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A reprint from American Scientist the magazine of Sigma Xi, The Scientific Research Society

This reprint is provided for personal and noncommercial use. For any other use, please send a request to Permissions, American Scientist, P.O. Box 13975, Research Triangle Park, NC, 27709, U.S.A., or by electronic mail to [email protected]. ©Sigma Xi, The Scientific Research Society and other rightsholders Invasion of the

Easily hidden in imported , some land flatworms are conquering the world.

Ronald Sluys

robably a million more Ameri- to have invaded , Europeans succinctly and appropriately described cans have heard the word already had cause for alarm: Another these land flatworms as follows: “ because of me,” says invasive land flatworm, In general form they resemble lit- my colleague Jean-Lou Jus- triangulatus, was known to have reduced tle slugs, but are very much nar- Ptine, who is an expert on these - numbers in the British Isles. rower in proportion, and several isms at the National Museum of Natu- Ancestors of terrestrial flatworms of the are beautifully co- ral History in Paris, as he wrote in an colonized the land, from the sea or loured with longitudinal stripes. email to me last . In 2014, Justine freshwater, hundreds of millions of announced the discovery in France of ago. The current worldwide oc- Darwin took some of the a land flatworm originally from New currence of these terrestrial worms is that he had collected in Tasmania on Guinea, manokwari, which is a testament to their remarkable evo- board the Beagle and managed to keep considered by the International Union lutionary success in occupying a new them alive for two months. Never shy- for the Conservation of Nature to be niche on land. Almost nothing appears ing away from experiments, he cut one of the 100 worst . It to eat these flatworms, and they are some in half and discovered was the first time that P. manokwari had able to regenerate even when cut in that after 25 days each piece had re- been seen on the European continent. two. A land flatworm also will repro- generated to an almost complete ani- This land flatworm is particularly noto- duce asexually by fragmentation: The mal. About 18 months earlier he had rious because it spreads easily and eats anterior and posterior halves of its collected other species of land flat- native and , thereby body break apart, and the posterior worms from forests along the Chilean affecting local ecosystems. In 2015, Jus- half crawls around headless until it coast. Always a keen observer, he had tine reported finding P. manokwari in grows a new head in about 15 days, noticed that when these worms experi- the United States. Before these two ma- while the front half grows a new tail. ence adverse conditions—for example, jor continental introductions, the New Until recently, this obscure group of when they are handled by humans— Guinea flatworm had been a problem had not received much they may very quickly, before one’s on a smattering of Indo-Pacific islands attention, even though a small group of , disintegrate into a slimy mass. but had not reached any mainland, at natural historians, including me, had Little could Darwin have suspected least not to anyone’s knowledge. But begun monitoring them. Justine’s lat- that 180 years later he would have been now they seem to be popping up ev- est discoveries sparked an avalanche of able to collect land flatworms in Eng- erywhere, and they are not the only records of land flatworm introductions land that originated from the Southern species doing so. and have brought attention to the ease Hemisphere. How could these appar- Land flatworms, a group of about 910 with which these organisms spread ently delicate animals have reached the species, typically live in tropical jungles and acclimate to new places. Although Northern Hemisphere—and what can or temperate wooded areas and can sur- the invasion has apparently acceler- we do to stop their continued spread? vive only in moist soil environments. ated and worsened in recent years, our A hint at an answer to the first ques- Many places in the world are being present knowledge is still limited. The tion was presented all the way back invaded by land flatworms that have time is ripe for biologists to unravel the in 1878, still during Darwin’s lifetime, stowed away in the soil of imported or- diversity, ecology, and natural history when a new species of tropical land flat- namental plants. Flatworms may not of land flatworms, so that the environ- was found in the hothouses of seem particularly worrisome or threat- mental implications of their spread the botanical gardens at Kew Park in ening, but they are voracious top-level may be understood and curbed. the London borough of Richmond upon predators of soil organisms, and their Thames. The species was aptly named presence