M. squamiger is a relatively small (up to 4 cm) solitary ascidian. It has a leathery, tough tunic of brown to reddish colour, with wrinkles and often covered by epibionts. The internal layer of the tunic is softe...
M. squamiger is a relatively small (up to 4 cm) solitary ascidian. It has a leathery, tough tunic of brown to reddish colour, with wrinkles and often covered by epibionts. The internal layer of the tunic is softer and purple in colour. Two siphons are concealed in contracted individuals.
It is considered native to Australia, but has spread worldwide in temperate waters. It was first recorded as introduced in the Mediterranean Sea in the 1960s (as M. exasperatus), and it is now abundant in all of the western Mediterranean as well as in the eastern central Atlantic (Iberian Peninsula, Madeira, Canary Islands). It was detected in Californian waters from the 1980s, and in South Africa in 2001, Mozambique in 2002, and India in 2007.
It its native range the species lives on rocky substrata and also on artificial substrata. In the introduced range the species is found mostly inside marinas, harbours and aquaculture facilities forming dense aggregates. It can, however, colonize adjacent natural communities, forming dense crusts that can outcompete native species, hence its consideration as an invasive species.
Described as Microcosmus claudicans subspecies squamiger by Michaelsen in 1927. The authorities are often incorrectly given as Hartmeyer and Michaelsen 1928, which is a posterior article. It is the same that was named as Microcosmus exasperatus subspecies australis by Michaelsen (1908), but not the Microcosmus australis sensu Herdman.
It has been repeatedly confused in the recent literature with Microcosmus exasperatus in European waters.
The individuals are globular in shape, up to 4 cm (normally less than 3 cm) in maximal dimension. They are surrounded by a hard and tough tunic. The external colouration ranges from brown to reddish, and they are often totally or partially covered by epibionts (See Pictures).
The inner tunic is softer and with purple tones. The mantle is orange coloured and strongly muscular. The two siphons are short, the buccal one in the antero-dorsal tip of the tunic, the atrial one in the posterior quarter of the animal. The inner tunic of the siphons bears short siphonal spines (0.01-0.02 mm long) of characteristic scale-like shape (See Pictures), hence the specific name.
Internally, the most prominent feature is the branchial sac, which is folded (See Pictures). There are more than 8 folds at least on one side. The number is variable, but normally the ventral-most fold in each side is not complete, and the next fold may also be so. There are normally one to two more folds on the right side than on the left. There are 15-25 longitudinal vessels on the folds, and one to two between the folds. In the oral part of the branchial sac there are stout, branched tentacles variable in number (more than 20). The opening of the neural duct forms a “U” directed anteriorly, with both extremes coiled into spirals (with more than two turns each).
The gut lies on the left side, and forms a narrow loop which reaches up to two thirds of the body length (See Pictures). The stomach is covered by the hepatic gland whose surface forms lamellae covered with small papillae. The intestine is narrow and forms a secondary loop as the main loop bends towards the ventral side. The anus opens close to the atrial siphon.
There is a gonad on each side, clearly divided in blocks. There are usually four blocks in the right gonad and three blocks in the left gonad, the distal-most one located inside the primary curve of the intestine, and the other in the secondary curve.
Larvae have been obtained by artificial fertilization (Rius et al., 2009a), they measure up to 1.3 mm, with a short trunk and well-developed tail. The larvae lack an ocellus, and there is only one pigmented spot in the sensory vesicle, corresponding to the statocyte.
It is accepted that the species is native to Australia. From there it has spread to other parts of the world. Genetic data confirmed an Australian origin for its worldwide distribution (Rius et al., 2008a). The species is found in warm temperate seas, mostly of Mediterranean climate.
Confusion between this species and M. exasperatus has made it difficult to ascertain its distribution, particularly in European waters. All reports prior to the 1990s must be revised. Turon et al. (2007), using material lodged in Museums and new collections, confirm that M. squamiger is now abundant in the western Mediterranean and Atlantic southern Europe (Spain, Portugal, Canary Islands, Madeira Islands).
There is a very old record of the species in the Gulf of Suez (Michaelsen, 1919). This record has been confirmed by examination of specimens from the Hamburg Museum (Turon et al., 2007). The possibility that the species is native and not introduced in the Indian Ocean should be kept in mind given the antiquity of this record and the lack of faunistic data on the eastern African coast until very recently. Recent reports in ports of South Africa and India; however, undoubtedly correspond to introduced populations.
The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.
