Biol Invasions https://doi.org/10.1007/s10530-020-02436-w (0123456789().,-volV)(0123456789().,-volV) REVIEW Negative impacts of invasive predators used as biological control agents against the pest snail Lissachatina fulica: the snail Euglandina ‘rosea’ and the flatworm Platydemus manokwari Justin Gerlach . Gary M. Barker . Cindy S. Bick . Philippe Bouchet . Gilianne Brodie . Carl C. Christensen . Timothy Collins . Trevor Coote . Robert H. Cowie . G. Curt Fiedler . Owen L. Griffiths . F. B. Vincent Florens . Kenneth A. Hayes . Jaynee Kim . Jean-Yves Meyer . Wallace M. Meyer III . Ira Richling . John D. Slapcinsky . Leigh Winsor . Norine W. Yeung Received: 1 March 2020 / Accepted: 8 December 2020 Ó The Author(s) 2020 Abstract Since 1955 snails of the Euglandina rosea snails. Since 1993 there have been unofficial releases species complex and Platydemus manokwari flat- of Euglandina within island groups. Only three official worms were widely introduced in attempted biological P. manokwari releases took place, but new populations control of giant African snails (Lissachatina fulica) are being recorded at an increasing rate, probably but have been implicated in the mass extinction of because of accidental introduction. Claims that these Pacific island snails. We review the histories of the 60 predators controlled L. fulica cannot be substantiated; introductions and their impacts on L. fulica and native in some cases pest snail declines coincided with predator arrival but concomitant declines occurred elsewhere in the absence of the predator and the Supplementary Information The online version contains declines in some cases were only temporary. In the supplementary material available at (https://doi.org/10.1007/ Hawaiian Islands, although there had been some s10530-020-02436-w). J. Gerlach (&) C. C. Christensen Á K. A. Hayes Á J. Kim Á 133 Cherry Hinton Road, Cambridge CB1 7BX, UK W. M. Meyer III Á N. W. Yeung e-mail: [email protected] Bernice Pauahi Bishop Museum, Honolulu, HI, USA G. M. Barker Landcare Research, Lincoln, New Zealand T. Collins Department of Biological Sciences, Florida International C. S. Bick University, Miami, FL, USA University of Michigan Museum of Zoology, Ann Arbor, MI, USA T. Coote B.P. 44 921, Fare Tony, Papeete, Tahiti, French Polynesia P. Bouchet Muse´um national d’Histoire naturelle, Paris, France R. H. Cowie Pacific Biosciences Research Center, University of G. Brodie Hawaii, Honolulu, HI, USA Institute of Applied Sciences, University of the South Pacific, Suva, Fiji G. C. Fiedler Division of Natural Sciences, Biology, University of Guam, Mangilao, GUAM, USA 123 J. Gerlach et al. earlier declines of native snails, the Euglandina rate is probably due in part to many snail species impacts on native snails are clear with rapid decline having very restricted geographical ranges, combined of many endemic Hawaiian Achatinellinae following with low mobility, making them very sensitive to predator arrival. In the Society Islands, Partulidae tree changes in land use, habitat quality and/or a range of snail populations remained stable until Euglandina non-native predators (Lydeard et al. 2004;Re´gnier introduction, when declines were extremely rapid with et al. 2015b; Chiba and Cowie 2016; Cowie et al. an exact correspondence between predator arrival and 2017). This high extinction in land snails may be tree snail decline. Platydemus manokwari invasion representative of invertebrates as a whole (Re´gnier coincides with native snail declines on some islands, et al. 2015a), but this is difficult to ascertain because of notably the Ogasawara Islands of Japan, and its the lack of data for the vast majority of invertebrate invasion of Florida has led to mass mortality of species (Bouchet et al. 2002; Brodie et al. 2017). Liguus spp. tree snails. We conclude that Euglandina However, because mollusc shells persist for some time and P. manokwari are not effective biocontrol agents, after the animal dies, it is possible to develop a better but do have major negative effects on native snail picture of historical distribution and extinction in ter- faunas. These predatory snails and flatworms are restrial snails than in other invertebrate groups generalist predators and as such are not suitable for (Pearce 2008). biological control. The majority of identified recent mollusc extinc- tions have been of gastropod land snails on tropi- Keywords Euglandina Á Platydemus Á Lissachatina Á cal islands (Re´gnier et al. 2009). Although some Invasion Á Biocontrol Á Extinction modern species may have gone extinct naturally before facing human influence, many extinctions have been attributed to early habitat loss following the arrival of people (Florens and Griffiths 2000; Introduction Richling and Bouchet 2013), although such