can change nutrient cycling, The First Invasive Land Flatworm kewense after this site. It was endanger native species, and alter an In our shared fascination with these immediately clear that the botanical ecosystem’s community. Indeed, worms, Justine and I have been fol- gardens at Kew represented a curious even before P. manokwari was found lowing in the footsteps of a notable location, because the native distribution predecessor, Charles Darwin. During of other species of Bipalium covers In- his HMS Beagle voyage, Darwin was dia, Southeast Asia, and Madagascar. Ronald Sluys is a senior researcher, specializing in struck by the fact that there is a group In the following years it became clear flatworms, at the Naturalis Biodiversity of free-living flatworms, or , that B. kewense had actually colonized Center in Leiden, the Netherlands. Email: ronald. that actually live on land (most planar- hothouses and similar artificial environ- [email protected]. ians live in freshwater or in the sea). He ments, such as plant nurseries and gar-

288 American Scientist, Volume 104 © 2016 Sigma Xi, The Scientific Research Society. Reproduction with permission only. Contact [email protected]. MYN/Gil Wizen/Nature Picture Library

The first introduced land flatworm discovered, , was found in the botanical generalist carnivores that prey on other gardens in Kew Park on the outskirts of London in 1878. Native to Southeast Asia and intro- organisms such as earth- duced to via the horticultural trade, this land flatworm has since spread throughout worms, snails, slugs, insect larvae, and much of the world. several , including isopods and springtails. Land planarians search den centers, all over the world. But it . From 1963 onward observa- for, attack, and capture prey much larger has also established itself outdoors—for tions of other nonnative land flatworm than themselves. For example, Peter Du- example, in gardens in California, Loui- species from the Southern Hemisphere cey of the State University of New York siana, , and the West Indies. have been reported in the British Isles. at Cortland found that in North America To a large extent B. kewense’s colo- Most of these worms probably orig- the introduced flatworm Bipalium ad- nizing success can be explained by the inated in or ventitium may attack earthworms that worm’s ability to propagate itself by and reached the United Kingdom by have more than 100 times its body mass. fragmentation, an asexual process that transport of ornamental plants. Al- The worms employ different techniques Darwin had already noticed during his though most introduced flatworms to subdue their prey. Among these are experiments on the Beagle. All species were found in greenhouses early on, by physical force, adhesive , and the of Bipalium are hermaphroditic, having the 1980s their numbers had increased use of an effective digestive secretion both testes and ovaries. But in temper- considerably, and the majority of these over the surface of the live prey—or ate regions B. kewense animals rarely new flatworm species had also estab- into it, using a protrusible . The develop a reproductive apparatus and lished themselves in outdoor environ- latter is a muscular, often tube-shaped they therefore are unable to sexually ments. One species, the New Zealand structure that can be protruded out of reproduce. However, on rare occasions flatworm, A. triangulatus, even reached a ventral opening about midway down this flatworm has been known to re- the remote . To date, 15 the flatworm’s lower body surface. This produce sexually as well. species of introduced land flatworms tube leading to the gut can be inserted Almost every year B. kewense is have been found in the British Isles. into the prey, sucking out its contents found in new places—for example, this As these introductions have con- by bits and pieces through peristaltic year they were found on São Miguel tinued, we still know little about the pumping of the pharyngeal muscles. Island in the Azores and on São Tomé myriad of potential ecological effects Recent experimental work by PhD Island in the Gulf of Guinea. It is pre- they could induce. But what we do student Piter Boll, from the Universi- sumed that B. kewense travels the world know does not bode well. dade do Vale do Rio dos Sinos in , as a result of the horticultural trade, has revealed that there are even land transported in pots of tropical plants. Problematic Eating Habits flatworms that specialize in eating oth- That many Britons are keen horticul- Nonnative flatworms can spread ers. The land flatworm that is being turists is well known. Therefore, it is quickly and broadly, and their dietary preyed upon immediately recognizes not surprising that over the years other habits can affect local ecology and na- the danger when it is touched by the land flatworms, hiding themselves in tive species. Darwin