The oldest introduction seems to be in the Mediterranean Sea, probably starting in ports in North Africa (Monniot, 1981). The first report was from Tunisia (1963), and then Italy, France and Spain, where the species was observed in the 1970s (Zibrowius, 1974; Ballesteros, 1978; Monniot, 1981). More recently, from the 1990s onwards, the species has been reported in the Atlantic waters of the Iberian Peninsula, Canary Islands and Madeira (Naranjo, 1995).
In the eastern Pacific, the species was first observed in southern California harbours in 1986, and then it spread to all major southern California harbours (Lambert and Lambert, 1998). Some years later, the species is well established and abundant in most southern Californian harbours, its distribution seemingly limited to south of Conception Point (Lambert and Lambert, 2003).
The species has been reported from Hawaii by Godwin (2003), but that author reports the species on the hull of a ship coming from California, with no indication on whether it has successfully established in the area, so it cannot be considered so far as present in Hawaii.
In South African ports on the Indian Ocean coast the species has been recorded only from 2001 (Monniot et al., 2001), and it is now abundant in the harbours of the south eastern littoral (M Rius, University of Cape Town, South Africa, personal communication, 2009). Finally, the species has been very recently recorded from Mozambique (Monniot, 2002, Ibo Island) and the southwest coast of India (Abdul and Sivakumar, 2007, from harbour installations).
There are no data that allow tracking of the exact routes of spread of M. squamiger, although it seems reasonable to assume, given the history of reports, that it was introduced first to the Atlanto-Mediterranean region, later on to California, and more recently to South African ports and India. The lack of faunistic studies over time for these zones and taxonomic uncertainties hinder a definitive assessment. For instance, Millar (1955; 1962) recorded M. exasperatus from South Africa, and it is not clear if these reports were in fact a misidentification of M. squamiger (Monniot et al., 2001).
In the only phylogeographical study of the species to date (Rius et al., 2008a), two main results were substantiated: first, that the origin of the worldwide distribution was in southeast Australia, which is also where the biggest ports and more intense ship traffic are found in the area; second, that the colonization process was likely not independent. Thus the species may have “jumped” from one place to another, possibly repeatedly, given the high genetic diversity found in introduced populations. Ascertaining the exact sequence of the colonization process will require the study of more informative genetic markers such as microsatellites, already developed for this species (Rius et al., 2008b).
In the introduced range the species is present in harbours, marinas, oyster farms and other man-made structures. In Australia it lives both on natural and artificial substrata (Kott, 1985). However, in some places in the introduced range M. squamiger can also live outside harbours, colonizing adjacent natural communities and outcompeting native species (e.g., Spain, Turon et al., 2007; South Africa, M Rius, University of Cape Town, South Africa, personal communication, 2009).
The spread is undoubtedly not deliberate and related to ship traffic and human activities such as aquaculture. It is not clear whether the larvae of this species, which are short-lived as is characteristic of ascidians (Rius et al., 2009), can survive in ballast waters. However, the adults are found among hull fouling (Godwin, 2003). Big ships can mediate the dispersion to new areas, and small recreational vessels can contribute to its spread in new ranges.
It is also likely that the species can be introduced in relation to bivalve farming, although no instance has been reported. Although it is not listed, to our knowledge, as a pest, M. squamiger is a nuisance in oyster farms in Australia (Kott, 1985) and California (L Rodriguez, University of California, USA, personal communication, 2009).
It seems unavoidable that the species continues its spread, probably limited only by environmental conditions. For instance, in several places there is a well marked northern limit to its distribution (Lambert and Lambert, 2003), and the species has not been reported either from latitudes below 9-10°, so temperature may be a key factor regulating where the species can establish successful populations.
M. squamiger is found in shallow littoral communities; the highest abundance is from the water line down to 10 m, although it has been recorded down to 35 m (Kott, 1985). In the native range (Australia), the species is found on rocky substrates, on concrete, on cave walls and in both sheltered and exposed habitats (Kott, 1985). In the introduced range it is always found on artificial structures or on nearby rocky substrata in shallow waters (Ramos-Esplá, 1988; Lambert and Lambert, 2003; Turon et al., 2007). In the introduced range it usually forms dense aggregates (See Pictures), which can exist also in the native area (Kott, 1985). Densities up to 2300 individuals per square metre have been reported (Rius et al., 2009b). Naranjo et al. (1996) pointed out that M. squamiger can be considered as indicator of perturbed areas subject to sedimentation, pollution and water stagnation stresses. Lowe (2002) highlighted the ability of M. squamiger to withstand reduced salinity conditions which can be found in periods of high rainfall in California harbour habitats.
