Robert H. Cowie

The Global Decline of Nonmarine Mollusks

Abstract Invertebrate species represent more than 99% of animal diversity; however, they receive much less publicity and attract disproportionately minor research effort relative to vertebrates. Nonmarine mollusks (i.e., terrestrial and freshwater) are one of the most diverse and imperiled groups of animals, although not many people other than a few specialists who study the group seem to be aware of their plight. Nonmarine mollusks include a number of phylogenetically disparate lineages and species-rich assemblages that represent two molluscan classes, Bivalvia (clams and mussels) and Gastropoda (snails, slugs, and limpets). In this article we provide an overview of global nonmarine molluscan biodiversity and conservation status, including several case studies documenting the diversity and global decline of nonmarine mollusks. We conclude with a discussion of the roles that mollusks and malacologists should play in conservation, including research, conservation management strategies, and education and outreach.

Can snails ever be effective and safe biocontrol agents

The use of snails as biocontrol agents against other snails and against aquatic weeds is reviewed, evaluating their success and their impacts on non-target organisms. The predatory snail Euglandina rosea (and other species), although widely used against Achatina fulica (the giant African land snail) on Pacific and Indian Ocean islands, has not been shown to control A. fulica but has seriously impacted endemic island species. The facultative predator Rumina decollata , used in California against Helix aspersa (brown garden snail), is widely considered to be environmentally benign. However, evidence of its effectiveness is weak and it will also consume native snails. Ampullariid and thiarid freshwater snails have been used as competitors (and incidental predators) of snail vectors of human schistosomes, the parasites causing schistosomiasis (bilharzia). Successful control has been reported but impacts on native biotas have been essentially ignored. Ampullariids have been used in attempts to control aquatic weeds, sometimes successfully, but again with little consideration of impacts on native biota. Most snails have generalist feeding habits. Thus they are inappropriate biocontrol agents because of their potential nontarget effects. Rarely has adequate pre-release testing of snails been undertaken and post-release monitoring of non-target impacts has always been incidental. The use of non-native snails for biocontrol purposes is poorly regulated; many introductions are unofficial and sometimes illegal. Use of snails as biocontrol agents, if implemented, must be based on adequate pre-release testing, post-release monitoring and genuine concern for preservation of native biodiversity.

Rapid spread of an invasive snail in South America: the giant African snail, Achatina fulica, in Brasil

Beginning around 1800, but primarily since the early and mid-twentieth century, the giant African snail, Achatina (Lissachatina) fulica Bowdich, 1822, has been introduced throughout the tropics and subtropics and has been considered the most important snail pest in these regions. In Brasil, specimens probably brought from Indonesia were introduced into the state of Paraná in the 1980s for commercial purposes (“escargot” farming) that were not successful. Achatina fulica is now widespread in at least 23 out of 26 Brasilian states and the Federal District, including the Amazonian region and natural reserves. Among the reasons for the species’ rapid invasion are its high reproductive capacity and the tendency for people to release the snails into the wild. Achatina fulica occurs in dense populations in urban areas where it is a pest in ornamental gardens, vegetable gardens, and small-scale agriculture. Also of concern is the damage caused to the environment, and potential competition with native terrestrial mollusks. It can also act as an intermediate host of Angiostrongylus cantonensis, a nematode that can cause meningoencephalitis in people, and it may be a potential host of A. costaricensis, which causes abdominal angiostrongylosis, a zoonosis that occurs from the southern United States to northern Argentina. Management and control measures for A. fulica are under way in Brasil through a national plan implemented by the Brasilian government.

Molecular biogeography and diversification of the endemic terrestrial fauna of the Hawaiian Islands