thought that land predator or comes across the predator’s imported potted ornamental plants, flatworms feed on rotten wood, but he slime trail and then frantically tries to es- have been introduced into the United was wrong about that. The animals are cape (see: https://youtu.be/-kTUr1t6Z- www.americanscientist.org © 2016 Sigma Xi, The Scientific Research Society. Reproduction 2016 September–October 289 with permission only. Contact [email protected]. The map above of the current distribution of the flatworm, —which­ is considered by the International Union for the Conservation of Nature to be among the top 100 worst invasive species in the world—shows how far the organism has ventured from its native range in New Guinea. The flatworm’s invasion was thought to be confined to the Indo-Pacific region until 2014, when a study led by Jean-Luc Justine of the French National Museum of Natural History showed that its distribution was much broader and more concerning (blue dots). By 2015, Justine had documented additional introductions (red dots). In the photograph at left, P. manokwari is shown eating a Mediterranean by sucking up the prey’s contents through its tubelike pharynx on the underside of its body. Be- cause they are top carnivores in soil ecosystems, some species of invasive land flatworms have caused declines in populations of native earthworms and snails. (Figure from J.-L. Justine et al., PeerJ 3:e1037; photograph by Pierre Gros, from Wikimedia.) yU). There are even situations in which In the northern part of the United States on local ecosystems. In several stud- one species of land flatworm preys on and in native earthworms all ies published between 1989 and 1995, another species of land planarian that but disappeared during the last Ice Rod Blackshaw, who was then at the itself preys on still other species of land Age, which ended about 12,000 years Department of Agriculture in Northern flatworms. ago. New earthworm species arrived Ireland, found that the New Zealand One of the biggest threats that inva- in the New World with the first Euro- flatworm A. triangulatus had a negative sive flatworms present is that they as- pean settlers, and later with fishing bait, effect both on population densities and sault native earthworms that maintain and these species subsequently spread on the species diversity of earthworms soil ecology. Because the so-called Aus- along with roads and human settle- in fields in . That was tralian flatworm, sanguin- ments. Currently in North America as one of the reasons that Hugh Jones, then ea, feeds exclusively on earthworms, much as 30 percent of the earthworm at the University of Manchester, and there was legitimate reason for concern species are . Many his coworkers launched a national flat- in the United Kingdom about the nega- people and organizations in northern worm hunt in 1995, asking gardeners tive impact that this introduced flat- North America try to restrict the spread to search for these worms under paving worm might have on earthworm popu- of the nonindigenous earthworms. In stones, planks, logs, plastic sacks, and lations in agricultural fields. The soil this attempt they probably get some so forth. The responses of 318 people biologist Daniel Dindal from the State help from invasive land flatworms. revealed that introduced Australian and University of New York had shown in Still, native earthworm species left in New Zealand flatworms had infested 1970 that the introduced land flatworm the southern United States could be many regions of the British Isles. It was B. adventitium had become a pest in negatively affected by predatory flat- also clear that their spread was the re- North America because of its preda- worms. Even though introduced spe- sult of the activities of gardeners, who tions in commercial earthworm beds. cies, such as Bipalium pennsylvanicum were transporting potted plants from More recent studies by Ducey on the and B. adventitium, may be ranked as one place to another. distribution and predatory activities of welcome helpers in the battle against B. adventitium have revealed that the nonnative earthworms in North Ameri- Early Land Planarian Finds species is most abundant in areas near ca, another land flatworm that has been The current effort to understand and gardens with exotic and transplanted introduced there, Bipalium vagum, pre- respond to the problem of invasive ornamental plants and that it feeds on fers mollusks as prey. So, according to flatworms began in 1998 with an inter- many species of earthworms. In this Ducey, B. vagum could reduce numbers national workshop on terrestrial flat- North American setting one could ar- of rare native snails, although such ef- worms funded by an intergovernmen- gue that potential eradication or at least fects have not yet been studied in detail. tal agency called the Organization for a reduction in numbers of earthworms Outside North America, ecologists Economic Cooperation and Develop- is no reason for panic, because the have identified other negative effects ment (OECD). The conference was held earthworms themselves are interlopers. that invasive land flatworms have had in New Zealand, at the University of

