Terebrasabella heterouncinata

Invasion History

First Non-native North American Tidal Record: 1996
First Non-native West Coast Tidal Record: 1996
First Non-native East/Gulf Coast Tidal Record:

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General Invasion History:

Terebrasabella heterouncinata is a small sabellid worm, which can be found burrowing into the shells of several species of gastropods on the Atlantic and Indian Ocean shores of South Africa. Its most common native hosts were the abalone Haliotis midae, the whelks Burnapena spp., and the turban shells Turbo sarmaticus and T. cidaris. It was found in lower frequencies in limpets (Patella spp., Argobuccinum pustulosum) and the winkles Oxystele (Fitzhugh and Rouse 1999).

Terebrasabella heterouncinata escaped notice on the US West Coast until it was first discovered in California abalone (Haliotis spp.) aquaculture in 1990. The burrows of the polychaete caused deformation of the abalone shells, retarding the mollusks' growth. This worm is considered a serious pest in aquaculture systems (Kuris and Culver 1999). An eradication program was undertaken and no infected snails have been found since 1998 (Culver and Kuris 2000, Moore et al. 2013). Infestations of abalones have been reported in closed-circulation aquaculture systems in Chile (Moreno 2006) and Iceland (Bower 2006).

North American Invasion History:

Invasion History on the West Coast:

In 1990-1993, Red Abalone (Haliotis rufescens), in culture facilities in California (CA), were observed to develop deformed, brittle domed shells. The shells were found to be perforated with thousands of burrows containing tiny sabellid worms. The mode of infection was unique, with larval worms settling on the lip of the shell, where calcium was deposited. Terebrasabella heterouncinata was found to be new to science and was described, named, and traced to abalones (H. midae) brought from South Africa for experimental aquaculture (Fitzhugh and Rouse 1999; Kuris and Culver 1999; Culver and Kuris 2000). In 1996, T. heterouncinata was discovered 'in the wild', in the discharge area of an aquaculture facility near Cayucos, CA infesting native Red Abalones (H. rufescens) and other gastropods (primarily Tegula funebralis, the Black Turban Snail). An eradication program was begun in 1996, by removing infected animals in order to break the chain of transmission. Over 1.6 million snails were removed. The polychaete was apparently eradicated by April 1998 (Culver and Kuris 2000). Surveys of shoreline mollusks adjacent to 25 other California abalone aquaculture facilities, from Crescent City to La Jolla, conducted from 2001 to 2009, found no other cases of T. heterouncinata escaping from culture operations (Moore et al. 2007; Moore et al. 2013).

Invasion History Elsewhere in the World:

Terebrasabella heterouncinata is now recognized as a severe pest in abalone aquaculture in its native South Africa (Simon et al. 2004) and in other places where abalone are raised. Infestations have been reported in closed-circulation aquaculture systems in Chile (Moreno et al. 2006) and Iceland (Bower 2006).

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Description

Terebrasabella heterouncinata is a small sabellid polychaete which bores into the shells of gastropods. The adult worm has eight thoracic and three abdominal chaetigers. The head bears a branchial crown with two pairs of radioles, with ciliated pinnules, in a comb-like arrangement. Many of the features of other sabellids, such as radiolar eyes, flanges, and ventral lips are absent. The branchial crown is supported by a skeleton. The branchial lobes are fused along the dorsal midline, and the ventral margins of lobes have rounded flanges. The anterior and posterior rings are indistinct and lack eyespots, but are surrounded by a distinct collar. The collar has dorsal and ventral incisions, with projecting ventral lappets. Parapodia are absent, but thoracic chaetigers 2-8 bear clusters of notopodial chaetae and neuropodial uncini (stout, deeply embedded beak-like chaetae). The notopodial chaetae have hooded (widened) tips. The uncini on chaetigers 2-6, have a bent beak, bearing a large central tooth, flanked by two smaller teeth, and are accompanied by companion setae. Thoracic segments 6, 7, and 8 are large and swollen. The uncini on setigers 7 and 8 are greatly modified, with a short handle and a large bent beak, and do not have companion setae. The abdomen, consisting of setigers 9-11 and the pygidium, is bluntly tapered. The chaetigers have notopodal uncini and neuropodial setae. The abdominal uncini have long handles, with a beak containing a large main tooth surrounded by smaller teeth. Adults range from 1.0 to 2.4 mm in size (Fitzhugh and Rouse 1999; Simon et al. 2005b; Murray and Rouse 2007).

