Invasive Land Snails and Slugs in North America
National Plant Diagnostic Network Malacology Workshop UC Davis 16-17 June 2015
David G. Robinson USDA APHIS PPQ National Malacology Laboratory Academy of Natural Sciences of Drexel University, Philadelphia, PA INTRODUCTION
Most snails and slugs found associated with human habitation and agricultural areas, and other areas of human disturbance (= synanthropic species) belong to invasive (non-native) species Native terrestrial species are generally found in undisturbed areas, and may be used as indicators of the relative health of a natural environment; native species as part of a high biodiversity indicate a stable habitat that more likely to be resistant to invasives Do invasive species outcompete native species, or merely occupy disturbed areas where the native species have already been driven out ? The external characters of a slug, or the snail’s shell has traditionally been used to identify the species Increasingly, the genitalia are required to identify the snail’s species Molecular techniques are also being used to further separate cryptic species that are inseparable using anatomical or shell characters Selected quarantine-significant species that are invasive in the continental United States and their diagnostic characters will be discussed here Pulmonate slug (from Kerney & Cameron, 1979)
Traditionally slugs were described using external morphological characters Introduced terrestrial slug families AGRIOLIMACIDAE
LIMACIDAE
MILACIDAE
Pulmonate slugs (from Herbert, 1997) ARIONIDAE
VERONICELLIDAE
Pulmonate slugs (from Herbert, 1997) As malacologists began to study the internal anatomy, especially the genitalia, this led to the recognition that there were many more species than previously thought, while external characters (e.g. color) became less important
Basic dissection of terrestrial slug (from Kerney & Cameron, 1979) In 1999, the USDA initiated the North American Slug Project, to document all the invasive slugs and their distributions in the United States and Canada Slugs are being submitted from across the country, with the ultimate goal of documenting all invasives and their distribution , on a county by county basis Dissection of all specimens is required, with molecular analysis (using CO1 and 16S genes) being used to check dubious identifications
Deroceras laeve (Müller, 1774) Genitalia of D. laeve (from Barker, 1999) Deroceras invadens (Reise et al., 2011) (photo courtesy H. Reise)
(Reproductive anatomy from G. Barker, 1999)
Lehmannia valentiana (A. de Férussac, 1821) Unfortunately, the molecular analysis of the Palearctic Arionidae has made identification of the species more complicated Arion s.s. consists of 3 anatomically-defined taxa: Arion ater (Linné, 1758), A. rufus (Linné, 1758), and A. vulgaris Moquin-Tandon, 1855 (= A. lusitanicus non Mabille, 1868); from molecular evidence, there are 4 distinct clades, designated A,B,C, & D. However, the 3 anatomical taxa do not correspond exactly with the molecular clades: A. ater consists of clade A A. rufus consists of clades A, B & D A. vulgaris consists of clades A & C
Arion vulgaris Moquin-Tandon, 1855 from Germany (photo courtesy of I. Richling) In the United States and Canada, we have found no evidence of any anatomical A. ater ALL of the large Arion slugs (i.e. Arion s.s.) analyzed from North America are anatomically A . rufus, almost all belonging to clades B & D; only a single clade A specimen has been found to date (in OR)
Arion rufus (Linné, 1758) (photo at top courtesy of M. Hitchcox; middle photo courtesy of P. Marquez; bottom photo courtesy of I. Richling) Similarly, the anatomical species A. subfuscus (Draparnaud, 1801) consists of at least two species, including the cryptic A. fuscus (Müller, 1744) , plus at least 5 subclades, S1-S5
In North America, we have confirmed the presence of A. fuscus and A. subfuscus – subclades S1 and S2, with the latter restricted to the northeast USA At present we are far from documenting all the invasive slugs in the United States, and our molecular studies are only at the early stages of the project Pulmonate snail shell (from Kerney & Cameron, 1979)
Similarly, in the “GOOD OL’ DAYS,” conchologists identified snails described the shell using diagnostic characters Species descriptions were often based on long dead (faded) museum specimens Little or nothing was known of the living animal or its anatomy
