Batillaria attramentaria

Invasion History

First Non-native North American Tidal Record: 1924
First Non-native West Coast Tidal Record: 1924
First Non-native East/Gulf Coast Tidal Record:

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General Invasion History:

Batillaria attramentaria is native to the Northwest Pacific, from the shores of the Sakhalin and Kuril Islands in the Sea of Okhotsk, Russia (Golikov 1976; Academy of Natural Sciences of Philadelphia 2009) south to Okinawa, Japan; Taiwan; and Hong Kong (Golikov 1976; Huang 2001; Academy of Natural Sciences of Philadelphia 2009). Its preferred habitat is shallow subtidal to mid-intertidal mudflats and marshes (Abbott 1974; Golikov 1976; Byers 1999).

North American Invasion History:

Invasion History on the West Coast:

In 1924, Batillaria attramentaria was first collected near transplanted Pacific Oysters (Crassostrea gigas) in Samish Bay, Washington (WA). It was spread to many West coast locations with oysters transplanted from Washington State (Carlton 1979, Byers 1999). In 1926, it was found in Bellingham Bay, WA, but its date of first record in Puget Sound proper is uncertain. It was well established at Dosewallips Flats, on the Hood Canal, by 1977 (Carlton 1979). By 1964, it ranged north to Comox, Vancouver Island, British Columbia (Carlton 1979). Its northern limit is currently Pendrell Sound, British Columbia (Gillespie et al. 2007). Sometime between 2000 and 2007, B. attramentaria became established in Willapa Bay, on the Pacific coast of Washington (Weiskell et al. 2007).

Batillaria attramentaria was first collected in California in Tomales Bay in 1941 (Carlton 1979; Byers 1999). In 1955, it was collected in Bolinas Lagoon and Elkhorn Slough (Byers 1999). Byers found small populations in Drakes Estero in 1996 (Byers 1999). These estuaries all had transplants of Pacific Oysters, between 1928 and 1955 (Byers 1999). One deformed shell was collected near Sausalito in San Francisco Bay in 1958 – Carlton (1979) suggests that it might have been discarded by a shell collector or dealer (Carlton 1979). In 2006, B. attramentaria was found in large numbers in Loch Lomond Marina, San Rafael, on San Francisco Bay. In 2007, another new population was found in Bodega Harbor. Eradication of both of these new, localized populations was attempted, but was unsuccessful (Weiskel et al. 2007; Houle 2011; Zabin, personal communication 4/22/13). While oyster transplants were the likely vector for early introductions, boat trailers, fishing gear, or fisherman's boots are possible vectors for the recent spread in areas where no oyster culture is now occurring. A well-studied population in Elkhorn Slough has shown dramatic declines at many sites, especially those with unrestricted tidal flow and high crab (Pachygrapsus crassipes spp.). However, the causes of the decline are not clear (Wasson et al. 2020).

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Description

The names Batillaria attramentaria and B. cumingi are both widely used for this snail. Currently 'attramentaria' is the species name accepted by the World Registry of Marine Species (WoRMS, Appeltans et al. 2013) and the Integrated Taxonomic Information System (ITIS 2013). The shell is dextrally coiled and has a tall, strongly conical spire. Illustrated specimens have ~10 whorls. The sutures are shallow and the whorls have numerous spiral threads. Varices or axial ribs (running across the whorls) occur on the upper whorls, but fade out on the lower ones. The aperture projects outward, with a short and twisted siphonal canal. The outer lip is smooth inside. The operculum has multiple spirals. The size of adult shells ranges from 10 to 34 mm (Abbott 1974; McLean, in Carlton 2007). The color of the shell is highly variable. The shell is usually gray-brown, often with a white band below the suture, but can range from light brown to dirty-black (Abbott 1974; McLean, in Carlton 2007). Miura et al. (2007) suggest that in Japan, much of the color variation may result from selection related to temperature, with darker colors being favored in colder climates, for heat absorption. Dark colors are still common in warmer regions, suggesting that selection is relaxed there. To our knowledge, these geographical patterns have not been reported in North America.