Oceanic islands have played a central role in biogeography and evolutionary biology. Here, we review molecular studies of the endemic terrestrial fauna of the Hawaiian archipelago. For some groups, monophyly and presumed single origin of the Hawaiian radiations have been confirmed (achatinelline tree snails, drepanidine honeycreepers, drosophilid flies, Havaika spiders, Hylaeus bees, Laupala crickets). Other radiations are derived from multiple colonizations (Tetragnatha and Theridion spiders, succineid snails, possibly Dicranomyia crane flies, Porzana rails). The geographic origins of many invertebrate groups remain obscure, largely because of inadequate sampling of possible source regions. Those of vertebrates are better known, probably because few lineages have radiated, diversity is far lower and morphological taxonomy permits identification of probable source regions. Most birds, and the bat, have New World origins. Within the archipelago, most radiations follow, to some degree, a progression rule pattern, speciating as they colonize newer from older islands sequentially, although speciation often also occurs within islands. Most invertebrates are single-island endemics. However, among multi-island species studied, complex patterns of diversification are exhibited, reflecting heightened dispersal potential (succineids, Dicranomyia). Instances of Hawaiian taxa colonizing other regions are being discovered (Scaptomyza flies, succineids). Taxonomy has also been elucidated by molecular studies (Achatinella snails, drosophilids). While molecular studies on Hawaiian fauna have burgeoned since the mid-1990s, much remains unknown. Yet the Hawaiian fauna is in peril: more than 70 per cent of the birds and possibly 90 per cent of the snails are extinct. Conservation is imperative if this unique fauna is to continue shedding light on profound evolutionary and biogeographic questions.

Patterns of introduction of non-indigenous non-marine snails and slugs in the Hawaiian Islands

The native snails of the Hawaiian Islands are disappearing. One cause is predation by introduced carnivorous snails. Habitat destruction/modification is also important, facilitating the spread of other non-indigenous snails and slugs. Eighty-one species of snails and slugs are recorded as having been introduced. Thirty-three are established: 12 freshwater, 21 terrestrial. Two or three species arrived before western discovery of the islands (1778). During the nineteenth century about one species per decade, on average, was introduced. The rate rose to about four per decade during the twentieth century, with the exception of an especially large number introduced in the 1950s as putative biocontrol agents against the giant African snail, Achatina fulica. The geographical origins of these introductions reflect changing patterns of commerce and travel. Early arrivals were generally Pacific or Pacific rim species. Increasing trade and tourism with the USA, following its annexation of Hawaii, led to an increasing proportion of American species. More general facilitation of travel and commerce later in the twentieth century led to a significant number of European species being introduced. African species dominated the 1950s biological control introductions. The process continues and is just part of the homogenization of the unique faunas of tropical Pacific islands.

Decline and homogenization of Pacific faunas: the land snails of American Samoa

Native Pacific island biotas are disappearing rapidly. Among these native biotas the land snails are especially recognized not only for their high diversity and high levels of endemism but also for being under severe threat, with many species already extinct. Many non-indigenous snail species are being introduced, leading to a homogenization of land snail faunas across the Pacific. Field survey work in American Samoa in 1998 recorded 19 of the 42 previously known native land snail species, 11 of the 12 alien species, and three of the six cryptogenic (unknown origin) species previously known from American Samoa. Eight species were recorded from American Samoa for the first time: three described species that are presumed to be native, four non-indigenous species; and one cryptogenic species. Two undescribed and presumed endemic species were discovered, as was one unidentified and perhaps undescribed species. One species, previously thought to be extinct was rediscovered, although in very small numbers. The known island by island distributions of 11 species (five native, five alien, one cryptogenic) were extended. Comparisons with surveys undertaken predominantly in the 1920s and 1930s, 1975, and 1992 showed that: the majority of native species are declining; some native species may be stable or even increasing, with one species abundant; only seven of the non-indigenous and cryptogenic species are declining or probably declining, while six are increasing, and for others no trend was assessed; some non-indigenous species are extremely abundant. Threats to the fauna include: alien predators, predominantly rats and predatory snails introduced in attempts to control the giant African snail; possible competitors, including non-indigenous snail species; invasive plants and habitat modification; development, including recreational, agricultural, and domestic/urban development. A review should be undertaken of the IUCN and US Fish and Wildlife Service listings of endangered land snail species in American Samoa.

Invertebrate Invasions on Pacific Islands and the Replacement of Unique Native Faunas: A Synthesis of the Land and Freshwater Snails*Contribution no. 2001-001 of Bishop Museum's Pacific Biological Survey.

The once immense diversity of native Pacific island land snail species, with high single island or archipelago endemism, is declining dramatically. The native/endemic species are being replaced by a much smaller number of widespread tropical ‘tramps’, that is, those species that are most readily transported by humans. The 82 introduced (including 14 ‘cryptogenic’) land snail species recorded include some that were distributed accidentally by Pacific islanders before European exploration of the Pacific and that are now widespread. However, the majority are modern introductions, with many recent accidental introductions often associated with the horticultural trade. Native freshwater faunas were less diverse than the terrestrial faunas and exhibited much lower endemism. Among the 59 alien freshwater species recorded (including 38 ‘cryptogenic’ species), the most diverse and widespread are the thiarids. Predation by and competition with these aliens (as well as habitat loss) are probably important mechanisms underlying the loss of native taxa, but almost no quantitative or experimental work has been done to demonstrate such ecological interactions. Prevention of further spread and of new introductions should be the main approach. Increased public education and development of public trust is essential to the success of these efforts.