Currently malacologists dissect the snail’s body to find diagnostic characters Initial preparation of snail (drowning in water for 12 hours, then preserving in 75- 80% ethanol) [Optionally anesthetize using tobacco, menthol crystals, etc.] Removal of the snail from its shell Exposure of organs by opening the body cavity between the head and the mantle [Optionally access the body cavity through the lung area, above the mantle] Genitalia usually pure white in color, on the right side of Basic dissection of terrestrial pulmonate snail the body (from Kerney & Cameron, 1979) Male and female tracts unite at the atrium, which opens through the genital pore (= gonopore) The “Brown garden snail” – Cornu aspersum (Müller, 1774) (= Helix aspersa, Cryptomphalus aspersus, Cantareus aspersus) An edible snail widely (and intentionally) introduced worldwide, in temperate, subtropical and tropical zones Introduced into the continental United States in the 1850s A pest of a wide range of agricultural and horticultural plants, especially Citrus spp. Currently costs $7-10 million in control/suppression programs in California alone Currently widespread along the West Coast (CA, OR, WA), the southern tier of states, with periodic infestations elsewhere (e.g. NJ, PA, NC, etc.) with control programs in place As an example of pulmonate Cornu aspersum (Müller, 1774) genitalic anatomy: Genitalia of C. aspersum (Müller, 1774) (from Kerney & Cameron, 1979) FEMALE: One large dart sac (= stylophore) containing a large calcareous dart Two mucus glands, with numerous branches (“spaghetti”) Very long bursa copulatrix duct that branches into two, one leading to the diverticulum, the other to the bursa copulatrix reservoir MALE: The phallus extends from the atrium to (usually) where the penial retractor muscle is attached The epiphallus extends from (usually) the penial retractor muscle attachment to where the vas deferens connects The flagellum extends beyond where the vas deferens connects The vas deferens connects to the prostate (not shown) The relative lengths and shape of male genitalia can be diagnostic Introduced species: Theba pisana (Müller, 1774) - HELICIDAE Theba pisana is considered by most agricultural authorities worldwide to be the worst snail pest It is believed to be originally from western North Africa (Morocco area); it spread throughout the Mediterranean Basin during Roman times Introduced to California in 1914 (Hanna, 1966), and subsequently re-introduced several times after being “successfully eradicated” (or perhaps it was never completely eradicated ?) In the mid-1990’s, the last program by the California Department of Food and Agriculture (CDFA) was stopped just short of a complete eradication; the remaining population was reportedly in an isolated area in San Diego County, and presumably not considered a threat to agriculture A USDA PPQ survey in June 2005 showed that T. pisana is staging a “come-back” and was found throughout San Diego County Introduced species: Theba pisana (Müller, 1774) (continued) Theba pisana is a very serious pest in southern Australia causing severe losses in wheat, barley, and oilseed rape It also reaches such high numbers that it clogs up harvesting machinery T. pisana is a pest as (a) a voracious plant feeder and (b) due to its massing behavior
Heavy infestations of T. pisana in the York Peninsula, South Australia; snails massing on fence posts, and on wheat stubble after harvest (photos courtesy of M. Leyson and A. Lush) Introduced species: Theba pisana (Müller, 1774) (continued)
2012-2014 infestations of Theba pisana and other species introduced into Australia from the Mediterranean species are the worst in Australia’s history and many farmers are selling or abandoning their farms
Introduced species: Theba pisana (Müller, 1774) (continued)
Infestations of Theba pisana on ornamental fruit trees in San Diego County
Infestations of Theba pisana on grass on low shrubs in San Diego County Introduced species: Theba pisana (Müller, 1774) (continued)