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Taxonomy

Ecology

General:

Batillaria attramentaria is a snail inhabiting the middle portions of tidal marshes and is rare above the mean high-tide line or in subtidal zones (Whitlach and Obreski 1980; Swinbanks and Murray 1981; Behrens Yamada 1982). Egg-laying first occurs in snails about 1-2 years old at about 1.3 - 2 mm in length. This snail lays egg capsules, containing single embryos, on the sediment surface. The eggs have direct development, hatching into crawling larvae (Whitlach 1974; Behrens Yamada and Sankurathri 1977). However, juvenile or just-mature snails (~ 1-2 mm in length) can disperse locally by floating on the water surface (Adachi and Wada 1999). Populations in British Columbia and California had a longevity somewhere between 6 and 10 years (Whitlatch 1974; Behrens Yamada 1982).

Batillaria attramentaria inhabits the middle intertidal of tidal marshes in its native Northwest Pacific and in its introduced range in the Northeast Pacific. It is rare above the mean monthly high-tide line and in subtidal waters (Swinbanks and Murray 1981; Whitlach and Obreski 1980; Behrens Yamada 1982; Ivanova et al. 2008). The snail partially buries itself in mud to avoid desiccation at low tide and leaves extensive grazing trails on the surface, while feeding (Swinbanks and Murray 1981). In Japan, it inhabits tidepools on rocky shores, as well as soft substrates (Adachi and Wada 1999), but in North America it appears to be confined to marsh and mud environments (Whitlach and Obreski 1980; Behrens Yamada 1982). It tolerates a wide range of temperature and salinity (Miura et al. 2007; Ivanova et al. 2008).

Batillaria attramentaria feeds on plant detritus and benthic diatoms (Whitlach and Obreski 1980; Sakamaki and Richardson 2008). In Asian waters, B. attramentaria hosts a variety of parasites, but only one, a trematode, Cercaria batillariae has been found in North America populations (Torchin et al. 2005). This parasite castrates the snail and causes it to grow larger (Miura et al. 2006). Predators of B. attramentaria include shorebirds, crabs, and fishes. Several species of fishes are intermediate hosts of C. batillariae, while fish-eating birds are probably the final hosts (Torchin et al. 2005).

Food:

Detritus, microalgae

Trophic Status:

Deposit Feeder

DepFed

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Habitats

General Habitat	Unstructured Bottom	None
General Habitat	Grass Bed	None
General Habitat	Salt-brackish marsh	None
General Habitat	Mangroves	None
General Habitat	Oyster Reef	None
Salinity Range	Polyhaline	18-30 PSU
Salinity Range	Euhaline	30-40 PSU
Tidal Range	Subtidal	None
Tidal Range	Low Intertidal	None
Tidal Range	Mid Intertidal	None
Vertical Habitat	Epibenthic	None

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Tolerances and Life History Parameters

Minimum Temperature (ºC)	-2	Freezing temperatures in northern Japanese estuaries, Miura et a. 2007
Maximum Temperature (ºC)	40	Field, summer on southern Japan mudflats, Miura et a. 2007
Minimum Salinity (‰)	7	Field, Uglovoy Bay, Amur estuary, Russia (Ivanova et al. 2008)
Maximum Salinity (‰)	33	Field, Tanaba Bay, Japan (Adachi and Wada 1999)
Minimum Length (mm)	1.3	Approximate size at first reproduction (Whitlach 1974)
Maximum Length (mm)	34	Abbott 1974, but shells over 25 mm may be rare (Behrens and Yamada 1977).
Broad Temperature Range	None	Cold temperate-Warm temperate
Broad Salinity Range	None	Polyhaline-Euhaline

General Impacts

Batillaria attramentaria has no reported economic impacts, but its ecological effects on native communities have been well-studied. This snail's convenient size, high abundance, and localized distribution in the intertidal zone have facilitated ecological research. A particular conservation concern is its apparent role in the decline of a native California Hornsnail, Cerithidea californica (Byers 1999; Byers 2000a; Byers 2000b; Byers and Goldwasser 2001).