loss continues and its effects are exacerbated by more Species extinction rates are currently higher than recent predation by introduced species (Cowie et al. background levels, representing a sixth mass extinc- 2017). Nonetheless, there have been no attempts to tion event (Waters et al. 2014; Ceballos et al. 2015). quantify either the range of plausible anthropogenic The levels of extinction are not evenly spread across drivers of extinction, or the interactions and synergies taxa with particularly high levels reported for land among these drivers, on land snail declines in tropical snails (Lydeard et al. 2004;Re´gnier et al. and subtropical oceanic island systems. This is despite 2009, 2015a, b) estimated overall at 10% loss and an growing international recognition that our ability to extraordinary 75% extinction of Polynesian island partition species losses among multiple drivers is land snails (Re´gnier et al. 2015a). This high extinction critical to advancing our understanding and mitigation O. L. Griffiths I. Richling Bioculture Ltd., Senneville, Rivie`re des Anguilles, Stuttgart State Museum of Natural History, Stuttgart, Mauritius Germany F. B. V. Florens J. D. Slapcinsky Tropical Island Biodiversity, Ecology and Conservation Florida Museum of Natural History, Gainesville, Pole of Research, University of Mauritius, Le Re´duit, FL, USA Mauritius L. Winsor J.-Y. Meyer College of Science and Engineering, James Cook De´le´gation a` la Recherche de la Polyne´sie franc¸aise, University, Townsville, QLD, Australia Papeete, Tahiti, French Polynesia W. M. Meyer III Pomona College Biology Department, Claremont, CA, USA 123 Negative impacts of invasive predators used as biological control of extinction processes (Sala et al. 2000). Among non- commonly accidentally through human activities. native predators adversely affecting land snails, Eug- These include predatory snails such as Gulella bicolor, landina ‘rosea’ (Spiraxidae) (now known to be a Streptostele musaecola and Oxychilus alliarius complex of species, of which at least two have been (Cowie 1997; Meyer and Cowie 2010; Curry et al. widely introduced: Meyer et al. 2017) has been 2016, 2020), various flatworms, carabid beetles, ants, considered most important (Lydeard et al. 2004; phorid and sarcophagid flies, nemertean ribbon- Re´gnier et al. 2009). Introduced deliberately by agri- worms, and not inconsiderable numbers of helminth culture authorities since the 1950s (Cowie 1998a)asa parasites (Barker 2004). For the most part, the impact biological control agent for the giant African snail of these non-native species on land snail communities Lissachatina fulica (Achatinidae), an estimated 134 has yet to be examined in any depth and is beyond the land snail extinctions have been attributed to preda- scope of this review. tion by it (Re´gnier et al. 2009). More recently, the New Guinea flatworm, Platydemus manokwari has emerged as an important threat to land snails; it is a Methods particularly voracious predator (Sugiura 2010) that will even climb trees to prey on arboreal snails This review covers areas where Euglandina spp. and (Sugiura and Yamaura 2009). Following a 1981 Platydemus manokwari have been introduced delib- release in the Philippines (Muniappan et al. 1986)as erately as biological control agents (principally for a biological control agent for L. fulica, P. manok- control of Lissachatina fulica), and where they have wari has spread and continues to spread to Pacific been spread inadvertently to locations other than those island and continental sites (a greenhouse in France, where the biocontrol programs were implemented. For mainland North America and south-east Asia; Justine each of these predators, data on their historical et al. 2014, 2015) and has been heavily implicated in distribution, impacts and present status are collated. native land snail population declines and extinctions These are summarised in the text below and in Table 1 (Sugiura and Yamaura 2009; Chiba and Cowie 2016; for each geographic region, with specific details given Cowie et al. 2017). Due to their impacts on land snail for areas where introductions are known to have populations both Euglandina ‘rosea’ and Platydemus limited impacts (Western Indian Ocean), high impacts manokwari are listed in ‘100 of the World’s Worst (Polynesia), are currently spreading (Florida) or are of Invasive Species’ (Lowe et al. 2000). We synthesized historical interest (New Guinea). The only introduc- information regarding the distribution and status of the tion of Euglandina species to the African mainland is Euglandina rosea species complex and of Platydemus not considered here, as the only information associated manokwari, and their impacts on L. fulica and native with this attempt to control introduced