FEMALE: One dart sac (=stylophore) containing a large calcaerous dart Two mucus glands, not branched with distinct alveolar structure MALE: The phallus is swollen; internally with a double verge, the first very broad, the second protruding into atrial section of phallus The epiphallus is well developed, but flagellum is rudimentary (barely visible)
Genitalia of Theba pisana (Müller, 1774) (from Schileyko, 2006) Introduced species: Theba pisana (Müller, 1774) (continued)
Distribution of Theba pisana (Müller, 1774) in the continental United States: San Diego County, California Introduced species: Trochoidea elegans (Gmelin, 1791) - HYGROMIIDAE Established in a graveyard in Charleston, SC, in the late 1800s, and still surviving well into the 1940s USDA PPQ surveys in 2002, 2004, and 2005 did not find any specimens Introduced into Sunny Point, NC, possibly in November 1999; detected May 2000; eradicated within a year Up to 8 mm in height, and 10 mm in maximum diameter. Shell conical above, very flattened below, with sharply keeled, somewhat overlapping, flattened whorls. Genitalia of T. elegans (Gmelin, 1791) 4 functional stylophores (from Pilsbry, 1939) Long flagellum Introduced species: Trochoidea elegans (Gmelin, 1791) (continued)
Distribution of T. elegans (Gmelin, 1791 in the continental United States: Charleston, SC (died out ?), and MOTSU, Wilmington, NC (eradicated) Introduced species: Xeropicta sp. - HYGROMIIDAE Introduced into Sunny Point, NC, possibly in November 1999; detected May 2000; eradicated within a year Xeropicta sp. have very distinctive genitalia: An inner pair of stylophores and an outer pair of accessory sacs (lacking darts) that are always longer than the dart sacs, Four mucus glands, each of which is biramous Genitalia of Xeropicta krynickii (Krynicki, 1833) (producing 8 branches) (from Schileyko, 1978) A large sarcobellum is associated with the male genitalia. The epiphallus is cylindrical and longer than the phallus, with the retractor muscle attached to its anterior portion, rather than to the penis itself Introduced species: Xeropicta sp. (continued)
Distribution of Xeropicta sp. in the continental United States: MOTSU, Wilmington, NC (eradicated) Introduced species: Cernuella cisalpina (Rossmässler, 1837) - HYGROMIIDAE Long established in Virginia and North Carolina (since WWII ?) and misidentified as Helicopsis striata (Müller, 1774) Shell highly variable; up to 8mm in height, and 12mm in diameter Open umbilcus; shell with fine radial riblets Two stylophores (side by side, almost indistinguishable), to one side of the vagina, only the outer one functional
Genitalia of C. cisalpina (Rossmässler, 1837) (from Manganelli & Giusti, 1987) Introduced species: Cernuella cisalpina (Rossmässler, 1837) (continued)
Distribution of C. cisalpina (Rossmässler, 1837) in the continental United States: barrier islands and coastal North Carolina and Virginia Introduced species: Cernuella virgata (da Costa, 1778) - HYGROMIIDAE
The species is another major pest of cereal crops in southern Australia Together with the helicid Theba pisana, massive eradication/suppression programs are being conducted in Australia Up to 19 mm in height, and 25 mm in maximum diameter. It differs from its congener, C. cisalpina, by having a higher spire, lacking fine regular riblets, and by the umbilicus sometimes more obscured by the reflected lip.
(photos courtesy of P. Marquez) Introduced species: Cernuella virgata (da Costa, 1778) (continued)
Together with Theba pisana, this species can reach such high numbers that it interferes with agricultural production, especially of cereals At times, the biomass of the snails exceeds that of the grain being harvested
Populations of C. virgata (da Costa, 1778) on wheat in southern Australia (photos courtesy of J. Coupland) Introduced species: Cernuella virgata (da Costa, 1778) (continued) Two stylophores (side by side, almost indistinguishable), to one side of the vagina, only the outer one functional Virtually indistinguishable from Cernuella cisalpina – are they the same species ? Molecular studies being conducted at the University of Siena, Italy on the entire group
Genitalia of C. virgata (da Costa, 1778) (dissection and photos courtesy of P. Marquez) Introduced species: Cernuella virgata (da Costa, 1778) (continued)
Distribution of C. virgata (da Costa, 1778) in the continental United States: Seattle, Washington (currently being eradicated), and San Diego, California (status unknown) Introduced species: Hygromia cinctella (Draparnaud, 1801) - HYGROMIIDAE