The genetics of this species have been extensively studied. Genetic information on M. squamiger is available in public databases (such as GenBank) as cytochrome oxidase subunit I sequences that can be used as barcodes for species identification. Partial sequences of the 18S gene, as well as microsatellite clones, are also available. The genetic dataset in GenBank has been used to study the dispersal of this species worldwide and as such is very useful for studying the invasion pathways of this species.
The only studies to date on the biology of M. squamiger have been performed in the northwest Mediterranean, in the introduced range of the species (Rius et al., 2009b). No data are available for Australian populations. It will be necessary to compare the biological cycles of the species between the native and introduced populations, and across the latitudinal gradient.
M. squamiger is a simultaneous hermaphrodite and broadcast spawner, both eggs and sperms are released into the water column where fertilization and embryonic development occur. The potential for reproduction is very high, as typical of organisms that broadcast huge quantities of gametes. The embryos hatch as tadpole larvae, which do not feed and have to settle in a matter of hours before exhausting their reserves. Under laboratory conditions at 20°C, embryonic time is less than 14 h and free-swimming time is less than 24 h (Rius et al., 2009a).
In the Mediterranean, the gonad indices (See Pictures) and gonad histology show that the species has a seasonal reproduction with peak gonad development in summer and a major spawning episode at the end of summer. The pattern of biomass follows a similar trend (See Pictures), with a minima after summer, which are due to the death of old individuals while the new recruits are still too small to be observed. The study of size-frequency structure over time indicates that the species has a two-year cycle, in which specimens recruit after summer, grow to maturity during the next winter and spring and remained in the population until summer of the following year, disappearing thereafter (Rius et al., 2009b).
As all ascidians, M. squamiger is a filter-feeder that captures particles down to bacterial sizes using a mucous secretion of the endostylar gland. The filtering organ is the enlarged pharynx (branchial sac) which bears numerous minute slits whose rims are covered by powerful cilia. The movement of these cilia keeps the water flowing from the buccal siphon to the atrial siphon passing through the perforated pharynx where particles are retained and passed down, embedded in a mucus string, to the gut.
The tunic of the species is commonly covered by epibionts, often leaving only the open siphons visible. The epibiotic community of species of M. can be very complex (Monniot, 1965), and consists mostly of algae, hydrozoans, bryozoans, and other ascidians. These epibionts do not cause any harm to the ascidian, and may help conceal it to predators.
M. squamiger seems to prefer eutrophicated habitats of strong turbidity (Naranjo et al., 1996), at least in the introduced populations. It can withstand pollution, stagnation, and low salinities (Naranjo et al., 1996; Lowe, 2002), making it a typical fouling species able to thrive in many disturbed habitats.
Natural enemies of ascidians include fish, gastropods, crabs, flatworms and sea stars (Monniot et al., 1991). For solitary ascidians with hard tunics, as is the case of M. squamiger, boring gastropods are the main predators on adults. However, many other organisms can prey on juvenile stages, and indeed there is some evidence of intense mortality of recruits of this species (Rius et al., 2009a, b).
The only confirmed observations of predators in this species have been in Spain, where the native gastropod Stramonita haemastoma has adopted the introduced M. squamiger as one of its favourite sources of prey (See Pictures). Densities of Stramonita can be up to six individuals per square metre in M. squamiger beds (Rius et al., 2009). Considering that Stramonita is consumed locally as seafood, this raises an interesting possibility of using it as a pest control while gaining some profit. However, no plans have been established in this respect so far.
M. squamiger only reproduces sexually, so its natural dispersal relies on the time that gametes and embryos spend in the water column, and the free-swimming lifespan of the larvae. In general, these times are limited in ascidians (Svane and Young, 1989). In the case of M. squamiger, total time from spawning to settlement may be less than 30 h (Rius et al., 2009, under laboratory conditions). It is clear that these short times confer to this species a very restricted dispersal capability. The swimming ability of the larvae, on the other hand, is useful for substratum selection, but water currents are the main method of dispersal. It seems likely that the natural dispersal capabilities of the species are in the range of a few kilometres.
On the other hand, non-natural dispersion via ships is global. The species is able to settle on artificial substrata such as hulls of ships, possibly in places like sea chests where the conditions are less stressful, and then spawning can occur in the ports of arrival, whereby a population can be established. There is a surprisingly high genetic diversity in populations located in confined environments (Rius et al., 2008a), which indicates that transport via ships is probably recurrent in many regions of the world. The possibility of transport related to aquaculture activities must be kept in mind, too, although no instance has been described so far.
