arms before settling to the bottom. The arms of the juveniles tend to be more projecting and less rounded compared to juvenile asteroids. In some species the posterolateral arms remain functional and a second juvenile develops.
Yolky eggs (lecithotrophic development) are the commonest means of reproduction in ophiuroids, but many of the larvae produced are brooded or benthic, so will not be caught in plankton nets. Some of these eggs develop into non-feeding ophioplutei with 1-3 pairs of arms, or armless larvae with vestigial pluteus structures. These are classified as vitellaria larvae.
Mesogen (Echinoidea, Asteroidea and Ophiuroidea)
Mesogen larvae are a type reported from a few echinoids, asteroids and ophiuroids. They are a direct developing larva that may be brooded or pelagic, lack the typical larval body plan or metamorphosis and have unique development (Figure 7). They vary in appearance and at least some are not even bilaterally symmetrical. They are rare so are unlikely to be sampled and may not even occur in European waters.
Figure 7. Mesogen larva (After Kaufman 1968).
Further information: Balser 2002; Byrne & Selvakumaraswamy 2002; Emlet et al. 2002; Geiger 1964; Larink & Westheide 2006; McEdward et al. 2002; McEdward & Miner 2001; McEdward et al. 2002; Newell & Newell 1963; Sewell & McEuen 2002; Smith & Johnson 1996; Southward & Campbell 2006; Todd et al 1991.
|Back to top|
Coloured areas: abundance (scale is log10 (x+1)); blank areas: no sampling, or no presence data recorded; open circle: species never recorded; black diamond: only 1 presence; +: > 1 presence data.
Data from Continuous Plankton Recorder Survey, 1958-1999.
Reproduced from Beaugrand et al, 2004.
|Back to top|