Introduced into Detroit, MI, in September 2004; eradicated almost immediately; officially declared eradicated 2007 Shell angulate at periphery, pale brown with a distinct white strip along the edge Two stylophores of equal size, set to one side of the vagina Twisted darts are shot by a characteristic conical structure located in the vagina Phallus and epiphallus of medium length (flagellum very small) Long bursa copulatrix duct leading to a barely differentiated bursa
Genitalia of H. cinctella (Draparnaud, 1801) (from Giusti & Manganelli, 1987)
(photo courtesy of J. Zablotny) Introduced species: Hygromia cinctella (Draparnaud, 1801) (continued)
Distribution of H. cinctella (Draparnaud, 1801) in the continental United States: one container yard in Detroit, Michigan - exterminated; new population in Columbus, Ohio (2012) Introduced species: Xerolenta obvia (Menke, 1828) - HYGROMIIDAE Reported established in southern Canada over 20 years ago Introduced into Detroit, MI; detected 2002; eradication currently in progress The shell of the Detroit populations is atypical: the last whorl descends considerably at the aperture (cf. Helicella itala (Linné, 1758)) Characterized by a single pair of stylophores, squared off at the base, placed on either side of the oviduct below the mucus glands, that contain Genitalia of Xerolenta obvia (Menke, 1828) simple, hollow, elongated (from Schileyko, 1978) conical darts. The epiphallus is much shorter than the phallus, the tip of the verge squared off. The bursa copulatrix has a characteristic shape. Introduced species: Xerolenta obvia (Menke, 1838) (continued)
Distribution of X. obvia (Menke, 1838) in the continental United States: several container yards in Detroit, Michigan (and also in Windsor, Canada); new populations in Cascade and Chouteau counties, Montana (2012) Introduced species: Xerolenta obvia (Menke, 1828) – (continued)
Populations of X. obvia (Menke, 1828) in the Detroit area, MI Introduced species: Xerolenta obvia (Menke, 1828) – (continued)
Populations of X. obvia in Montana
Variation of X. obvia in Montana [photos courtesy of P. Marquez)
Compare with X. obvia from Detroit, MI Introduced species: Candidula intersecta (Poiret, 1801) - HYGROMIIDAE Detected in 2004 in Detroit; eradicated. Seattle populations currently being eradicated Long established (1940s ?) population in 2 counties (Coos and Curry Co.) in Oregon are currently being assessed; submissions from a third county are awaiting confirmation Shell up to 8 mm in height, and 13 mm in maximum diameter. Shell somewhat C. intersecta (Poiret, 1801) in Coos Bay, OR depressed, with axial (photo courtesy of M. Hitchcox) riblets; coloration very variable Shell also has fine spiral striations, particularly noticeable between the axial riblets A serious pest of stone fruit, and also of spring wheat Introduced species: Candidula intersecta (Poiret, 1801) (continued)
Distribution of C. intersecta (Poiret, 1801) in the continental United States: Oregon and Washington Introduced species: Candidula intersecta (Poiret, 1801) (continued)
Candidula species have a thick, short phallus, a slightly longer epiphallus, and a short flagellum One large stylophore (dart-sac) that is characteristically pointed A hammer-shaped bursa copulatrix reservoir
Genitalia of C. intersecta (Poiret, 1801) (dissection and photos courtesy of P. Marquez) Introduced species: Monacha cartusiana (Müller, 1774) - HYGROMIIDAE First detected in Dover, DE, in 1999 Substantial populations found in Chicago, IL, in 2002; a suppression program is currently in place A small population was detected in Detroit, MI, in 2004, and was quickly exterminated Plain white shell with a tiny umbilicus Monacha species lack stylophores, which are replaced by a long “appendicula” – a vestigial stylophore ? “The shorter, broader basal section of the appendicula is rather well delimited against the Genitalia of M. cartusiana (Müller, 1831) long, narrow apical section. (from Hausdorf, 2000) There is a distinct bulge at the vagina. The two glandulae mucosae (mucus glands) are slightly ramified. The bursa of the bursa copulatrix is ± rounded triangular.” (Hausdorf, 2000) Introduced species: Monacha cartusiana (Müller, 1774) (continued)