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Taxonomy

Ecology

General:

Terebrasabella heterouncinata is a small, suspension-feeding sabellid polychaete. Because it burrows in the shell matrix of gastropods, and interferes with shell growth (Fitzhugh and Rouse 1999; Kuris and Culver 1999), it can be considered an epibiotic parasitoid, although it does not consume gastropod tissue directly. This polychaete can survive, even when the live host is absent (Simon et al., 2002). The juvenile polychaetes settle under the abalone?s mantle at the shell edge or under the lip of the shell, where calcium deposition and shell growth is occurring, so that calcium is deposited around the worms (Kuris and Culver 1999). Terebrasabella heterouncinata is rapidly reproducing and hermaphoditic, with spermiogenesis occurring in chaetiger 8 and oogenesis occurring in chaetigers 9-10 (Fitzhugh and Rouse 1999). It is unique in having a single spermatheca located ventrally to the mouth (Simon & Rouse 2005). Eggs are deposited within the parent's tube, and hatch into benthic, crawling larvae. The larvae crawl out of the parental tube, onto the shell margin, where they form mucous tubes, which are soon coated with the gastropod's nacreous shell material, forming an opaque calcareous tube within the shell. The larvae develop their tentacular crowns within a week after settlement, and reach reproductive maturity in about a month. The worms can live for over four years. When shells of two mollusks came into contact, the new host was readily infected (Kuris and Culver 1999). The highest number of sabellids settle near the respiratory pores of abalones, thus providing a feeding advantage for their settlement (Gray & Kaiser 2007).

As noted above, T. heterouncinata is a suspension-feeder, feeding on phytoplankton. The natural habitat of this worm is rocky shorelines, inhabited by gastropods, including abalones, turban shells, limpets, and whelks (Fitzhugh and Rouse 1999). The nutrient-rich habitats of abalone aquaculture facilities are favorable to the growth of planktonic algae, providing both plenty of food and a high density of potential hosts (Simon et al. 2005b). The abalone diet could not have a direct role on the infestation intensity at least not at the early stage in the worm?s life cycle (Gray and Kaiser 2007). In South Africa, the most frequent hosts are abalone Haliotis midae, the whelks Burnapena spp., and the turban shells Turbo sarmaticus and T. cidaris, but other gastropods are also infested (Fitzhugh and Rouse 1999). At the aquaculture discharge site, in Cayucos, California, where the sabellid had escaped into the 'wild', the most frequently infected gastropod was the Black Turban Shell (Tegula funebralis), a common intertidal snail. Other snails, including limpets (Lottia spp.), whelks (Nucella emarginata; Acanthina punctulata), and the lower intertidal Brown Turban Shell (T. brunnea) were rarely infected (Culver and Kuris 2000). Of 15 common native California littoral gastropods tested, six, including Red Abalone (Haliotis rufescens), limpets (Lottia spp.; Fissurella volcano), Black Turban Snails, and Wavy Turban Snails (Megastraea undosa) were highly susceptible to infection by the sabellid in aquaria (Culver and Kuris 2004). Since the Black Turban Snails were the most heavily infected, the eradication attempt focused on removing enough infected and uninfected snails of this species to break the chain of transmission (Culver and Kuris 2000; Moore et al. 2007).

Food:

Phytoplankton (Diatoms and protists)

Trophic Status:

Suspension Feeder

SusFed

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Habitats

General Habitat	Grass Bed	None
General Habitat	Rocky	None
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

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Tolerances and Life History Parameters

Minimum Reproductive Temperature	11.2	Lowest tested, in abalone culture tanks (Finley et al. 2001)
Maximum Reproductive Temperature	20.9	Highest tested, in abalone culture tanks (Finley et al. 2001)
Minimum Length (mm)	1	Fitzhugh and Rouse 1999; Simon et al. 2005; Murray and Rouse 2007
Maximum Length (mm)	2.4	Fitzhugh and Rouse 1999; Simon et al. 2005; Murray and Rouse 2007
Broad Temperature Range	None	Warm temperate
Broad Salinity Range	None	Polyhaline-Euhaline

General Impacts

Although the sabellid polychaete Terebrasabella heterouncinata has not become established in the wild, it has imposed significant costs on abalone culture facilities in California, Chile, and Iceland (Kuris and Culver 1999; Culver and Kuris 2000; Bower 2006; Moreno et al. 2007; Moore et al. 2013). Within culture facilities, the sabellid has been controlled by improved hygiene, including the use of freshwater to kill the parasitoid (Moore et al. 2007).