Alien Non-Marine Snails and Slugs of Priority Quarantine Importance in the United States: A Preliminary Risk Assessment

Abstract: In 2002, the U.S. Department of Agriculture requested assistance from the American Malacological Society in the development of a list of non-native snails and slugs of top national quarantine significance. From a review of the major pest snail and slug literature, together with our own experience, we developed a preliminary list of gastropod species displaying significant potential to damage natural ecosystems or agriculture, or human health or commerce, and either entirely absent from the United States to our knowledge or restricted to narrow areas of introduction. Comments on the list from the worldwide malacological community were then solicited and led us to modify the original list. We then evaluated the taxa on this list by ranking them according to 12 attributes—seven biological variables and five aspects of human interaction—based on thorough review of the detailed literature. The ranked list that emerged from this risk assessment process included 46 taxa (species or species-groups) in 18 families. The highest ranked taxa were in the Ampullariidae, Hygromiidae, Cochlicellidae, Helicidae, Veronicellidae, Succineidae, Achatinidae, and Planorbidae. We validated the risk assessment model by scoring a suite of non-native snail and slug species already present in the United States. The list is not definitive but rather is offered as a framework for additional research. There remain important gaps in biological knowledge of many of the taxa evaluated, and rigorous reporting of economic impacts is extremely limited. We expect the prioritizing and listing of taxa to be dynamic, not only as these knowledge gaps are filled but also as environmental, agricultural, international trade, and societal factors change.

Insights from an Integrated View of the Biology of Apple Snails (Caenogastropoda: Ampullariidae)

ABSTRACT Apple snails (Ampullariidae) are among the largest and most ecologically important freshwater snails. The introduction of multiple species has reinvigorated the field and spurred a burgeoning body of research since the early 1990s, particularly regarding two species introduced to Asian wetlands and elsewhere, where they have become serious agricultural pests. This review places these recent advances in the context of previous work, across diverse fields ranging from phylogenetics and biogeography through ecology and developmental biology, and the more applied areas of environmental health and human disease. The review does not deal with the role of ampullariids as pests, nor their control and management, as this has been substantially reviewed elsewhere. Despite this large and diverse body of research, significant gaps in knowledge of these important snails remain, particularly in a comparative framework. The great majority of the work to date concerns a single species, Pomacea canaliculata, which we see as having the potential to become a model organism in a wide range of fields. However, additional comparative data are essential for understanding this diverse and potentially informative group. With the rapid advances in genomic technologies, many questions, seemingly intractable two decades ago, can be addressed, and ampullariids will provide valuable insights to our understanding across diverse fields in integrative biology.

Mass extinction in poorly known taxa

Significance Since the 1980s, many biologists have concluded that the earth is in the midst of a massive biodiversity extinction crisis caused by human activities. Yet fewer than 1,000 of the planet’s 1.9 million known species are officially recorded as extinct. Skeptics have therefore asked “Is there really a crisis?” Mammals and birds provide the most robust data, because the status of almost all has been assessed. Invertebrates constitute over 99% of species diversity, but the status of only a tiny fraction has been assessed, thereby dramatically underestimating overall levels of extinction. Using data on terrestrial invertebrates, this study estimates that we may already have lost 7% of the species on Earth and that the biodiversity crisis is real. Since the 1980s, many have suggested we are in the midst of a massive extinction crisis, yet only 799 (0.04%) of the 1.9 million known recent species are recorded as extinct, questioning the reality of the crisis. This low figure is due to the fact that the status of very few invertebrates, which represent the bulk of biodiversity, have been evaluated. Here we show, based on extrapolation from a random sample of land snail species via two independent approaches, that we may already have lost 7% (130,000 extinctions) of the species on Earth. However, this loss is masked by the emphasis on terrestrial vertebrates, the target of most conservation actions. Projections of species extinction rates are controversial because invertebrates are essentially excluded from these scenarios. Invertebrates can and must be assessed if we are to obtain a more realistic picture of the sixth extinction crisis.