Distribution of M. cartusiana (Müller, 1774) in the continental United States: Chicago, IL, Detroit, MI (eradicated), and Dover, DE Introduced species: Monacha cartusiana (Müller, 1774) (continued)
First detected in the container yard at Schiller Park (Chicago), IL, in 2002 Currently a suppression program is in place; complete eradication may not be possible
Monacha cartusiana in Schiller Park, IL Introduced species: Monacha syriaca (Ehrenberg, 1831) - HYGROMIIDAE
Monacha syriaca was introduced on military containers into Sunny Point (MOTSU), NC, possibly in November 1999; detected May 2000 A small isolated population was found in Fort Navajo, AZ in June 2000 and was immediately eradicated The Sunny Point population eradicated within a year. Cost: approximately $1.4 million After three years of negative surveys, officially declared as eradicated Periodic surveys for this species and other hygromiids are still being made Genitalia of M. syriaca (Ehrenberg, 1831) Brightly colored shell, lacking an (from Hausdorf, 2002) umbilicus Vagina lacks the bulge seen in Monacha cartusiana (Müller, 1774) Introduced species: Bradybaena similaris (A. de Férussac,1822) - BRADYBAENIDAE
Introduced into the United States in the 18th century Up to 12 mm in height, 18 mm in maximum diameter. Shell globular, with moderately elevated spire. Plain reddish- brown or straw colour, some individuals with a dark brown peripheral band. Umbilicus open, partly concealed by the reflected peristome. One central stylophore with two to three mucus glands Genitalia of B. similaris (Rang, 1831) attached to it (from Schileyko, 2004) Curved, swollen phallus, with epiphallus starting at the sharp constriction Introduced species: Bradybaena similaris (A. de Férussac, 1822) (continued)
Distribution of B. similaris (A. de Férussac, 1822) in the continental United States: widespread in Gulf and southeastern states, and in botanical gardens nationwide Introduced species: Bradybaena similaris (A. de Férussac, 1822) (continued)
Bradybaena similaris is a serious pest of Citrus in Puerto Rico (García, 2004) It has been reported as a pest in Louisiana (Dundee & Cancienne, 1978) Most Citrus-growing states in the United States seem to be oblivious to the potential damage this snail could to their industries Damage by B. similaris on grapefruit should B. similaris cease to be a minor (Citrus paradisi) (photos: W. García) nuisance and become a serious pest, resulting from a slight shift in biotic and abiotic factors The snail is also known as a serious pest of coffee
Damage by B. similaris on ethrog (Citrus medica) (photos: W. García) Introduced species: Bradybaena similaris (A. de Férussac, 1822) (continued) A serious Citrus pest in southern China, where it is probably native Bradybaena similaris has been reported a serious pest in vegetable and flower gardens in Java. It is considered to be one of the most important pests of grape in Taiwan, feedings on leaf- and flower-buds, defoliation of new leaves, destruction of the flowers and spoilage of the fruit, as well as a variety of commercial and ornamental trees, including “all principal crop species” in Taiwan but with preference for longan (Dimocarpus longan) and mango (Mangifera indica). It has also been shown to damage various Citrus sp. in Louisiana, by rasping through the outer peel of the unripe and ripe fruit Damage by B. similaris on (Citrus sp.) down to the inner peel, whereupon (photo: Deng S.-L.) the fruit is attacked by rot fungi. This then attracts nitidulid beetles which damage the fruit further. The species has also been associated with damage to starfruit (Carambola) in the Homestead area of Florida
Introduced species: Cathaica fasciola (Draparnaud, 1801) - HYGROMIIDAE Detected June, 2008 in Detroit, MI; eradication currently in progress. Up to 7.7 mm in height, 14.5 mm in maximum diameter. Shell thick, depressed, almost discoid, very slightly raised apex, with shallow sutures. Axial sculpture of fine riblets. Strong internal apertural rib, that appears as a thick white band behind the aperture. Color a dull white or pale brown,with a chestnut-brown peripheral band One massive stylophore with two very branched mucus glands connected to it by two ducts Genitalia of C. fasciola (Draparnaud, 1831) Thick cylindrical duct connects (from Schileyko, 2004) to the bursa copulatrix (“spermatheca”) Narrow, very elongated phallus Flagellum and epiphallus absent Introduced species: Cathaica fasciola (Draparnaud, 1801) (continued)
