Teredo navalis

Invasion History

First Non-native Panama (Caribbean) Tidal Record: 1960

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Panama Invasion History:

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Invasion history elsewhere in the world:

As discussed above, the native region of T. navalis is unknown. We regard it as cryptogenic in the northeast Atlantic and Indo-Pacific. In the northeastern Atlantic, it occurs in the Black and Mediterranean Seas, and along the European coast north to Norway, Iceland, and the Faroe Islands. It occurs in the Baltic Sea as far as eastern Germany (Nair 1959; Kristensen 1979; Reise 1999; Hoppe 2002; Borges et al. 2010; Sen et al. 2010; Didziulis 2011; Borges et al. 2014). The occurrence of catastrophic outbreaks in dikes in the Netherlands in the 18th century suggested to people at the time that it may have been introduced (Sellius 1733, cited by Hoppe 2003), but the occurrence of shipworms in the Mediterranean has been known since ancient times. In the 16th century, attacks by shipworms on ships of the Spanish Armada in French and Portuguese harbors may have contributed to the collapse of the attack on England (Hoppe 2002).

In the Western Atlantic, introduced populations of T. navalis are established in temperate and subtropical waters, including Florida, Bermuda, southern Brazil and Argentina, but records are scarce in tropical waters (Brown 1953; Wallour 1960; Junqueira et al. 1989; Martins Silva et al. 1988; Museum of Comparative Zoology 2007). In the Eastern Atlantic, this shipworm may have been one of the earliest invaders to South Africa, but the first published records are from Cape Town and Port Elizabeth in the late 1800s (Noble 1886, cited by Mead et al. 2011a; 2011b).

In the Indo-West Pacific and northwest Pacific, we consider T. navalis to be cryptogenic. In tropical waters, such as India (Pati et al. 2012), its records are scattered, and it co-occurs with a large number of tropical species (Wallour 1960; Turner 1966; Museum of Comparative Zoology 2008; U.S. National Museum of Natural History 2013). It appears to be more common in the northwest Pacific, where it is common and widespread around China, Japan, Korea, and north to the Vladivostok region of Russia (Turner 1966; Golikov et al. 1976; Tsunoda 1979; Huang 2001).

In the southwest Pacific, T. navalis is apparently introduced to the southern coast of Australia. As in other regions, it was probably introduced at a much earlier date, but it was first reported from Port Jackson, Sydney in 1928, as T. austini (Iredale 1928, cited by Turner 1966). To our knowledge, it has not been reported from New Zealand.

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Description

Teredo navalis belongs to the family Teredinidae (shipworms), which are highly modified mollusks, hardly recognizable as bivalves, adapted for boring into wood. The shell is reduced to two small, ridged valves, which cover the head and are used for grinding and tearing wood fibers. The body is naked and elongated, and ends with two siphons, protected by elaborate calcareous structures called pallets (Turner 1966).

The shell of T. navalis, like those of other species, has three subglobular lobes. The smallest of these is the auricle, which is semicircular and subtriangular. The interior of the shell has a long curved process (styloid apophysis). The pallets are variable, but have a relatively short stalk, shorter than the cap, and lack a transverse ridge. The distal margin of the inner face is slightly to moderately concave, while the outer face is excavated at the tip, forming a U-shape. The distal third of the cap is made of periostracum, which is pale yellow, covering the distal half and extending to form narrow distal margins. Variability in the shells and pallets has led to many specific names (e.g. Bartsch 1923; Turner 1966), which are now treated as synonyms. Description from: Turner 1966; Turner 1971; Abbott 1974; Coan et al. 2000; NIMPIS 2013.

Veligers of T. navalis have a typical D-shape on release, at ~70-90 μm length. Initially their length exceeds their height, but they become proportionately taller, and roughly circular at ~100 μm. By settlement, the height of T. navalis veligers (~200-240 μm) exceeds the length (~190-220 μm) (Chanley and Andrews 1971; Fuller et al. 1989). Transformation and development of the larval shell into the greatly modified adult form is described by Fuller et al. (1989). Teredo navalis becomes mature at about 15 mm length, and may reach 500-1000 mm in length (Grave 1928; Mann and Gallager 1985).

Potentially misidentified species - The diversity of shipworms in tropical waters is very great, but decreases at higher latitudes. Most of the species listed below have been reported in Florida, Caribbean, West Coast, or Hawaiian waters. However, in temperate waters, many collectors historically identified all or most shipworms as T. navalis, including the Northwest Atlantic native Bankia gouldi.

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Taxonomy

Ecology

General:

Shipworms dig long burrows in submerged wood in marine environments. They burrow by rocking and abrading the wood fibers. The mantle covers most of the length of the body, and secretes a calcareous lining along the interior of the burrow. They normally have their anterior end, with head and shells inside the burrow, and their siphons protruding. The pallets plug the burrow when the siphons are retracted (Barnes 1983).