Competition: In the presence of Batillaria attramentaria, the native snail Cerithidea californica declined an average of 27% over a 3-year period in coexisting California populations (Byers 1999). In experiments, Batillaria attramentaria was superior to C. californica in food conversion (Byers 2000a), hypoxia tolerance (Byers 2000b), and parasitism resistance (Byers and Goldwasser 2001; Torchin et al. 2005). Cerithidea californica is absent in Elkhorn Slough, but may have been previously present, based on sketchy historical records and its presence to the north and south (Byers 1999). Based on observations in three other estuaries, B. attramentaria may have eliminated C. californica from Elkhorn Slough (Byers 1999). Mathematical modelling indicates that B. attramentaria may drive C. californica extinct in 55-70 years. A major factor is B. attramentaria's lower mortality rate, due in part to lower rates of parasitism (Byers and Goldwasser 2001). Batillaria attramentaria had equal prevalence of parasites in Bolinas Lagoon, California, but only one species (Ceracia batillariae, introduced) compared to 10 species for C. californica (Torchin et al. 2005).

Habitat Change: In Padilla Bay, Washington, Batillaria attramentaria was shown to alter habitats in several ways that had positive effects on native species. The numerous dead shells provided habitat for attachment or shelter for the introduced slipper shell Crepidula convexa and the anemone Diadumene lineata, and the native hermit crabs Pagurus hirsutiusculus and P. granosimanus. In manipulative experiments, the introduced seagrass Zostera japonica increased in the presence of B. attramentaria. The increase in Z. japonica probably results from bioturbation, modifying oxygen and nutrient concentrations in sediment (Wonham et al. 2005).

Trophic Cascade (indirect effects): In manipulative experiments, the introduced snail Nassarius fraterculus increased in the presence of B. attramentaria. The increase in N. fraterculus may result from differential grazing by B. attramentaria, resulting in increasing microalgae favored by N. fraterculus (Wonham et al. 2005).