290 American Scientist, Volume 104 © 2016 Sigma Xi, The Scientific Research Society. Reproduction with permission only. Contact [email protected]. Canterbury in Christchurch. Selected Invasive Flatworms New Zealand ranks as one of the global hotspots of land common name flatworm diversity and was species (if applicable) native range nonnative range the country of origin of sev- eral of the species introduced into the British Isles. Arthurdendyus New Zealand Faroe Islands, Ireland, triangulatus atworm New Zealand United Kingdom There are about 86 species known to be native to New Zealand and many more re- exulans New Zealand United Kingdom main to be described. The OECD workshop estimated Australoplana Australian a land flatworm fauna in sanguinea atworm Australia United Kingdom New Zealand in excess of Bipalium 100 species, a number that adventitium unknown United States dwarfs the handful of native species in both and All over world, North America. From that including the United perspective, more introduc- Bipalium Kingdom and United tions from New Zealand are kewense Indochina States to be expected, a fact that Bipalium France, , and prompted Brian Boag of the multilineatum Japan maybe South Korea Scottish Crop Research Insti- tute in Dundee to nickname Bipalium these invasions the “colo- pennsylvanicum unknown United States nial’s revenge” in one of his Bermuda, journal articles. Bipalium vagum unknown United States In addition to estimating the number of species still Italy, , the to be discovered, as well as Netherlands, United the number of introductions bicolor Australia Kingdom of alien species, the work- , France, shop participants identified New Zealand, Norfolk other gaps in knowledge Caenoplana Australian blue Islands, Spain, United about land flatworms and coerulea garden atworm Australia Kingdom, United States suggested methods for de- Spain, United tecting and controlling alien striata Indomalaysia Kingdom, United States terrestrial flatworms. A vol- ume summarizing the sym- posium was published later andersoni New Zealand United Kingdom that year, and since then has France, the become a benchmark publi- Netherlands, United cation on land flatworms in Marionfyfea sp. New Zealand Kingdom general and invasive species in ­particular. France, Guernsey, Italy, Spain, United Some workshop attendees nungara Brazil Kingdom from the United Kingdom— Boag and Jones, the latter now France, Ireland, at the Natural History Mu- Parakontikia Mexico, New Zealand, seum in London—continued ventrolineata Australia South Africa, United to monitor the flatworm inva- Kingdom, United States sions and their effects in the France, Japan, New British Isles. Unfortunately, Caledonia, , because of the sparseness of , the active experts, worldwide ef- , Tahiti, the Maldives, the Solomon forts to document and man- Islands, United States, age the invasions tapered off various other islands after the 1998 workshop. Platydemus New Guinea in the southeastern Outside the United King- manokwari atworm New Guinea Pacic dom, little action or research was undertaken, prob- ably because of the highly This selection of species of introduced land flatworms, including some of the most pernicious invaders, ­restricted number of special- shows their widespread distribution. www.americanscientist.org © 2016 Sigma Xi, The Scientific Research Society. Reproduction 2016 September–October 291 with permission only. Contact [email protected]. On this 1998 grid map, the number of species of land planarians is shown by location. Colors rived for the first time on two mainland range from the maximum in red to the minimum in dark blue. Over the past 18 years new discov- continents, Europe and North America. eries have added to the number of native species recognized as well as the number of invasive The flood of new European records of species discovered in new places. The current pattern of biodiversity remains similar to the one invasive land flatworms started off in shown here. Still, it should be noted that, for example, about 20 new native species are now rec- 2014 with Justine’s reports on the occur- ognized in Europe, 40 in southeastern and southern Brazil and northeastern Argentina, 9 in the rence in France of the Australian blue Australian territories, and 6 in New Zealand (Figure from R. Sluys, Pedobiologia 42:492). garden flatworm, C. coerulea, and then the New Guinea flatworm P. manokwari. ists and the fact that thus far only a Before the workshop, we biologists In particular, the finding of the latter small number of alien land flatworms