Shipworms are protandrous hermaphrodites, beginning life as male and transforming to female, but they have no capacity for self-fertilization. Males release sperm into the water column, which fertilizes eggs for the female. The fertilized eggs are then brooded in the gills. Females may produce 1-5 million eggs during a season (Grave 1928). Larvae are retained in the gills to the veliger stage (Hoagland 1986a; Richards et al. 1984). Teredo navalis releases larvae at 11-30°C. The larvae of T. navalis are planktotrophic for 11-35 days (Culliney 1975; Hoagland 1986a; Hoagland 1986b; Richards et al. 1984). They settle in the pediveliger stage, and then rapidly metamorphose and begin boring into wood within 2-3 days. They quickly develop a calcified shell, pallets, and burrow lining (Turner and Johnson 1971). Shipworms may obtain most of their nutrition from plankton (Paalvast and van der Velde 2013), but some comes from wood, which consists largely of cellulose. Symbiotic bacteria fix nitrogen, essential for protein synthesis (Turner and Johnson 1971; Barnes 1983).

Teredo navalis is known from driftwood, pilings, vessels, and other wooden structures (Verrill and Smith 1873; Richards et al. 1984; Hoagland 1986b; Hoppe 2002). Adults tolerate water temperatures from 0 to 30°C and salinities of 6 to 45 PSU (Hoagland 1986b). Humic substances in the water, derived from soil and vegetation, may cause premature settlement and interfere with site selection in T. navalis larvae. This may be one factor accounting for the scarcity of T. navalis in southeastern US estuaries, and the dominance of the more tolerant Bankia gouldi (Culliney 1975). In tropical waters, other species of Teredo and Lyrodus may be more successful at higher temperatures (Hoagland 1986b). As long as their piece of wood is intact, shipworms have few predators, but when the riddled wood disintegrates, they are rapidly eaten by fishes, crabs, and other predators. They are vulnerable to protozoan parasites, such as Minchinia teredinis, which can cause extensive mortality (Hillman et al. 1990). Populations of T. navalis and other shipworms are subject to great year-to-year variations in abundance, settlement, and resulting damage to wooden structures. These are often attributed to variations in temperature, salinity, water quality, etc., but often the causes are not clear (Nelson 1922; Brown 1953; Richards et al. 1984; Hoppe 2002).

Food:

Wood; phytoplankton

Consumers:

Protozoan parasites

Competitors:

Other shipworms, gribbles (Limnoria spp.)

Trophic Status:

Herbivore

Herb

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Habitats

General Habitat	Coarse Woody Debris	None
General Habitat	Marinas & Docks	None
General Habitat	Vessel Hull	None
Salinity Range	Mesohaline	5-18 PSU
Salinity Range	Polyhaline	18-30 PSU
Salinity Range	Euhaline	30-40 PSU
Tidal Range	Subtidal	None
Tidal Range	Low Intertidal	None
Vertical Habitat	Epibenthic	None
Vertical Habitat	Pelagic	None

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Life History

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Tolerances and Life History Parameters

Minimum Temperature (ºC)	0	Field Data: Grave 1928; Hoagland 1986a; Richards et al. 1984
Maximum Temperature (ºC)	30	Field Data: Grave 1928; Hoagland 1986a; Richards et al. 1984
Minimum Salinity (‰)	5	Field and Experimental Data: Chanley 1971; Hoagland 1986a; Richards et al. 1984
Maximum Salinity (‰)	45	Field and Experimental Data: Chanley 1971; Hoagland 1986a; Richards et al. 1984
Minimum Reproductive Temperature	11	Hoagland 1986a; Richards et al. 1984
Maximum Reproductive Temperature	30	Highest temperature for larval release (Culliney 1975)
Minimum Reproductive Salinity	9	Hoagland 1986a; Richards et al. 1984
Minimum Duration	11	Culliney 1975; Grave 1928; Turner 1971; Richards et al. 1984
Maximum Duration	35	Culliney 1975; Grave 1928; Turner 1971; Richards et al. 1984
Minimum Length (mm)	15	Minimum size at maturity (male) Mann and Gallager 1985
Maximum Length (mm)	1,000	Sizes are highly variable. Animals grew up to 193 mm in 113 days in culture (Mann and Gallager 1985). Maximum sizes in the field may reach ~1000 mm, but 370-600 are more usual maxima (Grave 1928; Kristenen 1979; Paalvast and van der Velde 2011).
Broad Temperature Range	None	Cold temperate-Tropical
Broad Salinity Range	None	Mesohaline-Euhaline

General Impacts

Teredo navalis is probably the most widespread marine wood-borer in the world, and has been a major factor in human maritime activities for many centuries. It has destroyed ships, boats, docks, pilings, buoys, and seawalls around the world (Atwood 1922; Turner 1966; Hoppe 2002). Sudden invasions, range-extensions, and population fluctuations have ravaged ports and coastlines where shipworms were previously rare or unknown (Manley 1893; Atwood 1922; Nelson 1922; Turner 1973; Cohen and Carlton 1995; Hoppe 2002). Shipworm invasions have probably also had considerable impacts on coastal habitats by speeding the breakup and recycling of wood, but this has not been studied. In addition, human attempts to protect wood against shipworm invasions, by using metals, tar, creosote, and other substances has had doubtless impacts on water quality and the biota of harbors.

