Cercarial morphology and molecular genetic data for the schistosome from H. japonica indicate that these cercariae are not A. variglandis, a schistosome previously reported in San Francisco Bay, and the only species previously implicated in dermatitis outbreaks on the Pacific Coast. We obtained A. variglandis schistosomes from gulls but not from snails in the San Francisco Bay area. The H. japonica–transmitted schistosome is the second species reported to cause dermatitis after introduction of an exotic snail in California coastal waters. We found this schistosome in an opisthobranch snail in western North America. The only other schistosome known to be obtained from an opisthobranch snail is G. huttoni from H. a. guadalupensis snails obtained in Florida (23,29,32). Except for schistosomes collected from 2 species of Siphonaria (Pulmonata: Siphonariidae) snails (33,34), all other marine schistosomes have been obtained from caenogastropodid snails.

Cercariae from H. japonica closely resemble those of G. huttoni, for which sequence data are not available. DNA sequence data for cercariae from H. japonica did not match with those of any known schistosome species, including the congener G. huronensis Najim 1950. Cercariae from H. japonica did not group with other marine schistosomes, but belong to the BTGD clade that, until now, included only freshwater species that use pulmonate snails as intermediate hosts (Figure 5). The only other known marine schistosomes belong to species of the genera Austrobilharzia and Ornithobilharzia Ohdner 1912, which are distantly related to the BTGD clade (Figure 4). We exposed parakeets and chicks to cercariae from H. japonica snails but were unable to obtain adult worms for comparison with described species.

Schistosomes from H. japonica and those of G. huttoni are probably closely related because they are found in haminoeid snails and have morphologically similar cercariae. However, they differ from all other species in the genus Gigantobilharzia Ohdner 1910 in habitat (salt water rather than fresh water) and snail host (opisthobranchid rather than pulmonate). When appropriate genetic material becomes available, analyses may show that G. huttoni schistosomes and those from H. japonica snails should be placed in a separate genus.

Gigantobilharzia spp. have been reported in several gull species (35). Gulls are common at Robert Crown Memorial Beach, often resting on the beach flats at low tides and sometimes foraging in tide pools that contain H. japonica snails (A.N. Cohen, unpub. data). Gulls are thus a likely host for schistosomes from H. japonica, although we did not find them in gulls at the Oakland Airport near Robert Crown Memorial Beach. Leigh (36) and Kinsella et al. (37) found fragments of adult worms that they identified as Gigantobilharzia sp., and which closely resembled G. huttoni worms, in pelicans in Florida. Small flocks of brown pelicans and, rarely, white pelicans have been observed in shallow water off Robert Crown Memorial Beach, although not on the beach or in tide pools (A.N. Cohen, unpub. data). Pelicans are thus another possible host for schistosomes from H. japonica.

Other birds commonly observed at Robert Crown Memorial Beach include shorebirds that are most common in winter when water temperatures are probably less conducive to cercarial emergence (surface temperatures near this beach are typically 16°C–20°C in summer and 8°C–12°C in winter). Cormorants, grebes, and ducks are found in near-shore waters, and mallard ducks sometimes forage in tide pools. Larger wading birds (snowy and great egrets, and occasionally herons), oystercatchers, and several species of terns are sometimes seen in small numbers foraging on the beach or in shallows. Marine schistosomes have been reported in gulls, ducks, terns, herons, cormorants, and turnstones (14,17,19,23), and Gigantobilharzia spp. have been reported in grebes and cattle egrets (23,35). Thus, various bird species might serve as hosts for schistosomes from H. japonica.

Cercarial dermatitis is commonly acquired in fresh water (38). It is less common in marine or estuarine waters; most cases are reported from the northwestern Atlantic Ocean or Australia. This disease was observed on the Pacific Coast of North America during an outbreak at Robert Crown Memorial Beach in 1954–1956, when cercariae identified as A. variglandis were found in I. obsoleta, an Atlantic snail introduced before 1907. The schistosome was likely introduced with this snail and remained undetected until the 1950s (1). In June 2005, cercarial dermatitis was again reported at Robert Crown Memorial Beach. Initial cases were found among elementary school groups that visited the beach at the end of the academic year. Since 2005, dermatitis has occurred annually at this beach (90 cases in 2005, 3 in 2006, 14 in 2007, and 31 in 2008).

Schistosome cercariae in H. japonica snails, large numbers of these snails at Robert Crown Memorial Beach, and the apparent absence of schistosomes in other common snails at this site indicate that schistosomes from H. japonica are responsible for the recent dermatitis outbreak. H. japonica snails were first seen in California in 1999 (22) and except for the 1954 outbreak attributed to A. variglandis, cercarial dermatitis was not reported in San Francisco Bay until shortly after the arrival of H. japonica.