knew that B. kewense also inhabits many set alarm bells ringing among ecolo- had been observed. At the time of the places in North America, where it may gists. This flatworm may reach a length workshop a few alien species of land be found outdoors as far north as North of 45 millimeters, or occasionally even flatworms had already been found on Carolina. There are three other nonin- 70 millimeters, and a body width of the European continent, and they were digenous species of Bipalium in North about 5 millimeters. Its natural range is likely inadvertently introduced by 19th- America: B. adventitium (found in 12 indeed presumably New Guinea, but it century horticulturists via the transport states), B. pennsylvanicum (thus far only currently has a much broader distribu- of potted plants. These species included in Pennsylvania), and B. vagum (record- tion in the Indo-Pacific region. It has B. kewense and also the Indo-Malayan ed in Florida, Texas, and Bermuda). been accidentally introduced, probably species Dolichoplana striata, the latter Because only a smattering of species again via the horticultural trade, to a having been reported for the first time were known to have been introduced large number of islands, such as , in 1943 in North America. Three years to places outside the United Kingdom, Palau, , Micronesia, French earlier Parakontikia ventrolineata was re- few people were on the lookout for Polynesia, Samoa, Rotuma, and the is- ported in Texas, taken from shipments them and fewer still were concerned land continent Australia. of flowers from Mexico. Clearly, this about preventing their spread. At other Pacific locations (Bugsuk, Australian species was not an original Philippines; Yokohama, Japan; and member of the North American fauna. New Introductions of Land Flatworms the Maldives) P. manokwari was delib- The species is now established in gar- As a result of the increasing number of erately introduced to control another dens in California. The originally Aus- records of land flatworm introductions, problematic invasive species—the giant tralian species now some new workers recently became in- African snail, Achatina fulica. This snail also in gardens in Florida, Geor- terested in these creatures, including is native to East Africa but has been gia, and California and is frequently Justine, who made the discovery that introduced to many other parts of the found together with P. ventrolineata. the New Guinea land flatworm had ar- world as a food resource, through the

292 American Scientist, Volume 104 © 2016 Sigma Xi, The Scientific Research Society. Reproduction with permission only. Contact [email protected]. pet trade, or just by accident. The snail feeds voraciously on all kinds of plants and thus outcompetes rare, endemic species of snails that are found only on remote Pacific islands. The fact that the New Guinea flatworm will feed on giant African snails may seem a rea- son for optimism in places where both species now live together. But, alas, the worm does not care what it eats, giant African snails or endemic snails. So far it has failed to eradicate the invasive species while at the same time causing declines in populations of native snails. The finding of P. manokwari in France, far outside its known Indo- Pacific distribution, kindled a world- wide interest. As a result, informa- tion on new findings of Platydemus poured in. It turned out that this in- vasive land flatworm was also pres- The largest South American land flatworm, Obama eudoximariae, from the Rio de Janeiro ent in, for example, Singapore, New forest in Brazil, can reach lengths of 29 centimeters, but most land flatworms are no more than Caledonia, and the . several centimeters long. It is coincidence that the flatworm has the same name as the current Clearly, these new records fell within President of the United States: Obama means “leaf ” in the extinct of its already known Indo-Pacific range Brazil. Although this species is not found outside its native range, a closely related Brazilian of distribution. But there were also species, , which was previously unknown to science, was recently found in new findings way outside that range, several locations in Europe. (Photograph by Fernando Carbayo.) in Florida and Puerto Rico. In France, Platydemus was found only in a hot- and amount of travel as globalization the Netherlands, respectively, that ex- house, but in Singapore, New Caledo- progresses has made the spread of the ternally looked very much alike. So we nia, Florida, and the Solomon Islands, worms accelerate in recent years. decided to join forces and to find out it occurs in the wild. Recent invasions not only concern which species they might be. Through Over the past two years the Europe- already known species, but also may examination of microscope prepara- an continent has been quickly catching involve animals completely