Economic Impacts

Shipping - Teredo navalis and other shipworms have plagued navigators since the early days of saltwater boating and shipping. The Naval Shipworm has been especially important because of its wide tolerance to variable temperature and salinity, and its ability to survive in estuaries, coastal waters, and moderately polluted harbors. Ship hulls were often sheathed in copper or lead, treated with tar, or constructed of woods that are less palatable to the worms, including oaks and some tropical hardwoods. Pilings, wooden railroad trestles, wharves, buoys, and floats in harbors are especially vulnerable. These were often treated with creosote, or with salts of toxic metals, such as copper, chromium, or arsenic (Atwood 1922; Hoppe 2002). Teredo navalis has frequently appeared in harbors or estuaries where shipworms had been rare or absent, either as a result of invasions, or of changing environmental conditions (or both), including Barnegat Bay, New Jersey (Nelson 1922; Turner 1973); Boston Harbor, Massachusetts (Manley 1893); the southern Gulf of St. Lawrence, Canada (Kindle 1918); San Francisco Bay, California (Atwood 1922; Carlton 1979; Cohen and Carlton 1995); and the western Baltic (Hoppe 2002; Didziulis 2011). Since these ports used vast quantities of untreated wood, shipworm populations could increase very rapidly, causing catastrophic damage. In the 1920s, an outbreak of T. navalis in San Francisco Bay caused an estimated $615 million dollars (in 1992 currency rates) in damage (Cohen and Carlton 1995). In 1946, shipworms were reported to cause an annual $55 million ($500 million in current dollars) of damage to waterfront structures in the United States (Clapp 1946, cited by Scheltema and Truitt 1954). The transition to metal ships, and the use of concrete, fiberglass, plastic, and other materials has resulted in decreased shipworm populations and damage.

Preservation of existing piers involves wrapping them in plastic (polyvinyl chloride or polyethylene) or encasing them, with a jacket of PVC or fiberglass, then filling the space with epoxy or cement grout. The latter method is much more expensive, but protects the pilings against floating debris, ship damage, etc (Abood et al. 1995). Costs of these repairs in a large port area can amount to hundreds of millions of dollars (Foderaro 2011).

Fisheries - Teredo navalis frequently causes damage to lobster pots, oyster-trays, and other wooden fisheries structures (Nelson 1922; Grave 1928).

Industry - In coastal areas where logging occurs, or where logs are imported, they may be transported or stored in floating rafts. In British Columbia, the decline of logging has led to a decrease in the abundance of a population of T. navalis in Pendrell Sound (Quayle 1992). Storage of logs in harbors was a common practice in Japan, and shipworms were considered a serious problem for the lumber industry (Tsunoda 1979).

Health (Safety) - In the 18th century in the Netherlands, shipworms destroyed 50 km of wooden seawalls, which had to be replaced by stone. The worms were declared to be a plague sent by God (Hoppe 2002; Wolff 2005). In general, the collapse of waterfront structures due to shipworms is a serious safety concern in harbor areas, especially where abandoned piers are used by children and fishermen.

Aesthetic - With the consolidation and mechanization of modern shipping and fishing, much waterfront property, including docks and piers, are used for tourism and recreation. In New York Harbor, where T. navalis has returned and caused extensive damage, due to improved water quality, New York City is planning to spend $200 million over the next few decades to encase and preserve piers to be used as part of waterfront parks (Foderaro 2011). In the Baltic Sea, a different concern is the destruction of archaeologically important shipwrecks, which up to now have been preserved from borers by the low salinity (Hoppe 2002).

Ecological Impacts 

The ecological implications of T. navalis invasions are not well studied. However, T. navalis tolerates a wide range of temperature and salinity and has an extensive global range. It quickly damages wooden manmade structures, and in doing so, speeds the breakdown and recycling of wood in estuaries and coastal waters. Damaged wood may provide habitat for small animals, but the consumption of coarse woody debris may also remove shelter for those animals. Further, shipworms, can aid the transport of other invading species, by opening holes and creating galleries of decaying wood in the hulls of wooden ships, where sedentary organisms can reside (Carlton and Hodder 1995). In addition to impacts directly caused by shipworms, the various toxic substances used to prevent or discourage shipworm attacks have added to the burden of pollution in many of the world's harbors.

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