The most popular water-contact activities at Robert Crown Memorial Beach are kite surfing and wind surfing at high tide and wading, exploring, and playing in shallow pools at low tide. In part because of cool water temperatures at this beach, swimming is uncommon, and kite and wind surfers usually wear wetsuits. Most dermatitis cases at this beach were contracted by persons wading in tide pools. Dermatitis usually occurred on the feet or legs. Only 1 case was reported among kite surfers and wind surfers. Since 2005, three biologists working at this beach have contracted dermatitis, usually on their hands or forearms (Figure 6). In experiments with G. huttoni schistosomes obtained near Miami, Florida, cercariae emerged only when temperatures were >22°C, regardless of season or light intensity (32). In San Francisco Bay, the highest numbers of cercariae from H. japonica may be released in beach flat tide pools that warm up during daytime low tides.

There are at least 3 ways in which schistosomes we found in H. japonica snails could have recently emerged as a disease agent in San Francisco Bay. First, an unknown native schistosome may be present in native birds and snails, which switched hosts to the introduced H. japonica snail. Some evidence shows that schistosomes are capable of switching hosts (39). Neither of 2 native Haminoea species found in western North America between Baja, California and Alaska (H. vesicula [Gould 1855] and H. virescens) (22) is known to host schistosomes or is found in the study area. However, if an undetected native schistosome is present in 1 of these species, or in a Haminoea species further south on the Pacific Coast, migration of its bird host over San Francisco Bay could have resulted in infection of the H. japonica population at Robert Crown Memorial Beach, greatly increasing the potential for human dermatitis. The range of G. huttoni schistosomes may extend from Florida through the Caribbean and (by bird movements) up the Pacific Coast.

Second, the schistosomes could be a species from Asia recently introduced into San Francisco Bay in infected H. japonica snails. This introduction would require adult snails (eggs and larvae do not contain schistosomes) that harbor male and female cercariae; both sexes would have to colonize the same bird to initiate egg-producing infections. This event occurred on 1 occasion when A. variglandis schistosomes and I. obsoleta snails were introduced into western North America. Whether H. japonica snails arrived in San Francisco Bay directly from Asia or indirectly through Washington State is unknown. H. japonica snails may have been introduced into Washington State, where they were first observed in the early 1980s (40), in Pacific oysters (Crassostrea gigas Thunberg 1793) imported from Japan for mariculture (17). Pacific oysters from hatcheries or oyster farms in Japan, Washington, Oregon, and California were placed in San Francisco Bay for commercial mariculture in the 1930s, for occasional experimental use until 1981, for bioaccumulation studies during 1991–2002, and were introduced illegally at 1 site in 1999. A population recently discovered in South San Francisco Bay appears to have been introduced during the late 1990s (A.N. Cohen, D. Goodwin, unpub. data). These occurrences may be related to the initial appearance of H. japonica snails in 1999 in South San Francisco Bay.

Third, the schistosomes could be a species from Asia found in migrating birds that infected H. japonica snails after these snails became established. Because some birds excrete schistosome eggs for <10–28 months postinfection (19,23), some schistosomes may survive in a bird host long enough to complete a long-distance migration. However, because no bird species are known to routinely migrate across the Pacific Ocean between the native region of H. japonica snails in Asia and regions in the western United States, introduction by this mechanism seems unlikely.

Much remains to be learned about factors favoring outbreaks of cercarial dermatitis in new areas. Native Haminoea spp. should be surveyed for parasites to assess whether host switching may be involved, and H. japonica snails should be surveyed in their native range and in Washington State to determine whether trans-Pacific schistosome colonization events have occurred and by what mechanisms. Molecular analysis of G. huttoni schistosomes would increase the taxonomic status of the species we isolated from San Francisco Bay. The definitive avian host in this region could be determined by examination of feces for eggs and carcasses for adult schistosomes.

The molecular signatures we have provided may be present in schistosomes isolated from birds or snails in other areas, which would help establish how this zoonotic infection reached California. Potential effects on native biota, especially endangered birds that might serve as hosts (such as the California least tern or California brown pelican), should be assessed. Whether this schistosome will become established in other locations along the Pacific Coast and affect beach users is unknown. Improved understanding of the biology and mechanism of establishment of this schistosome may enable better management of human exposure and infection, control of its spread, and prevention of other schistosome introductions or outbreaks.