new to tions it became clear that the animals up with the United Kingdom, as find- science. During the 12th International that Jones had obtained were taxo- ings of introduced species of land flat- Symposium on Flatworm in nomically the same as the ones that I worms have continued there. Species Stockholm, Sweden, in 2012, Jones and examined. But it also became clear that that were already known to be in the I discovered that we had independent- the animals could not be assigned to United Kingdom, such as P. ventrolinea- ly obtained specimens of a land flat- any species of land flatworm currently ta and D. striata, have now been found worm from the United Kingdom and known to science. It turned out that in Spain, and the former has also been sighted in France. The Australian blue garden flatworm, C. coerulea, already known to be in the United Kingdom, has been found not only in France, but also in Spain. Another species from this of flatworms, Caenoplana bicolor, has been sighted in Italy, Spain, and the Netherlands. And B. kewense, that notorious world traveller, now has company in Europe from Bipalium mul- tilineatum, a species native to Japan that has been found in France and Italy. Although one may be inclined to as- cribe this upsurge in sightings of alien land flatworms to better communica- tion between natural historians because of the Internet or to the participation of citizen scientists—and these fac- tors may indeed partly explain this Some land flatworms not only prey on soil invertebrates but also may eat other species of land flat- increase—flatworm­ researchers believe worms. Above, a neotropical land flatworm, multicolor, swallows a land flatworm belong- that these factors do not fully explain ing to another species, septemlineata, from Hawaii and Brazil. The arrow points to the it. We believe that the increasing speed clear pharynx, a tube that the flatworm can protrude to consume prey. (Photograph by Piter Boll). www.americanscientist.org © 2016 Sigma Xi, The Scientific Research Society. Reproduction 2016 September–October 293 with permission only. Contact [email protected]. If You Find a Land Flatworm. . . If you happen to have a close encounter with a critter resembling a pos- sible alien land flatworm, I suggest three actions. The first is to take a picture (preferably including a scale of some sort) and post it to an ap- propriate portal, such as iNaturalist (http://www.inaturalist.org/), together with information about the precise geographic location and the date of the observation. In many countries there are additional local portals for uploading natural history records and observations. The second action that you may want to take is contacting the relevant biosecurity agencies in the country where you found the flatworm and pointing them to the records you submitted to the website(s). Third, it may be useful to collect the animal(s) for further investigation, be- cause external appearances can be deceptive. The best and simplest method is: Pick up the animal with a soft artist’s paint brush or with a leaf, and put it into a container. When the animal undertakes its normal gliding movement and is as fully stretched as possible, quickly pour hot water over it. This kills

Jason Bazzano/Alamy Stock Photo the worm immediately and also minimizes contractions. After that, put the worm in a well-sealed tube or a small jar with 70-percent ethanol (or, if etha- nol is not available, surgical spirit or rubbing alcohol). Place a label, written in pencil, inside the tube, specifying the date, location, and collector.

Some land planarians, such as this Bipalium species from Southeast Asia, are quite colorful. Others are harder to spot, but the dark, wet corners of greenhous- es and gardens are a good place to start looking for them. they belong to the genus ­Marionfyfea, ma for “animal.” This genus of land centers, plant nurseries, earthworm the name that Leigh Winsor, of James flatworms is native to Brazil and in- farms, grassy fields, and ornamental Cook University in Australia, has cludes the largest South American land plant pots. coined for a species of land planar- flatworm—the impressive and colorful Most of these recent new findings ian from subantarctic Campbell Island, species Obama eudoximariae, which may of alien land flatworms in Europe are New Zealand. (The name acknowl- reach a length of 29 centimeters. from outdoor localities such as gar- edges the previous research of zoolo- Spread of a new species may go un- dens and orchards. Some species thus gist Marion Fyfe on New Zealand land noticed because externally a flatworm far have only been reported from plant flatworms.) So, with respect to the ori- can very much resemble another spe- nurseries, but that is no reason to think gin of this new introduced species of cies. That is, the external appearance of that they will not spread. Everything