The escape of this sabellid in the discharge of an abalone farm in Cayucos, California in 1996, prompted a massive eradication program. The primary infected host was the native Black Turban Snail (Tegula funebralis) in the intertidal zone. The eradication program was based on epidemiological theory, which holds that if the host population is sufficiently reduced, transmission of the pathogen becomes impossible. In 1996, State personnel, abalone farmers, and volunteers removed 1.6 million snails from the discharge area. Regular surveys were conducted at 25 abalone culture sites covering the whole coastline of California from 2001 to 2009. No infected gastropods were found in more than 10 years after the removal effort, so this eradication attempt appears to have been successful, and is an example for future responses to introduced marine pest species (Culver and Kuris 2000; Moore et al. 2007; Locke and Hanson 2009; Moore et al. 2013). In abalone aquaculture systems in South Africa, anesthesia (to prevent worms from withdrawing), followed by ultrasound, was an effective method of control (Henderson 2006). 

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Regional Impacts

NEP-V	Northern California to Mid Channel Islands		Economic Impact	Fisheries
In 1990-1993, a disease causing deformation of shells and abnormal growth was observed in commercial aquaculture facilities on the California coast. Infestation of the shells by T. heterouncinata was identified as the cause. This parasite-like sabellid was recognized as a serious pest in culture facilities, and a threat to wild abalone populations. Several abalone culture facilities went bankrupt, while other suffered financial losses. Improved hygienic procedures controlled the infestation. However, the sabellid escaped into the 'wild', in the discharge area of a culture facility in Cayucos CA. It primarily infected the native Black Turban Snail (Tegula funebralis. This outbreak prompted an organized and apparently successful eradication program, in which 1.6 million snails were removed by state personnel, abalone farmers, and volunteers, in order to break the chain of transmission. Subsequent surveys of 25 abalone culture sites, along California's coastline, from Crescent City to La Jolla were conducted between 2001 and 2009 (Culver and Kuris 2000; Moore et al. 2007; Moore et al. 2013). The eradication program was apparently successful, with no subsequent occurrences of the worm (Moore et al. 2013). We do not know the cost of the damage to the cultured abalone crop, or of the resulting research, eradication, and monitoring programs, but it was probably significant.
P069	_CDA_P069 (Central Coastal)		Economic Impact	Fisheries
None
CA	California		Economic Impact	Fisheries
In 1990-1993, a disease causing deformation of shells and abnormal growth was observed in commercial aquaculture facilities on the California coast. Infestation of the shells by T. heterouncinata was identified as the cause. This parasite-like sabellid was recognized as a serious pest in culture facilities, and a threat to wild abalone populations. Several abalone culture facilities went bankrupt, while other suffered financial losses. Improved hygienic procedures controlled the infestation. However, the sabellid escaped into the 'wild', in the discharge area of a culture facility in Cayucos CA. It primarily infected the native Black Turban Snail (Tegula funebralis. This outbreak prompted an organized and apparently successful eradication program, in which 1.6 million snails were removed by state personnel, abalone farmers, and volunteers, in order to break the chain of transmission. Subsequent surveys of 25 abalone culture sites, along California's coastline, from Crescent City to La Jolla were conducted between 2001 and 2009 (Culver and Kuris 2000; Moore et al. 2007; Moore et al. 2013). The eradication program was apparently successful, with no subsequent occurrences of the worm (Moore et al. 2013). We do not know the cost of the damage to the cultured abalone crop, or of the resulting research, eradication, and monitoring programs, but it was probably significant., nan