The economic impact of M. squamiger is mainly due to its interference with oyster cultures, where it competes for food and space. This has been reported only for Australia (Albany and Tasmania, Kott, 1985) and California (L Rodriguez, University of California, USA, personal communication, 2009), but is likely to be widespread when the species coexists with bivalve cultures.
The fouling capacity of M. squamiger can also have an impact on immersed structures, pipelines, and refrigeration filters, although this has never been formally reported.
There is an impact of M. squamiger on the natural environment in the introduced areas, when the species spreads outside harbours and confined environments. While not common, there are instances reported in the Mediterranean (Turon et al., 2007) and South Africa (M Rius, University of Cape Town, South Africa, personal communication, 2009). When this happens, dense populations can be found in shallow waters, basically carpeting the substrate available and outcompeting other species. So far this impact seems to be quite restricted to particular places, and no protected area has been threatened. On the other hand, the species forms crusts with many interstices and spaces available, so it is a “structure-forming” species. This can enhance abundances of some other organisms. A formal comparative study of the diversity in M. squamiger-dominated communities and equivalent non-altered communities is lacking.
Competition is intense for substratum in the communities where M. squamiger is abundant, and there is a report of the detrimental effects of recruits of another fouling ascidian, Styela plicata, on the survival and growth of M. squamiger (Rius et al., 2009a).
The species can be confused in the field with other solitary ascidians commonly found as fouling on artificial substrata. It is easily distinguished from Ciona intestinalis, Corella eumoyota and Ascidiella aspersa because they have translucent and soft tunics. Styela clava is stalked and can therefore be easily distinguished. M. squamiger can potentially be confused with Styela plicata, particularly when the latter’s tunic (which is whitish) is covered with epibionts and debris. However, Styela plicata has big, round protuberances in the tunic, very different from the lightly wrinkled surface of M. squamiger. In case of doubt, dissecting the specimens will easily solve it: Styela has only four folds per side in the branchial sac.
The more problematic confusion is with its congener M. exasperatus. The main difference between both species lies in the siphonal spines, which are scale-shaped in M. squamiger and pointed in M. exasperatus (See Pictures). However, observation of this character is not easy for non-specialists. A fragment of the inner tunic of the siphons has to be obtained and observed under the microscope. Other characters that can help telling one species from the other are also difficult to discern for non-specialists: M. exasperatus has a more pronounced secondary loop, branchial folds lower and more separated (with up to four longitudinal vessels in between) and less coils in the “horns” of the neural opening. Overall, advice from a specialist should be sought when in doubt to avoid spreading further the existing confusion between these species.
Management of this species is highly problematic. As its main means of dispersal is by ships, its entrance in harbours is almost inevitable. Regulations concerning ballast water can be of little use if, as suspected, the species uses mostly ship hulls and sea chests for its transport.
It seems that in most cases M. squamiger will be contained within confined areas (harbours, bays, estuaries), so no particular action would be required, as these are highly altered habitats, and its competitors would be mostly other introduced species. However, monitoring and surveillance of the species abundance and spread are necessary. The surveys conducted in Californian habours over many years (Lambert and Lambert, 1998; 2003) should be followed in other regions.
In cases where the species is found on natural substrata in the introduced areas, eradication is hardly an option given the abundances observed and the small size of the individuals. Mitigation due to the action of local predators such as gastropods is suggested. It has been mentioned that some of these predators are marketable, and a profitable fishery of native gastropods can be set up in zones where M. squamiger has been introduced.
Other species of M. (and other genera of Pyuridae) have been traditionally consumed as seafood in some countries. However, the small size and the type of habitat where the species occurs make it highly unlikely that it can be marketed in the future. The possibility remains, though, of using its flesh for other purposes, such as bait (as done with other ascidians) or as food for other animals. None of these possibilities has been formally analysed, nor have any eradication or control plans for this species been setup to our knowledge (X Turon, Center for Advanced Study of Blanes, Girona, Spain, personal communication, 2009).
Future research concerning this species should focus on monitoring communities in the vicinity of harbours and bays where the species is known to occur. There is a lack of knowledge on the biology of the species, which has been studied only in one of its areas of distribution. In particular, comparisons of the biological parametres in the native and introduced populations, and over the latitudinal range where the species live, are necessary. In introduced populations, interactions with local predators should be analyzed carefully.
Genetic studies with highly polymorphic markers are also necessary to reconstruct the history of the introductions of this species and to track their sources.