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Regional Impacts

P110	Tomales Bay		Ecological Impact	Competition
The native snail Cerithidea californica declined an average of 27% over a 3-year period in coexisting California populations (Byers 1999). In experiments, Batillaria attramentaria was superior to C. calfornica in food conversion (Byers 2000a), hypoxia tolerance (Byers 2000b), and parasitism resistance (Byers and Goldwasser 2002).
P100	Drakes Estero		Ecological Impact	Competition
The native snail Cerithidea californica declined an average of 27% over a 3-year period in coexisting California populations (Byers 1999). In experiments, Batillaria attramentaria was superior to C. calfiornica in food conversion (Byers 2000a), hypoxia tolerance (Byers 2000b), and parasitism resistance (Byers and Goldwasser 2002).
P095	_CDA_P095 (Tomales-Drakes Bay)		Ecological Impact	Competition
The native snail Cerithidea californica declined an average of 27% over a 3-year period in coexisting California populations (Byers 1999). In experiments, Batillaria attramentaria was superior to C. calfiornica in food conversion (Byers 2000a), hypoxia tolerance (Byers 2000b), and parasitism resistance (Byers and Goldwasser 2002).
P080	Monterey Bay		Ecological Impact	Competition
The native snail Cerithidea californica is absent in Elkhorn Slough, but may have been previously present, based on sketchy historical records and its presence to the north and south (Byers 1999). Based on observations in three other estuaries, B. attramentaria may have eliminated Cerithidea californica from Elkhorn Slough (Byers 1999).
P293	_CDA_P293 (Strait of Georgia)		Ecological Impact	Habitat Change
In Padilla Bay, Washington, Batillaria attramentaria was shown to alter habitats in several ways that had positive effects on native species. The numerous dead shells provided habitat for attachment or shelter for the introduced slipper shell Crepidula convexa, the anemone Diadumene lineata, and the native hermit crabs Pagurus hirsutiusculus and P. granosimanus. In manipulative experiments, the introduced seagrass Zostera japonica increased in the presence of B. attramentaria. The increase in Z. japonica probably results from bioturbation, modifying oxygen and nutrient concentrations in sediment (Wonham et al. 2005).
P293	_CDA_P293 (Strait of Georgia)		Ecological Impact	Trophic Cascade
In manipulative experiments, the introduced snail Nassarius fraterculus increased in the presence of B. attramentaria. The increase in N. fraterculus may result from differential grazing by B. attramentaria, resulting in increasing microalgae favored by N. fraterculus (Wonham et al. 2005).
NEP-III	Alaskan panhandle to N. of Puget Sound		Ecological Impact	Habitat Change
In Padilla Bay, Washington, Batillaria attramentaria was shown to alter habitats in several ways that had positive effects on native species. The numerous dead shells provided habitat for attachment or shelter for the introduced slipper shell Crepidula convexa, the anemone Diadumene lineata, and the native hermit crabs Pagurus hirsutiusculus and P. granosimanus. In manipulative experiments, the introduced seagrass Zostera japonica increased in the presence of B. attramentaria. The increase in Z. japonica probably results from bioturbation, modifying oxygen and nutrient concentrations in sediment (Wonham et al. 2005).
NEP-III	Alaskan panhandle to N. of Puget Sound		Ecological Impact	Trophic Cascade
In manipulative experiments, the introduced snail Nassarius fraterculus increased in the presence of B. attramentaria. The increase in N. fraterculus may result from differential grazing by B. attramentaria, resulting in increasing microalgae favored by N. fraterculus (Wonham et al. 2005).
NEP-V	Northern California to Mid Channel Islands		Ecological Impact	Competition
The native snail Cerithidea californica declined an average of 27% over a 3-year period in coexisting California populations (Byers 1999). In experiments, Batillaria attramentaria was superior to C. calfornica in food conversion (Byers 2000a), hypoxia tolerance (Byers 2000b), and parasitism resistance (Byers and Goldwasser 2002). The native snail Cerithidea californica is absent in Elkhorn Slough, but may have been previously present, based on sketchy historical records and its presence to the north and south (Byers 1999). Based on observations in three other estuaries, B. attramentaria may have eliminated Cerithidea californica from Elkhorn Slough (Byers 1999).
WA	Washington		Ecological Impact	Habitat Change
In Padilla Bay, Washington, Batillaria attramentaria was shown to alter habitats in several ways that had positive effects on native species. The numerous dead shells provided habitat for attachment or shelter for the introduced slipper shell Crepidula convexa, the anemone Diadumene lineata, and the native hermit crabs Pagurus hirsutiusculus and P. granosimanus. In manipulative experiments, the introduced seagrass Zostera japonica increased in the presence of B. attramentaria. The increase in Z. japonica probably results from bioturbation, modifying oxygen and nutrient concentrations in sediment (Wonham et al. 2005).
WA	Washington		Ecological Impact	Trophic Cascade
In manipulative experiments, the introduced snail Nassarius fraterculus increased in the presence of B. attramentaria. The increase in N. fraterculus may result from differential grazing by B. attramentaria, resulting in increasing microalgae favored by N. fraterculus (Wonham et al. 2005).
CA	California		Ecological Impact	Competition
The native snail Cerithidea californica declined an average of 27% over a 3-year period in coexisting California populations (Byers 1999). In experiments, Batillaria attramentaria was superior to C. calfornica in food conversion (Byers 2000a), hypoxia tolerance (Byers 2000b), and parasitism resistance (Byers and Goldwasser 2002). The native snail Cerithidea californica is absent in Elkhorn Slough, but may have been previously present, based on sketchy historical records and its presence to the north and south (Byers 1999). Based on observations in three other estuaries, B. attramentaria may have eliminated Cerithidea californica from Elkhorn Slough (Byers 1999)., The native snail Cerithidea californica is absent in Elkhorn Slough, but may have been previously present, based on sketchy historical records and its presence to the north and south (Byers 1999). Based on observations in three other estuaries, B. attramentaria may have eliminated Cerithidea californica from Elkhorn Slough (Byers 1999)., The native snail Cerithidea californica declined an average of 27% over a 3-year period in coexisting California populations (Byers 1999). In experiments, Batillaria attramentaria was superior to C. calfornica in food conversion (Byers 2000a), hypoxia tolerance (Byers 2000b), and parasitism resistance (Byers and Goldwasser 2002)., The native snail Cerithidea californica declined an average of 27% over a 3-year period in coexisting California populations (Byers 1999). In experiments, Batillaria attramentaria was superior to C. calfiornica in food conversion (Byers 2000a), hypoxia tolerance (Byers 2000b), and parasitism resistance (Byers and Goldwasser 2002)., The native snail Cerithidea californica declined an average of 27% over a 3-year period in coexisting California populations (Byers 1999). In experiments, Batillaria attramentaria was superior to C. calfiornica in food conversion (Byers 2000a), hypoxia tolerance (Byers 2000b), and parasitism resistance (Byers and Goldwasser 2002).

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