References

Bower, S. 2006 Synopsis of infectious diseases and parasites of commercially exploited shellfish: Sabellid polychaete infestation disease in abalone. <missing URL>



Culver, Carolynn S.; Kuris, Armand M. (2000) The apparent eradication of a locally established introduced marine pest., Biological Invasions 2: 245-253

Culver, Carolynn S.; Kuris, Armand M. (2004) Susceptibility of California gastropods to an introduced South African sabellid polychaeta, Terebrasabella heterouncinata, Invertebrate Biology 123(4): 316-323

Finley, Carl A.; Mulligan, Timothy J.; Friedman, Carolyn S. (2001) Life of an exotic sabellid polychaeta, Terebrasabella heterouncinata: fertilization strategy and infliuence of temperature on reproduction., Journal of Shellfish Research 20(2): 883-888

Fitzhugh, K., Rouse, G.W. (1999) A remarkable new genus and species of fan worm (Polychaeta: Sabellidae: Sabellinae) associated with marine gastropods, Invertebrate Biology 118(4): 357-390

Gray, Michael S.; Kaiser, Horst (2007) Settlement pattern and survival of a shell-infesting sabellid polychaete, Terebrasabella heterouncinata, on South African abalone, Haliotis midae, fed two diets, African Journal of Aquatic Science 32(3): 275-279

Kuris, A.M., Culver, C.S. (1999) An introduced sabellid polychaete pest infesting cultured abalones and its potential spread to other California gastropods, Invertebrate Biology 118(4): 391-403

Locke, Andrea; Hanson, John Mark (2009) Rapid response to non-indigenous species. 1. Goals and history of rapid response in the marine environment., Aquatic Invasions 4(1): 237-247

Moore, James D.; Juhasz, Christy I.; Thea T. Robbins; Edwin D. Grosholz (2007) The introduced sabellid polychaete Terebrasabella heterouncinata in California: Transmission, methods of control and survey for presence in native gastropod populations., Journal of Shellfish Research 26(3): 869-876

Moore, James D.; Marshman, Blythe C.; Robbins, Thea T.; Juhasz, Christy I. (2013) Continued absence of sabellid fan worms (Terebrasabella heterouncinata) among intertidal gastropods at a site of eradication in California, USA, California Fish and Game 99(3): 115-121

Moreno, Rodrigo A.; Neill, Paula E.; Rozbaczylo, Nicolás (2006) Native and non-indigenous boring polychaetes in Chile: a threat to native and commercial mollusc species., Revista Chilena de Historia Natural 79: 263-278

Murray, Anna; Rouse, Greg W. (2007) Two new species of Terebrasabella (Annelida: Sabellidae: Sabellinae) from Australia, Zootaxa 1434: 51-68

Myers, Judith H.,; Simberloff, Daniel; Kuris, Armand M.; Carey, James R. (2000) Eradication revisited: Dealing with exotic species, Trends in Ecology and Evolution 15(8): 316-320

Simon, C. A.; Kaiser, H.; Britz, P. J. (2005) The effect of age on the reproductive output of the abalone pest Terebrasabella heterouncinata (Polychaeta: Sabellidae: Sabellinae), African Journal of Marine Science 272: 513-516

Simon, Carol A.; Kaiser, Horst; Britz, Peter J. (2005) The life history responses of the abalone pest, Terebrasabella heterouncinata, under natural and aquaculture conditions, Marine Biology 147: 135-144

Simon, Carol A.; Kaiser, Horst ; Britz, Peter J. (2004) Infestation of the abalone, Haliotis midae, by the sabellid, Terebrasabella heterouncinata, under intensive culture conditions, and the influence of infestation on abalone growth., Aquaculture 232: 29-40

Simon, Carol A.; Kaiser, Horst; Booth, Anthony J.; Brit, Peter J. (2002) The effect of diet and live host presence on the growth and reproduction of Terebrasabella heterouncinata (Polychaeta: Sabellidae), Invertebrate Reproduction and Development 41(1-3): 277-286

Simon, Carol A.; Rouse, Greg W. (2005) Ultrastructure of spermiogenesis, sperm, and the spermatheca in Terebrasabella heterouncinata (Polychaeta: Sabellidae: nSabellinae), Invertebrate Biology 124: 39-49.

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