Marionfyfea, all we can say is that its an animal usually gives insufficient in- we know about their adaptability and original area of distribution probably formation to reliably determine which ease of transport suggests that in the is somewhere in the New Zealand ter- species it is. The finding of an Obama longer term many of these species will ritories. Understanding the nature of species in Europe exemplifies the fact establish themselves outdoors and the invasion is complicated by the fact that in flatworms looks can be deceiv- over a much vaster area, through hu- that biologists still do not have a com- ing. At first, these European animals man agency. This exact phenomenon plete picture of the flatworm taxa, and were thought to belong to the species has already happened in the United often invaders show up before anyone Obama marmorata, which is confined Kingdom with the New Zealand flat- even knows their original point of ori- to Brazil. But examination of their mi- worm, A. triangulatus, and the Austra- gin or what their ecology is. croscopic anatomy and also their ge- lian flatworm, A. sanguinea. These new alien species in Europe netic composition revealed that these are all from the East—that is, from European specimens are different from Control Measures Southeast Asia, Australia, or New Zea- O. marmorata and all other known spe- It is critically important to undertake land. But that does not hold true for a cies of Obama. But that was not all. control measures to stop the spread species of the genus Obama that recent- The same species was found in Brazil, of land flatworms, but the animals are ly has been found in the British Isles, where the newly discovered organ- so prolific, adaptable, easily hidden, Spain, France, and Italy. The name of isms possibly occur alongside O. mar- and poorly understood that curbing the genus Obama was not coined in morata. So, recently, this new form of their spread will be enormously chal- honor of the current president of the Obama from Europe and lenging. Bioinvasion may have unpre- United States. It is instead derived was described under the name Obama dictable and adverse effects on local from two words in the extinct Tupi lan- nungara. In both Europe and Brazil O. plants and animals. But thus far, most guage, which was spoken by the native nungara is found in human-modified countries have not developed clear or Tupi people of Brazil: oba for “leaf” and environments, such as parks, garden stringent enough legislation to prevent

294 American Scientist, Volume 104 © 2016 Sigma Xi, The Scientific Research Society. Reproduction with permission only. Contact [email protected]. continued and increasing introduc- In several countries, legislation and limited inspection of imports into Eu- tions of land flatworms. Best practices regulations have been designed to con- rope and open trade within Europe will to prevent spread of introduced land trol harmful invasive species, but for inevitably lead to more alien species be- flatworms have been suggested by pri- the most part these still largely over- ing found and distributed. Even if more vate and public agencies in Europe, look land flatworms. Such regulations countries include invasive flatworms including governmental departments are important because the problem in their quarantine pest lists and legis- responsible for agriculture in Northern with invasive, alien species is that one lation, enforcement may be complex, Ireland, Wales, and the United King- never knows which of them will de- as is the case in the United Kingdom, dom as a whole; Dove Associates, a velop into a major disaster and cause where adherence to the regulatory code horticultural consultancy company great economic damage or extinction is patchy. Therefore, realistically, at best based in the United Kingdom, and the of native species. we may be able to minimize new intro- European and Mediterranean Plant In the United Kingdom it is illegal ductions and to contain those species Protection Organization (EPPO). under the Wildlife and Countryside that already have invaded. For some organisms that have es- Act to knowingly distribute A. triangu- So, I, along with my colleagues tablished themselves in the wild, such latus, A. sanguinea, Kontikia andersoni, around the world, continue to keep a as the New Guinea flatworm, biologi- and P. ventrolineata. For other coun- close watch for new flatworm invad- cal control methods are unknown and tries, suggested control measures, such ers. Earlier this year a new intruder probably nonexistent, because these as the EPPO standard on A. triangula- from New Zealand was discovered in organisms are top-level predators that tus, are merely guidelines and recom- the United Kingdom, Artioposthia exu- have little to fear from other predators mendations that as yet have not led to lans, illustrating that we have not yet in the soil ecosystem. In other words, European Union legislation. Although seen the last of the invaders. under natural conditions there are the E.U. Regulation on Invasive Alien no—or only very few—animals that Species entered into force on January Bibliography feed on terrestrial flatworms. Part of 1, 2015, and a list of invasive species Àlvarez-Presas, M., E. Mateos, À. Tudó, H. the reason may be that they do not has been drawn up, so far it does not Jones, and M. Riutort. 