Distribution of C. fasciola (Draparnaud, 1801) in the continental United States: a container yard in Detroit, MI - eradicated Introduced species: Lissachatina fulica (Bowdich, 1822) - ACHATINIDAE
We cannot forget the giant African snail, Lissachatina fulica (Bowdich, 1822) This species, at least, can still be identified from its shell; dissection of the genitalia is hardly necessary Once established in Miami-Dade, Florida – introduced in 1966, and finally detected in 1969 By 1973, some 18,000 snails and innumerable eggs had been destroyed and by 1975, the infestation was declared successfully eradicated at a cost of over $1 million It threatens the United States once again, as it is now established throughout the West Indies, South American, and in Miami, Florida It is a principal vector of Angiostrongylus cantonensis, a parasitic nematode that causes cerebral angiostrongyliasis in humans and livestock Potential risk for GAS infestation on the U.S. mainland – (courtesy of G. Fowler & J. Smith (CPHST PERAL) Introduced species: Lissachatina fulica (Bowdich, 1822) (continued)
GAS is regularly intercepted in passenger baggage from Hawai‘i, South American and the West Indies Pet snails already in the US may escape into the environment - GAS forms a valuable part of an illegal pet trade Other large achatinid snails (at left) have also been found being offered for sale in pet stores or over the Internet In 1994 and the early part of 1995, the USDA conducted a public information campaign and a “blitz” in pet stores, classrooms and elsewhere, seizing almost 7000 A. fulica snails (and innumerable eggs) Achatina achatina Archachatina marginata
Introduced species: Achatina (Lissachatina) fulica Bowdich, 1822 (continued)
Total # seizures # Snails seized State
Wisconsin 75 1364 Michigan 18 1553 Ohio 5 3139 Illinois 8 98 Indiana 5 300 Pennsylvania 1 170 Virginia 3 143 West Virginia 1 102 New Jersey 1 1 Puerto Rico 1 1 Giant African snails seized by USDA APHIS PPQ SITC officers in 2004-early 2005 SUMMARY
All possible pathways into the US need to be monitored, including maritime ports and airports, border crossings (including Canada), as well as mail and international shipping services (FedEX, DHL, etc.) The USDA currently has a reduced presence at US ports, inspecting only horticultural imports (live plants); all other imported commodities are inspected by DHS Our ability to detect invasive terrestrial snails and slugs from the United States depends on our ability to identify the species correctly and as quickly as possible Pet shops, swap meets etc. should be monitored for “pet” snails being sold that may be dangerous agricultural pests or disease carriers We urge all biologists and other cooperators nationwide to be on the alert for new, previously unreported invasive land snails or slugs Potential invasive species should be submitted for confirmation of ID as quickly as possible Existing control programs notwithstanding, the possibility that snail and slug species have already spread further afield from known infestation sites has to be taken into account
ACKNOWLEDGMENTS
Dick Hoenisch, National Plant Diagnostic Network USDA APHIS PPQ Port Identifiers, especially Fred Zimmerman (Miami FL), Willie Tang (Miami FL), Greg Bartman (Los Angeles CA), Patrick Marquez (San Diego CA), Jim Zablotny (Detroit MI) Geoff Baker and Angela Lush, CSIRO, Australia Gary Barker, New Zealand USDA APHIS PPQ Pest Survey Specialists, especially Mark Hitchcox (OR), Jim Manor (MI), Brian Kopper (NC), Norberto Gabriel (PR), Avi Eitam (OH) USDA APHIS PPQ SITC officers Brian Sullivan (USDA APHIS PPQ Michigan) Gary Adams and Ian Foley (USDA APHIS PPQ Montana) Donna Rise and Cam Lay (Montana Department of Agriculture) Carolyn Cohen, USDA APHIS Angela Fields, University of the West Indies at Cave Hill, Barbados Igor Muratov, Natal Museum, South Africa Anatoly Schileyko, Moscow Zoological Museum, Moscow, Russian Federation Norman Barr and Matt Ciomperlik, USDA APHIS PPQ CPHST Gary Rosenberg, Academy of Natural Sciences, Philadelphia PA the numerous Safeguarding officers of USDA APHIS PPQ nationwide