2014. Diversity of in- taste good, which has been vouched include any land flatworms. troduced terrestrial flatworms in the Iberian Peninsula: A cautionary tale. PeerJ 2:e430. for by Winsor. He devoted his In Australia the new Biosecurity Act Boll, P. K., and A. M. Leal-Zanchet. 2016. Pref- to the study of Australian land flat- and its associated regulations came erence for different prey allows the coex- worms, and he did not hesitate to into force on June 16, 2016. One of its istence of several land planarians in areas gather such esoteric information, writ- objectives is to control the movement of the Atlantic Forest. 119:162–168. ing in a journal article that he found of plants and animals, but it does not Carbayo, F., M. Àlvarez-Presas, H. D. Jones, the taste of Platydemus “astringent.” single out land flatworms as focal or- and M. Riutort. 2016. The true identity of Obama (Platyhelminthes: ) flat- Several flatworm experts have al- ganisms. Similar legislation is in effect worm spreading across Europe. Zoological ready commented on or explored the in New Zealand. Journal of the Linnean Society 177:5–28. plausibility of using sanitation mea- The United States has a body of laws Ducey, P. K., M. McCormick, and E. Davidson. sures on imported plants to kill land and regulations controlling the trans- 2007. Natural history observations on Bipa- flatworms and prevent their spread port of animals and plants under the lium cf. vagum Jones and Sterrer (Platyhel- in potted plants. Immersing potted jurisdiction of the federal agency Ani- minthes: Tricladida), a terrestrial broadhead planarian new to North America. Southeast- plants in water heated to 34 degrees mal and Plant Health Inspection Ser- ern Naturalist 6:449–460. Celsius for at least five minutes (after vice (APHIS), which is within the U.S. Jones, H. D., and R. Sluys (in press). A new sealing the portion of the plant con- Department of Agriculture. Each state terrestrial planarian species of the genus tained within the soil in a plastic bag), also has its own regulations regarding Marionfyfea (Platyhelminthes, Tricladida) is fully effective, killing within one the import and transport of animals found in Europe. Journal of Natural History. hour any indi- and plants. The Code of Federal Reg- Justine, J.-L., L. Winsor, D. Gey, P. Gros, and J. Thévenot. 2014. The invasive New Guinea viduals present inside the pot. Similar ulations does not mention flatworms flatworm Platydemus manokwari in France, simple methods, such as heating the specifically, but a representative from the first record for Europe: Time for action soil, might be equally effective to pre- APHIS pointed out to me in an email is now. PeerJ 2:e297. vent further spread of the worms. The that the agency nevertheless considers Justine, J.-L., et al. 2015. The invasive land pla- New Guinea flatworm appears to be a flatworms to be a general predator that narian Platydemus manokwari (Platyhelmin- hardier species in that it is killed only is subject to their regulation of biologi- thes, Geoplanidae): Records from six new localities, including the first in the USA. after immersion for five minutes in hot cal control agents. This representative PeerJ 3:e1037. water of at least 43 degrees Celsius, also pointed out that land flatworms as reported in 2008 by Shinji Sugiura, can be considered an indirect plant then at the Forestry and Forest Prod- pest because they feed on earthworms. ucts Research Institute in Japan. The Bioinvasion effectively homogeniz- flatworms generally are attracted to es the world’s biodiversity. Flatworm dark and damp places, and therefore aficionados can get excited about new For relevant Web links, consult this ­issue of American Scientist Online: one may also actively hunt them down findings of exotic, introduced land flat- in garden centers and plant nurseries, worms, but all of us would prefer to http://www.americanscientist.org/ or in one’s own garden, by looking un- see them restricted to their natural sur- issues/id.122/past.aspx der objects such as loose pieces of turf, roundings. Sanitation measures for im- plant pots, rocks, and nontransparent ported plants might prevent or reduce plastic on the soil surface.­ the spread of nonnative flatworms, but www.americanscientist.org © 2016 Sigma Xi, The Scientific Research Society. Reproduction 2016 September–October 295 with permission only. Contact [email protected].